MouseDevelopmentPatterning, Morphogenesis, and Organogenesis

Janet Rossant

Patrick P. L. Tam

Contributors

xiii

IV. Specification of the Polarity of the Anterior -About the Editors

xvii

Posterior Axis of the Fetus?

29V Conclusions

3 2

References

33

I Establishment

of Body Patterns

3 Anterior Posterior Patterning of th eMouse Body Axis at Gastrulation

1 Fertilization and Activation

Stew-Lan Ang and Richard R . Behringe r

of the Embryonic Genome

I . Introduction

37Davor Softer, Wilhelmine N. de Vries, Alexei V. Evsikov,

II . Gastrulation

38Anne E. Peaston, Frieda H . Chen,

and Barbara B . Knowles

III . The Node : Morphogenesis, Cell Fate, an d

I. Introduction

5

Cell Movement

3 8

II. Oogenesis

6

IV. The Organizer Phenomenon : ConservedProperties of Vertebrate Organizers

4 0III.Meiosis and the Beginning of

Oocyte Asymmetry

7

V. The Vertebrate Organizer is a Dynamic,Nonhomogeneous, and Renewable Cel l

IV.Fertilization

8

Population at Gastrulation

4 0V Transcription andlts Control

8

VI . Insights into the Function of the MouseVI. mRNA Utilization during Oocyte Maturation

Organizer Gained from Genetic an dand Preimplantation Development

1 0

Embryological Studies

4 1VII. Gene Expression in the Early

VII . Genetic Analysis of Organizer Function : Mous eMouse Embryo

1 1

Mutants Showing Defects i nVIII. Functional Analysis

13

Organizer Function

42References

15

VIII . Inhibitory Signals Secreted by the Organize rand Its Derivatives

44

2 Asymmetry and Prepattern in

IX. Specification of the Primitive Streak an d

Mammalian Development

the Organizer

44X. Role of the AVE in Anterior Patternin g

R. L. Gardner

in Mouse

45I. Introduction

21

XI . Embryological and Genetic Analysi sII.Asymmetries in Early Development

23

of the Function of the AVE i nIII.Asymmetry of the Blastocyst

27

Anterior Patterning

46

XII.A Model for AVE Function in

IV. CNS Dorsal-Ventral Patterning Involves aAnterior Patterning

47

Tug of War between Dorsal and

XIII.Conclusions and Future Directions 48

Ventral Signaling

120

References

49

V. Summary

122References

12 2

4 Left-Right Asymmetry

Hiroshi Hamada

7 Somitogenesis : Segmentation of th e1 . Introduction

55

Paraxial Mesoderm and the Delineation o fll . Morphological Left-Right Asymmetries

56

Tissue CompartmentsIII . Genetic/ Molecular Pathway Governing Left-

Achim Gossler and Patrick P. L . TamRight Determination

58

I . Overview of Somite Development

127IV Molecular Readout of the

II . Allocation of Progenitor Cells to th eFirst Asymmetry

61

Paraxial Mesoderm

132V Role of the Midline

64

III . Cells Are in Transit in the Presomiti cVl . Readout of Left-Right Asymmetry in

Mesoderm

132Later Development

65

IV Regionalized Genetic Activity Points to aVII. Miscellaneous Mutations/

Prepattern of Prospective Somites

133Gene Factors

67

V. Emergence of Anterior-Posterio rVIII.Diversity among Vertebrates

68

Somite Compartments

13 4IX.Future Challenges

69

Vl . Role of Notch Signaling in the Establishmen tReferences

70

of Somite Borders and Anterior-Posterio rPolarity

134VII . A Molecular Clock Operates in the Paraxia l

5 Patterning, Regionalization, and Cell

Mesoderm to Control the Kinetics of

Differentiation in the Forebrain

Somite Formation

138

Oscar Marin and John L . R . Rubenstein

VIII . Specification of Lineage Compartments by

1 . Organization of the Forebrain

75

Inductive Interactions

139

ll . Early Patterning and Regional Specification of

IX . Summary and Open Questions

142

the Forebrain

78

References

14 4

III . Morphogenetic Mechanisms in th eForebrain

85IV Control of Neurogenesis and Cell-Type

If Lineage S Specification andSpecification in the Forebrain

87

PReferences

97

Differentiation8 Extraembryonic Lineages

6 Establishment of Anterior-Posterior and

Janet Rossant and James C . Cros s

Dorsal-Ventral Pattern in the Early Central

I . Introduction

15 5

Nervous System

Il . Early Development of the Trophoblast an d

Alexandra L . Joyner

Primitive Endoderm Lineages

15 6

1 . Overview of Early CNS Development

III . Cell Lineage Analysis and th e

and Patterning

107

Extraembryonic Lineages

1 5 6

11 . Anterior-Posterior Patterning

IV Setting Aside the Blastocyst Lineages

1 5 8

of the Mesencephalon and

V Molecular Specification of the Blastocys tMetencephalon

110

Cell Lineages

15 9

111 . Hindbrain Anterior-Posterior Patterning

VI . Differentiation of the Yolk Sacs

16 1Involves Segmental Units

VII . Morphogenetic Events in Development of th eof Development

117

Chorioallantoic Placenta

161

VIII.Comparative Aspects of Development of

V Future Directions

206Extraembryonic Membranes

162

References

206IX.Molecular Control of Primitiv e

Endoderm Development

16 4X. Signaling Pathways in Early

1 1 Vasculogenesis and Angiogenesi s

Trophoblast Development

1 66

Thomas N. Sato and Siobhan Loughn a

XI. Control of Spongiotrophoblast and Giant

I . Introduction

21 1

Cell Fate

168

II . Overview of Vascular Development

21 1

XII. Trophoblast Giant Cell Development :

III . Generation of Endothelial Cells

21 2

Gene Pathways and Control of

IV. Vascular Morphogenesis

220Endoreduplication

169

V. Concluding Remarks

22 8XIII. Initiating Chorioallantroic Fusion

170

References

228XIV. Gcm 1 Regulates the Initiation of

Chorioallantoic Branching

170

XV. Growth Factor Signaling Regulates Branching

12 Stem Cells of the Nervous Syste m

Morphogenesis of the Labyrinth

171

Sean J . Morrison

XVI. Placental Development and

I . Introduction

235

Pregnancy Complications

173

II . Lineage Determination of Neura l

References

174

Stem Cells

23 7III . Do Stem Cells Retain Broad or Narrow

Neuronal Potentials?

24 1

9 Germ Cells

IV. Regulation of Neural Stem Cel lSelf-Renewal

242Christopher Wylie and Robert Anderson

V.I. General Concepts

181

Differences between Hematopoietic Stem Cell sand Neural Stem Cells

243II. Early Appearance of Germ Cells in

VI . In Vivo Function of Neura lthe Mouse

182

Stem Cells

244III.Specification of Germ Cells in

VII . Surprising Potential of Neura lthe Mouse

183

Stem Cells

245IV.Migration of Germ Cells

185

VIII . Are Neural Stem Cells Involve dV. Motility of Germ Cells

185

in Disease?

246VI. Guidance of Germ Cell Migration

186

IX . Outstanding Issues

248VII.Adhesive Behavior of Germ Cells

References

248during Migration

18 7VIII.Survival and Proliferation of Germ Cell s

during Migration

188

1 3 Cellular and Molecular Mechanism s

References

189

Regulating Skeletal Muscle DevelopmentAtsushi Asakura and Michael A. Rudnick i

I . Introduction

253

10 Development of the Vertebrate

II . Embryonic Origin of Skeletal Muscle

254

Hematopoietic System

III . MyoD Family of Myogenic Regulatory

Nancy Speck, Marian Peeters, and Elaine Dzierzak

Factors

25 6

I. Introduction

191

IV. Muscle-Specific Transcriptiona l

II. Cellular Aspects of Blood Development in the

Regulation

262

Mouse Embryo

192

V. Inductive Mechanism s

III.Molecular Genetic Aspects of Blood

of Myogenesis

26 2

Development in the Mouse Embryo

202

VI . Specification of Muscle Fiber Types

268

IV.Current Cellular and Molecular Conceptual

VII . Muscle Regeneration

269

Frameworks for Hematopoietic

VIII . Conclusion

27 2Ontogeny

205

References

272

1 4 Deconstructing the Molecular Biology

III . A Conserved Pathway for Cardiac Inductio n

of Cartilage and Bone Formation

and Morphogenesis

33 4

Benoit de Crombrugghe, Veronique Lefebvre,

IV Cardiac Induction : The Rol e

and Kazuhisa Nakashima

of Endoderm

334

I. Introduction

279

V. Bone Morphogenetic Proteins as Cardia c

II. Sox Transcription Factors : Essential Roles in the

Inducing Molecules

33 6

Chondrocyte Differentiation Program

28 1

VI . Other Factors Involved i n

III. Parathyroid Hormone-Related Peptide (PTHrP)

Cardiac Induction

33 6

and Parathyroid Hormone (PTH) /PTHrP

VII . A Role for Anterior Visceral Endoderm i n

Receptor: Gatekeepers of the Zone of

Cardiac Induction in the Mouse?

338

Hypertrophic Chondrocytes

284

VIII . The Heart Morphogenetic Field

33 9

IV.FGFs and FGF Receptor 3 : Counterintuitive

IX . The Size and Shape of th eInhibitors of Chondrocyte

Heart Field

339Proliferation

286

X. The Timing and Stability of Cardia cV. Ihh: A Central Coordinator of Endochondral

Induction

34 0Bone Formation

287

XI . Migration of Cardiac Precursors

340VI. The Two Roles of the Transcription Factor

XII . Cellular Proliferation and Death in theCbfa 1 in Endochondral

Forming Heart

34 1Bone Formation

288

XIII . Cardiac Myogenesis

34 1VII. Other Transcription Factors Involved in

XIV. Modulation of Myogenesis i nBone Formation

290

Heart Chambers

343VIII.Gelatinase B and Vascular Endothelial Growth

XV. Regionality in the Developing Heart

343Factor : Additional Coordinators of

XVI . Plasticity of Heart Regionalization

344Endochondral Bone Formation

290IX.Conclusion

291

XVII . The Segmental Model•ofCardiac Morphogenesis

344References

292

XVIII . An Inflow/Outflow Model of Early HeartTube Patterning

34 5

111 Organogenesis

XIX . A Role for Retinoic Acid Signaling in Inflow /Outflow Patterning

346

15 Development of the Endoderm

XX. A Role for the Delta/Notch Pathway in Primar yHeart Patterning

347and Its Tissue Derivatives

XXI . Cardiac Chamber Formation

347

Brigid L. M. Hogan and Kenneth S . Zaret

XXII . Ventricular Specification : Knock-Out andI. Introduction and Overview

301

Transgenic Phenotypes

348II. Endoderm Development prior to

XXIII . Transcriptional Circuits Acting i nOrganogenesis

302

Chamber Formation

35 1III.Patterning and Differentiation of the

XXIV. The Cardiac Left-Right is

35 1Digestive Tract

307

XXV. Developmental Pathways and Congenita lIV Development of Tissues That Bud from

Heart Disease

35 6the Endoderm

310

XXVI . Horizons

35 7V. Perspectives and Remaining Issues on

References

358Organogenesis from the Endoderm

32 2References

322

1 7 Sex Determination and Differentiatio nAmanda Swain and Robin Lovell-Badg e

1 6 Molecular Determinants of Cardiac

I . Introduction

37 1

Development and Congenital Disease

II . Gonad Development

372

Richard P. Harvey

III . Sex Determination

37 6I. Introduction

332

IV. Testis Differentiation

38 0

II. Overview of Heart Structure

V. Cell Movement and Proliferation in theand Development

332

Early Gonad

382

VI. Ovary Differentiation

384

21 Development of the EyeVII. Sexual Development

384

Hisato Kondo hVIII. Evolution and Sex Determination

386

L Overview of Eye Development

51 9IX. Conclusion

388

II . Development of the Retina

52 1References

389

III . Lens Development

52 8IV. Conservation and Divergence of th e

1 8 Development of the Excretory System

Transcriptional Regulatory Systems in th e

Gregory R. Dressler

Eye Development

533

I . Introduction

395

References

53 5

IL Patterning of th eIntermediate Mesoderm

396

22 Development of the Mouse Inner EarIII . Growth of the Nephric Duct and Ureteric

Amy E. Kiernan, Karen P. Steel, and Donna M . FeketeBud Diverticulum

400

I . Introduction

53 9IV. Inductive Interactions

404

II . Anatomy of the Inner Ear

54 0V Mesenchyme to Epithelial

III . Development of the Inner Ear

54 1Conversion

407VI. Glomerular Development and

IV. Early Development of the Otic Blacod e

Vascularization

412

and Otocyst

542

VII. Developmental Basis of Human

V. Pattern Formation in the Inner Ear

546

Renal Disease

414

VI . Sensory Differentiation

55 2

VIII. Future Perspectives

416

VII . Neurogenesis

55 8

References

416

VIII . The Stria Vascularis

55 9IX. Future Directions

560

19 Craniofacial Development

References

56 1

Michael J . Depew, Abigail S . Tucker, and Paul T . Sharp e

I. Introduction

421

23 Integumentary StructuresII. Primordial Cells of the Head

422

Carolyn Byrne and Matthew Hardma n

Ill . Organ Development

433

I . Introduction

567IV. Conclusion

454

II . Mature Skin

569V. Appendix 1 : Descriptive

III . Non-Neural Embryonic Ectoderm

570Dental Development

454

IV. Stratification

57 1VI . Appendix 2 : Morphological Organization of

V. Dermal Development

57 2the Murine Skull

456

VI . Epidermal Appendag eVII . Appendix 3 : Molecular Regulators

Morphogenesis

574of Craniofacial Pattern

VII . Model for Follicle Formation: The Firs tand Development

465

Dermal Signal

57 4References

481

VIII . Follicle Spacing

57 7IX. Follicle Morphogenesis an d

20 Pituitary Gland Development

Differentiation

57 8Sally Camper, Hoonkyo Suh, Lori Raetzman,

X. Follicle Morphogenesis an dKristin Douglas, Lisa Cushman, Igor Nasonkin,

Follicle Cycling

57 8Heather Burrows, Phil Gage, and Donna Martin

XI . Molecular Parallels betweenI. Pituitary Gland Anatomy

Skin Tumorigenesis andand Function

499

Skin Development

57 9II. Development of the Pituitary Primordia and

XII . Early Terminal Differentiation

579Cell Specification

500

XIII . Regulation of Transit to Late Stages ofIII.Expansion of Committed Cell Types

510

Terminal Differentiation

580IV.Conclusion

512

XIV. Late Terminal Differentiation : Formation o fReferences

513

Stratum Corneum and Skin Barrier

581

XV. Periderm Disaggregation

583

Author Index

59 1

XVI. Conclusions and Future Directions

584

Subject Index

69 1

References

584