MOLECULAR CONTROL OF EMBRYONIC PATTERN FORMATION
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1 MOLECULAR CONTROL OF EMBRYONIC PATTERN FORMATION
2 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 impact on our understanding of the genetic basis of vertebrate development.
3 Christiane Nüsslein-Volhard Eric Wieschaus Nobel Prize in Physiology or Medicine for 1995 jointly to Christiane Nüsslein-Volhard and Eric F. Wieschaus for their discoveries concerning "the genetic control of early embryonic development".
4 The genetic control of segmentation involves a cascade of gene regulation occurring largely before the onset of the cellular blastoderm stage. The cascade begins with the diffusion of spatially localized maternal factors, the products of the maternal coordinate genes (i.e. bicoid, nanos, etc.), from the anterior and posterior poles of the embryo. These control the spatial patterns of transcription of the gap genes (i.e. hunchback. Krüppel, knirps, etc.). The gap genes are amongst the earliest expressed zygotic genes and they encode transcription factors. The gap genes are expressed overlapping territories along the anterior to posterior axis of the fly embryo. These genes act to sub-divide the embryo into broad domains (anterior, middle, posterior). The gap genes regulate each other and the next set of genes in the hierarchy, the pair-rule genes (even-skipped, fushi-tarazu). Pair-rule genes are expressed in 7 stripes of cells corresponding to every other segment. Pair-rule genes encode transcription factors that establish the expression of the segment polarity genes (wingless, engrailed), many of which are expressed in 14 segmentally repeated stripes. Unlike the other classes of segmentation genes, the segment polarity genes include regulatory proteins other than transcription factors (i.e. secreted signaling molecules, receptors, kinases, etc.) and they mediate interactions between cells. The end result of the hierarchy is a series of segments that have identical repeated segment polarity gene expression patterns.
5 THE MATERNAL EFFECT GENES (MATERNAL COORDINATE GENES) The maternal effect genes (maternal coordinate genes) expressed in the mother's ovaries produce messenger RNAs that are placed in different regions of the egg. These messages encode transcriptional and translational regulatory proteins that diffuse through the syncytial blastoderm and activate or repress the expression of certain zygotic genes. Maternal-effect genes are transcribed only during oogenesis in the nurse cells. Three sets of maternal effect genes define the anterior-posterior axis. These are the anterior group, the posterior group and the terminal group genes. Anterior group bicoid exuperantia swallow staufen Posterior group nanos vasa valois tudor pumilio oskar staufen Terminal group torso torso-like trunk
6 Anterior group genes The anterior system is one of the four maternal systems for assuring proper polarity of the oocyte prior to fertilization. Genes affecting the localization of Bicoid belong to the anterior group. Bicoid is the principle protein for structuring the head and thorax of the developing fly, and Bicoid messenger RNA is transported to the anterior pole of the oocyte during oocyte development. Localization of Bicoid mrna is divided into three phases. In the previtellogenic stage, Bicoid mrna is localized to the apex of each of the nurse cells of the ovule. In vitellogenesis, the contents of the nurse cells are transported into the oocyte by a cytoskeletal based mechanism of cytoplasmic streaming. In a third process, Bicoid mrna is transported along the microtubule network of the oocyte to its anterior pole. The latter process requires direction action of Exuperantia, Swallow and Staufen.
7 Normal larvae Bicoid mutant Oocyte Bicoid mrna
8 Maternal bicoid mrna in the mature egg Bicoid protein gradient in embryo
9 Posterior group genes Unlike the bicoid protein, however, nanos protein does not act directly as a morphogen to specity the abdominal pattern. It has a quite different role. Its function is to suppress, in a graded way, the translation of the maternal mrna of another gene, hunchback, so that a clear gradient of zygotically expressed hunchback protein can be subsequently established and act as a morphogen for the next stage of patterning. Other posterior group genes (oskar, staufen) are involved in the transport and localization of nanos mrna. Just as with Bicoid the ovarian nurse cells express and export nanos mrna to the oocyte. At the end of oogenesis nanos mrna is localized to the posterior pole while hunchback mrna distributed throughout the mature egg. Fertilization triggers translation of Nanos protein and establishment of the nanos gradient. Mid oogenesis Completion of oogenesis Embryo
10 Hb m RNAm 3 UTR Nanos protein 5 3 An 5 3 An Nanos recognition sequence Hbm protein Prevents the translation of the hunchback message ANTERIOR POSTERIOR Control of hunchback maternal mrna translation by Nanos. In the anterior of the embryo hunchback mrna can be translated into Hunchback protein. In the posterior of the embryo, where Nanos protein is found, Nanos prevents the translation of the hunchback message.
11 Maternal nanos mrna in the mature egg Nanos protein gradient in embryo
12 Terminal group genes The terminal group genes are maternal expressed in both the nurse cells and the follicle cells. The nurse cell produces torso mrna and export it to the developing oocyte. It distributes throughout the oocyte in an "inactive" state. The anterior and posterior most follicle cells express Torso-like, a maternal protein that activates Torso just in the terminal regions of the egg.
13 ZYGOTIC GENES The zygotic genes regulated by maternal factors are expressed in certain broad (about three segments wide), partially overlapping domains. These genes are called gap genes (because mutations in them cause gaps in the segmentation pattern), and they are among the first genes transcribed in the embryo. Differing concentrations of the gap gene proteins cause the transcription of pair-rule genes, which divide the embryo into periodic units. The transcription of the different pair-rule genes results in a striped pattern of seven vertical bands perpendicular to the anterior-posterior axis. The pair-rule gene proteins activate the transcription of the segment polarity genes, whose mrna and protein products divide the embryo into 14 segment-wide units, establishing the periodicity of the embryo. Gap genes hunchback Krüppel knirps tailless Pair-rule genes fushi tarazu even-skipped Segment polarity genes engrailed wingless
14 Gap genes are responsible for basic subdivisions along the embryo s anterior-posterior axis and mutations in these genes cause gaps in the animal s segmentation Pair-rule genes define pattern in terms of pairs of segments and mutations in these genes result in embryos having half the normal number of segments. Segment polarity genes set the anterior-posterior axis of each segment and mutations in these genes produce segments where part of the segment mirrors another part of the same segment. The products of many of the segmentation genes are transcription factors which activate the next set of genes.
15 Fushi tarazu The striped patterns of activity of pair-rule genes in the Drosophila embryo Fushi tarazu Even-skipped
16 Products of the maternal genes regulate the regional expression of the gap genes Gap genes control the localized expression of the pair-rule genes Pair rule genes activate specific segment polarity genes in different parts of each segment Segment polarity genes activate homeotic genes Hierarchy of Gene Activation Maternal genes Segmentation genes of embryo Gap genes Pair-rule genes Segment polarity genes
17 THE HOMEOTIC SELECTOR GENES After the segmental boundaries have been established, the characteristic structures of each segment are specified. This specification is accomplished by the homeotic selector genes. There are two regions of Drosophila chromosome 3 that contain most of these homeotic genes. One region, the Antennapedia complex, contains the homeotic genes labial (lab), Antennapedia (Antp), sex combs reduced (scr), deformed (dfd), and proboscipedia (pb). The labial and deformed genes specify the head segments, while sex combs reduced and Antennapedia contribute to giving the thoracic segments their identities. The second region of homeotic genes is the Bithorax complex. There are three proteincoding genes found in this complex: ultrabithorax (ubx), which is required for the identity of the third thoracic segment; and the abdominal A (abda) and Abdominal B (AbdB) genes, which are responsible for the segmental identities of the abdominal segments. The chromosome region containing both the Antennapedia complex and the bithorax complex is often referred to as the homeotic complex (Hom-C). Because these genes are responsible for the specification of fly body parts, mutations in them lead to bizarre phenotypes in which one structure replaces another.
18 Homeotic Genes of Drosophila
19 Homeotic mutations Proboscipedia mutation transform proboscis into leg.
20 NORMAL Antennapedia mutation transform antennae into legs.
21 NORMAL Ultrabithorax mutation transform halteres into wings.
22 VERTEBRATE HOX GENES Patterning along the antero-posterior axis in all vertebrates involves the expression of a set of genes that specify positional identity along the axis. These are the Hox genes, members of the large family of homeobox genes that are involved in many aspects of development. Mammals have 39 Hox genes clustered into four chromosomal groups (clusters) (HOXA, HOXB, HOXC, HOXD)
23 Homeotic transformation of vertebrae due to deletion of Hoxc8 in the mouse. In loss-offunction homozygous mutants of Hoxc8, the first lumbar vertebra is transformed into a rib-bearing thoracic vertebra. L1
24 Colinearity is correspondence of order of genes on the chromosome with the order of body parts that are under the control of these genes. The correspondence between the order of the Hox genes on their chromosome and the anterior-to-posterior sequence of the structures that express them has been called spatial colinearity. 3 Hox genes are expressed first, whereas more 5 Hox genes are expressed later and sequentially. This phenomenon has been called temporal colinearity.
25 Hox gene expression provides a possible molecular basis for the positional identity of both the rhombomeres and the neural crest. Hox genes are expressed in the mouse embryo hindbrain in a well defined pattern, which closely correlates with the segmental pattern. For example, Hoxb3 has its most anterior region of expression at the border of rhombomeres 4 and 5, while Hoxb2 has its anterior border at the border of rhombomeres 2 and 3. The pattern of Hox gene expression in the ectoderm and branchial arches at a particular position along the antero-posterior axis is similar to that in the neural tube and neural crest, and it may be that the crest cells induce their positional values in the overlying ectoderm during their migration.
26 Hox b.2 Hox b.4 Expression domains of Hox genes in a mouse. The photographs show whole embryos displaying the expression domains of two genes of the HoxB complex (blue stain). These domains can be revealed by in situ hybridization or, as in these examples, by constructing transgenic mice containing the control sequence of a Hox gene coupled to a LacZ reporter gene, whose product is detected histochemically. Each gene is expressed in a long expanse of tissue with a sharply defined anterior limit. The earlier the position of the gene in its chromosomal complex, the more anterior the anatomical limit of its expression. Thus, with minor exceptions, the anatomical domains of the successive genes form a nested set, ordered according to the ordering of the genes in the chromosomal complex.
27 The mammalian Hox/HOX genes are numbered from 1 to 13. The equivalent genes in each mouse complex (such as Hoxa-1, Hoxb-1, and Hoxd-1) are called a paralogous group. It is thought that the four mammalian Hox complexes were formed from chromosome duplications. Because there is not a one-to-one correspondence between the Drosophila Hom-C genes and the mouse Hox genes, it is likely that independent gene duplications have occurred since these two animal branches diverged. The four Hox clusters of mice (A, B, C and D) are paralogous, and the Hoxa1 is paralogous to the Hoxb1 gene and Hoxd1 clusters (Hoxc1 has been lost from the mouse HoxC cluster). Consequently, the genes of a paralogous group are structurally and functionally more closely related to one another than to their neighbours within each cluster.
28 The four Hox gene clusters found in mammals are conserved from the Drosophila Hom-C complex in terms of nucleotide sequence and colinear expression. During embryonic development, the genes are expressed in a pattern that correlates with the chromosomal positioning, depicted here for human and mouse. The 3 genes are expressed both earlier and more anteriorly than the 5 genes.
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