Developmental SCOTT F. GILBERT SWARTHMORE COLLEGE Biology
Preface xi PART I : PATTERNS OF DEVELOPMENT Chapter 1 : An introduction to animal development 3 Introduction 4 Origins of sexual reproduction 15 Principal features of development 4 Colonial eukaryotes : The evolution o f Our eukaryotic heritage 7 differentiation 19 Development among the unicellular The Volvocales 19 eukaryotes 10 Dictyostelium 23 Control of developmental Developmental patterns among metazoans 26 morphogenesis in Acetabularia 10 Protostomes and deuterostomes 26 Differentiation in the amoeboflagellate Naegleria 1 3 Chapter 2 : Fertilization: beginning a new organism 31 Introduction 32 Gamete fusion and prevention o f Structure of the gametes 32 polyspermy 5 0 Sperm 32 Fusion between sperm and oocyte cell Egg 36 membranes 5 0 Recognition of sperm and egg : Action at a Prevention of polyspermy 5 3 distance 40 Fusion of the genetic material 58 Sperm attraction 40 Early responses 6 3 The acrosome reaction 41 Late responses 6 5 Recognition of sperm and egg : Contact of Rearrangement of egg cytoplasm 66 gametes 44 Sidelights & Speculations : The nonequivalence of Species-specific recognition in sea mammalian pronuclei 6 1 urchins 44 Activation of egg metabolism 62 Gamete binding in mammals 47
Chapter 3 : Cleavage: creating multicellularity 73 introduction 74 Sidelights & Speculations : The cell surface and PATTERNS OF EMBRYONIC CLEAVAGE 75 the mechanism of compaction 94 Radial holoblastic cleavage 77 Formation of the inner cell mass 94 The sea cucumber, Synapta 77 Sidelights & Speculations : Twins 97 Sea urchins 78 Meroblastic cleavage types 98 Amphibians 82 Discoidal cleavage 98 Spiral holoblastic cleavage 84 Superficial cleavage 98 Bilateral holoblastic cleavage 88 MECHANISMS OF CLEAVAGE 102 Rotational holoblastic cleavage 89 Summary 107 Chapter 4 : Gastrulation: reorganizing the embryonic cells 110 Introduction: General features of Cell movements and construction of th e gastrulation 111 archenteron 12 6 Sea urchin gastrulation 112 Epiboly of the ectoderm 13 0 Ingression of primary mesenchyme 112 Gastrulation in birds 13 1 First stage of archenteron invagination 116 Overview of avian gastrulation 13 1 Second stage of archenteron Mechanisms of avian gastrulation 13 7 invagination 117 Gastrulation in mammals 139 Amphibian gastrulation 118 Overview of mammalian gastrulation 139 Cell movements during amphibian Sidelights & Speculations : The roles of the gastrulation-an overview 118 chorion 144 End of the blastula stage an d positioning of the blastopore 122 Chapter 5: Early vertebrate development : neurulation and ectoderm 149 The vertebrate pattern of development 150 Development of the eye 17 2 Neurulation 152 The neural crest and its derivatives 17 8 The neural tube and the origins of the Sidelights & Speculations : The mechanism for central nervous system 155 neural crest migration 183 Mechanism of neural tube formation 158 Pluripotentiality of neural crest cells 183 Differentiation of the neural tube 159 The epidermis and the origin of cutaneou s Sidelights & Speculations : The evolution of structures 184 cerebral development 165 Cutaneous appendages 18 6 Chapter 6 : Early vertebrate development: mesoderm and endoderm 190 Introduction 191 Sidelights & Speculations : Differentiation an d MESODERM 191 the cell cycle 20 1 Dorsal mesoderm: Differentiation of somites 191 Osteogenesis: Development of bones 202 Myogenesis: Differentiation of skeletal Lateral plate mesoderm 204 muscle 196 Formation of extraembryonic membranes 205
Heart and circulatory system 208 Sites of hematopoiesis 222 The heart 208 ENDODERM 223 Formation of blood vessels 209 Pharynx 223 Sidelights & Speculations : Redirecting blood flow The digestive tube and its derivatives 226 at birth 216 Liver, pancreas, and gallbladder 22 7 Sidelights & Speculations : Tumor-induced The respiratory tube 228 angiogenesis 216 Sidelights & Speculations : Teratocarcinoma 229 Development of blood cells 21 8 Pluripotential stem cells and hematopoietic microenvironments 21 8 PART II : MECHANISMS OF CELLULAR DIFFERENTIATION Chapter 7 : Progressive determination 237 Introduction 238 Hans Spemann and Hilde Mangold : Preformation and epigenesis 238 Primary embryonic induction 25 9 August Weismann: The germ-plasm theory 241 Regional specificity of induction 26 0 Wilhelm Roux: Mosaic development 243 Sidelights & Speculations : The mechanism of Hans Driesch: Regulative development 244 primary embryonic induction 26 3 Sven Hörstadius: Potency and oocyte Competence and secondary induction 26 5 gradients 24 7 Hans Spemann : Progressive determinatio n of embryonic cells 25 4 Chapter 8 : Determination by cytoplasmic specification 26 9 Cytoplasmic specification: Mosaic Sidelights & Speculations : Intracellular development 270 localization and movements of Cytoplasmic specification in tunicate morphogenic determinants 276 embryos 270 Cytoplasmic localization in mollusc embryos 277 Cytoplasmic localization of germ cell Germ cell determination in amphibians 28 8 determinants 281 The nature of cytoplasmic determinants 29 0 Germ cell determination in nematodes 281 Summary 29 3 Germ cell determination in insects 283 Chapter 9 : Genomic equivalence and differential gene expression : embryological investigations 297 Introduction 298 Amphibian cloning : Restriction of cell Genomic equivalence 298 potency 30 5 Transdetermination 300 Amphibian cloning : Exceptions to restriction 308 Metaplasia 300 Sidelights & Speculations : Cloning 314
Chapter 10 : Genomic equivalence and differential gene expression: molecular investigations 318 Introduction 319 Changes in lymphocyte genes 329 Molecular biology techniques: Nucleic acid Sidelights & Speculations : Gene alterations 33 8 hybridization and gene cloning 319 Differential RNA synthesis 339 Differential gene expression 325 Chapter 11 : Transcriptional regulation of gene expression : the nature of eukaryotic genes 348 Introduction 349 RNA polymerase III recognition 36 8 Structure of the eukaryotic genome 349 RNA polymerase I recognition 369 Structure of eukaryotic chromatin : Sidelights & Speculations : Promoter structur e Nucleosomes 355 and differentiation 370 Regulation of gene accessibility on the DNA methylation 370 nucleosome 357 Sidelights & Speculations : Z-DNA an d Sidelights & Speculations : Transcriptional nucleosome structure 372 regulation by the nuclear matrix 362 Structure of eukaryotic genes : Exons and Structure of eukaryotic genes: RNA introns 373 polymerase recognition sites 362 Mechanism for RNA splicing 379 RNA polymerase II recognition 363 Summary 38 1 Sidelights & Speculations : Enhancers 36 6 Chapter 12 : Transcriptional regulation of gene expression: transcriptional changes in developing cells 38 6 Introduction 387 Visualization of transcription fro m Heterochromatin 387 amplified genes 397 Paternal heterochromatin in meally Drosophila chorion genes 39 9 bugs 387 Selective gene transcription 39 9 Mammalian X chromosome inactivation 389 Chromosomal puffs and lampbrush Sidelights & Speculations : Mechanism of X chromosomes 400 chromosome inactivation 393 Ovalbumin synthesis 403 Amplified genes 393 Sidelights & Speculations : Coordinated gene Amplification of ribosomal RNA genes 393 expression 407 Mechanism of ribosomal gene Globin gene transcription 40 9 amplification 394 Chapter 13 : Control of development by RNA processing 41 3 Introduction 414 Control of development by nrna Transcriptional model of developmental processing 420 regulation 414 Sidelights & Speculations : Mechanisms for Heterogeneous nuclear RNA 417 specific nuclear RNA processing 425 Complexity of nuclear and messenger RNAs 419 Evidence for unprocessed message precursors in the nucleus 427
Selection of alternative proteins by RNA, Sidelights & Speculations : Other roles of processing 428 differential RNA processing in antibod y Widespread use of differential RNA gene regulation 429 processing 428 Summary 43 1 Chapter 14 : Translational and posttranslational regulation of developmental processes 43 3 TRANSLATIONAL REGULATION OF Translational control of casein synthesis 45 3 DEVELOPMENT 434 The widespread use of translationa l Mechanism of eukaryotic translation 434 regulation 45 4 Translational control of coordinated protein Sidelights & Speculations : Other types of synthesis: Ribosomes and translational control 45 5 hemoglobin 437 POSTTRANSLATIONAL REGULATION O F Translational control of oocyte messages 441 GENE EXPRESSION 456. Evidence of maternal regulation of early Activation of proteins by posttranslationa l development 441 modifications 456 Stored messenger RNA 443 Inactivation of proteins by posttranslationa l Characterization of maternal messages 447 modifications 456 Mechanisms for translational control of Subcellular localization of proteins b y oocyte messages 448 posttranslational modifications 46 1 Maternal mrna and embryonic Supramolecular assembly 46. 2 cleavage 452 Collagen: An epitome of posttranslationa l Sidelights & Speculations : Maternal RNA in regulation 463 mammals 453 PART III : CELL INTERACTIONS IN DEVELOPMENT Chapter 15 : Spatial development: the role of the cell surface 47 1 Introduction 472 Sidelights & Speculations : Cell sorting and self- Structure of the cell surface 472 assembly 4. 9 6 Cell membrane 472 Sidelights & Speculations : Two systems of Cell membrane changes during adhesive specificity and their development 477 developmental significance 49 9 Extracellular matrix 479 Differential cell affinity in anima l Sidelights & Speculations : Oncofetal antigens 480 development 50 0 Cell surface modifications 485 Sea urchin gastrulation 504 Locomotion 487 The reeler and staggerer mutants of th e Differential cell affinity 489 mouse 502 Stationary cultures 489 Cell recognition in vivo : The T-complex Rotary cultures 491 of the mouse 504 The thermodynamic model of sorting out 493 Sidelights & Speculations : Glycosyltransferase s Adhesive specificity model of sorting out 495 and intercellular recognition 508
Chapter 16 : Proximate tissue interactions : secondary induction 51 5 Introduction 516 Coordinated differentiation and Instructive and permissive interactions 516 morphogenesis in the pancreas 53 0 Intercellular coordination in proximate The nature of proximity in epitheliointeractions 518 mesenchymal inductions 53 1 Epithelio-mesenchymal interactions 521 Mechanism of branching in the formation o f Regional specificity of induction 522 parenchymal organs 53 7 Genetic specificity of induction 523 Induction of plasma cells 540 Sidelights & Speculations : Development and Sidelights & Speculations : Crosslinking and macroevolution 525 induction 543 Formation of parenchymal organs 526 Induction of the chick limb 547 Chapter 17 : Pattern formation 55 5 Introduction 556 Specification of positional informatio n Pattern formation during limb development 556 in imaginal discs 57 6 The limb field 557 Pattern formation in the vertebrate nervou s Polarization along the limb axes 558 system 57 9 Regeneration of limb tissues 563 Direction of axonal growth 57 9 Polar coordinate model of pattern Mechanisms of synaptic specificity 582 formation 565 Qualitative neuronal differences 58 9 Genetics of pattern formation in Drosophila 569 Sidelights & Speculations : Cell surface address Compartmentalization in insect markers and lymphocyte migration 590 development 569 Development of behaviors 59 1 Mutations affecting the number of Sidelights & Speculations : Morphogenesis by segments 572 specific cell death 593 Mutations affecting segmentation : The Pattern formation in Hydra and Duglesia : bithorax complex 574 Morphallaxis 594 Sidelights & Speculations : Genetic control of segmentation 576 Chapter 18 : Cell interactions at a distance : hormones as mediators of development 603 Introduction 604 Hormonal control of insect Metamorphosis : The hormonal reactivation metamorphosis 622 of development 604 Sidelights & Speculations : Precocenes 62 5 Amphibian metamorphosis 605 Multiple hormonal interactions in mammary The phenomenon of amphibian gland development 62 6 metamorphosis 605 The embryonic stage 62 6 Hormonal control of amphibian Adolescence 62 9 metamorphosis 607 Pregnancy 63 0 Sidelights & Speculations : Neoteny 615 Puberty as a variation on the theme o f Metamorphosis in insects 616 metamorphosis 63 0. Control of cell proliferation: Chalones 634
Chapter 19 : Sex determination 638 Introduction 639 Sidelights & Speculations : The development of Chromosomal sex determinant in mammals 639 sexual behaviors 65 5 The developing gonads 641 Environmental sex determination 65 7 The H-Y antigen 643 Temperature-dependent se x The H-Y receptor 646 determination in reptiles 65 7 Sidelights & Speculations : The hormone-like Sidelights & Speculations : The extinction of effects of H-Y 649 dinosaurs 65 8 Secondary sex determination 649 Location-dependent sex determinatio n Chromosomal sex determination in in Bonellia and Crepidula 65 8 Drosophila 654 Hermaphroditism 66 0 Chapter 20 : The saga of the germ line 664 Introduction 665 Oogenesis 678 Germ cell formation 665 Oogenic meiosis 67 8 Germ cell migration in amphibians 665 The maturation of the oocyte in Germ cell migration in mammals 667 amphibians 680 Germ cell migration in birds and Sidelights & Speculations : Natura l reptiles 668 parthenogenesis 68 1 Meiosis 670 Oogenesis in meroistic insects 68 7 Spermatogenesis 673 Oogenesis in humans 69 1 Spermiogenesis 676 Sidelights & Speculations : The maintenance and Gene expression during sperm breaking of meiotic arrest 69 6 development 67 6 Sources for Chapter-Opening Quotations 703 Author Index 705 Subject Index 712