Neuronal Development PDF
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Neuronal Development CURRENT TOPICS IN NEUROBIOLOGY Series Edi lor Samuel H. Barondes Professor of Psychilliry School of Medicine Universihj of Cillifomill, Sml Diego Lil Jolla, Clllifomill Tissue Culture of the Nervous System Edited by Gordon Sato Neuronal Recognition Edited by Samuel H. Barondes Pep tides in Neurobiology Edited by Harold Gainer Neuronal Development Edited by Nicholas C. Spitzer Neuroimmunology Edited by Jeremy Brockes A continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediatedly upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher. Neuronal Development Edited by Nicholas C. Spitzer University of California, San Diego La Jolla, California PLENUM PRESS • NEW YORK AND LONDON Library of Congress Cataloging in Publication Data Main entry under title: Neuronal development. (Current topics in neurobiology) Includes bibliographical references and index. 1. Developmental neurology. I. Spitzer, Nicholas C. II. Series. [DNLM: 1. Ner· vous system-Embryology. 2. Nervous system-Growth and development. WI CU82P v. 4/WL 0101 N493] QP363.5.N49 591.3'34 82-3693 ISBN-13: 978-1-4684-1133-1 e-ISBN-13: 978-1-4684-1131-7 AACR2 DOl: 10.1007/978-1-4684-1131-7 © 1982 Plenum Press, New York Softcover reprint of the hardcover 1st edition 1982 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 Cont ribu tors KATE F. BARALD Department of Anatomy and Cell Biology University of Michigan Medical School Ann Arbor, Michigan DARWIN K. BERG Department of Biology University of California, San Diego La Jolla, California SETH S. BLAIR Department of Molecular Biology University of California, Berkeley Berkeley, California W. MAXWELL COWAN Salk Institute for Biological Studies San Diego, California JOHN S. EDWARDS Department of Zoology University of Washington Seattle, Washington THOMAS E. FINGER Department of Anatomy University of Colorado Medical Center Denver, Colorado v vi Contributors MURRAY S. FLASTER Department of Biological Sciences Columbia University New York, New York COREY S. GOODMAN Department of Biological Sciences Stanford University Stanford, California MARCUS JACOBSON Department of Anatomy School of Medicine University of Utah Salt Lake City, Utah PAUL C. LETOURNEAU Department of Anatomy University of Minnesota Minneapolis, Minnesota EDUARDO R. MACAGNO Department of Biological Sciences Columbia University New York, New York JOHN PALKA Department of Zoology University of Washington Seattle, Washington ROBERT S. SCHEHR Department of Biological Sciences Columbia University New York, New York GUNTHER S. STENT Department of Molecular Biology University of California, Berkeley Berkeley, California D AVID C. V AN ESSEN Division of Biology California Institute of Technology Pasadena, California Contributors vii DAVID A. WEISBLAT Department of Molecular Biology University of California, Berkeley Berkeley, California SAUL 1. ZACKSON Department of Molecular Biology University of California, Berkeley Berkeley, California Foreword Studies of simple and emerging systems have been undertaken to un derstand the processes by which a developing system unfolds, and to understand more completely the basis of the complexity of the fully formed structures. The nervous system has long been particularly in triguing for such studies, because of the early recognition of a multitude of distinctly differentiated states exhibited by nerve cells with different morphologies. Anatomical studies suggest that one liver cell may be very like another, but indicate that neurons come in a remarkable di versity of forms. This diversity at the anatomical level has parallels at the physiological and biochemical levels. It is becoming increasingly easy to characterize the different cellular phenotypes of neurons. The repeatability with which these phenotypes are expressed may account in part for the specificity and reliability with which neurons form con nections, and it has allowed precise description of the first appearance and further development of the differentiated characteristics of individ ual neurons from relatively undifferentiated precursor cells. This rep resents a major advance over our knowledge of development at the level of tissues, and makes it feasible to define and address questions about the underlying molecular mechanisms involved. Central to these advances has been the clear recognition that there is no single best preparation for the study of neuronal development. Furthermore, it has become evident that no single technique can tell us all we want to know. As this volume demonstrates, a multitude of techniques, many of them developed only recently, are being brought to bear on a wide variety of preparations. The breadth of the approaches has not only advanced our knowledge rapidly, but has simultaneously thrown into relief the similarities and divergences found among different nervous systems, potentially aiding in the recognition of general principles. ix x Foreword The fundamental question that the authors have addressed is "How does the nervous system acquire its differentiated state?" While each chapter approaches this from a different perspective, there are several common themes. The first of these is to ask, "What is the cell lineage or mitotic ancestry of particular neurons?" Several ingenious methods have been devised that permit the tracing of cell lineages. The answer to this question frames the next, which is "What is the role of cell lineage in the differentiation of particular cells? What are the relative contri butions of the cytoplasm and its interaction with the genome, versus the contributions of the environment?" A second major theme is to ask, "What are the rules and the underlying molecular mechanisms that give rise to differentiated states, such as extended neurites or specific, sta bilized synapses? What are the constraints on the normal outcome of development, and what macromolecules play roles in the expression of neuronal phenotypes?" Implicit throughout all of the authors' efforts is a concern with developing working hypotheses, or explicitly devising testable models, that shape the course of further experimentation. The first five chapters are concerned with defining the lineage of the nervous system or of specific nerve cells in different organisms. Stent, Weisblat, Blair and Zacks on have injected horseradish peroxidase or a fluorescently labeled D-amino acid peptide (not subject to digestion by intracellular proteases) into identified blastomeres of the leech, and examined the distribution of label to their progeny. In this system cell lineage appears to be a major determinant of cell fate, since ablation of specific blastomeres leads to the absence of their progeny; no replace ment by progeny of other cells occurs. Jacobson has used the horseradish peroxidase tracer to evaluate the role of lineage in a vertebrate nervous system; his results indicate that ablation of small numbers of identified blastomeres causes no deficit in the development of neurons to which they normally give rise, and that some regulation occurs in the devel opment of the frog embryo. He is led to conclude, however, that there are larger regions (that he terms compartments) in early embryos, which are committed from early stages to form whole regions of the nervous system; removal of all the cells in a compartment results in the absence of cellular structures they normally generate. A provocative theory is presented, supported by his experimental results, which directly chal lenges the organizer concept of Spemann and Mangold and explains the organization of the eNS by the early specification of compartments. Barald has used a different probe to study the development of chick ciliary ganglion neurons. Monoclonal antibodies recognizing cell sur face components of the neurons have been found to recognize a small proportion of the neural crest cells from which they are derived, as well. Foreword xi This finding raises the possibility of using immunological methods to map neuronal lineage; the role of lineage in development can then be assessed by complement-mediated ablations of cells at different stages in the early embryo. Goodman has focused on an invertebrate with a meroblastic cleavage that permits separation of the embryo from its associated yolk; it has been possible to make direct observations of mitotic ancestry in the grasshopper nervous system, by microscopic examination of living embryos of increasing age, comparable to the studies of developing nematodes. A role for lineage in development of this nervous system is suggested by the observation that all of the prog eny of one neuroblast come to contain the same neurotransmitter. Palka has employed a genetic analysis of Drosophila to assess the role of the genome (and thus lineage) in directing neuronal development. Studies of pathways followed by outgrowing neurites in homeotic mutants sug gest that some cuticular mutations do not affect the sensory axons, which develop normal projections in spite of the altered environment. Furthermore, sensory fibers ignore the classical compartment bounda ries in the periphery, as they establish their paths, although the opposite result obtains in the CNS; the dominant guiding factors seem to be different for these two regions. These five chapters detail some of the most imaginative approaches to understanding the role of lineage in neuronal development. The work of these investigators, and others not included here, indicates that the relative contribution depends not only on the embryo studied but on the stage of development as well. Five chapters are concerned with neurite extension and pathway formation. This typical feature of neuronal differentiation has received much attention because its characterization is straightforward, although its determinants may be complex. Three authors provide convergent evidence for a role of early developing pioneer fibers in directing sub sequent neuronal outgrowth. Edwards' studies of development of the cercal nerve in the cricket are the most direct. Laser ablations of the peripheral pioneer cell bodies lead to disorganization of the ingrowing sensory axon bundles, when made at early stages; after pioneer tracts are established, the lesions are without effect. Goodman describes the earliest outgrowth of neurites in the grasshopper CNS, from midline precursor cells; since these are the first to lay down axonal pathways, which are followed by other outgrowing neurites, they appear to serve the role of pioneers. Palka is led to a similar conclusion for the devel opment of peripheral sensory fiber pathways in Drosophila. Moreover, Flaster, Macagno and Schehr, in their investigations of the development of the visual system of the crustacean Daphnia, provide evidence for substrate guidance of axonal growth by a glial cell column; destruction
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