Table Of ContentUltrastructure of Human Gametogenesis and Early Embryogenesis
ELECTRON MICROSCOPY IN BIOLOGY
AND MEDICINE
Current Topics in Ultrastructural Research
SERIES EDITOR: P. M. MOTTA
Already published in this series
Vol. 1 Motta, P. M. (ed.): Ultrastructure of Endocrine Cells and Tissues.
ISBN: 0-89838-568-7.
Vol. 2 Van Blerkom, J. and Motta, P. M. (eds.): Ultrastructure of Reproduction: Gametogenesis,
Fertilization, and Embryogenesis. ISBN: 0-89838-572-5.
Vol. 3 Ruggeri, A. and Motta, P. M. (eds): Ultrastructure of the Connective Tissue Matrix. ISBN:
0-89838-600-4
Vol. 4 Motta, P. M., Fujita, A. (eds.): Ultrastructure of the Digestive Tract. ISBN: 0-89838-893-7.
Series Editor
P. M. MOTTA, Department of Anatomy, Faculty of Medicine, University of Rome, Viale R Elena 289,
00161 Rome, Italy
Advisory Scientific Committee
D.J. ALLEN (Toledo, Ohio, USA)/ A. AMSTERDAM (Rehovot, Israel)/P.M. ANDREWS
(Washington, DC, USA) / L. BJERSING (Umea, Sweden) / I. BUCKLEY (Canberra, Australia) / F.
CARAMIA (Rome, Italy) / A. COIMBRA (Porto, Portugal) II. DICULESCU (Bucharest, Romania) /
L.J.A. DIDIO (Toledo, Ohio, USA)/M. DVORAK (Brno, Czechoslovakia)/H.D. FAHIMI (Heidel
berg, FRG)/H.V. FERNANDEZ-MORAN (Chicago, III., USA)/H. FUJITA (Osaka, Japan)/T.
FUJITA (Niigata, Japan)/E. KLIKA (Prague, Czechoslovakia)/L.C.U. JUNQUEIRA (Sao Paulo,
Brazil)/RG. KESSEL (Iowa City, Iowa, USA)/F.N. LOW (New Orleans, Louisiana, USA)/B.L.
MUNGER (Hersey, Pa., USA)/T. MURAKAMI (Okayama, Japan)/O. NILSSON (Uppsala,
Sweden)/K.R PORTER (Boulder, Colo., USA)/ J.A.G. RHODIN(Tampa,Fla., USA)/K. SMETANA
(Prague, Czechoslovakia) / K. TANA KA (Y onago, Japan) / K. T ANIKAW A (Kurume, Japan) / I.
TORO (Budapest, Hungary)/J. VAN BLERKOM (Boulder, Colo., USA)
Ultrastructure of Human Gametogenesis
and Early Embryogenesis
edited by
Jonathan Van Blerkom Ph.D.
Department of Molecular, Cellular and Developmental Biology,
University of Colorado, Boulder, Colorado
and
Reproductive Genetics in Vitro, Denver, Colorado
and
Pietro M. Motta Ph.D., M.D.
Department of Anatomy, University of Rome, Rome, Italy
111....
"
1989 Kluwer Academic Publishers
BOSTON DORDRECHT LONDON
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for the United States and Canada: Kluwer Academic Publishers
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bution Centre, P.O. Box 322, 3300 AH Dordrecht, The
Netherlands
Library of Congress Cataloging in Publication Data
Ultrastructure of human gametogenesis and early embryo
genesis I edited by Jonathan Van Blerkom, Pietro Motta.
p. cm. - (Electron microscopy in biology and
medicine)
Includes bibliographies and index.
ISBN-13: 978-1-4612-8982-1 e-ISBN-13: 978-1-4613-1749-4
001: 10.1007/978-1-4613-1749-4
1. Gametogenesis. 2. Embryology. 3. Germ cells -
Ultrastructure.
I. Van Blerkom, Jonathan, 1947- II. Motta,PietroM.
III. Series.
[DNLM: 1. Embryo - ultrastruct. 2. Gametogenesis.
3. Oocytes-ultrastruct. QS 604 U47j
QM60l.U45 1988
612'.6 - dc 19
DNLM/DLC
for Library of Congress 88-15890
CIP
© 1989 By Kluwer Academic Publishers, Boston.
Softcover reprint of the hardcover 1st edition 1989
All rights reserved. No part of this publication may be repro
duced, stored in a retrieval system, or transmitted in any form
or by any means, mechanical, photocopying, recording, or
otherwise, without the prior written permission of the publisher,
Kluwer Academic Publishers, 101 Philip Drive, Assinippi Park,
Norwell, MA 02061
Preface
In the last few years, the adoption and worldwide proliferation of clinical procedures for medically
assisted conception have been associated with the examination and analysis of spermatozoa, oocytes and
early embryos under a variety of in vivo and in vitro conditions. These analyses have enabled correlations
to be made between the behavior of gametes, the pattern of early embryonic development and the
initiation of a normal pregnancy. Collectively, the findings have not only enormously increased our
understanding of the process of early human development, but also have provided new insights into the
origin and causes of reproductive failure in man.
The research presented in this volume describes recent results derived from the study of normal and
abnormal patterns of human spermatogenesis, oogenesis and early embryogenesis. The chapters discuss
aberrations in morphodynamic and morphophysiological processes that have clinical relevance in human
infertility and conception. Two of the chapters describe, respectively, the basic research that allows the
cryopreservation of human oocytes and embryos, and the development of in vitro systems that permit the
study of cell differentiation and interaction during the peri-implantation period. When relevant, each
chapter extrapolates findings from in vitro experimentation to the comparable situation that is observed
in vivo.
The rapid clinical application of basic research findings in the treatment of human infertility under
scores the necessity of having a comprehensive and fundamental understanding of the morphogenetic and
morphophysiological bases of normal and abnormal gametogenesis and embryogenesis. This volume is
intended to provide such information, especially as it relates to the causes and treatments of infertility.
Because each chapter is a discussion of the current state of knowledge, the authors indicate both where
information is still incomplete and what specific research is required to expand our understanding of the
origins of infertility and early developmental failure.
1. VAN BLERKOM and P.M. MOTTA
Contents
Preface by the editors ................................................................. v
Contributing authors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IX
1. Mammalian spermatogenesis and its disorders in man by C. DeMartino, S. Francavilla, A.
Fabbrini & L. Accinni ............................................................ 1
2. Life history of the human female germ cell: Ultrastructural aspects by S. Makabe, S.A.
Nottola, & P.M. Motta. . . . . . . .. . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 33
3. Ultrastructure of fetal ovary including oogenesis by H. Wartenberg ...................... 61
4. The ovary and ovulation: A three-dimensional ultrastructural study by G. Familiari, S.
Makabe, & P.M. Motta ........................................................... 85
5. Developmental failure in human reproduction associated with preovulatory oogenesis and
preimplantation embryogenesis by J. Van Blerkom . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
6. Effects of culture and cryopreservation on human oocyte and embryo ultrastructure and
function by A.H. Sathananthan & A. Trounson . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 181
7. In vitro studies of the peri-implantation phase of human embryos by S. Lindenberg & P.
Hyttel .......................................................................... 201
Index .............................................................................. 213
Contributing authors
Dr. L. Accinni, Regina Elena Institute for Cancer Research, Viale R. Elena, Rome, Italy
Prof. C. De Martino, Regina Elena Institute for Cancer Research, Viale R. Elena, Rome, Italy
Prof. M. Fabbrini, Regina Elena Institute for Cancer Research, Viale R. Elena, Rome, Italy
Prof. G. Familiari, Department of Anatomy, University of Rome "LA SAPIENZA", Rome, Italy
Prof. S. Francavilla, Regina Elena Institute for Cancer Research, Viale R. Elena, Rome, Italy
Prof. P. Hytell, Dept. of Obstetrics and Gynecology, Rigshospitalet, University of Copenhagen,
Blegdamsvej 9, DK-2100, Denmark
Dr. S. Lindenberg, Chromosome Lab 4041, Dept. of Obstetrics and Gynecology, Rigshospitalet,
University of Copenhagen, Blegdamsung 9, Denmark
Dr. S. Makabe, Dept. of Obstetrics and Gynecology, Toho Univ. School of Medicine, 6-11-1
Ohmorinishu 6 Chome, Tokyo, 143 Japan
Prof. P.M. Motta, Dept. of Anatomy, University of Rome "LA SAPIENZA", Rome, Italy
Dr. S. Nottola, Department of Anatomy, University of Rome "LA SAPIENZA", Rome, Italy
Dr. A.H. Sathananthan, Lincoln School of Health Sciences, LaTrobe University, 625 Swanston Street,
Carlton, Victoria, 3053 Australia
Prof. A. Trounson, Centre for Early Human Development, Monash Medical Centre, Clayton Road,
Clayton, Victoria 3168, Australia
Prof. J. Van Blerkom, Dept. of Molecular, Cellular and Developmental BioI. University of Colorado,
Boulder, Colorado USA
Prof. H. Wartenberg, Anatomisches Institut Der Rheinischen Friedrich-Wilhelms Universitat, Nussalle
10, D 5300 Bonn 1, Federal Republic of Germany
Ultrastructure of Human Gametogenesis and Early Embryogenesis
CHAPTER I
Mammalian spermatogenesis and its disorders in man
CESARE DE MARTINO, SANDRO FRANCAVILLA, ALDO FABBRINI, & LIDIA ACCINNI
1. Introduction appear to be alike in morphology with the ex
ception of the chromosome set. The second period
In mammals, spermatogenesis begins at puberty of development occurs when the gonads and sex
and results in the formation of a unique popula begin to diverge. In the course of develop
tion of haploid cells, the spermatozoa. This pro ment, the primordial sex cords appear within the
cess continues throughout the life of the animal inner zone of the male gonad, whereas the outer
and involves the constant renewal of the stem zone thins out and gives rise to the albuginea (Fig.
cells, the spermatogonia. In contrast to oogenesis, I-Id). In the eight-week-old human fetus, the sex
spermatogenesis is a continuous process that pro cords contain the support cells, which are somatic
ceeds without pauses at specific stages of sperm cell precursors of the Sertoti cells, and the pri
development. An exception to this rule is ob mordial germ cells, now known as gonocytes. In
served in mammals with seasonal cycles, such as man, during this period, which is often called pre
the coyote, fox, ground squirrel, and free-ranging spermatogenesis, the gonocytes go through a mi
monkey. During the nonbreeding period for these totic activity intercalated with cell degeneration.
mammals, the seminiferous tubules are almost In addition, a direct interaction between somatic
exclusively composed of Sertoli cells and a single and germ cells occurs. However, this second period
layer of spermatogonia. is not always well-defined and probably does not
exist in many animals in which the process of
spermatogenesis begins almost immediately after
2. Development of male germ cells germ cells become localized in the gonad (1).
Even in those animals in which a pre-spermato
The development of male germ cells may be di genic period occurs, it is difficult to define pre
vided into three main periods. In the first, or ex cisely when it ends and when the third period,
tragonadal period, the so-called primordial germ spermatogenesis proper, begins.
cells are identified in the mammal in the endo
dermal yolk sac and in the hindgut epithelia (see
as review, I). These cells are capable of mitotic 3. Spermatogenesis
divisions and amoeboid movements and rapidly
migrate through the primitive intestine toward The interval between birth and the triggering of
the genital ridge (Figs. I-Ia and b). During their spermatogenesis varies among mammals. In the
migration, the primordial germ cells often follow rat, for example, spermatogenesis begins on the
an aberrant path and acquire an ectopic location fourth postnatal day with the appearance of type
in extragonadal tissues and/or organs (Fig. I-Ic). A spermatogonia, whereas in primates, it com
During this period, the germ cells of both sexes mences several years (three to seven) after birth.
2
