THE NEUROBIOLOGY OF THE ASCIDIAN TADPOLE LARVA: Recent Developments in an Ancient Chordate

Size: px
Start display at page:

Download "THE NEUROBIOLOGY OF THE ASCIDIAN TADPOLE LARVA: Recent Developments in an Ancient Chordate"

Transcription

1 Annu. Rev. Neurosci : doi: /annurev.neuro Copyright c 2004 by Annual Reviews. All rights reserved THE NEUROBIOLOGY OF THE ASCIDIAN TADPOLE LARVA: Recent Developments in an Ancient Chordate Ian A. Meinertzhagen, 1,2 Patrick Lemaire, 3 and Yasushi Okamura 4,5 1 Marine Biological Laboratory, Woods Hole, Massachusetts Life Sciences Centre, Dalhousie University, Halifax, Canada B3H 4J1; iam@dal.ca 3 Laboratoire de Génétique et Physiologie du Développement, IBDM, CNRS/INSERM/Université delaméditerranée/ap de Marseille, Case 907, Campus de Luminy, F Marseille Cedex 09, France; lemaire@ibdm.univ-mrs.fr 4 Section of Developmental Neurophysiology, Okazaki Institute for Integrative Bioscience, Nishigonaka 38, Myodaiji, Okazaki , Aichi, Japan 5 Molecular Neurobiology Group, Neuroscience Research Institute, National Institute of Advanced Industrial Science, Higashi 1 1, Tsukuba, Ibaraki 305, Japan; maboya@dc4.so-net.ne.jp Key Words chordate evolution, neural plate, neurulation, cell lineage, ion channels Abstract With little more than 330 cells, two thirds within the sensory vesicle, the CNS of the tadpole larva of the ascidian Ciona intestinalis provides us with a chordate nervous system in miniature. Neurulation, neurogenesis and its genetic bases, as well as the gene expression territories of this tiny constituency of cells all follow a chordate plan, giving rise in some cases to frank structural homologies with the vertebrate brain. Recent advances are fueled by the release of the genome and EST expression databases and by the development of methods to transfect embryos by electroporation. Immediate prospects to test the function of neural genes are based on the isolation of mutants by classical genetics and insertional mutagenesis, as well as by the disruption of gene function by morpholino antisense oligo-nucleotides. Coupled with high-speed video analysis of larval swimming, optophysiological methods offer the prospect to analyze at single-cell level the function of a CNS built on a vertebrate plan. INTRODUCTION Nothing in biology makes sense except in the light of evolution. (Dobzhansky 1973) Animals in which a back and belly can be recognized, so-called bilaterians, fall into two major groups. Protostomes include model systems such as Drosophila X/04/ $

2 454 MEINERTZHAGEN LEMAIRE OKAMURA and Caenorhabditis elegans, and deuterostomes include the vertebrates such as ourselves. Three main groups of deuterostomes, echinoderms, hemichordates, and chordates, are widely held to have diverged from a common ancestor during the Cambrian explosion around 550 mya (Valentine et al. 1996). Although the debate about vertebrate ancestry, whether a hypothetical ancestor arose from a freeswimming ancestor or by a process of pedomorphosis from sessile forms like adult sea squirts, is still ongoing, many recent accounts (e.g., Wada 1998, Swalla et al. 2000) favor descent from a basal, free-swimming chordate. The chordate lineage, which comprises two sibling groups, cephalochordates such as amphioxus and true chordates such as the more familiar vertebrates, is distinguished by possessing a larval notochord and dorsal tubular central nervous system (CNS). Urochordates, the sibling ancestral group, survive as a number of forms. Larvaceans, such as Oikopleura, develop directly from an embryo that possibly arose from a urochordate ancestor by neoteny (e.g., Garstang 1928). In contrast, sea squirts, or ascidians, have a metamorphic development, the adult stage of the life cycle arising from a transient free-swimming tadpole larva. The larval body comprises a trunk or head region and a motile tail and has a miniature CNS with many chordate credentials (Katz 1983, Meinertzhagen & Okamura 2001). Finally, the salps and doliolids, closely related to ascidians, are metamorphic but live a pelagic life (Bone 1998) and are not accessible to most laboratories. Analysis of the development and physiology of ascidian tadpoles can thus shed light on the origins of the chordate phylum. Given its phylogenetic significance, the ascidian tadpole larva has long attracted the attention of biologists. Nevertheless, many studies on ascidian larvae have remained somewhat specialized, at least until recently. A number of new developments are rapidly reversing this longstanding neglect (Corbo et al. 2001, Holland 2002), however, especially for the neurobiology of this simple animal. Ascidian larvae indeed have features favorable to neurobiological study (Bone & Mackie 1982, Burighel & Cloney 1997), chief among which is that cell number is very small and largely, if not wholly, fixed. As a result, their simple nervous system should enable us to study the neuroethology of a chordate larva, cell by cell, by the identified-neuron strategy widely adopted in invertebrate systems (e.g., Hoyle 1983). Three recent topics, in particular, underpin significant research themes in ascidian larval neurobiology. First is the recent release of the genome sequences for the common sea squirt Ciona intestinalis (Dehal et al. 2002) and of the related Ciona savignyi ( These simple genomes are 20 times smaller than the mouse genome, yet they harbor most gene families found in vertebrates. They are thought to be related to the ancestral condition of the chordate genome before it underwent the two complete duplications that are proposed to have occurred in the evolution of craniates (Holland et al. 1994). The simplicity of the Ciona genomes thus parallels the anatomical simplicity of their larva. These genomic milestones consummate earlier studies to provide access to the genes that underlie the organization, function, and development of the larval nervous system and to new molecular tools to analyze these.

3 ASCIDIAN LARVAL NEUROBIOLOGY 455 Second is the long history of experimental embryology of the ascidian embryo, initiated by Chabry s (1887) cell ablation experiments and by Conklin s pioneering work on cell lineage (Conklin 1905) and now revisited with molecular approaches (Satoh 2001). Third is the appearance of analytical studies on larval behavior, especially on larval swimming and phototaxis, that have started to provide insights into the outcome of neural development and function, as well as methods to assay perturbations induced in these. Analysis of the underlying circuits and their neurophysiology has, by contrast, been traditionally frustrated by the problems of the small sizes of larval nerve cells and the tough tunic that surrounds the larva, from which urochordates derive their alternative name, tunicates. Some recent progress has, however, occurred in this field as well. Despite numerous important reports on various other species, there is a progressive canonization of Ciona (intestinalis or savigny) and Halocynthia roretzi in most recent work. Each has particular advantages, and the question of species is still vexed. Adult Halocynthia roretzi are more robust, and their embryos are larger and more suited to experimental embryology. Both blastomere injection and recombination experiments are more routine and allow cell lineage to be defined from blastomere injections (Nishida & Satoh 1985, Nishida 1987). The larva is also better suited to electrophysiology (Ohmori & Sasaki 1977). A database (MAGEST: provides data on DNA sequences and expression patterns of expressed sequence tags (ESTs) from maternal mrnas (Kawashima et al. 2000, 2002). The commercial fishery of this species provides an additional incentive to its study, even if its Pacific distribution effectively restricts experimental work to Japan. Ciona, by contrast, is pandemic in temperate waters. Both the anatomy (Nicol & Meinertzhagen 1991) and behavior (e.g., Kawakami et al. 2002) of its larva are reported in great detail. The recent draft release of the Ciona genome has been complemented by large-scale cdna and EST projects (Satou et al. 2002a,b, 2003b; Satoh et al. 2003), as well as by expression profiles of genes at different developmental stages (e.g., tailbud embryos, Satou et al. 2001; swimming larvae, Kusakabe et al. 2002). Transient, en masse transfection by electroporation (Corbo et al. 1997b) can be used to label individual cells, including neurons (Okada et al. 2001), to examine gene function (Hotta et al. 2000), and to execute large- or small-scale promoter analyses (Corbo et al. 1997b, Harafuji et al. 2002). Investigators have recently reported transposon-mediated germline transgenesis using the Minos transposon (Sasakura et al. 2003a). Thanks to the relatively short life cycle (three months), hermaphroditism, and success of sperm cryopreservation techniques, mutagenesis screens (Moody et al. 1999; Nakatani et al. 1999; Sordino et al. 2000a,b, 2001) carry the prospect of isolating developmental mutants of the nervous system. Finally, injection of morpholino antisense oligonucleotides (Satou et al. 2001) provides an alternative way to analyze loss of gene function. Collectively, these technical developments in Ciona provide powerful tools for future studies on the development and function of the larval nervous system. The current mood is very confident, which is why much of the emphasis presented in this

4 456 MEINERTZHAGEN LEMAIRE OKAMURA review is on Ciona. Ascidian larvae are highly diverse, however, comprising 3000 species (Jefferey 1997), of which Ciona has a relatively simple and unspecialized larval form. Therefore, one should perhaps remember that the prime mover in much of the recent attention paid to Ciona, which for most workers is to understand evolution in chordates, ultimately may not be well served by undue focus on this one form. As Ciona s larva becomes a model in neurobiology, it seems inevitable that strange hands will use her to their own ends, different investigators pursuing different goals. Two important goals emerging are (a) to provide a basis to analyze the action of vertebrate neural specification and neurogenesis genes in a more accessible embryo and (b) to examine the genetic determination/regulation of neural circuits underlying chordate behavior. The latter can be facilitated by the analysis of behavioral and connectivity mutants. STRUCTURAL ORGANIZATION The larva of Halocynthia contains an estimated 3000 cells (Yamada & Nishida 1999); that of Ciona contains even fewer, with 2600 cells (Satoh 1999). In the Ciona larva, these include 40 notochord and 36 muscle cells, which exhibit clear constancy between individuals. The CNS has, by contrast, over 330 cells (Nicol & Meinertzhagen 1991), and the constancy of this number is less clear. These are the progeny of no more than 13 divisions (compared with, for example, the Drosophila embryo, which undergoes 13 nuclear cleavages prior to blastoderm formation). The CNS: Structural Divisions and Their Genetic Bases Many investigations have sought to define the structural divisions of the larval brain and, latterly, the gene expression territories within these. The motivation is obvious: Like searching the family photo album for likenesses among remote relatives, such studies aim to establish the identity of ancestral chordate features. ANTERO-POSTERIOR DIVISIONS OF THE NEURAXIS Unlike other invertebrates, but much like vertebrates, the CNS of ascidian larvae develops from a neural plate. The caudo-rostral pattern by which it rolls up to form the neural tube resembles that seen during amphibian neurulation. The ascidian neural plate differs from its amphibian homologue by having fewer blastomeres and by undergoing relatively more of its cleavages and neurulation before sinking beneath the ectoderm than in vertebrate embryos (Nicol & Meinertzhagen 1988). In contrast to vertebrates, however, the anteriormost region of the neural plate does not roll up and internalize but contributes to the so-called dorso-anterior epidermis, which includes the adhesive organs, or palps, head sensory neurons, and pharynx (Nishida 1987). The posterior part of the neural plate gives rise to three structural divisions of the larval ascidian CNS that have long been recognized (reviewed in Bone & Mackie 1982). These

5 ASCIDIAN LARVAL NEUROBIOLOGY 457 are (a) a rostral sensory vesicle containing the sensory receptor systems, with a pigmented ocellus (Dilly 1964) and, anterior to it, a pigmented otolith (Dilly 1962) (this region constitutes most of the neural cells, totaling around 215 in Ciona); (b) a caudal nerve cord (65 cells, mostly ependymal); and, between these, (c) a visceral ganglion containing the motoneurons (about 45 cells). In addition to these three, a slender neck region connecting the sensory vesicle and visceral ganglion has since been distinguished in Ciona and comprises six cells (Nicol & Meinertzhagen 1991). The caudal nerve cord is the simplest geometric configuration: a row of ventral keel cells, left and right lateral rows, and a dorsal row of capstone cells, thus four cells in cross section (Nicol & Meinertzhagen 1991). Additional cells derived from the lateral cell rows augment the cell population of the visceral ganglion and its cross section; in the sensory vesicle the cells are far more numerous, especially in the posterior wall of the vesicle, and are not easily related to the caudal fourcell cross section (Cole & Meinertzhagen 2004). Each of these antero-posterior subdivisions of the ascidian CNS is itself patterned along the dorso-ventral axis. This patterning, which is not easily seen at the morphologic level, is revealed by the expression of specific marker genes (see below). UROCHORDATE BRAINS COMPARED Although they generally retain the above tripartite organization, ascidian brains are as diverse as ascidian larvae themselves, with considerable variation in the ocellus and otolith of the sensory vesicle, for example (Berrill 1950, Vorontsova 1988), and the smallest numbers in the larvae of solitary forms such as Ciona. Cell number in urochordate brains is generally small, but numbers in other urochordate groups differ somewhat from those in ascidian larvae. In the third urochordate group, the salps, the numbers of cells are not as reduced in the symmetrical dorsal ganglion, which is thus more easily compared with the more complex brains of chordates (Lacalli & Holland 1998). By contrast, in larvaceans such as Oikopleura and Fritillaria, cell number is even smaller than in ascidians such as Ciona. For example, with a body length at least one order of magnitude greater than in a Ciona larva, and with far greater behavioral complexity (Bone 1985), the CNS in an adult Oikopleura nevertheless has only about a quarter the number of cells found in Ciona. The following sections focus on the nervous systems of larval Ciona intestinalis and Halocynthia roretzi. The reader should remember, however, that a closer study of other tunicate brains will be required to gain a global view of the organization and evolution of these early chordate nervous systems. COMPARISONS BETWEEN UROCHORDATE AND CRANIATE BRAINS Ascidian orthologues of developmental genes are expressed in individual territories along the neuraxis, in patterns that resemble closely those that regionalize the vertebrate brain. Their expression patterns are similar in both Ciona and Halocynthia, providing the most authoritative basis to compare brain regions in different groups. Even though structure alone is insufficient to arbitrate such homologies with vertebrate brain divisions, these have in fact been assumed in some early reports (e.g.,

6 458 MEINERTZHAGEN LEMAIRE OKAMURA Katz 1983). Recent reviews (Meinertzhagen & Okamura 2001, Lemaire et al. 2002) summarize details for many sections that follow. Initially the patterns of Otx, Pax-2/5/8, and Hox genes indicated the tripartite organization of the neuraxis (Wada et al. 1998) and thus intimated the homology of these three regions to the vertebrate fore-, mid-, and hindbrain, respectively. Proceeding rostrally along the neuraxis, patterns of correspondence support homology between the anterior region of the caudal nerve cord and the anterior vertebrate spinal cord (Hox5), between the posterior visceral ganglion and rhombomeres 5 8 of the vertebrate brain (Hox3), and between the anterior visceral ganglion and rhombomere 4 (Hox 1). Thus although ascidian motoneurons originate in the visceral ganglion, the gene-expression code of this region is more similar to the vertebrate rhombencephalon than to that of the vertebrate spinal cord, the motoneurons occupying instead the same genetic territory as vertebrate-descending brainstem reticulospinal neurons. The neck region of the ascidian CNS is of particular interest. Sandwiched between the Otx territory of the sensory vesicle and the Hox3 territory of the anterior visceral ganglion, it expresses Pax2/5/8, engrailed, and FGF8/17/18 (Imai et al. 2002a, Jiang & Smith 2002) in a manner similar to the vertebrate isthmus or mid-hindbrain boundary (MHB) (reviewed in Wurst & Bally-Cuif 2001), although in a somewhat different rostro-caudal sequence. Note, the neck region is reported to comprise only six cells (Nicol & Meinertzhagen 1991). Regardless of where one draws the borders, the correct attribution of Pax2/5/8, Fg f9/16/20, and Fg f8/17/18 coexpression sites among these cells must therefore have a very sharp focus. This is particularly striking because the current version of the sequenced genome lacks a clear orthologue for Gbx, one of the genes that helps position the MHB in vertebrates. Although the genetic program of the neck appears very much similar to that of the MHB organizer, so far nothing indicates that the neck transmits signals that organize its neighboring regions. Finally, the posterior sensory vesicle is similar to the metencephalon (Fgf9/ 16/20; engrailed), whereas the anterior sensory vesicle corresponds to the di-/mesencephalon brain (Otx). On the other hand, if the neck is the MHB, i.e., is the mes-/met-encephalon boundary, then the posterior sensory vesicle is part of the mesencephalon, which fits with the fact that it expresses Otx (see Hudson et al. 2003). Only one telencephalon marker, emx, so far has been examined and is expressed in the dorso-anterior epidermal territory originating from the anteriormost aspect of the neural plate. This finding suggests that ascidians, like amphioxus (Holland & Holland 2001), lack a true homologue of the telencephalon. Analysis of the patterning of the diffuse, superficial nervous system of a more basal deuterostome, the hemichordate Saccoglossus kowalevskii (Lowe et al. 2003), suggests that the chordate CNS was generated by the internalization of a well-patterned superficial neural network. The epidermal expression domain of emx may thus correspond to the forerunner of the telencephelon, the formation of a CNS from an ancestral, diffuse network occurring in several steps. Thus, although the enormous overgrowth of the forebrain is a vertebrate invention, these territories may have arisen from an ancestral territory that preexisted in urochordates.

7 ASCIDIAN LARVAL NEUROBIOLOGY 459 DORSO-VENTRAL DIVISIONS OF THE NEURAXIS Similarities and/or homologies between the ascidian larval CNS and the vertebrate brain also extend to dorsoventral patterning. The ventralmost row of cells in the caudal neural tube expresses HNF3β (Corbo et al. 1997a) and sonic hedgehog (Takatori et al. 2002) and is thus comparable to the vertebrate floor plate. In more lateral territories, expression of Ciona gsx, like vertebrate Gsh, is detected in intermediate cells of the neural tube, though expression of the ascidian orthologue is restricted to the anterior territories. Finally, two ascidian bone morphogenetic protein (Bmp) genes, orthologues of Bmp5/7/8 and Bmp2/4, are expressed in the midline epidermal territories flanking or abutting the neural region. This finding parallels the situation in vertebrate embryos, suggesting the existence of a neural crest like identity (see below). Expression of Pax3/7, Snail, and distal-less in the dorsal neural tube or flanking epidermis reinforces both that dorso-ventral regionalization of the vertebrate and ascidian neural tissues is very similar and that the dorsal territories display a genetic program similar to that in vertebrate neural crest. The Ascidian Peripheral Nervous System Like the CNS, the peripheral nervous system (PNS) of ascidians exhibits similarities with that of vertebrates. Ascidian larvae have a system of epithelial neurons in both the tail (dorso- and ventro-caudal epidermal neurons) and head, or trunk (apical- and rostral-trunk epidermal neurons), which form a simple PNS (Takamura 1998). At least some of these peripheral neurons likely are mechanoreceptors. They are embedded in the epithelium (Jia 1987), extend long cilia into the tunic of the tail (Crowther & Whittaker 1994), and contribute or are connected to nerves that run back to the sensory vesicle. In neither Ciona nor Halocynthia do the tail epidermal neurons derive from the neural plate but rather from the midline epidermal territories (Nishida 1987). The dorsal epidermal tail sensory neurons originate from a territory that expresses a neural crest like genetic program; this is not the case for the ventral sensory neurons. HOMOLOGIES OF ASCIDIAN BRAIN STRUCTURES These similarities between urochordate and vertebrate brains are at the level of the patterning of the nervous system and do not necessarily reflect the orthology of their differentiated structures. For the neuromuscular apparatus, in particular, Bone (1992) has spoken against considering the ascidian tadpole larva as a chordate prototype. For the larval CNS, too, there are major differences. The larval brain lacks clear signs of segmentation and laminae and retains the character of a hollow epithelial tube, whereas chordate, especially craniate, brains undergo lamination by radial migration. Given this difference, the fact that Ciona has the gene reelin, which in mammals plays a role in organizing the brain s layers (Rice & Curran 2001) is interesting, and it remains to be seen what ancestral functions of lamination reelin may mediate in urochordates, possibly in the more complex brain of adults. Associated with the lack of lamination is a lack of stem cells in the developing brain

8 460 MEINERTZHAGEN LEMAIRE OKAMURA of ascidian embryos, in which cells arise through equal cleavages, at least as so far identified. The relative absence of radial cell migration and of massive cell death also distinguish this simple brain from its more complex vertebrate counterpart. Likewise, the absence of myelinated nerves and axons in both fiber tracts of the CNS (Katz 1983) and peripheral nerves (Torrence 1983), confirmed by the absence of myelin-related genes in the Ciona genome (Dehal et al. 2002), bespeaks a lack of rapid conduction pathways and a simpler, possibly ancestral chordate organization. The latter possibly correlates with, in the case of myelination genes, (a) the lack of neuregulins, which are involved in axon-oligodendrocyte signaling (Canoll et al. 1996), and of orthologues for the oligodendrocyte determinants Olig1 and 2 (Zhou et al. 2000); and (b) the lack of neurotrophins and their receptors (Dehal et al. 2002), the presence of which promotes survival and neurite extension. Despite these differences, there are many obvious homologies, which we consider next. Structural Homologies Between Ascidian and Vertebrate Brains The line of chordate descent has bequeathed to vertebrates a number of structural homologues that must already have been present in the larval brains of the common ancestor with ascidian (Meinertzhagen & Okamura 2001). Some structures reflect the corresponding patterns of homeobox gene expression along the neuraxis, reported above. SOME FRANK STRUCTURAL HOMOLOGUES In addition to the most obvious embryonic homologue, the neural plate itself, many structures of the differentiated CNS show clear structural similarities to those in vertebrates. 1. An epithelium of ciliated ependymal cells lines the neural canal (Mackie & Bone 1976, Katz 1983), as in the vertebrate CNS. 2. Secreted by these ependymal cells, a thread running within the neural canal is the claimed homologue of Reissner s fiber in vertebrates (Olsson 1972). This complex of glycoproteins from the vertebrate subcommissural organ binds monoamines present in the ventricular cerebrospinal fluid and transports them along the central canal (Rodriguez & Caprile 2001); such a function is untested for the ascidian larval CNS, in which the homology is solely based upon ultrastructural criteria. 3. Coronet cells form a group of 18 cells on the left side of the sensory vesicle (Dilly 1969, Eakin & Kuda 1971, Nicol & Meinertzhagen 1991). These cells structurally resemble rather closely cells of the saccus vasculosus in the vertebrate hypothalamus (Svane 1982). From an old theory of Dammerman, the latter may function as hydrostatic pressure detectors (Kühlenbeck 1977), a function also proposed for their ascidian counterparts (Eakin & Kuda 1971). Originally designated as an alternate photoreceptor system (Dilly 1969), in fact no evidence exists that coronet cells have a sensory function at all

9 ASCIDIAN LARVAL NEUROBIOLOGY 461 (Torrence 1983), nor do hydrostatic pressure increases influence larval swimming (Tsuda et al. 2003). 4. Pigment spots of the ocellus and otolith both contain melanin and its key synthetic enzyme tyrosinase (Sato & Yamamoto 2001), expression of which is an early marker for these cells (Whittaker 1973, 1979). Melanin is typical of vertebrate sensory organs, where in visual organs it screens light, and may play a more general role in sensory transduction (Dräger & Balkema 1987). The melanin is distributed as granules in the ocellus and as a single large spherical granule in the ocellus. Sato & Yamamoto (2001) present a comprehensive summary of ascidian pigment cells. 5. The 18 or so photoreceptors, 3 lens cells, and pigment cell of the rightsided ocellus form an obvious candidate homologue of the vertebrate eye. As in vertebrates, ascidian photoreceptors are ciliary in origin (Eakin & Kuda 1971) and hyperpolarize to light (Gorman et al. 1971). The single ocellus expresses the eye determination gene Pax-6 (Glardon et al. 1997), but differing interpretations have been placed upon which eye(s) is/are its vertebrate homologue. Early interpretations homologized the ascidian ocellus and the vertebrate epiphysis (pineal), in keeping with the lateral position of the pigment cell precursor in the neural plate (Nishida & Satoh 1989). Photoreceptors in Ciona express Ci-Opsin1, which shows highest homology to both vertebrate retinal and pineal opsins (Kusakabe et al. 2001). On the basis of similarities in sequence data and development, Kusakabe et al. (2001) propose that the median eye of basal vertebrates and the ascidian ocellus may represent the ancestral state of chordate photoreceptors. Comparative studies on larval development have suggested an alternative view: that the ascidian ocellus is a homologue of what in vertebrates gave rise to the right lateral eye (Sorrentino et al. 2000). OTHER CASES ARE STRUCTURALLY MORE CRYPTIC In addition to such obvious cases of structural homology, expression patterns of certain genes in ascidian embryos are likely harbingers of those seen during early developmental stages of a number of vertebrate neural structures. Such patterns may have therefore already existed in the last common ancestors of all chordates, even if their representation in ascidians is structurally cryptic. Vertebrate neural features with such representation in the ascidian larval brain include the following: placodes, neural crest, and the neurohypophysis. Placodes and neural crest are two defining structures of the vertebrate nervous system (Northcutt & Gans 1983), and their derivatives ramify throughout the vertebrate body. Even though structural counterparts have long been thought lacking in ascidians, there is evidence for the existence of gene expression patterns ancestral to those structures, which suggests that placodes and neural crest arose by stages and that these stages first arose before the divergence of urochordates and chordates. For example, epidermal sensory neurons in the trunk, which apparently derive from progeny of the anterior animal a8.26 cell pair, line up along the edge of the presumptive neural tube (Ohtsuka et al. 2001), in a region corresponding

10 462 MEINERTZHAGEN LEMAIRE OKAMURA topologically to the territory of the neural crest in vertebrate embryos, and where the ascidian homologue of Pax3/7 and snail also act (Wada et al. 1997, Wada & Saiga 1999). Thus the development of ascidian epidermal sensory neurons shares these features with that of vertebrate placodes and neural crest. Wada (2001) suggests that neural crest may have arisen from ancestral ectoderm represented by ascidian dorsal midline ectoderm, to which were added properties of pluripotency, delamination, and migration, and the possession of antero-posterior positional information. Gostling & Shimeld (2003) propose further that the evolution of a dorsal neural expression domain for genes of the vertebrate Zic family was an important step in the evolution of the neural crest. Indeed, an ascidian Zic orthologue is expressed in the neural plate, commencing during neurulation (see below). Different placodes are thought to have had different evolutionary origins (Graham 2000, Shimeld & Holland 2000), with at least two of the vertebrate s sensory placodes present already in the last ancestors of ascidians and chordates. They are 1. the acousticolateralis system. The atrial siphon primordium of adult ascidians is a proposed homologue of the otic placode (Shimeld & Holland 2000), insofar as it gives rise to sensory neurons resembling hair cells of the acousticolateralis system (Bone & Ryan 1978) and expresses the ascidian orthologue of the Pax-2/5/8 gene family (Wada et al. 1998). On the other hand, the mechanoreceptors of the cupular organ are primary sensory neurons and thus structurally less well qualified as candidate homologues for vertebrate hair cells than the anaxonal secondary neurons of the coronal organ in Botryllus, which have a peripheral synapse and an afferent sensory axon arising from a central neuron (Burighel et al. 2003). 2. the pituitary. Confirming a historical suggestion (Willey 1894), the neurohypophysial duct in larval ascidians is a proposed homologue of the vertebrate olfactory/adenohypophyseal/hypothalamic placode (Ruppert 1990, Manni et al. 2001), which gives rise to the neurohypophysis. The duct forms from an anterior prolongation of the neural tube (Willey 1894, Manni et al. 1999, Cole & Meinertzhagen 2001), which, in a duality reminiscent of the pituitary, becomes abutted by an ectodermal invagination from the pharyngeal primordium, the cells of which express the ascidian pituitary homeobox gene, Pitx (Shimeld & Holland 2000, Christiaen et al. 2002). Progeny of the duct, moreover, express immunoreactivity to GnRH (Mackie 1995), as do progeny of the olfactory placode. NEURAL DEVELOPMENT Cleavage and Cell Lineage Ascidian embryos undergo early determinate cleavages that are radial, rapid (initially every 30 min in Ciona), and symmetric about the midline. Cleavage 1 divides the embryo into left and right, cleavage 2 into anterior and posterior, and

11 ASCIDIAN LARVAL NEUROBIOLOGY 463 cleavage 3 into animal hemispheres (lower-case letters a and b) and vegetal hemispheres (upper-case letters A and B). Each blastomere has a two-part number: the generation number (1 14), followed by the individual blastomere number within this generation, which, in the early generations at least, decreases with proximity to the vegetal pole (Conklin 1905). At each division, the progeny of a given blastomere are assigned individual blastomere numbers that double those of its progenitor: For example, the daughters of a4.2 are a5.3 and a5.4; those of B7.4 are B8.8 and B8.7. The invariant pattern of cleavage allows the fate of each cell to be followed to a point in the 110-cell stage in Halocynthia when most contribute to a single tissue type (Nishida 1987) and to be extended to 226 of the 330 CNS cells in the larva of Ciona (Cole & Meinertzhagen 2004). It is remarkable that the lineage is so very well conserved among ascidians, even between phylogenetically distant forms such as Halocynthia and Ciona (Swalla et al. 2000). This conserved pattern of cleavage contrasts with the situation in nematodes, in which, for example, C. elegans develops with a fixed cleavage pattern, whereas marine nematodes such as Enoplus brevis show no signs of such invariance (Lemaire & Marcellini 2003). Investigators first took the existence of an invariant cell lineage to indicate autonomous differentiation of blastomeres, and consequently they saw the ascidian embryo as a typical example of mosaic development (Lemaire & Marcellini 2003). This interpretation is, however, wrong for many lineages including some that give rise to neural tissue. Cell lineage can play both a topographical and a typological role in the assignment of cell fate (Meinertzhagen 2002). For example, the a- lineage from a4.2, which gives rise to anterior neural tube, requires inductive mechanisms like those in vertebrates (see below). In this case, the fixed cleavage pattern provides the precise positioning of the induced blastomere with respect to its inducing neighbors. In contrast, in the A-lineage from A4.1, which gives rise to posterior neural tube, a generic neural identity is achieved cell autonomously, and the role of the fixed cleavage is to partition maternal determinants precisely into different blastomeres. The overall descriptive sequence of cleavage has been summarized elsewhere (Nicol & Meinertzhagen 1988, Satoh 1994, Lemaire et al. 2002), and its details are not fundamental for this review. A recent reexamination using confocal imaging of wholemount embryos (Cole & Meinertzhagen 2004) indicates the following: The caudal nerve cord derives from b9.37 (dorsal), A9.32 and A9.29 (lateral), and A10.29 and A10.25 (ventral); the visceral ganglion derives from b9.38 (dorsal), A9.29, A9.30, and A10.31 (lateral), and A10.30 (ventral); and the posterior sensory vesicle derives from b9.38 (dorsal), A10.32 (lateral), and A10.26 (ventral); except for four ventral cells from A9.14, the remaining sensory vesicle and neurohypophysis derives from a-line blastomeres. Initial Specification of a Neural Cell Fate AUTONOMOUS SPECIFICATION OF NEURAL IDENTITY IN THE A-LINE The posterior A-line neural tissue originates from two pairs of blastomeres at the 32-cell stage: the A6.2 and 6.4 pairs. At the next cleavage (64-cell stage), each of these

12 464 MEINERTZHAGEN LEMAIRE OKAMURA blastomeres contributes one daughter restricted to the notochord and one restricted to the posterior nerve cord. The fate distinction between notochord and posterior nerve cord precursors results from the reception by the notochord precursor of a combination of basic fibroblast growth factor (FGF)-like and BMP signals between the 32- and 64-cell stages (Nishida 2002). Although a generic neural identity is acquired cell-autonomously in the A-line, not all posterior neural fates are acquired in the absence of cell communication. As in vertebrates (Holowacz & Sokol 1999), formation of the posteriormost neural cells requires externally regulated kinase (ERK) signaling. ERK is activated in the presumptive posterior neural cells by the 32-cell stage, and the inhibition of MAP- ERK kinase (MEK) signaling at this stage respecifies the fate of visceral ganglion and tail nerve cord precursors into posterior sensory vesicle (Hudson et al. 2003). INDUCTION OF ANTERIOR NEURAL PLATE FATES IN a-line ECTODERM The anterior neural plate is derived from the a4.2 blastomeres. Unlike A4.1, a4.2 requires instruction from its vegetal neighbors to adopt a neural fate (Reverberi et al. 1960; reviewed in Lemaire et al. 2002). The neural-inducing signal originates principally from the A4.1 progeny, and the competence to form anterior neural tissue is restricted to the a4.2 progeny (Lemaire et al. 2002, Hudson et al. 2003). Little is known at present about the molecular mechanisms that spatially restrict animal competence (see Lemaire et al. 2002), although more is known about the inducing signals and their temporal response. These signals show both parallels to and differences from the situation in vertebrate embryos, in which the FGF and BMP signaling pathways both play a crucial role in the binary decision between neural and epidermal fates (Wilson & Edlund 2001). In ascidian embryos, antagonizing the BMP pathway appears neither necessary nor sufficient to specify a CNS fate (Darras & Nishida 2001). Although these experiments fail to exclude a role for the inhibition of BMP signaling in the anteriormost neural plate fates (the palps), they do at least suggest that the role of the BMP pathway is much less important in ascidian neural induction than it is in vertebrates. Ascidian embryos more closely resemble vertebrates when considering the role of the FGF signaling pathway. According to gain- and loss-of-function analyses of the FGF pathway, this pathway is crucial to initiate a stable program of anterior neural differentiation in a-line blastomeres (Lemaire et al. 2002). Recent investigations confirm the molecular identification of FGF9/16/17 as the vegetally secreted ascidian early neural inducer (Bertrand et al. 2003). Furthermore, analysis of the Cis-regulatory regions of Ci-otx, a direct FGF target, reveals that the action of the neural inducer is mediated by two maternal transcription factors, ETS1/2 and GATAa. The former mediates FGF responsiveness in both animal and vegetal lineages, whereas the activity of the latter is restricted to the animal hemisphere, thus preventing the formation of neural tissue in vegetal territories. Finally, trypsin-like serine proteases of the subtillisin family are necessary and sufficient to trigger neural induction in isolated ascidian animal explants (Ortolani et al. 1979, Okado & Takahashi 1993). Whether, or how, this finding relates to

13 ASCIDIAN LARVAL NEUROBIOLOGY 465 the role of FGF 9/16/20, and whether it reflects an ascidian peculiarity or a more general phenomenon, is unclear at present. TAIL EPIDERMAL SENSORY NEURONS AND DORSAL NEURAL TUBE ARISE FROM b- LINE ECTODERM The b-line ectoderm gives rise to two types of neural tissue: the dorsalmost row of cells in the neural tube (Nishida 1987, Nicol & Meinertzhagen 1988), and the midline tail epidermis, which includes the tail epidermal sensory neurons (Y. Ohtsuka & Y. Okamura, unpublished observations). Very little is known about the mechanisms presiding over the adoption of the dorsal neural tube fate, in part owing to the lack of specific markers; this problem should find a solution in several current large-scale in situ hybridization screens (e.g., Ogasawara et al. 2001). Formation of the tail epidermal sensory neurons is better understood and requires an induction between the b-line ectoderm and B-line vegetal blastomeres (Hudson & Lemaire 2001, Ohtsuka et al. 2001). The b-line cells lose competence between the 110-cell and neurula stages, but induction in vivo may take place earlier. Blastomere isolation experiments, and identification of the natural inducer, will help solve this issue. Although the action of the natural inducer can be mimicked by FGF (Hudson & Lemaire 2001, Ohtsuka et al. 2001), inhibition of ERK activation with pharmacological MEK inhibitors fails to prevent the formation of tail epidermal sensory neurons (Hudson et al. 2003). This finding suggests that an additional class of (posterior) neural inducers exists. Recombination experiments indicate that these factors are secreted from B-line, but not A-line, blastomeres (Ohtsuka et al. 2001). Neural Specification in Ascidians and Vertebrates Summarizing the previous section, comparing the specification of neural fate in ascidians and vertebrates allows us to pinpoint some likely ancestral strategies that led to a tripartite chordate neural tube. In both systems, rostral neural tissue is induced, an induction that involves FGF signaling and an initial binary decision between a fate as either epidermis or anterior neural plate. More posteriorly, a binary decision takes place in ascidians between trunk/tail mesoderm and the posterior neural plate, which forms cell-autonomously. Although this seems at odds with current vertebrate models, mutation of the Tbx6 gene in the mouse leads to the conversion of somitic tissue into spinal cord (Chapman & Papaioannou 1998). Furthermore, dorsal mesoderm (prechordal plate and notochord) in zebrafish embryos that are mutant for Nodal signaling changes its identity to become neural (reviewed in Harland 2000 and Schier & Talbot 2001). Finally, in mice, localized inhibition of broadly dispersed trunk mesoderm-inducing signals is vital to allow the formation of a neural plate (Perea-Gomez et al. 2002). A neural-to-mesoderm binary decision may thus be a shared feature of all chordates. Finally, in both systems, formation of the caudal neural tube requires ERK signaling. One obvious difference between ascidians and vertebrates involves the role of BMP signaling. This difference may concern epidermis specification more than

14 466 MEINERTZHAGEN LEMAIRE OKAMURA neural induction, however. In contrast to vertebrates in which it is induced by BMPs, epidermis differentiates autonomously in ascidians (Nishida 2002). Assuming that the role of BMP inhibition in vertebrates is to prevent epidermis from forming, this function is likely to be accomplished by a different process in ascidians. Genes Acting Downstream of the Acquisition of a Generic Neural Identity FROM NEURAL SPECIFICATION TO NEURONAL DIFFERENTIATION Even though ascidian embryos are renowned for specifying embryonic fates earlier than in vertebrates, the a-lineage may not acquire a stable neural fate until the end of gastrulation. Zic and Sox genes participate in the early gene network that links neural induction and neurogenesis in vertebrates (Sasai 1998). In ascidians, inhibiting the function of Halocynthia HrZicN prevents neural differentiation in both A- and a- line blastomeres. In the A-line, in which HrZicN is first expressed during cleavage stages, early neural markers are never activated. In the a-line, in which HrZicN is first expressed during gastrulation, inhibiting HrZicN leads to the progressive loss of a-line neural markers by the mid-gastrula (Wada & Saiga 2002). Conversely, the PNS is not as affected by ZicN loss of function as is the CNS. Other ascidian species are likely similar. For example, Cs-ZicL is also expressed pan-neurally during gastrula stages in Ciona savignyi and is likewise required in that species to express at the tailbud stage the pan-neural marker ETR (Imai et al. 2002b). Sox 2 and 3 genes are expressed throughout the neural plate in vertebrate embryos. In contrast, the single Halocynthia orthologue of the SoxB class, HrSoxB1, is restricted to the posterior neural plate from late gastrula stages. As for its vertebrate counterpart, overexpressing HrSoxB1 is not sufficient to drive production of ectopic neural tissue in Halocynthia. In vertebrates, Sox2 possibly acts to modify the competence to form neural tissue, and to test this idea in ascidians would be interesting. The effects of loss of function for this gene have yet to be reported in tunicates. Finally, the Notch cascade plays a crucial role in the lateral inhibition between neighboring cells that controls neurogenesis in both flies and vertebrates. Single copies of the Notch, delta, and serrate/jagged genes exist in the Ciona genome (Satou et al. 2003a). Furthermore, overexpression of a constitutively active form of Notch in Halocynthia inhibits the formation of PNS neurons, which suggests that lateral inhibition is used by ascidians to specify at least some of their larval neurons (Akanuma et al. 2002). FINE-SCALE REGIONALIZATION OF THE NEURAL TUBE In parallel with the determination of neuronal identity, the neural plate is progressively regionalized during gastrulation. This regionalization is exemplified by the discovery that a number of genes are expressed by the late gastrula in either a single or a few bilateral pairs of cells in the neural plate (e.g., gsx; Hudson & Lemaire 2001). In parallel, individual

15 ASCIDIAN LARVAL NEUROBIOLOGY 467 classes of neurons and glia begin to differentiate from regionalized neural plate cells. Compared with early embryonic development, the differentiation of frank phenotypes among cells in the developing larval brain has been studied little, and the recent identification of a panel of neuronal markers (Mochizuki et al. 2003) will help to classify and identify different cell types. Although our understanding of the mechanisms that lead to the regionalization of the neural plate is still very poor, in general the different steps of pigment cell formation form a paradigm for further studies. Following neural induction and the activation of general markers such as otx, the tyrosinase-related protein gene (TRP)is first broadly expressed in the neural plate and becomes progressively restricted to the pigment-cell lineage during gastrulation. This gene is directly controlled by Otx (Wada et al. 2002). As Otx is expressed throughout the anterior neural plate, however, restriction of TRP expression to the dorsal pigment cell lineage must involve additional regulators. The pigment cells originate from the progeny of a8.25, the lateralmost cells of neural plate row III in the 110-cell stage, and their precursors are in contact with cells expressing bmpb, orthologous to vertebrate Bmp2/4. As in vertebrates, during gastrulation Bmp2/4 acts as a dorsalizing signal in some ascidian neural plate cells, including the pigment-cell lineage (Darras & Nishida 2001). Whereas a combination of Ci-otx and BMP signaling could account for the activation and progressive restriction of TRP expression, embryos treated during gastrulation with a pharmacological MEK inhibitor also fail to develop pigment cells (Hudson et al. 2003), which suggests the involvement of multiple pathways in this lineage. By the neurula stage, the left and right a8.25 cells express TRP and can both form either ocellus or otolith. The decision of which sensory organule to make, ocellus or otolith, is made by left-right interactions between the cell pair progeny (Nishida 1987) after the neural tube closes and the precursors align along the anteroposterior axis (Nishida & Satoh 1989). This decision again involves an antagonism between BMP2/4 and its antagonist CHORDIN (Darras & Nishida 2001). The former specifically induces the differentiation of the anterior pigment cell into the otolith, whereas the latter, which suppresses BMP activity in the posterior cell, allows an ocellus to differentiate. STRUCTURAL DIFFERENTIATION AND THE FORMATION OF CONNECTIONS Few studies address this important aspect of larval brain development (Meinertzhagen & Okamura 2001). The greatest need is for markers to distinguish between, and determine the onset of expression in, each of the cell types in the CNS because existing markers, such as immunoreactivity to UA301 (Takamura 1998) and β- tubulin (Miya & Satoh 1997), are expressed pan-neuronally. The form of larval neurons in Ciona was revealed using electroporation (Corbo et al. 1997b) to transfect neural-plate progeny transiently with a green fluorescent protein (GFP) gene (Okada et al. 2001). The neurons have a simple form with either no or few dendrites, an axon, and a simple terminal, features confirmed by serial-em reconstructions (Stanley MacIsaac 1999). Unlike GFP transfection methods, the latter sample all

16 468 MEINERTZHAGEN LEMAIRE OKAMURA neurons, leaving us with a familiar hard choice: one larva in its entirety at resolution sufficient to analyze synaptic connectivity, or single neurons at lower resolution from many larvae. Consistent with the simple morphology of ascidian neurons, genomic evidence suggests that axon pathfinding may be much simpler than in vertebrate embryos (Dehal et al. 2002). Even so, sensory neurons or motoneurons of the tail must navigate the two main tracts, left and right, some time during the second half of tail elongation because such axons are lacking at the mid-tailbud stage (Burighel & Cloney 1997). Twitching movements of the tail prior to larval hatching indicate, however, that axon growth must be complete and at least some motor circuits formed by that time. Previous studies identify synaptic contacts in hatched larvae, in the sensory vesicle (Barnes 1971), and in the visceral ganglion (Stanley MacIsaac 1999). They form, in vertebrate pattern, on the cell body of the postsynaptic neuron and are revealed by simple active zones at which a small cumulus of presynaptic vesicles clusters opposite membrane densities at postsynaptic sites. Little structural differentiation exists among the synapses of the visceral ganglion (Stanley MacIsaac 1999), so as to reveal different types. The late development of neuromuscular transmission in Halocynthia includes a rapid increase in sensitivity to acetylcholine (ACh) at 63% of embryonic development. The appearance at 80% of embryonic development of giant excitatory junctional potentials (ejps) is interpreted as random synchronized presynaptic activity, currently providing the only evidence for the timing of synaptogenesis. These giant ejps are followed in a few hours by the miniature ejps typical of the free-swimming larva (Ohmori & Sasaki 1977). Attainment of Cell Number and the Role of Cell Death The final differentiation of neuronal cell types involves regulation of the pool of each type of cell. Cell death plays a crucial role in shaping the development of vertebrate brains, which incorporates a regressive step, using cell death to sculpt cell number from a larger number of blastomere progeny (Kuan et al. 2000). Core components of the cell death machinery exist in the Ciona genome (Terajima et al. 2003), and apoptoses, dependent on the actions of caspases and signaled by cell death markers such as TUNEL, are conspicuous during tail resorption (Chambon et al. 2002, Cole & Meinertzhagen 2004), which involves cell death in the nerve cord. In the embryo, by contrast, TUNEL labeling has not been seen among neural plate progeny (Cole & Meinertzhagen 2004). In molgulids, one claim suggests that programmed cell death is initiated in the CNS and epidermis but that affected cells do not die until metamorphosis, their apoptosis requiring the action of FoxA5 and Manx genes (Jeffery 2002a). In Styela, embryos treated with antisense oligonucleotides for proliferating cell nuclear antigen exhibit nuclear DNA fragmentation typical of programmed cell death and become boomerang-shaped larvae that swim in circles (Jeffery 2002b). From these reports, however, it is not clear whether cell death actually shapes the number of neural cells in hatchling larvae. In fact, embryonic neural cell death was thought unlikely in Ciona from the outset (Nicol

9/4/2015 INDUCTION CHAPTER 1. Neurons are similar across phyla Thus, many different model systems are used in developmental neurobiology. Fig 1.

9/4/2015 INDUCTION CHAPTER 1. Neurons are similar across phyla Thus, many different model systems are used in developmental neurobiology. Fig 1. INDUCTION CHAPTER 1 Neurons are similar across phyla Thus, many different model systems are used in developmental neurobiology Fig 1.1 1 EVOLUTION OF METAZOAN BRAINS GASTRULATION MAKING THE 3 RD GERM LAYER

More information

Cellular Neurobiology BIPN 140 Fall 2016 Problem Set #8

Cellular Neurobiology BIPN 140 Fall 2016 Problem Set #8 Cellular Neurobiology BIPN 140 Fall 2016 Problem Set #8 1. Inductive signaling is a hallmark of vertebrate and mammalian development. In early neural development, there are multiple signaling pathways

More information

Question Set # 4 Answer Key 7.22 Nov. 2002

Question Set # 4 Answer Key 7.22 Nov. 2002 Question Set # 4 Answer Key 7.22 Nov. 2002 1) A variety of reagents and approaches are frequently used by developmental biologists to understand the tissue interactions and molecular signaling pathways

More information

Developmental Biology 3230 Midterm Exam 1 March 2006

Developmental Biology 3230 Midterm Exam 1 March 2006 Name Developmental Biology 3230 Midterm Exam 1 March 2006 1. (20pts) Regeneration occurs to some degree to most metazoans. When you remove the head of a hydra a new one regenerates. Graph the inhibitor

More information

SUPPLEMENTARY INFORMATION

SUPPLEMENTARY INFORMATION doi:10.1038/nature11589 Supplementary Figure 1 Ciona intestinalis and Petromyzon marinus neural crest expression domain comparison. Cartoon shows dorsal views of Ciona mid gastrula (left) and Petromyzon

More information

MCDB 4777/5777 Molecular Neurobiology Lecture 29 Neural Development- In the beginning

MCDB 4777/5777 Molecular Neurobiology Lecture 29 Neural Development- In the beginning MCDB 4777/5777 Molecular Neurobiology Lecture 29 Neural Development- In the beginning Learning Goals for Lecture 29 4.1 Describe the contributions of early developmental events in the embryo to the formation

More information

Early Development in Invertebrates

Early Development in Invertebrates Developmental Biology Biology 4361 Early Development in Invertebrates October 25, 2006 Early Development Overview Cleavage rapid cell divisions divisions of fertilized egg into many cells Gastrulation

More information

Neural development its all connected

Neural development its all connected Neural development its all connected How do you build a complex nervous system? How do you build a complex nervous system? 1. Learn how tissue is instructed to become nervous system. Neural induction 2.

More information

Role of Organizer Chages in Late Frog Embryos

Role of Organizer Chages in Late Frog Embryos Ectoderm Germ Layer Frog Fate Map Frog Fate Map Role of Organizer Chages in Late Frog Embryos Organizer forms three distinct regions Notochord formation in chick Beta-catenin localization How does beta-catenin

More information

Developmental Biology Lecture Outlines

Developmental Biology Lecture Outlines Developmental Biology Lecture Outlines Lecture 01: Introduction Course content Developmental Biology Obsolete hypotheses Current theory Lecture 02: Gametogenesis Spermatozoa Spermatozoon function Spermatozoon

More information

Cell-Cell Communication in Development

Cell-Cell Communication in Development Biology 4361 - Developmental Biology Cell-Cell Communication in Development October 2, 2007 Cell-Cell Communication - Topics Induction and competence Paracrine factors inducer molecules Signal transduction

More information

10/2/2015. Chapter 4. Determination and Differentiation. Neuroanatomical Diversity

10/2/2015. Chapter 4. Determination and Differentiation. Neuroanatomical Diversity Chapter 4 Determination and Differentiation Neuroanatomical Diversity 1 Neurochemical diversity: another important aspect of neuronal fate Neurotransmitters and their receptors Excitatory Glutamate Acetylcholine

More information

Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain

Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain Developmental Biology 285 (2005) 298 315 www.elsevier.com/locate/ydbio Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain Cristian Cañestro,

More information

Early specification of ascidian larval motor neurons

Early specification of ascidian larval motor neurons Developmental Biology 278 (2005) 310 322 www.elsevier.com/locate/ydbio Early specification of ascidian larval motor neurons Yu Katsuyama a,b, *, Toshiaki Okada a,c, Jun Matsumoto a,d, Yukio Ohtsuka a,

More information

1. What are the three general areas of the developing vertebrate limb? 2. What embryonic regions contribute to the developing limb bud?

1. What are the three general areas of the developing vertebrate limb? 2. What embryonic regions contribute to the developing limb bud? Study Questions - Lecture 17 & 18 1. What are the three general areas of the developing vertebrate limb? The three general areas of the developing vertebrate limb are the proximal stylopod, zeugopod, and

More information

Animal Origins and Evolution

Animal Origins and Evolution Animal Origins and Evolution Common Features of Animals multicellular heterotrophic motile Sexual reproduction, embryo Evolution of Animals All animals are multicellular and heterotrophic, which means

More information

MBios 401/501: Lecture 14.2 Cell Differentiation I. Slide #1. Cell Differentiation

MBios 401/501: Lecture 14.2 Cell Differentiation I. Slide #1. Cell Differentiation MBios 401/501: Lecture 14.2 Cell Differentiation I Slide #1 Cell Differentiation Cell Differentiation I -Basic principles of differentiation (p1305-1320) -C-elegans (p1321-1327) Cell Differentiation II

More information

Developmental Zoology. Ectodermal derivatives (ZOO ) Developmental Stages. Developmental Stages

Developmental Zoology. Ectodermal derivatives (ZOO ) Developmental Stages. Developmental Stages Developmental Zoology (ZOO 228.1.0) Ectodermal derivatives 1 Developmental Stages Ø Early Development Fertilization Cleavage Gastrulation Neurulation Ø Later Development Organogenesis Larval molts Metamorphosis

More information

BIOLOGY - CLUTCH CH.32 - OVERVIEW OF ANIMALS.

BIOLOGY - CLUTCH CH.32 - OVERVIEW OF ANIMALS. !! www.clutchprep.com Animals are multicellular, heterotrophic eukaryotes that feed by ingesting their food Most animals are diploid, and produce gametes produced directly by meiosis Animals lack cell

More information

Questions in developmental biology. Differentiation Morphogenesis Growth/apoptosis Reproduction Evolution Environmental integration

Questions in developmental biology. Differentiation Morphogenesis Growth/apoptosis Reproduction Evolution Environmental integration Questions in developmental biology Differentiation Morphogenesis Growth/apoptosis Reproduction Evolution Environmental integration Representative cell types of a vertebrate zygote => embryo => adult differentiation

More information

Building the brain (1): Evolutionary insights

Building the brain (1): Evolutionary insights Building the brain (1): Evolutionary insights Historical considerations! Initial insight into the general role of the brain in human behaviour was already attained in antiquity and formulated by Hippocrates

More information

Spatio-Temporal Expression Patterns of Eight Epidermis-Specific Genes in the Ascidian Embryo

Spatio-Temporal Expression Patterns of Eight Epidermis-Specific Genes in the Ascidian Embryo Spatio-Temporal Expression Patterns of Eight Epidermis-Specific Genes in the Ascidian Embryo Author(s): Kouichi Ishida, Tatsuya Ueki, and Noriyuki Satoh Source: Zoological Science, 13(5):699-709. Published

More information

Cell Cell Communication in Development

Cell Cell Communication in Development Biology 4361 Developmental Biology Cell Cell Communication in Development June 25, 2008 Cell Cell Communication Concepts Cells in developing organisms develop in the context of their environment, including

More information

Sonic hedgehog (Shh) signalling in the rabbit embryo

Sonic hedgehog (Shh) signalling in the rabbit embryo Sonic hedgehog (Shh) signalling in the rabbit embryo In the first part of this thesis work the physical properties of cilia-driven leftward flow were characterised in the rabbit embryo. Since its discovery

More information

Developmental processes Differential gene expression Introduction to determination The model organisms used to study developmental processes

Developmental processes Differential gene expression Introduction to determination The model organisms used to study developmental processes Date Title Topic(s) Learning Outcomes: Sept 28 Oct 3 1. What is developmental biology and why should we care? 2. What is so special about stem cells and gametes? Developmental processes Differential gene

More information

Chapter 18 Lecture. Concepts of Genetics. Tenth Edition. Developmental Genetics

Chapter 18 Lecture. Concepts of Genetics. Tenth Edition. Developmental Genetics Chapter 18 Lecture Concepts of Genetics Tenth Edition Developmental Genetics Chapter Contents 18.1 Differentiated States Develop from Coordinated Programs of Gene Expression 18.2 Evolutionary Conservation

More information

Unicellular: Cells change function in response to a temporal plan, such as the cell cycle.

Unicellular: Cells change function in response to a temporal plan, such as the cell cycle. Spatial organization is a key difference between unicellular organisms and metazoans Unicellular: Cells change function in response to a temporal plan, such as the cell cycle. Cells differentiate as a

More information

Biology 218, practise Exam 2, 2011

Biology 218, practise Exam 2, 2011 Figure 3 The long-range effect of Sqt does not depend on the induction of the endogenous cyc or sqt genes. a, Design and predictions for the experiments shown in b-e. b-e, Single-cell injection of 4 pg

More information

Paraxial and Intermediate Mesoderm

Paraxial and Intermediate Mesoderm Biology 4361 Paraxial and Intermediate Mesoderm December 7, 2006 Major Mesoderm Lineages Mesodermal subdivisions are specified along a mediolateral axis by increasing amounts of BMPs more lateral mesoderm

More information

Life Sciences For NET & SLET Exams Of UGC-CSIR. Section B and C. Volume-08. Contents A. BASIC CONCEPT OF DEVELOPMENT 1

Life Sciences For NET & SLET Exams Of UGC-CSIR. Section B and C. Volume-08. Contents A. BASIC CONCEPT OF DEVELOPMENT 1 Section B and C Volume-08 Contents 5. DEVELOPMENTAL BIOLOGY A. BASIC CONCEPT OF DEVELOPMENT 1 B. GAMETOGENESIS, FERTILIZATION AND EARLY DEVELOPMENT 23 C. MORPHOGENESIS AND ORGANOGENESIS IN ANIMALS 91 0

More information

Maternal Control of GermLayer Formation in Xenopus

Maternal Control of GermLayer Formation in Xenopus Maternal Control of GermLayer Formation in Xenopus The zygotic genome is activated at the mid-blastula transition mid-blastula fertilized egg Xenopus gastrulae early-gastrula 7 hrs 10 hrs control not VP

More information

Nature Neuroscience: doi: /nn.2662

Nature Neuroscience: doi: /nn.2662 Supplementary Figure 1 Atlastin phylogeny and homology. (a) Maximum likelihood phylogenetic tree based on 18 Atlastin-1 sequences using the program Quicktree. Numbers at internal nodes correspond to bootstrap

More information

THE PROBLEMS OF DEVELOPMENT. Cell differentiation. Cell determination

THE PROBLEMS OF DEVELOPMENT. Cell differentiation. Cell determination We emphasize these points from Kandel in Bi/CNS 150 Bi/CNS/NB 150: Neuroscience Read Lecture Lecture Friday, October 2, 2015 Development 1: pp 5-10 Introduction Brains evolved All higher animals have brains

More information

Outline. v Definition and major characteristics of animals v Dividing animals into groups based on: v Animal Phylogeny

Outline. v Definition and major characteristics of animals v Dividing animals into groups based on: v Animal Phylogeny BIOSC 041 Overview of Animal Diversity: Animal Body Plans Reference: Chapter 32 Outline v Definition and major characteristics of animals v Dividing animals into groups based on: Body symmetry Tissues

More information

posterior end mark, a novel maternal gene encoding a localized factor in the

posterior end mark, a novel maternal gene encoding a localized factor in the Development 122, 2005-2012 (1996) Printed in Great Britain The Company of Biologists Limited 1996 DEV5066 2005 posterior end mark, a novel maternal gene encoding a localized factor in the ascidian embryo

More information

!!!!!!!! DB3230 Midterm 2 12/13/2013 Name:

!!!!!!!! DB3230 Midterm 2 12/13/2013 Name: 1. (10 pts) Draw or describe the fate map of a late blastula stage sea urchin embryo. Draw or describe the corresponding fate map of the pluteus stage larva. Describe the sequence of gastrulation events

More information

Name KEY. Biology Developmental Biology Winter Quarter Midterm 3 KEY

Name KEY. Biology Developmental Biology Winter Quarter Midterm 3 KEY Name KEY 100 Total Points Open Book Biology 411 - Developmental Biology Winter Quarter 2009 Midterm 3 KEY All of the 25 multi-choice questions are single-answer. Choose the best answer. (4 pts each) Place

More information

3/8/ Complex adaptations. 2. often a novel trait

3/8/ Complex adaptations. 2. often a novel trait Chapter 10 Adaptation: from genes to traits p. 302 10.1 Cascades of Genes (p. 304) 1. Complex adaptations A. Coexpressed traits selected for a common function, 2. often a novel trait A. not inherited from

More information

Mesoderm Induction CBT, 2018 Hand-out CBT March 2018

Mesoderm Induction CBT, 2018 Hand-out CBT March 2018 Mesoderm Induction CBT, 2018 Hand-out CBT March 2018 Introduction 3. Books This module is based on the following books: - 'Principles of Developement', Lewis Wolpert, et al., fifth edition, 2015 - 'Developmental

More information

Axis Specification in Drosophila

Axis Specification in Drosophila Developmental Biology Biology 4361 Axis Specification in Drosophila November 2, 2006 Axis Specification in Drosophila Fertilization Superficial cleavage Gastrulation Drosophila body plan Oocyte formation

More information

v Scientists have identified 1.3 million living species of animals v The definition of an animal

v Scientists have identified 1.3 million living species of animals v The definition of an animal Biosc 41 9/10 Announcements BIOSC 041 v Genetics review: group problem sets Groups of 3-4 Correct answer presented to class = 2 pts extra credit Incorrect attempt = 1 pt extra credit v Lecture: Animal

More information

Axis Specification in Drosophila

Axis Specification in Drosophila Developmental Biology Biology 4361 Axis Specification in Drosophila November 6, 2007 Axis Specification in Drosophila Fertilization Superficial cleavage Gastrulation Drosophila body plan Oocyte formation

More information

Bio 127 Section I Introduction to Developmental Biology. Cell Cell Communication in Development. Developmental Activities Coordinated in this Way

Bio 127 Section I Introduction to Developmental Biology. Cell Cell Communication in Development. Developmental Activities Coordinated in this Way Bio 127 Section I Introduction to Developmental Biology Cell Cell Communication in Development Gilbert 9e Chapter 3 It has to be EXTREMELY well coordinated for the single celled fertilized ovum to develop

More information

Biosc 41 9/10 Announcements

Biosc 41 9/10 Announcements Biosc 41 9/10 Announcements v Genetics review: group problem sets Groups of 3-4 Correct answer presented to class = 2 pts extra credit Incorrect attempt = 1 pt extra credit v Lecture: Animal Body Plans

More information

Research article. Summary. Introduction. Kaoru S. Imai*, Kyosuke Hino*, Kasumi Yagi, Nori Satoh and Yutaka Satou

Research article. Summary. Introduction. Kaoru S. Imai*, Kyosuke Hino*, Kasumi Yagi, Nori Satoh and Yutaka Satou Research article 4047 Gene expression profiles of transcription factors and signaling molecules in the ascidian embryo: towards a comprehensive understanding of gene networks Kaoru S. Imai*, Kyosuke Hino*,

More information

Animal Diversity. Animals are multicellular, heterotrophic eukaryotes with tissues that develop from embryonic layers 9/20/2017

Animal Diversity. Animals are multicellular, heterotrophic eukaryotes with tissues that develop from embryonic layers 9/20/2017 Animal Diversity Chapter 32 Which of these organisms are animals? Animals are multicellular, heterotrophic eukaryotes with tissues that develop from embryonic layers Animals share the same: Nutritional

More information

Paraxial and Intermediate Mesoderm

Paraxial and Intermediate Mesoderm Biology 4361 Paraxial and Intermediate Mesoderm December 6, 2007 Mesoderm Formation Chick Major Mesoderm Lineages Mesodermal subdivisions are specified along a mediolateral axis by increasing amounts of

More information

The Radiata-Bilateria split. Second branching in the evolutionary tree

The Radiata-Bilateria split. Second branching in the evolutionary tree The Radiata-Bilateria split Second branching in the evolutionary tree Two very important characteristics are used to distinguish between the second bifurcation of metazoans Body symmetry Germinal layers

More information

8/23/2014. Introduction to Animal Diversity

8/23/2014. Introduction to Animal Diversity Introduction to Animal Diversity Chapter 32 Objectives List the characteristics that combine to define animals Summarize key events of the Paleozoic, Mesozoic, and Cenozoic eras Distinguish between the

More information

Caenorhabditis elegans

Caenorhabditis elegans Caenorhabditis elegans Why C. elegans? Sea urchins have told us much about embryogenesis. They are suited well for study in the lab; however, they do not tell us much about the genetics involved in embryogenesis.

More information

UNIVERSITY OF YORK BIOLOGY. Developmental Biology

UNIVERSITY OF YORK BIOLOGY. Developmental Biology Examination Candidate Number: UNIVERSITY OF YORK BSc Stage 2 Degree Examinations 2017-18 Department: BIOLOGY Title of Exam: Developmental Biology Desk Number: Time allowed: 1 hour and 30 minutes Total

More information

Chapter 10 Development and Differentiation

Chapter 10 Development and Differentiation Part III Organization of Cell Populations Chapter Since ancient times, people have wondered how organisms are formed during the developmental process, and many researchers have worked tirelessly in search

More information

PRACTICE EXAM. 20 pts: 1. With the aid of a diagram, indicate how initial dorsal-ventral polarity is created in fruit fly and frog embryos.

PRACTICE EXAM. 20 pts: 1. With the aid of a diagram, indicate how initial dorsal-ventral polarity is created in fruit fly and frog embryos. PRACTICE EXAM 20 pts: 1. With the aid of a diagram, indicate how initial dorsal-ventral polarity is created in fruit fly and frog embryos. No Low [] Fly Embryo Embryo Non-neural Genes Neuroectoderm Genes

More information

Conclusions. The experimental studies presented in this thesis provide the first molecular insights

Conclusions. The experimental studies presented in this thesis provide the first molecular insights C h a p t e r 5 Conclusions 5.1 Summary The experimental studies presented in this thesis provide the first molecular insights into the cellular processes of assembly, and aggregation of neural crest and

More information

DEVELOPMENT. Clare Hudson*, Sonia Lotito and Hitoyoshi Yasuo

DEVELOPMENT. Clare Hudson*, Sonia Lotito and Hitoyoshi Yasuo Access the Development most First recent posted version epress online at on online http://dev.biologists.org/lookup/doi/10.1242/dev.002352 29 August publication 2007 as 10.1242/dev.002352 date 29 August

More information

Lecture 7. Development of the Fruit Fly Drosophila

Lecture 7. Development of the Fruit Fly Drosophila BIOLOGY 205/SECTION 7 DEVELOPMENT- LILJEGREN Lecture 7 Development of the Fruit Fly Drosophila 1. The fruit fly- a highly successful, specialized organism a. Quick life cycle includes three larval stages

More information

Paraxial and Intermediate Mesoderm

Paraxial and Intermediate Mesoderm Biology 4361 Paraxial and Intermediate Mesoderm December 6, 2007 Mesoderm Formation Chick Major Mesoderm Lineages Mesodermal subdivisions are specified along a mediolateral axis by increasing amounts of

More information

Axis Specification in Drosophila

Axis Specification in Drosophila Developmental Biology Biology 4361 Axis Specification in Drosophila July 9, 2008 Drosophila Development Overview Fertilization Cleavage Gastrulation Drosophila body plan Oocyte formation Genetic control

More information

Biology 340 Comparative Embryology Lecture 4 Dr. Stuart Sumida. Overview of Pre-Metazoan. and Protostome Development (Insects)

Biology 340 Comparative Embryology Lecture 4 Dr. Stuart Sumida. Overview of Pre-Metazoan. and Protostome Development (Insects) Biology 340 Comparative Embryology Lecture 4 Dr. Stuart Sumida Overview of Pre-Metazoan and Protostome Development (Insects) Plants Fungi Animals In1998 fossilized animal embryos were reported from the

More information

Exam 1 ID#: October 4, 2007

Exam 1 ID#: October 4, 2007 Biology 4361 Name: KEY Exam 1 ID#: October 4, 2007 Multiple choice (one point each) (1-25) 1. The process of cells forming tissues and organs is called a. morphogenesis. b. differentiation. c. allometry.

More information

Supplementary Figure 1: Mechanism of Lbx2 action on the Wnt/ -catenin signalling pathway. (a) The Wnt/ -catenin signalling pathway and its

Supplementary Figure 1: Mechanism of Lbx2 action on the Wnt/ -catenin signalling pathway. (a) The Wnt/ -catenin signalling pathway and its Supplementary Figure 1: Mechanism of Lbx2 action on the Wnt/ -catenin signalling pathway. (a) The Wnt/ -catenin signalling pathway and its transcriptional activity in wild-type embryo. A gradient of canonical

More information

Chapter 37 Active Reading Guide Neurons, Synapses, and Signaling

Chapter 37 Active Reading Guide Neurons, Synapses, and Signaling Name: AP Biology Mr. Croft Section 1 1. What is a neuron? Chapter 37 Active Reading Guide Neurons, Synapses, and Signaling 2. Neurons can be placed into three groups, based on their location and function.

More information

MOLECULAR CONTROL OF EMBRYONIC PATTERN FORMATION

MOLECULAR CONTROL OF EMBRYONIC PATTERN FORMATION MOLECULAR CONTROL OF EMBRYONIC PATTERN FORMATION Drosophila is the best understood of all developmental systems, especially at the genetic level, and although it is an invertebrate it has had an enormous

More information

Bio Section III Organogenesis. The Neural Crest and Axonal Specification. Student Learning Objectives. Student Learning Objectives

Bio Section III Organogenesis. The Neural Crest and Axonal Specification. Student Learning Objectives. Student Learning Objectives Bio 127 - Section III Organogenesis The Neural Crest and Axonal Specification Gilbert 9e Chapter 10 Student Learning Objectives 1. You should understand that the neural crest is an evolutionary advancement

More information

18.4 Embryonic development involves cell division, cell differentiation, and morphogenesis

18.4 Embryonic development involves cell division, cell differentiation, and morphogenesis 18.4 Embryonic development involves cell division, cell differentiation, and morphogenesis An organism arises from a fertilized egg cell as the result of three interrelated processes: cell division, cell

More information

Divergent mechanisms specify chordate motoneurons: evidence from ascidians

Divergent mechanisms specify chordate motoneurons: evidence from ascidians RESEARCH ARTICLE 1643 Development 138, 1643-1652 (2011) doi:10.1242/dev.055426 2011. Published by The Company of Biologists Ltd Divergent mechanisms specify chordate motoneurons: evidence from ascidians

More information

5/4/05 Biol 473 lecture

5/4/05 Biol 473 lecture 5/4/05 Biol 473 lecture animals shown: anomalocaris and hallucigenia 1 The Cambrian Explosion - 550 MYA THE BIG BANG OF ANIMAL EVOLUTION Cambrian explosion was characterized by the sudden and roughly simultaneous

More information

Exam 2 ID#: November 9, 2006

Exam 2 ID#: November 9, 2006 Biology 4361 Name: KEY Exam 2 ID#: November 9, 2006 Multiple choice (one point each) Circle the best answer. 1. Inducers of Xenopus lens and optic vesicle include a. pharyngeal endoderm and anterior neural

More information

A conserved role for FGF signaling in chordate otic/atrial placode formation

A conserved role for FGF signaling in chordate otic/atrial placode formation Available online at www.sciencedirect.com Developmental Biology 312 (2007) 245 257 www.elsevier.com/developmentalbiology A conserved role for FGF signaling in chordate otic/atrial placode formation Matthew

More information

Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate

Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate Development 124, 2335-2344 (1997) Printed in Great Britain The Company of Biologists Limited 1997 DEV9537 2335 Dorsoventral patterning of the vertebrate neural tube is conserved in a protochordate Joseph

More information

Axon guidance I. Paul Garrity March 15, /9.013

Axon guidance I. Paul Garrity March 15, /9.013 Axon guidance I Paul Garrity March 15, 2004 7.68/9.013 Neuronal Wiring: Functional Framework of the Nervous System Stretch reflex circuit Early theories of axonogenesis Schwann: many neurons link to form

More information

Animal Diversity. Features shared by all animals. Animals are multicellular, heterotrophic eukaryotes with tissues that develop from embryonic layers

Animal Diversity. Features shared by all animals. Animals are multicellular, heterotrophic eukaryotes with tissues that develop from embryonic layers Animal Diversity Animals are multicellular, heterotrophic eukaryotes with tissues that develop from embryonic layers Nutritional mode Ingest food and use enzymes in the body to digest Cell structure and

More information

"PRINCIPLES OF PHYLOGENETICS: ECOLOGY AND EVOLUTION" Integrative Biology 200B Spring 2011

PRINCIPLES OF PHYLOGENETICS: ECOLOGY AND EVOLUTION Integrative Biology 200B Spring 2011 "PRINCIPLES OF PHYLOGENETICS: ECOLOGY AND EVOLUTION" Integrative Biology 200B Spring 2011 Evolution and development ("evo-devo") The last frontier in our understanding of biological forms is an understanding

More information

Control and Integration. Nervous System Organization: Bilateral Symmetric Animals. Nervous System Organization: Radial Symmetric Animals

Control and Integration. Nervous System Organization: Bilateral Symmetric Animals. Nervous System Organization: Radial Symmetric Animals Control and Integration Neurophysiology Chapters 10-12 Nervous system composed of nervous tissue cells designed to conduct electrical impulses rapid communication to specific cells or groups of cells Endocrine

More information

An essential role of a FoxD gene in notochord induction in Ciona embryos

An essential role of a FoxD gene in notochord induction in Ciona embryos Development 129, 3441-3453 (2002) Printed in Great Britain The Company of Biologists Limited 2002 DEV5028 3441 An essential role of a FoxD gene in notochord induction in Ciona embryos Kaoru S. Imai*, Nori

More information

Homeotic Genes and Body Patterns

Homeotic Genes and Body Patterns Homeotic Genes and Body Patterns Every organism has a unique body pattern. Although specialized body structures, such as arms and legs, may be similar in makeup (both are made of muscle and bone), their

More information

Roles of retinoic acid and Tbx1/10 in pharyngeal segmentation: amphioxus and the ancestral chordate condition

Roles of retinoic acid and Tbx1/10 in pharyngeal segmentation: amphioxus and the ancestral chordate condition Koop et al. EvoDevo 2014, 5:36 RESEARCH Open Access Roles of retinoic acid and Tbx1/10 in pharyngeal segmentation: amphioxus and the ancestral chordate condition Demian Koop 1, Jie Chen 2, Maria Theodosiou

More information

Name. Biology Developmental Biology Winter Quarter 2013 KEY. Midterm 3

Name. Biology Developmental Biology Winter Quarter 2013 KEY. Midterm 3 Name 100 Total Points Open Book Biology 411 - Developmental Biology Winter Quarter 2013 KEY Midterm 3 Read the Following Instructions: * Answer 20 questions (5 points each) out of the available 25 questions

More information

Developmental genetics: finding the genes that regulate development

Developmental genetics: finding the genes that regulate development Developmental Biology BY1101 P. Murphy Lecture 9 Developmental genetics: finding the genes that regulate development Introduction The application of genetic analysis and DNA technology to the study of

More information

Bi 117 Final (60 pts) DUE by 11:00 am on March 15, 2012 Box by Beckman Institute B9 or to a TA

Bi 117 Final (60 pts) DUE by 11:00 am on March 15, 2012 Box by Beckman Institute B9 or to a TA Bi 117 Final (60 pts) DUE by 11:00 am on March 15, 2012 Box by Beckman Institute B9 or to a TA Instructor: Marianne Bronner Exam Length: 6 hours plus one 30-minute break at your discretion. It should take

More information

Mutations affecting tail and notochord development in the ascidian Ciona

Mutations affecting tail and notochord development in the ascidian Ciona Development 126, 3293-3301 (1999) Printed in Great Britain The Company of Biologists Limited 1999 DEV6405 3293 Mutations affecting tail and notochord development in the ascidian Ciona savignyi Yuki Nakatani,

More information

Cell Death & Trophic Factors II. Steven McLoon Department of Neuroscience University of Minnesota

Cell Death & Trophic Factors II. Steven McLoon Department of Neuroscience University of Minnesota Cell Death & Trophic Factors II Steven McLoon Department of Neuroscience University of Minnesota 1 Remember? Neurotrophins are cell survival factors that neurons get from their target cells! There is a

More information

Information processing. Divisions of nervous system. Neuron structure and function Synapse. Neurons, synapses, and signaling 11/3/2017

Information processing. Divisions of nervous system. Neuron structure and function Synapse. Neurons, synapses, and signaling 11/3/2017 Neurons, synapses, and signaling Chapter 48 Information processing Divisions of nervous system Central nervous system (CNS) Brain and a nerve cord Integration center Peripheral nervous system (PNS) Nerves

More information

Introduction Principles of Signaling and Organization p. 3 Signaling in Simple Neuronal Circuits p. 4 Organization of the Retina p.

Introduction Principles of Signaling and Organization p. 3 Signaling in Simple Neuronal Circuits p. 4 Organization of the Retina p. Introduction Principles of Signaling and Organization p. 3 Signaling in Simple Neuronal Circuits p. 4 Organization of the Retina p. 5 Signaling in Nerve Cells p. 9 Cellular and Molecular Biology of Neurons

More information

7.013 Problem Set

7.013 Problem Set 7.013 Problem Set 5-2013 Question 1 During a summer hike you suddenly spot a huge grizzly bear. This emergency situation triggers a fight or flight response through a signaling pathway as shown below.

More information

Revision Based on Chapter 25 Grade 11

Revision Based on Chapter 25 Grade 11 Revision Based on Chapter 25 Grade 11 Biology Multiple Choice Identify the choice that best completes the statement or answers the question. 1. A cell that contains a nucleus and membrane-bound organelles

More information

Mesoderm Development

Mesoderm Development Quiz rules: Spread out across available tables No phones, text books, or (lecture) notes on your desks No consultation with your colleagues No websites open other than the Quiz page No screen snap shots

More information

Nervous System Organization

Nervous System Organization The Nervous System Chapter 44 Nervous System Organization All animals must be able to respond to environmental stimuli -Sensory receptors = Detect stimulus -Motor effectors = Respond to it -The nervous

More information

Biology 224 Human Anatomy and Physiology - II Week 1; Lecture 1; Monday Dr. Stuart S. Sumida. Review of Early Development of Humans.

Biology 224 Human Anatomy and Physiology - II Week 1; Lecture 1; Monday Dr. Stuart S. Sumida. Review of Early Development of Humans. Biology 224 Human Anatomy and Physiology - II Week 1; Lecture 1; Monday Dr. Stuart S. Sumida Review of Early Development of Humans Special Senses Review: Historical and Developmental Perspectives Ontogeny

More information

Chapter 32, 10 th edition Q1.Which characteristic below is shared by plants, fungi, and animals? ( Concept 32.1)

Chapter 32, 10 th edition Q1.Which characteristic below is shared by plants, fungi, and animals? ( Concept 32.1) Chapter 32, 10 th edition Q1.Which characteristic below is shared by plants, fungi, and animals? ( Concept 32.1) A) They are multicellular eukaryotes. B) They are heterotrophs. C) Their cells are supported

More information

Comparative Anatomy Biology 440 Fall semester

Comparative Anatomy Biology 440 Fall semester Comparative Anatomy Biology 440 Fall semester TuTh 10:00 11:15 G23 Lab at 1:00 in 3106 or 3108 Comparative Anatomy Biology 440 Spring semester TuTh 11:30-12:45 G23 Lab at 2:00 in either 3108 or 3106 Dr.

More information

Evolution of bilaterian central nervous systems: a single origin?

Evolution of bilaterian central nervous systems: a single origin? Holland et al. EvoDevo 2013, 4:27 REVIEW Open Access Evolution of bilaterian central nervous systems: a single origin? Linda Z Holland 1*, João E Carvalho 2, Hector Escriva 3, Vincent Laudet 4, Michael

More information

Drosophila Life Cycle

Drosophila Life Cycle Drosophila Life Cycle 1 Early Drosophila Cleavage Nuclei migrate to periphery after 10 nuclear divisions. Cellularization occurs when plasma membrane folds in to divide nuclei into cells. Drosophila Superficial

More information

Supplementary Figures

Supplementary Figures Supplementary Figures Supplementary Fig. S1: Normal development and organization of the embryonic ventral nerve cord in Platynereis. (A) Life cycle of Platynereis dumerilii. (B-F) Axonal scaffolds and

More information

Chapter 4 Evaluating a potential interaction between deltex and git in Drosophila: genetic interaction, gene overexpression and cell biology assays.

Chapter 4 Evaluating a potential interaction between deltex and git in Drosophila: genetic interaction, gene overexpression and cell biology assays. Evaluating a potential interaction between deltex and git in Drosophila: genetic interaction, gene overexpression and cell biology assays. The data described in chapter 3 presented evidence that endogenous

More information

From DNA to Diversity

From DNA to Diversity From DNA to Diversity Molecular Genetics and the Evolution of Animal Design Sean B. Carroll Jennifer K. Grenier Scott D. Weatherbee Howard Hughes Medical Institute and University of Wisconsin Madison,

More information

purpose of this Chapter is to highlight some problems that will likely provide new

purpose of this Chapter is to highlight some problems that will likely provide new 119 Chapter 6 Future Directions Besides our contributions discussed in previous chapters to the problem of developmental pattern formation, this work has also brought new questions that remain unanswered.

More information

Nature Biotechnology: doi: /nbt Supplementary Figure 1. Overexpression of YFP::GPR-1 in the germline.

Nature Biotechnology: doi: /nbt Supplementary Figure 1. Overexpression of YFP::GPR-1 in the germline. Supplementary Figure 1 Overexpression of YFP::GPR-1 in the germline. The pie-1 promoter and 3 utr were used to express yfp::gpr-1 in the germline. Expression levels from the yfp::gpr-1(cai 1.0)-expressing

More information

BILD7: Problem Set. 2. What did Chargaff discover and why was this important?

BILD7: Problem Set. 2. What did Chargaff discover and why was this important? BILD7: Problem Set 1. What is the general structure of DNA? 2. What did Chargaff discover and why was this important? 3. What was the major contribution of Rosalind Franklin? 4. How did solving the structure

More information

Principles of Experimental Embryology

Principles of Experimental Embryology Biology 4361 Developmental Biology Principles of Experimental Embryology June 16, 2008 Overview What forces affect embryonic development? The embryonic environment: external and internal How do forces

More information