A COMPARATIVE OVERVIEW OF MAMMALIAN FERTILIZATION

A COMPARATIVE OVERVIEW OF MAMMALIAN FERTILIZATION

Edited by

Bonnie S. Dunbar Baylor College of Medicine Houston, Texas

and

Michael G. O'Rand University of North Carolina at Chapel Hill Chapel Hill, North Carolina

SPRINGER SCIENCE+BUSINESS MEDIA, LLC

L1brary of Congress Catalog1ng-1n-Publ1cat1on Data

A Comparative overv1ew of mammalian fertilization 1 edited by Bonnie S. Dunbar and M1chael G. O'Rand.

p. cm. Includes bibliographical references and index.

2. Mammals--Physiology. 1. Ferti11zation <Biology) 3. Physiology. Comparative. Michael G.

I. Dunbar, Bonnie S. II. O'Rand.

OP273.C59 1991 599'.03--dc20

ISBN 978-1-4757-8984-3

© 1991 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1991 Softcover re print of the hardcover 1 st edition 1991

Ali rights reserved

91-21138 CIP

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

ISBN 978-1-4757-8984-3 ISBN 978-1-4757-8982-9 (eBook)DOI 10.1007/978-1-4757-8982-9

Contributors

Barry D. Bavister Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wisconsin 53715

J. Michael Bedford Departments of Obstetrics and Gynecology and Cell Biology and Anat­omy, Cornell University Medical College, New York, New York 10021

Dorothy E. Boatman Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wisconsin 53715

Gary N. Cherr Bodega Marine Laboratory, University of California, Davis, Bodega Bay, California 94923

Elizabeth G. Crichton Department of Anatomy, University of Arizona, Tucson, Arizona 85724

C. J. De Jonge Department of Obstetrics and Gynecology, Rush University, Rush-Pres­byterian-St. Luke's Medical Center, Chicago, Illinois 60612

Erma Z. Drobnis Departments of Zoology and Obstetrics and Gynecology, University of California, Davis, California 95616

Gil L. Dryden Biology Department, Slippery Rock University, Slippery Rock, Pennsylvania 16057

Bonnie S. Dunbar Department of Cell Biology, Baylor College of Medicine, Houston, Texas 77030

N. L. First Department of Meat and Animal Science, University of Wisconsin, Madison, Wisconsin 53706

George L. Gerton Division of Reproductive Biology, Department of Obstetrics and Gynecol­ogy, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6080

v

vi Contributors

Erwin Goldberg Department of Biochemistry, Molecular Biology, and Cell Biology, North­western University, Evanston, Illinois 60208

R. H. F. Hunter Center for Research on Animal Reproduction, Faculty of Veterinary Medicine, University of Montreal, Saint-Hyacinthe, Quebec J2S 7C6, Canada. Present address: University of Edinburgh, Edinburgh EH16 5NT, Scotland, United Kingdom

Kristen A.lvani Animal Reproduction and Biotechnology Laboratory, Colorado State Univer­sity, Fort Collins, Colorado 80523

Gregory S. Kopf Division of Reproductive Biology, Department of Obstetrics and Gynecol­ogy, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6080

Philip H. Krutzsch Department of Anatomy, University of Arizona, Tucson, Arizona 85724

Susan E. Lanzendorf Division of Reproductive Biology and Behavior, Oregon Regional Primate Research Center, Beaverton, Oregon 97006. Present address: The Jones Institute for Reproductive Medicine, Department of Obstetrics/Gynecology, Eastern Virginia Medical School, Norfolk, Virginia 23510

Frank J. Longo Department of Anatomy, University of Iowa, Iowa City, Iowa 52242

Cherrle A. Mahi·Brown California Primate Research Center, University of California, Davis, California 95616

Patricia M. Morgan Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wisconsin 53715. Present address: Department of Biochemistry, University College, Galway, Ireland

Barbara S. Nlkolajczyk Department of Cell Biology and Anatomy, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599

Gary E. Olson Department of Cell Biology, Vanderbilt University, Nashville, Tennessee 37232

Michael G. O'Rand Department of Cell Biology and Anatomy, University of North Carolina at Chapel Hill, Chapel Hill, North Carolina 27599

J. J. Parrish Department of Meat and Animal Science, University of Wisconsin, Madison, Wisconsin 53706

David M. Phillips The Population Council, New York, New York 10021

S. V. Prasad Department of Cell Biology, Baylor College of Medicine, Houston, Texas 77030

John C. Rodger Department of Biological Sciences, The University of Newcastle, Newcastle 2308, New South Wales, Australia

George E. Seidel, Jr. Animal Reproduction and Biotechnology Laboratory, Colorado State University, Fort Collins, Colorado 80523

Ruth Shalgl Department of Embryology and Teratology, Sadder School of Medicine, Tel­Aviv University, Ramat Aviv, Tel-Aviv 69978, Israel

Contributors vii

Bayard T. Storey Division of Reproductive Biology, Department of Obstetrics and Gynecol­ogy, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19104-6080

T. M. Timmons Department of Cell Biology, Baylor College of Medicine, Houston, Texas 77030

Pradeep K. Warikoo Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wisconsin 53715. Present address: Department of IVF, Saginaw General Hospital, Saginaw, Michigan 48602

Paul M. Wasserman Department of Cell and Developmental Biology, Roche Institute of Molecular Biology, Roche Research Center, Nutley, New Jersey 07110

David E. Wildt National Zoological Park, Smithsonian Institution, Washington, D.C. 20008

Virginia P. Winfrey Department of Cell Biology, Vanderbilt University, Nashville, Tennessee 37232

Don P. Wolf Division of Reproductive Biology and Behavior, Oregon Regional Primate Research Center, Beaverton, Oregon 97006, and Department of Obstetrics/Gynecology, Oregon Health Sciences University, Portland, Oregon 97201

Debra J. Wolgemuth Department of Genetics and Development, and Center for Reproductive Sciences, Columbia University College of Physicians and Surgeons, New York, New York 10032

L. J. D. Zaneveld Department of Obstetrics and Gynecology, and Department of Biochemis­try, Rush University, Rush-Presbyterian-St. Luke's Medical Center, Chicago, Illinois 60612

Preface

In 1964, the Fertilization and Gamete Physiology Research Training Program (FERGAP) was established at the Marine Biological Laboratories, Woods Hole, Massachusetts. Over the course of the next 12 years, under the directorship of Dr. Charles B. Metz, FERGAP brought together, trained, and inspired a generation of students in reproductive biology from all over the world.

As students of C. B. Metz and as FERGAP trainees, we would like to dedicate this collected work on comparative mammalian fertilization to our teacher and mentor, Dr. Charles B. Metz. Like a number of authors contributing to this volume, we have been struck by the significant impact that C. B. Metz and FERGAP had on the development of students of reproductive biology. Applying both the classical and molecular techniques of cell biology and immunology to problems of gamete biology, Dr. Metz emphasized a comparative and analytical approach that was reflected in his own research on fertilization in Paramecia, sea urchins, frogs, and mammals.

It is hoped that this volume will serve to stimulate students to discover the myriad of fascinating research problems in gamete and reproductive biology.

Houston, Texas Chapel Hill, North Carolina

ix

Bonnie S. Dunbar Michael G. O'Rand

Contents

2

Part I COMPARATIVE OVERVIEW OF MAMMALIAN GAMETES

The Coevolution of Mammalian Gametes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 J. Michael Bedford

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 2. Gamete Design . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4

2.1. Monotremes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 2.2. Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 2.3. Eutherians . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9

3. Gamete Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 3 .1. Oocyte Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 3.2. Sperm Maturation in the Male . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15 3.3. Capacitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

4. Gamete Interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20 5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 6. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 28

ComparatiYe Morphology of Mammalian Gametes David M. Phillips and GilL. Dryden

37

I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 37 2. Light Microscopy of Spermatozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 3. Structure of the Sperm Head . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 38 4. Mammalian Eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42 5. The Zona Pellucida . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42 6. The Cumulus Oophorus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 43 7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 46 8. References 48

xi

xii

3 A Comparison of Mammalian Sperm Membranes Gary E. Olson and Virginia P. Winfrey

Contents

51

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 51 2. Periacrosomal Plasma Membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 52 3. Postacrosomal Plasma Membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 53 4. Midpiece Plasma Membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 55 5. Principal Piece Plasma Membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 56 6. Endpiece Plasma Membrane . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 57 7. Structures at Domain Interfaces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 58 8. Concluding Comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60 9. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 60

4 Mammalian Sperm Acrosomal Enzymes and the Acrosome Reaction . . . . . . . . . 63 L. J. D. Zaneveld and C. J. De Jonge

5

6

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 63 2. Acrosomal Enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64

2.1. Proteinases and Peptidases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 64 2.2. Glycosidases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67 2.3. Lipases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68 2.4. Phosphatases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 68 2.5. Other Enzymes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 69

3. Acrosome Reaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12 3.1. Surface-Associated Changes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72 3.2. Ions and ATPase . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72 3.3. Second Messenger Systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73 3.4. Phospholipases, Cyclooxygenase, Lipoxygenase,

and Their Products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75 3.5. Acrosin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76

4. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76

Morphogenesis of the Mammalian Egg Cortex Frank J. Longo

81

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 81 2. Plasma Membrane and Microvilli . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 82 3. Cortical Cytoskeleton . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 85 4. Cortical Granules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 87 5. Organization of the Meiotic Spindle . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 88 6. Organization of Endoplasmic Reticulum and Endosomes . . . . . . . . . . . . . . . 90 7. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 8. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91

Comparative Structure and Function of Mammalian Zonae Pellucidae Bonnie S. Dunbar, S. V. Prasad, and T M. Timmons

97

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 97 2. Morphological Properties of Zonae Pellucidae . . . . . . . . . . . . . . . . . . . . . . . 97

Contents xiii

3. Physicochemical Properties of Zonae Pellucidae . . . . . . . . . . . . . . . . . . . . . . 100 4. Glycoproteins of Mammalian Zonae Pellucidae . . . . . . . . . . . . . . . . . . . . . . . 100 5. Carbohydrate Composition of Zonae Pellucidae . . . . . . . . . . . . . . . . . . . . . . . 101 6. Molecular Analysis of ZP Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 103 7. Synthesis of ZP Glycoproteins and Formation of

the Extracellular Matrix . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 104 8. Developmental Expression of ZP Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . 105 9. Ovarian Follicular Development and Formation of the Zona Pellucida . . . . 105

10. Sperm-ZP Interaction during Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . 106 11. Sperm Penetration of the Zona Pellucida during Fertilization . . . . . . . . . . . . 107 12. Changes in the Zona Pellucida following Fertilization . . . . . . . . . . . . . . . . . . 107 13. Antigenic Composition of Mammalian Zonae Pellucidae . . . . . . . . . . . . . . . 109 14. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 110

Part II STUDIES ON MAMMALIAN FERTILIZATION IN SELECTED SPECIES

7 Fertilization of Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117 John C. Rodger

1 . Background . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117 1. 1. Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117 1.2. Marsupial Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 117

2. Marsupial Spermatozoa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118 2.1. General Features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 118 2.2. Epididymal Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 121

3. Marsupial Oocytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122 3. 1. Oocyte Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122 3.2. Oocyte Vestments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 122

4. Collection of Gametes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 4.1. Induction of Ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 4.2. Semen Collection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

5. Gametes in the Female Tract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 5 .1. The Anatomy of the Female Tract . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123 5.2. Timing of Mating and Ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 5.3. Unpairing of Opossum Sperm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125

6. Postejaculatory Sperm Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126 6.1. Attempts to Induce Marsupial Sperm to Acrosome React . . . . . . . . . . 126 6.2. Acrosome Changes in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126 6.3. The Acrosome and Sperm-Egg Interaction . . . . . . . . . . . . . . . . . . . . . . 127 6.4. Do Marsupial Sperm Undergo Prefertilization Motility

Changes? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127 7. Gamete Interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129

7.1. Sperm-Egg Binding ........................................ 129 7 .2. Zona Pellucida Penetration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129 7.3. Sperm-Oocyte Membrane Fusion ............................. 130 7.4. Sperm Incorporation by the Egg . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

8. The Block to Polyspermy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130

xiv Contents

9. Egg Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132 10. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132 11. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132

8 Fertilization in Bats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137 Philip H. Krutzsch and Elizabeth G. Crichton

9

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 137 2. Patterns of Reproduction in Chiroptera ............................... 137

2.1. Asynchrony of Gamete Production and Sperm Storage . . . . . . . . . . . . . 137 2.2. Synchrony of Gamete Production ............................... 138

3. Morphology of the Male Gamete .................................... 138 4. Morphology of the Female Gamete .................................. 139 5. The Acrosome Reaction ........................................... 140 6. Fertilization in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 140 7. Fertilization in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 143 8. Conclusions and Future Directions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 146 9. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 14 7

Fertilization in the Mouse: I. The Egg Paul M. Wassarman

151

1. Introductory Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 151 2. Development of Unfertilized Mouse Eggs ........................... 152 3. Fertilization of Mouse Eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 155 4. Mouse Egg Components Directly Involved in Fertilization . . . . . . . . . . . . . . 157

4.1. Zona Pellucida . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 157 4.2. Plasma Membrane .......................................... 157 4.3. Cortical Granules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 158

5. Mouse Egg Primary Sperm Receptor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160 6. Mouse Egg Acrosome Reaction Inducer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 7. Mouse Egg Secondary Sperm Receptor ............................. 162 8. Mouse Egg Secondary Block to Polyspermy . . . . . . . . . . . . . . . . . . . . . . . . . 162 9. Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 162

10. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164

10 Fertilization in the Mouse: II. Spermatozoa .............................. 167 Bayard T. Storey and Gregory S. Kopf

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 2. Fertilization in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170

2.1. Sperm Distribution in the Female Reproductive Tract . . . . . . . . . . . . . . 170 2.2. Sperm Capacitation in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171 2.3. Sperm Acrosome Reaction in Vivo .............................. 172 2.4. Sperm-Egg Interaction in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 173 2.5. Summary of in Vivo Observations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 174

3. Fertilization in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 4 3 .1. Early Studies: Establishment of an in Vitro System . . . . . . . . . . . . . . . . 17 4 3.2. In Vitro Capacitation of Mouse Spermatozoa ..................... 176

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3.3. In Vitro Binding of Mouse Spermatozoa to the Zona Pellucida ....... 184 3.4. The Acrosome Reaction Induced by the Zona Pellucida in Vitro ...... 191 3.5. Zona Pellucida Penetration in Vitro ............................. 204 3.6. Sperm-Egg Fusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205 3. 7. Envoi . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 208

4. References ...................................................... 209

11 Fertilization in the Golden Hamster . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 Gary N. Cherr and Erma Z. Drobnis

12

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217 2. Advantages of the Hamster Model . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 217

2.1. Advantages in Common with Murine Rodents ................... 218 2.2. Advantages Specific to the Hamster ............................ 218 2.3. Disadvantages of the Hamster Model .......................... 219

3. Ovulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 219 4. Sperm Transport . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 220 5. Sperm Capacitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 222

5 .1. Factors Regulating Capacitation in Vitro . . . . . . . . . . . . . . . . . . . . . . . . 222 5.2. Cellular Changes during Capacitation .......................... 223

6. Hyperactivation ................................................. 224 7. Sperm Penetration of the Cumulus Cell Matrix . . . . . . . . . . . . . . . . . . . . . . . 224 8. Sperm-Zona Pellucida Interaction ................................. 226

8.1. Morphology of Sperm-Zona Interaction ........................ 226 8.2. Zona Receptor Activity in Sperm .............................. 228

9. The Acrosome Reaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230 9 .1. Induction of the Acrosome Reaction during Interaction with the

Oocyte-Cumulus Complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 230 9.2. Stimulation and Regulation of the Acrosome Reaction in Vitro ...... 232

10. Sperm Penetration of the Zona Pellucida ............................ 233 11. Zona Pellucida Structure and Composition . . . . . . . . . . . . . . . . . . . . . . . . . . . 234 12. Sperm-Egg Fusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 236 13. Egg Activation ................................................. 237 14. The Zona Reaction and Vitelline Block to Polyspermic Fertilization ...... 238

14.1. The Zona Reaction in Hamster Eggs .......................... 238 14.2. The Vitelline Block to Polyspermy in the Hamster .............. 239

15. References ..................................................... 239

Fertilization in the Rat Ruth Shalgi

245

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245 2. In Vivo Studies of Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245

2.1. Sperm Transport and Capacitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 245 2.2. Cumulus Penetration ......................................... 246 2.3. Zona Interaction ............................................. 247 2.4. Sperm-Vitellus Interaction .................................... 247

3. In Vitro Studies of Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 247 3.1. In Vitro Capacitation ......................................... 247

xvi Contents

3.2. Cumulus Penetration ......................................... 249 3.3. Sperm-Zona Interaction and the Acrosome Reaction ............... 250 3.4. Sperm-Vitellus Interaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 250 3.5. Source of the Egg for Fertilization .............................. 251

4. From Penetration to Fertilization .................................... 251 5. References ...................................................... 253

13 Fertilization in the Guinea Pig . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 George L. Gerton

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 2. Early Studies on Ovulation and Copulation . . . . . . . . . . . . . . . . . . . . . . . . . . . 257 3. Epididymal Maturation of Guinea Pig Sperm .......................... 257 4. Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 259

4.1. Fertilization and Early Development in Vivo . . . . . . . . . . . . . . . . . . . . . . 259 4.2. Fertilization in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 260

5. Sperm Capacitation and Acrosome Reaction . . . . . . . . . . . . . . . . . . . . . . . . . . 260 5.1. Sperm Capacitation: Effect on Guinea Pig Sperm . . . . . . . . . . . . . . . . . 260 5.2. Sperm Capacitation: Examination of Mechanism .................. 261 5.3. Guinea Pig Sperm Acrosome Reaction .......................... 262

6. The Sperm Surface . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 6.1. Involvement of Sperm Surface Molecules in Guinea Pig

Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 264 6.2. Sperm Binding to Eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 266 6.3. Sperm Fusion with the Egg . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 267

7. The Use of the PH-20 Protein as an Immunocontraceptive ............... 267 8. Concluding Comments: Future Studies ............................... 267 9. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 268

14 Fertilization in the Rabbit ............................................ 271 Michael G. 0' Rand and Barbara S. Nikolajczyk

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271 2. Maturation of the Gametes and the Timing of Fertilization . . . . . . . . . . . . . . . 272 3. Capacitation and the Acrosome Reaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 273 4. Zona Pellucida Binding and Penetration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274 5. Sperm Enzymes ................................................. 274 6. Spermatozoon-Oocyte Fusion ...................................... 276 7. Summary of the Steps of Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 276 8. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 277

15 Fertilization in Dogs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281 Cherrie A. Mahi-Brown

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 281 2. Basic Features of Canine Reproductive Biology ........................ 281

2.1. The Estrous Cycle of the Bitch ................................ 281 2.2. The Male Dog . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 282 2.3. Sperm Storage in the Female Reproductive Tract .................. 283

Contents xvii

3. Canine Gametes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284 3 .1. The Canine Oocyte . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 284 3.2. The Canine Spermatozoon .................................... 285

4. The Fertilization Process in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 286 4.1. Sperm Capacitation and Acrosome Reaction ...................... 286 4.2. Zona Pellucida Penetration and Sperm-Egg Fusion ................ 287 4.3. Egg Activation .............................................. 288 4.4. Penetration of Zona-Free Hamster Eggs ......................... 290

5. Fertilization in Vivo . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 290 6. Artificial Insemination and Embryo Transfer .......................... 292 7. Fertilization in other Carnivora . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293

7 .1. Canidae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 293 7 .2. Other Carnivores . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 294

8. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 294 9. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 295

16 Fertilization in Cats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299 David E. Wildt

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 299 2. General Reproductive Characteristics ................................ 300

2 .1. The Male Cat . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 300 2.2. The Female Cat ............................................. 301

3. Gamete Features . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 303 3 .1. The Ovum during the Natural Periestrous Interval . . . . . . . . . . . . . . . . . 303 3.2. Oocyte Maturation ........................................... 304 3.3. Sperm Capacitation .......................................... 307

4. Fertilization in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 309 4.1. Effect of hCG Dose and Interval from PMSG to hCG . . . . . . . . . . . . . . 310 4.2. Effect of Culture Medium and Protein Supplementation ............ 312 4.3. Features Associated with IVF of Mature Cat Oocytes .............. 314 4.4. In Vitro Maturation and Fertilization ............................ 314 4.5. The "Male Component" to Fertilization in Vitro .................. 316

5. Fertilization in Nondomestic Felid Species ............................ 318 5.1. Studies Using Heterologous Oocytes ............................ 319 5.2. Studies Using Homologous Oocytes ............................ 320

6. Conclusions ..................................................... 324 7. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 324

17 Fertilization in the Pig and Horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 R. H. F. Hunter

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 329 2. Pig ............................................................ 330

2.1. Preliminaries to Fertilization in Pigs . . . . . . . . . . . . . . . . . . . . . . . . . . . . 330 2.2. Semen Deposition and Uterine Transit ........................... 330 2.3. Ovulation and Egg 'ftansport .................................. 331 2.4. Sperm Physiology in the Oviducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 332 2.5. Activation of Secondary Oocytes ............................... 333

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Contents

2.6. Block to Polyspermy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 334 2.7. Chronology of Fertilization and Early Development ................ 337 2.8. Postovulatory Aging ................. , ....................... 337 2.9. Polyspermy in Pig Eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 339 2.10. Early Embryonic Loss . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 340

3. Horse . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 341 3 .1. Preliminaries to Fertilization in Equids . . . . . . . . . . . . . . . . . . . . . . . . . . 341 3.2. Semen Volume and Sperm Concentration ........................ 341 3.3. Estrus, Sperm Storage, and Survival . . . . . . . . . . . . . . . . . . . . . . . . . . . . 342 3.4. Fate of Seminal Plasma and Spermatozoa ........................ 342 3.5. Ovulation and Egg Transport .................................. 343 3.6. Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 343 3. 7. Abnormal Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344 3. 8. Cleavage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344 3. 9. Egg Progression in Equine Oviducts . . . . . . . . . . . . . . . . . . . . . . . . . . . . 344

4. References ...................................................... 346

Bovine in Vitro Fertilization l l Parrish and N. L. First

351

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351 2. Capacitation . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 351 3. Oocyte Maturation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 356 4. Interaction of Sperm and Egg . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 357 5. References ...................................................... 358

19 Fertilization in the Rhesus Monkey . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363 Barry D. Bavister, Dorothy E. Boatman, Patricia M. Morgan, and Pradeep K. Warikoo

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 363 2. Capacitation of Rhesus Sperm in Vitro . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 364 3. Ovarian Stimulation and Oocyte Collection . . . . . . . . . . . . . . . . . . . . . . . . . . . 368 4. In Vitro Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 369 5. Development of IVF Embryos ...................................... 371

5.1. Development of IVF Embryos in Vitro .......................... 371 5.2. Development of IVF Embryos following Transfer ................. 374

6. Use ofiVF for Studies on Oocyte Maturation ......................... 375 7. Use of IVF for Conservation of Endangered Species . . . . . . . . . . . . . . . . . . . . 378 8. Summary and Conclusions ......................................... 378 9. References ...................................................... 379

20 Fertilization in Man . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385 Don P. Wolf and Susan E. Lanzendorf

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385 2. Ovarian Hyperstimulation ........................................ 386 3. Egg Collection ................................................. 387 4. Egg Quality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 387 5. Epididymal Sperm .............................................. 390

Contents xix

6. Ejaculated Sperm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 390 7. Sperm Capacitation .............................................. 391

7 .1. Hyperactivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 392 7.2. Sperm-Zona Binding ....................................... 392 7.3. Acrosome Reaction ......................................... 392

8. Fertility Potential Measurement .................................... 393 9. Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 394

9 .1. Reinsemination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395 9.2. Embryo Banking ........................................... 395

10. Early Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 395 10.1. Kinetics and Morphology . . . . . . . . . . . . . . . .. . . . . . . . . . . . . .. .. .. 395 10.2. Cortical Activation and the Block to Polyspermy ................ 396 10.3. Maternal and Zygotic Control of Development .................. 396

11. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 397

Part Ill NEW APPROACHES FOR STUDYING MAMMALIAN GAMETES

21 Micromanipulation of Mammalian Gametes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403 Kristen A. Ivani and George E. Seidel, Jr.

1. Sperm-Centered Approaches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 403 1.1. Placing Gametes in Close Apposition . . . . . . . . . . . . . . . . . . . . . . . . . . . 403 1.2. Manipulation of the Zona Pellucida for Assisted Fertilization ........ 404 1.3. Sperm Microinjection ........................................ 406 1.4. Transgenic Animals from DNA Adsorbed to Sperm ................ 410

2. Oocyte-Centered Approaches ....................................... 410 2.1. Physical Activation of Oocytes with Micropipets . . . . . . . . . . . . . . . . . . 410 2.2. Removal of Chromosomes from Oocytes ......................... 411 2.3. Oocyte-Oocyte Fusion ....................................... 411 2.4. Fusion of Karyoplasts with Oocytes (Nuclear Transplantation) ....... 413 2.5. Injection of Mitochondria and Chromosomes ..................... 416

3. Closing Comments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 417 4. References ...................................................... 417

22 The Use of Molecular Biology to Study Sperm Function ................... 423 Erwin Goldberg

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423 2. Sperm Peptides Involved in Fertilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . 423 3. Testis-Specific Gene Expression ................................... 425 4. Lactate Dehydrogenase C4 Transcription and Translation ............... 426 5. Transcriptional Regulation of Testis-Specific Genes .................... 428 6. Translational Control during Spermatogenesis . . . . . . . . . . . . . . . . . . . . . . . . 431 7. Developmentally Regulated Gene Transcripts . . . . . . . . . . . . . . . . . . . . . . . . . 431 8. Stage-Specific mRNA Levels ...................................... 432 9. Conclusion and Summary . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 433

10. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 433

23 Use of Molecular Biology to Study Development and Function of Mammalian Oocytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 437 Debra 1 Wolgemuth

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 437 2. General Strategies to Identify Genes Expressed during Mammalian

Oogenesis ...................................................... 437 3. Particular Problems of Molecular Analysis of Mammalian Oocyte Gene

Expression and Recent Advances to Circumvent These Difficulties . . . . . . . . 440 3 .1. The Biology of Mammalian Oogenesis Complicates Studying Gene

Expression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440 3.2. Recent Technological Advances that Facilitate Molecular

Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 440 4. Approaches to Identify Function . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 442

4.1. Introduction to Genetic Strategies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 442 4.2. Negative Interference . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 443 4.3. Positive or Gain-of-Function Mutations .......................... 445

5. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 446

Index ............................................................. 449