Developmental Biology A COMPREHENSIVE SYNTHESIS

Volume 1

Oogenesis

Developmental Biology A COMPREHENSIVE SYNTHESIS

General Editor

LEON W. BROWDER University of Calgary Calgary, Alberta, Canada

Editorial Board

EVERETT ANDERSON Harvard Medical School

JOSEPH T. BAGNARA The University of Arizona

SAMUEL H. BARONDES University of California at San Diego

ANTON IE W. BLACKLER Cornell University

MARIE A. DiBERARDINO The Medical College of Pennsylvania

RALPH B. L. GWATKIN McMaster University

Volume 1 OOGENESIS

ELIZABETH D. HAY Harvard Medical School

RALPH S. QUATRANO Oregon State University

RUDOLF A. RAFF Indiana University

L. DENNIS SMITH Purdue University

IAN M. SUSSEX Yale University

Edited by Leon W. Browder Forthcoming

Volume 2 THE CELLULAR BASIS OF MORPHOGENESIS Edited by Leon W. Browder

Volume 3 THE CELL SURFACE IN DEVELOPMENT AND CANCER Edited by Malcolm S. Steinberg

Volume 4 MANIPULATION OF MAMMALIAN DEVELOPMENT Edited by Ralph B. L. Gwatkin

Developmental Biology A COMPREHENSIVE SYNTHESIS

Volume 1

Oogenesis

Edited by

LEON W. BROWDER University of Calgary Calgary, Alberta, Canada

PLENUM PRESS • NEW YORK AND LONDON

Library of Congress Cataloging in Publication Data

Main entry under title:

Developmental biology.

Includes bibliographies and index. Contents: v. 1. Oogenesis. 1. Developmental biology-Collected works. 1. Browder, Leon W.

QH491.D426 1985 574.3

ISBN-13: 978-1-4615-6816-2

DOl: 10.1007/978-1-4615-6814-8

e-ISBN-13: 978-1-4615-6814-8

85-3406

Cover illustration: Acridine Orange fluorescence micrograph of insect ovarian follicle. Micrograph prepared by Lois Nichols. Courtesy of Spencer j. Berry, Department of Biology, Wesleyan University.

© 1985 Plenum Press, New York Softcover reprint of the hardcover I st edition 1985

A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013

All rights reserved

No part of this book may be reproduced, stored in a retrieval system, or transmitted, in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher

Contributors

Rosemary Bachvarova Department of Cell Biology and Anatomy, Cor­nell University Medical College, New York, N.Y. 10021

Spencer J. Berry Department of Biology, Hall-Atwater and Shanklin Laboratories, Wesleyan University, Middletown, Connecticut 06457

Bruce P. Brandhorst Department of Biology, McGill University, Mon­treal, Quebec H3A lBl Canada

Anna Ruth Brummett Biology Department, Oberlin College, Oberlin, Ohio 44074

Marie-Christine Dabauvalle Institute of Cell and Tumor Biology, Ger­man Cancer Research Center, D-6900 Heidelberg 1, Federal Repub­lic of Germany

James N. Dumont Biology Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee 378~0

Lee Engstrom Developmental Biology Center, Department of Develop­mental Genetics and Anatomy, Case Western Reserve University, Cleveland, Ohio 44106

John J. Eppig The Jackson Laboratory, Bar Harbor, Maine 04609

Franco Giorgi Istituto di Istologia e Embriologia, 56100 Pisa, Italy

Richard G. Kessel Department of Biology, University of Iowa, Iowa City, Iowa 52242

Kenneth D. Konrad Developmental Biology Center, Department of Developmental Genetics and Anatomy, Case Western Reserve Uni­versity, Cleveland, Ohio 44106

Angela Kr:imer Division of Molecular Biology and Biochemistry, Insti­tute of Cell and Tumor Biology, German Cancer Research Center, D-6900 Heidelberg 1, Federal Republic of Germany

v

vi Contributors

Anthony P. Mahowald Developmental Biology Center, Department of Developmental Genetics and Anatomy, Case Western Reserve Uni­versity, Cleveland, Ohio 44106

James 1. Maller Department of Pharmacology, University of Colorado School of Medicine, Denver, Colorado 80262

Norbert Perrimon Developmental Biology Center, Department of Developmental Genetics and Anatomy, Case Western Reserve Uni­versity, Cleveland, Ohio 44106

John H. Postlethwait Department of Biology, University of Oregon, Eugene, Oregon 97403

Ulrich Scheer Institute of Cell and Tumor Biology, German Cancer Research Center, D-6900 Heidelberg 1, Federal Republic of Germany

Allen W. Schuetz Department of Population Dynamics, Johns Hopkins School of Hygiene and Public Health, Baltimore, Maryland 21205

Robin A. Wallace C. V. Whitney Laboratory, St. Augustine, Florida 32086

Preface

This book launches a new continuing series in developmental biology. Any new publishing venture in science can only be justified if it satisfies a need and fulfills that need in an exemplary way. I believe that there is an acute need for comprehensive treatises on specialized topics in developmental biology-especially because this is a very diverse field that receives con­tributions from a wide variety of disciplines. It is difficult to remain abreast of progress in multifaceted topics and to understand how the various aspects of a topic interrelate. The volumes that will comprise this series are designed to facilitate those processes.

Each volume of this series will attempt to convey the current status of research and thought on a specific topic in development, place current research within historical perspective, and lay the intellectual groundwork for future research. These volumes are intended to provide an in-depth background on these topics for advanced undergraduates, graduate stu­dents, and senior scientists. An investigator considering research in one of these areas will get an overview of the field as well as discover the status of recent research in the area.

The extent to which these volumes achieve their goal will be a mea­sure of their usefulness to the scientific community. Contributors are selected who are authorities in their fields and who can effectively com­municate their knowledge, understanding, and ideas. Every effort has been made to ensure that the writing is clear and logical. Where useful, high­quality illustrations are used to clarify the text. The references accompa­nying each chapter are selected to permit access to the primary literature in that area. One key word in the title of this series is "Comprehensive." An attempt has been made to cover the most significant aspects of each topic. However, most topics are open ended, and value judgments must be made about the relative significance of possible subjects to include in a book of moderate length; some areas must therefore be omitted.

The choice of oogenesis as a topic for the first volume of this series was made for a number of reasons. Clearly, differentiation of the oocyte lays

vii

viii Preface

the groundwork for development of the zygote. RNA and protein are syn­thesized, stored, and organized in the oocyte such that development can be initiated at fertilization of the egg without immediate nuclear involve­ment. Energy sources may be packaged in the oocyte to reduce or eliminate the need of the embryo to acquire the means to obtain food from exogenous sources. The oocyte acquires a number of specializations that enable it to function in fertilization and to respond to the sperm by initiating devel­opment. Thus, the oocyte becomes a highly specialized cell through a com­plex differentiation process. However, the ramifications of oocyte differ­entiation are extensive, since the program for development of the zygote begins in the oocyte.

Oocyte differentiation is very precisely regulated and is dependent upon growth of the organism and is correlated with sexual behavior, like­lihood of fertilization, and suitability of the environment for development of the zygote. Regulation of oogenesis is mediated by hormones, which have numerous profound effects on the oocyte, oocyte accessory cells, and other reproductive tissues.

Because of its many aspects, the study of oocyte differentiation is one of the most integrated areas of investigation in developmental biology. Molecular biologists, cell biologists, morphologists, and physiologists are actively involved in probing the events that occur and the modes of their control. It is intended that this volume will provide the reader with a com­prehensive understanding of the research conducted on oogenesis from a variety of perspectives. It is hoped that the following chapters will convey the excitement of contemporary research on oogenesis and stimulate investigators to further our understanding of this vital process.

The concept for this series was developed in consultation with Mr. Kirk Jensen, Life Sciences Editor of Plenum Publishing Corporation. Mr. Jensen has remained enthusiastic about this project through its long ges­tation and has been immeasurably helpful at all stages in the development of this book. His commitment to excellence in academic publishing is reflected in Plenum's biology books. It is intended that this series will fur­ther that tradition. I am fortunate to have been assisted in developing this series by an editorial board of outstanding developmental biologists. Their contribution is greatly appreciated.

I have also been greatly assisted in working on this series and in orga­nizing this volume by my secretary, Miss Margaret Hunik, and by my wife, Sandy, whose knowledge of publishing and patience with me have greatly eased my burden.

Leon Browder

Contents

1. Physiological and Morphological Aspects

Chapter 1 • Local Control Mechanisms During Oogenesis and Folliculogenesis

Allen W. Schuetz

1. Introduction ............................................ 3 2. Choice of Animals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 3. Folliculogenesis......................................... 12 4. Follicle (Granulosa) Cells and Oogenesis. . . . . . . . . . . . . . . . . . . . 17 5. Role of Steroids and Hormone Interactions in Follicular and

Oocyte Differentiation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21 6. Intercellular Transfer of Hormonal Signals of Differentiation. . . 30 7. Spontaneous Cellular Differentiation: The Dilemma of

Regulation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 35 8. Germinal Vesicle Breakdown and Meiotic Progression. . . . . . . . 39 9. Coordination of Ovulation and Oocyte Maturation. . . . . . . . . . . . 45

10. Postovarian Oocyte Maturation and Fertilization Mechanisms. . 51 11. Oocyte Maturation and the Block to Polypermy . . . . . . . . . . . . . . 56 12. Cytoplasmic Control of Sperm Nuclear Differentiation. . . . . . . . 60 13. Oocyte Maturation and Cytoplasmic Clocks ................. 66 14. Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73

Chapter 2 • Vitellogenesis in Insects John H. Postlethwait and Franco Giorgi

1. Strategies for Provisioning the Egg ......................... 85 2. How Insects Make Eggs. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 86 3. Regulation of Vitellogenin Synthesis and Secretion. . . . . . . . . . . 98 4. Regulation of Vitellogenin Sequestration. . . . . . . . . . . . . . . . . . .. 111 5. The Role of Yolk in Development. . . . . . . . . . . . . . . . . . . . . . . . .. 117

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6. Conclusion............................................. 119 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 119

Chapter 3 • Vitellogenesis and Oocyte Growth in Nonmammalian Vertebrates

Robin A. Wallace

1. Introduction............................................ 127 2. Vitellogenin and Vitellogenin Genes. . . . . . . . . . . . . . . . . . . . . . .. 128 3. Liver-Related Events. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 131 4. Blood-Related Events: Kinetics of Vitellogenin and VLDL

Turnover. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 137 5. Ovary-Related Events . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 141 6. Vitellogenesis and Oocyte Growth In Vitro .................. 161 7. Epilogue................................................ 163

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 166

Chapter 4 • Annulate Lamellae (Porous Cytomembranes): With Particular Emphasis on Their Possible Role in Differentiation of the Female Gamete

Richard G. Kessel

1. Introduction/Background................................. 179 2. Distribution in Oocytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 181 3. Ooplasmic Position and Variability. . . . . . . . . . . . . . . . . . . . . . . .. 184 4. Comparative Features of Nuclear Envelope/Annulate Lamellae 186 5. Origin and Morphogenesis of Annulate Lamellae and

Associations with Other Organelles ........................ 190 6. Morphogenesis of Pores ............................... , . .. 217 7. Experimental Alteration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 218 8. Proposed Functions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 220 9. Intranuclear Annulate Lamellae ........................... 221

10. Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 222 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 223

Chapter 5 • Egg Envelopes in Vertebrates James N. Dumont and Anna Ruth Brummett

1. Introduction ............................................ 235 2. Teleosts................................................ 235 3. Lampreys............................................... 246 4. Chondrichthyes......................................... 247 5. Primitive Osteichthyes ................................... 247 6. Amphibians............................................. 248 7. Reptiles................................................ 259

Contents xi

8. Birds................................................... 261 9. Monotremes ............................................ 269

10. Marsupials.............................................. 270 11. Placental Mammals ...................................... 271 12. Summary............................................... 276

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 277

Chapter 6 • Oocyte Maturation in Amphibians James L. Maller

1. Introduction ............................................ 289 2. Interrelations of Calcium and Cyclic AMP. . . . . . . . . . . . . . . . . .. 298 3. The Maturation-Promoting Factor. . . . . . . . . . . . . . . . . . . . . .. . .. 302 4. Summary............................................... 307

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 308

Chapter 7 • Oocyte-Somatic Cell Interactions During Oocyte Growth and Maturation in the Mammal

John J. Eppig

1. Introduction ............................................ 313 2. Metabolic Cooperativity .................................. 313 3. Occurrence of Gap Junctions During Oogenesis .............. 316 4. Role of Cell-to-Cell Communication During Oocyte Growth ... 316 5. Oocyte Maturation in Mammals ........................... 317 6. Hormonal Control of Cumulus Cell Function . . . . . . . . . . . . . . .. 332 7. Role of Somatic Cell-Oocyte Interactions in Ovarian

Teratocarcinogenesis and Parthenogenetic Development ...... 339 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 343

II. Gene Expression: Regulation and Consequences for Oogenesis and Early Development

Chapter 8 • RNA Synthesis and Storage During Insect Oogenesis Spencer J. Berry

1. Introduction ............................................ 351 2. Organization of Ovarian Follicles .......................... 353 3. Autoradiographic Studies of Ovarian RNA Synthesis ......... 362 4. Biochemical Analysis of Oocyte RNA. . . . . . . . . . . . . . . . . . . . . .. 365 5. Transport of RNA and RNP from Trophic Cells to Ooplasm. . .. 375 6. Activation of Transcription of the Embryonic Genome. . . . . . .. 376 7. RNA in Insect Morphogenesis-An Alternate Model of

"Determination" . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 377 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 380

xii Contents

Chapter 9 Functional Organization of the Amphibian Oocyte Nucleus

Ulrich Scheer and Marie-Christine Dabauvalle

1. Introduction............................................ 385 2. Lampbrush Chromosomes ................................ 387 3. Amplified Nucleoli. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 404 4. The Nuclear Envelope. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 413 5. The Nucleoplasm ........................................ 417 6. Storage at Two Different Levels: Proteins and Maternal mRNA. 422 7. Microinjection of DNA into Oocyte Nuclei .................. 423 8. Injection of Antibodies into the Oocyte Nucleus: A Means of

Interfering with Gene Expression in the Living Cell .......... 425 References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 425

Chapter 10 • 5 S Ribosomal Gene Transcription During Xenopus Oogenesis

Angela Kramer

1. Introduction............................................ 431 2. Isolation and Structural Organization of 5 S rRNA Genes of

Xenopus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 432 3. 5 S rRNA Synthesis During Oogenesis. . . . . . . . . . . . . . . . . . . . .. 434 4. Transcription of 5 S rRNA Genes. . . . . . . . . . . . . . . . . . . . . . . . . .. 436 5. The Role of a Positive Transcription Factor (TFIIIA) in the

Transcription of 5 S rRNA Genes. . . . . . . . . . . . . . . . . . . . . . . . . .. 440 6. Concluding Remarks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 447

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 448

Chapter 11 • Gene Expression During Oogenesis and Oocyte Development in Mammals

Rosemary Bachvarova

1. Introduction ............................................ 453 2. Description of Oogenesis and Oocyte Development in Mammals 454 3. RNA Synthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 462 4. Chromosomal Structure .................................. 473 5. Accumulation of Stable RNA During Oocyte Growth; RNA

Content of the Full-Grown Oocyte and Ovulated Egg. . . . . . . .. 487 6. Protein Synthesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 501 7. Role of Accumulated Products in Embryogenesis. . . . . . . . . . . .. 507 8. Summary............................................... 513

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 515

Contents xiii

Chapter 12 • Informational Content of the Echinoderm Egg Bruce P. Brandhorst

1. Introduction............................................ 525 2. Oogenesis in Sea Urchins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 526 3. Stored Maternal Messenger RNA in Sea Urchin Eggs. . . . . . . . .. 527 4. Characteristics of Maternal RNA Stored in Eggs. . . . . . . . . . . . .. 530 5. Functional Significance of Maternal RNA Molecules

Resembling Nuclear Precursors of Messenger RNA. . . . . . . . . .. 544 6. Mass of Maternal Messenger RNA Stored in the Egg. . . . . . . . .. 548 7. Activation of Translation of Maternal Messenger RNA. . . . . . .. 550 8. Stability of Maternal Messenger RNA. . . . . . . . . . . . . . . . . . . . . .. 554 9. Distribution of Maternal RNA Sequences in Eggs and Embryos. 560

10. Synthesis and Accumulation of RNA During Oogenesis. . . . . .. 561 11. Metabolism of Egg Proteins During Embryonic Development. .. 563 12. Speculations on the Roles of Stored Maternal RNA. . . . . . . . . .. 565 13. Summary and Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 566

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 567

Chapter 13 • Genetic Analysis of Oogenesis and the Role of Maternal Gene Expression in Early Development

Kenneth D. Konrad, Lee Engstrom, Norbert Perrimon, and Anthony P. Mahowald

1. Introduction ............................................ 577 2. Female Sterile Mutations ................................. 578 3. Maternal Effect Mutations ................................ 589 4. Conclusions............................................. 609

References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 611

Index ................. , ................. " ................ " 613