Table Of ContentGASTRULATION
Movements, Patterns, and Molecules
BODEGA MARINE LABORATORY
MARINE SCIENCE SERIES
Series Editor: James S. Clegg
Bodega Marine Laboratory
University of California, Davis
Bodega Bay, California
GASTRULATION: Movements, Patterns, and Molecules
Edited by Ray Keller, Wallis H. Clark, Jr., and Frederick Griffin
INVERTEBRATE HISTORECOGNITION
Edited by Richard K. Grosberg, Dennis Hedgecock, and Keith Nelson
MECHANISMS OF EGG ACTIVATION
Edited by Richard Nuccitelli, Gary N. Cherr, and Wallis H. Clark, Jr.
GASTRULATION
Movements, Patterns, and Molecules
Edited by
Ray Keller
University of California, Berkeley
Berkeley, California
Wallis H. Clark, Jr.
and
Frederick Griffin
Bodega Marine Laboratory
University of California, Davis
Bodega Bay, California
Plenum Press • New York and London
Library of Congress Cataloging in Publication Data
Bodega Marine Science Colloquium on Gastrulation: Movements, Patterns, and Molecules (3rd:
1990: Bodega Bay, Calif.)
Gastrulation: movements, patterns, and molecules / edited by Ray Keller, Wallis H. Clark,
J r., and Frederick Griffin.
p. em. -(Bodega Marine Laboratory marine science series)
"Proceedings of the Third Bodega Marine Science Colloquium on Gastrulation: Movements,
Patterns, and Molecules, held September 6-8,1990, in Bodega Bay, California.
Includes bibliographical references and index.
1. Gastrulation-Congresses. I. Keller, Ray. II. Clark, Wallis H. III. Griffin, Frederick. IV.
Ti tie. V. Series.
QL955.B64 1990 91-38428
59I.3'3-dc20 CIP
Cover: Transverse sections through embryos (stained with anti-twist antibodies) depicting four stages of
mesoderm invagination and internalization (dorsal is up). Top left: Embryo at the completion of cel
lularization. Top right: Early stage of ventral furrow formation. The apical (outer) surfaces of the twisl
expressing cells have become smooth, and the nuclei of the central 8-10 cells have begun to migrate away
from the apical cell surface. Bottom left: The apical sides of the central cells have constricted, and the
surface of the ventral epithelium is beginning to ident. Bottom right: The central cells have invaginated
completely, and the peripheral cells are following them into the furrow.
Proceedings of the Third Bodega Marine Science Colloquium on Gastrulation: Movements, Patterns,
and Molecules, held September 6-8, 1990, in Bodega Bay, California
ISBN-13: 978-1-4684-6029-2 e-ISBN-13: 978-1-4684-6027-8
DOl: 10.1007/978-1-4684-6027-8
© 1991 Plenum Press, New York
A Division of Plenum Publishing Corporation
233 Spring Street, New York, N.Y. 10013
Softcover reprint of the hardcover I st edition 1991
All righ ts 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
Brigitte Angres Douglas W. DeSimone
Max Planck Institute for Dept. of Anatomy and Cell Biology
Developmental Biology University of Virginia
Spemannstrasse 35 Box 439, Health Sciences Ctr.
D-74 00 Tubingen Charlottesville, Virginia 22908
Federal Republic of Germany
Tabitha Doniach
Jean-Claude Boucaut Department of Molecular and
Laboratoire de Biologie Experimentale Cell Biology
URA-CNRS-1135 University of California, Berkeley
Universitie Pierre et Marie Curie Berkeley, California 94720
9, Quai Saint-Bernard 75005
Paris, France Charles A. Ettensohn
Department of Biological Sciences
Jonathan Cooke Carnegie Mellon University
Laboratory of Embryogenesis 4400 Fifth Avenue
National Institute for Pittsburgh, Pennsylvania 15213
Medical Research
The Ridgeway, Mill Hill Rachael D. Fink
London, NW7 lAA, United Kingdom Department of Biological Sciences
Mount Holyoke College
Michael Costa South Hadley, Massachusetts 01075
Molecular Biology Department
Princeton University Nikolaos C. George
Princeton, New Jersey 08544 Department of Molecular and
Cell Biology
Thierry Darribere University of California, Berkeley
Universite Pierre et Marie Curie Berkeley, California 94720
Laboratorie de Biologie Experimentale
URA-CNRS-1135 John Gerhart
9, Quai Saint-Bernard 75005 Department of Molecular and
Paris, France Cell Biology
University of California, Berkeley
Michel Delarue Berkeley, California 94720
Universite Pierre et Marie Curie
Laboratorie de Biologie Experimentale Koichiro Hashimoto
URA-CNRS-1135 Division of Developmental Biology
9, Quai Saint-Bernard 75005 Meiji Institute of Health Science
Paris, France 540 Naruda, Odawara 250, Japan
v
vi Contributors
Jonathan J. Henry Maria Leptin
Department of Cell and Max Planck Institute for
Structural Biology Developmental Biology
University of Illinois Spemannstrasse 35
Urbana, Illinois 61801 D-7400 T-a.bingen
Federal Republic of Germany
James E. Howard
Laboratory of Embryogenesis David R. McClay
National Institute for Department of Zoology
Medical Research Duke University
The Ridgeway, Mill Hill Durham, North Carolina 27706
London NW7 lAA, United Kingdom
Martina Nagel
William R. Jeffery Max Planck Institute for
Bodega Marine Laboratory Developmental Biology
University of California, Davis Spemannstrasse 35
P.O. Box 247 D-7400 T-a.bingen
Bodega Bay, California 94923 Federal Republic of Germany
Kurt E. Johnson Norio Nakatsuji
Department of Anatomy Division of Developmental Biology
The George Washington University Meiji Institute of Health Science
Medical Center 540 Naruda
2300 I Street N.W. Odawara, 250 Japan
Washington, D.C. 20037
George Oster
Ray Keller Departments of Molecular and Cell
Department of Molecular and Biology and Entomology
Cell Biology 201 Wellman Hall
University of California, Berkeley University of California, Berkeley
Berkeley, California 94720 Berkeley, California 94720
Oded Khaner RudolfRaff
Department of Molecular and Institute for Molecular and
Cell Biology Cellular Biology, and
University of California, Berkeley Department of Biology
Berkeley, California 94720 Indiana University
Bloomington, Indiana 47405
Mary Constance Lane
Department of Molecular and David G. Ransom
Cell Biology Dept. of Anatomy and Cell Biology
University of California, Berkeley University of Virginia
Berkeley, California 94720 Bos 439, Health Sciences Ctr.
Charlottesville, Virginia 22908
Contributors vii
Jean-Francois Riou Michael Solursh
Laboratoire de Biologie Experimentale Department of Biology
URA-CNRS 1135 University of Iowa
Universitie Pierre et Marie Curie Iowa City, Iowa 52242
9, Quai Saint-Bernard 75005
Paris, France Claudio D. Stern
Department of Human Anatomy
University of Oxford
Gary C. Schoenwolf
South Parks Road
Department of Anatomy Oxford OX1 3QX, United Kingdom
School of Medicine
University of Utah Ronald Stewart
Salt Lake City, Utah 84132
Department of Molecular and
Cell Biology
University of California, Berkeley
Andreas Selchow
Berkeley, California 94720
Max Planck Institute for
Developmental Biology
Cornelia Stoltz
Spemannst.rasse 35
Max Planck Institute for
D-74 00 To.bingen
Developmental Biology
Federal Republic of Germany
Spemannstrasse 35
D-7400 Tubingen
Federal Republic of Germany
De Li Shi
Laboratoire de Biologie Experimentale
Dari Sweeton
URA-CNRS-1135
Molecular Biology Department
Universitie Pierre et Marie Curie
Princeton University
9, Quai Saint-Bernard 75005
Princeton, New Jersey 08544
Paris, France
Karen Symes
John Shih Department of Cell and
Department of Molecular and Molecular Biology
Cell Biology 385 LSA
University of California, Berkeley University of California, Berkeley
Berkeley, California 94720 Berkeley, California 94720
J.P. Trinkaus
Jim C. Smith Department of Biology
Laboratory of Embryogenesis Yale University
National Institute for New Haven, Connecticut 06511
Medical Research and
The Ridgeway, Mill Hill Marine Biological Laboratory
London NW7 lAA, United Kingdom Woods Hole, Massachusetts 02543
viii Contributors
Madeleine Trinkaus Paul Wilson
Department of Biology Department of Biochemistry and
Yale University Molecular Biology
New Haven, Connecticut 06511 Harvard University
and Cambridge, Massachusetts 02138
Marine Biological Laboratory
Woods Hole, Massachusetts 02543 Fred Wilt
Department of Molecular and
Cell Biology
371 LSA
University of California, Berkeley
Michael Weliky Berkeley, California 94720
Group in Neurobiology
University of California, Berkeley Rudolf Winklbauer
Berkeley, California 94720 Max Planck Institute for
Developmental Biology
Spemannstrasse 35
D-74 00 Tl1bingen
Federal Republic of Germany
Eric Wieschaus
Department of Biology Gregory A. Wray
Guyot Hall Friday Harbor Laboratories
Princeton University University of Washington
Princeton, New Jersey 08544-1003 Friday Harbor, Washington 68250
PREFACE
Gastrulation is a fundamental process of early embryonic development. It involves
virtually every aspect of cell and developmental biology and results in the formation of
fundamental structural elements around which a developing animal's body plan is
organized. As such it is not only an important process, but also one that is complicated
and not easily dissected into its component parts. To understand the mechanisms of
gastrulation one must acknowledge that gastrulation is fundamentally a biomechanical
process (that is, a problem of cells generating forces in a three dimensional array,
patterned in space and time such that appropriate tissue movements are executed).
Three intertwined questions emerge: what cell activities generate forces, how are these
cell activities patterned in space and time, and how are the resulting forces harnessed
in three dimensional domains? To address these issues it is important to define and
characterize regional cell behaviors and to learn how they are patterned in the egg
and/ or by subsequent cell and tissue interactions. At the biochemical level, what are
the cellular and extracellular molecules that control cell behavior? Finally, how are
specific patterns of cellular activity integrated to produce tissue behavior? The task of
answering the above questions, an immense task in itself, is compounded by the fact
that the morphogenetic movements of gastrulation and their underlying mechanisms
vary between different organisms. The third Bodega Marine Science Colloquium
attempted to examine gastrulation in a number of vertebrate and invertebrate groups
and to specifically address the issue of how these early developmental processes appear
in organisms at different phylogenetic levels. In addition to phylogenetic considerations
we attempted to choose participants who use diverse scientific approaches. Our attempt
at the above integration is presented in this volume, and though not comprehensive,
we believe it is a succesful and timely treatment of the subject. Each of the authors
focuses on his/her particular questions and research directions; however, common
themes and approaches are evident throughout the book and we urge the reader to
consider each chapter with this in mind.
The third Bodega Marine Science Colloquium was held at the Bodega Marine
Laboratory in September of 1990. The three day conference was attended by over 60
people and featured 20 invited speakers, prominent investigators in the field of
gastrulation, whose contributions constitute this volume. Both the success of the
conference and the compilation of contributed papers into this volume are the result
of efforts on the part of many who deserve recognition. The success of the conference
itself is due in large part to the efforts of Trisha Pedroia and Vicki Milam who
coordinated and oversaw the events and sessions. Eleanor Uhlinger, Bodega Marine
Laboratory Librarian, helped proof the manuscript. Diane Cosgrove is responsible for
the final package; she formed the camera ready manuscript that is this book. We also
thank the remainder of the staff of the Bodega Marine Laboratory for their help and
hospitality.
ix
WE GRATEFULLY ACKNOWLEDGE
THE FOLLOWING SOURCES OF FINANCIAL FUNDING
* California Sea Grant College Program *
* Bodega Marine Laboratory *
* Society for Developmental Biology *
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