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The Neural Crest, Second Edition The development of an organism from a single cell to a fertilized egg is one of the most marvelous and beautiful of all nature's creations. In the context of a rapidly advancing field of study, this fully revised edition of The Neural Crest contains the most current information about a structure unique to the verte brate embryo and which has only a transient existence in early embryonic life. The neural crest's component cells migrate throughout the embryo and home to specific sites, where they differentiate into a large variety of cell types, including the peripheral nervous system, pigment cells, endocrine cells, and mesenchymal derivatives. The latter provide a large contribution to the verte brate head as it gives rise to nearly all the skull and facial skeleton. The ontogeny of the neural crest embodies the most important issues in develop mental biology, as the neural crest is considered to have played a crucial role in evolution of the vertebrate phylum. Fifteen years ago, research on the neural crest centered on avian and amphi bian embryos. Included are new data that analyze neural crest ontogeny in murine and zebrafish embryos, two species that enable both genetic studies and single-cell analysis. Coverage of recent advances in our understanding of mar kers of neural crest cell subpopulations is also included, and a full chapter is devoted to cell lineage analysis, a field that has also significantly contributed to an understanding of the phenotypic segregation of neural crest cell subpopula tions. Since the first edition, perhaps the major research breakthrough has been the introduction of molecular biology to neural crest research, enabling the elucidation of many molecular mechanisms of neural crest development. These include effects of growth factors and receptors of the neurotrophin family, the endothelin family, bone morphogenetic proteins, etc. Likewise, elucidation of the molecular mechanisms leading to neural crest migration in the embryo characterizes the type of frontline research covered in this revised edition. This book is essential reading for students and researchers in developmental biology, cell biology, and neuroscience. Nicole M. Le Douarin is Professor at the College de France in Paris and Director of the Institute of Cellular and Molecular Embryology of the College de France and CNRS. Chaya Kalcheim is Professor in the Department of Anatomy and Cell Biology at the Hebrew University of Jerusalem-Hadassah Medical School. Developmental and cell biology series SERIES EDITORS Jonathan B. L. Bard, Department of Anatomy, Edinburgh University Peter W. Barlow, Long Ashton Research Station, University of Bristol David L. Kirk, Department of Biology, Washington University The aim of the series is to present relatively short critical accounts of areas of developmental and cell biology where sufficient information has accumulated to allow a considered distillation of the subject. The fine structure of cells, embryology, morphology, physiology, genetics, biochemistry and biophysics are subjects within the scope of the series. The books are intended to interest and instruct advanced undergraduates and graduate students and to make an important contribution to teaching cell and developmental biology. At the same time, they should be of value to biologists who, while not working directly in the area of a particular volume's subject matter, wish to keep abreast of developments relevant to their particular interests. RECENT BOOKS IN THE SERIES 18. C. J. Epstein The consequences of chromosome imbalance: principles, mechanisms and models 0521 25464 7 19. L. Saxen Organogenesis of the kidney 0521 30152 I 20. V. 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Lyndon The shoot apical meristem: its growth and development 0521 40457 6 35. D. Moore Fungal morphogenesis 0521 55295 8 36. N. Le Douarin & C. Kalcheim The neural crest, second edition 0521 62010 4 The Neural Crest Second Edition Nicole M. Le Douarin Institute of Cellular and Molecular Embryology, CNRS and College de France Chaya Kalcheim University of Jerusalem-Hadassah Medical School UCAMBRIDGE V UNIVERSITY PRESS CAMBRIDGE UNIVERSITY PRESS Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sao Paulo, Delhi, Dubai, Tokyo Cambridge University Press The Edinburgh Building, Cambridge CB2 8RU, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridge.org/9780521122252 © Cambridge University Press 1999 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 1999 This digitally printed version 2009 A catalogue record for this publication is available from the British Library Library of Congress Cataloguing in Publication data Le Douarin, N. The neural crest/Nicole M. Le Douarin and Chaya Kalcheim. -2nd ed. p. cm. -(Developmental and cell biology series : 36) Includes bibliographical references and index. 1. Neural crest. I. Kalcheim, Chaya. 1955- . II. Title. III. Series QL938.N484L4 1999 98-53256 573.8'6387 -dc21 CIP ISBN 978-0-521-62010-9 Hardback ISBN 978-0-521-12225-2 Paperback Additional resources for this publication at www.cambridge.org/9780521122252 Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. A mes petits-enfants Adrien, Helena, Antoine et Alexandre Nicole M. Le Douarin To my mother To Avi, Einat and Yoav Chaya Kalcheim Contents Foreword xvii Preface xix General Introduction xxi 1 Methods for Identifying Neural Crest Cells and Their Derivatives 1 1.1 Introduction 1 1.2 Extirpation or in situ destruction of the neural crest 2 1.3 Differential identification of neural crest cells throughout ontogeny 2 1.3.1 Intrinsic markers of neural crest cells 3 1.3.2 Extrinsic markers applied to neural crest precursor cells 9 l.3.3 The quail-chick marker system 10 2 The Migration of Neural Crest Cells 23 2.1 Introduction 23 2.2 Segregation of the neural crest from the neuroepithelium 24 2.2. l Induction of the neural crest 24 2.2.2 Epithelial-mesenchymal transition and the onset of neural crest migration 27 2.3 The cellular basis of neural crest migration 34 2.3.1 Pathways of migration related to fate 34 2.3.2 Similarities and differences in the pathways of migration between different species 38 2.4 The molecular basis of neural crest migration 44 2.4.1 Delayed migration along the subectodermal pathway: transient inhibition or the need for cell specification 45 ix x CONTENTS 2.4.2 Molecular signals controlling segmental migration in the trunk 48 2.5 Conclusions 58 3 The Neural Crest: A Source of Mesenchymal Cells 60 3.1 Historical overview 60 3.1.1 The notion of mesectoderm 60 3.1.2 Pioneering work on the amphibian embryo and lower vertebrates 61 3.1.3 The modern era 65 3.2 The fate of the mesectodermal cells in the head 65 3.2.1 Labeling the cephalic neural crest cells in the avian embryo 66 3.2.2 Derivatives of the cephalic neural crest 68 3.2.3 Analysis of the cephalic crest cell migration and fate in mammalian embryos 77 3.2.4 The fate of the anterior cephalic neural fold and neural plate corresponding to the prosencephalon studied in the avian embryo 82 3.3 Relationships between the cephalic paraxial mesoderm and the neural crest-derived mesectoderm 85 3.3.1 The contribution of the paraxial cephalic mesoderm to the skull 85 3.3.2 Analogies and differences between cephalic and truncal paraxial mesoderm 87 3.3.3 The notion of prechordal and chordal skull 90 3.4 Segmental nature of the brain primordium: molecular implications for neural crest development 91 3.4.1 The cellular basis of hindbrain segmentation 92 3.4.2 Molecular basis of hindbrain segmentation 93 3.4.3 Forebrain and midbrain segmentation 106 3.5 Relationships between brain segmentation and the development of the cranial, facial, and visceral skeleton 107 3.5.l Evidence for the contribution of each rhombomere to the branchial arches as revealed by Oil labeling 107 3.5.2 Determination of the long-term fate of neural crest cells of mesencephalic and rhombomeric origin 110 3.5.3 Regeneration capabilities of the cephalic neural crest 115 3.5.4 Patterning capacities of the neural crest 119 3.6 Genetic analysis of the development of the mesectodermal derivatives of the neural crest: roles of Hox genes and retinoic acid (RA) 124 3.6.1 Disruption of certain Hox genes of the first paralogous groups interferes with the development of neural crest-derived branchial arches structures 124