Neural Development Part IEmergence of Specificity in Neural Histogenesis

425 Pages·1980·10.003 MB·English

by  A.A. Moscona and Alberto Monroy (Eds.)

CONTRIBUTORS
MARTIN BERRY MARGARET HOLLYDAY
IRA B. BLACK R. KEVIN HUNT
MARIANNE E. BRONNER-FRASER K. KISHI
J. A. CAMPOS-ORTEGA GARY LYNCH
ALAN M. COHEN E. R. MACAGNO
KEVIN CONWAY PATRICIA McCONNELL
JONATHAN COOKE JACQUES MALLET
W. M. COWAN PAUL H. PATTERSON
KATHARINE FEIOCK LAURI SAXfiN
CHRISTINE GALL JOBST SIEVERS
B. B. STANFIELD
CURRENT TOPICS IN
DEVELOPMENTAL B I O L O G Y
EDITED BY
A. A. MOSCONA ALBERT0 MONROY
DEPARTMENTS OF BIOLOGY AND PATHOLOGY STAZIONE ZOOLOGICA
THE UNIVERSITY OF CHICAGO NAPLES, ITALY
CHICAGO, ILLINOIS
VOLUME 15
NEURAL DEVELOPMENT
PART I
Emergence of Specificity in
Neural Histogenesis
VOLUME EDITOR
R. KEVIN HUNT
THOMAS C. JENKINS DEPARTMENT OF BIOPHYSICS
THE JOHNS HOPKINS UNIVERSITY
BALTIMORE, MARYLAND
1980
ACADEMIC PRESS
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LIST OF CONTRIBUTORS
Numbers in parentheses indicate the pages on which the authors’ contributions begin.
MARTINB ERRYD, epartment of Anatomy, Medical School, University of
Birmingham, Birmingham B15 ZTJ, England (67)
IRA B. BLACKL, aboratory of Developmental Neurology, Department of
Neurology, Cornell University Medical College, New York, New
York 10021 (27)
MARIANNEE . BRONNER-FRASER,T”h omas C. Jenkins Department of
Bwphysics, The Johns Hopkins University, Baltimore, Maryland
21218 (1)
J. A. CAMPOS-ORTEGZAn, stitut fur Biologie III, Albert Ludwigs-
Uniuersitat, 7800 Freiburg im Breisgau, Federal Republic of Ger-
many (347)
ALANM . COHEN,D~.e partment of Cell Biology and Anatomy, The Johns
Hopkins University School of Medicine, Baltimore, Maryland
21205 (1)
KEVINC ONWAYT, homas C.J enkins Department of Biophysics, The
Johns Hopkins University, Baltimore, Maryland 21218 (217)
JONATHACNO OKED, ivision of Developmental Biology, National Insti-
tute for Medical Research, Mill Hill, London NW7 IAA, England
(373)
W. M. COWAN,$D epartment of Anatomy and Neurobiology, Washington
University School of Medicine, St. Louis, Missouri 63110 (103)
KATHARINFEE IOCKT, homas C. Jenkins Department of Biophysics, The
Johns Hopkins University, Baltimore, Maryland 2121 8 (217)
* Present address: Department of Physiology, California College of Medicine, Univer-
sity of California, Irvine, California 91719.
iP resent address: Department of Anatomy and Neurobiology, Washington Univer-
sity School of Medicine, St. Louis, Missouri 63110.
P Present address: The Salk Institute for Biological Studies, P.O. Box 85800, San
Diego, California 92138.
ix
X LIST OF CONTRIBUTORS
CHRISTINEG ALL,*D epartment of Psychobiology, University of Califor-
nia, Irvine, California 91 717 (159)
MARGAREHTO LLYDADYe, partment of Pharmacological and Physiologi-
cal Sciences, The University of Chicago, Chicago, Iilinois 60637
(181)
R. KEVINH UNTT, homas C.J enkins Department OfBiophysics, TheJ ohns
Hopkins University, Baltimore, Maryland 21218 (217)
K. KISHID, epartment of Anatomy and Neurobiology, Washington Uni-
versity School of Medicine, St. Louis, Missouri 63110 (103)
GARYL YNCH,D epartment of Psychobiology, University of California,
Irvine, California 91 71 7 (159)
E. R. MACAGNOD, epartment of Biological Sciences, Columbia Univer-
sity, New York, New York 10027 (319)
PATRICIMA CCONNELLN,e therlands Institute for Brain Research, Ijdijk
28, Amsterdam, The Netherlands (671
JACQUESM ALLETS, ervice de Neurobiologie, Departement de Biologie
Moleculaire, Institut Pasteur, 28 Rue du Docteur Roux, 75724,
Paris Cedex 15, France (41)
PAULH . PATTERSODNe,p artment of Neurobiology, Harvard Medical
School, Boston, Massachusetts 0211 5 (27)
LAURIS AXEND, epartment of Pathology, University of Helsinki, Hel-
sinki, Finland (409)
JOSSSTI EVERDSe,p artment of Neuroanatomy, University of Hamburg,
0-2000 Hamburg 20, Federal Republic of Germany (67)
B. B. STANFIELDD,?e partment of Anatomy and Neurobiology, Washing-
ton University School of Medicine, St. Louis, Missouri 63110 (103)
* Present address: Department of Neurology, School of Medicine, State University of
New York at Stony Brook, Long Island, New York 11794
I-P resent address: The Salk Institute for Biological Studies, P.O.B ox 85800, San
Diego, California 92138.
In the summer of 1977, the Editors of Current Topics in Develop-
mental Biology suggested a special project on neural development. The
hope was for a series of essays that would both evolve naturally from
the past traditions of Current Topics in Developmental Biology and also
would stand as a self-contained set of volumes offering a broad over-
view of neurogenesis. In the years of planning and production, the
project has grown to three volumes. The present collection, “Emer-
gence of Specificity in Neural Histogenesis,” is the first of these three
books. Yet, while the project has grown in scope and a number of addi-
tional contributors have been added to keep abreast of recent develop-
ments, the principal reasons for the volumes have not changed.
Developmental neurobiology has grown in leaps and bounds over
the past decade. Findings from the developing nervous system have
begun to inform on general issues of embryonic development and ought
to be shared with the general community of developmental biologists.
At the same time, as neuroscience has grown into a large interdiscipli-
nary area of scholarship, the need of developmental neurobiologists for
a continuing dialog with other members of the embryological commu-
nity is equally great. Finally, although a number of timely textbooks
have appeared in the area, no broad collection of essays on neural
development was then available.
Our aim in these volumes has been to present a broad panoramic
view of neural development, from the earliest stages of neural induc-
tion through the latest stages of physiological maturation. We have
tried, as well, to represent a broad range of viewpoints. Inevitably,
some topics have been slighted. If any overt prejudice has crept into the
organization of these volumes, it is the belief that most of the major
questions of neural development will ultimately be answered on the
molecular level; but those molecular answers will only be forthcoming
in studies that respect the cellular organization of the nervous system
and that yoke molecular approaches with careful anatomical and phys-
iological characterizations.
xi
xii PREFACE
We are deeply indebted to the staff of Academic Press for their
flexibility in scheduling the production of these volumes. The willing-
ness of Academic Press to bend to meet the busy schedules of our
contributors, and to make adjustments for chapters on areas that grew
in prominence during the period of production, made my task much
more enjoyable. Finally, I would like to thank the contributors them-
selves, who rose to the occasion and who have given the volumes what
enduring value they have.
More than 30 years ago, in a classic article, “Differentiation and
Growth of Nerve Cells and Fibers,” Professor Jean Piatt observed that
if the study of neural development was to have a future, that future lay
in drawing together workers from areas as diverse as biophysics,
neurophysiology, neuroanatomy, and experimental embryology. If the
present volume makes any single statement, it is surely that Professor
Piatt’s vision of the future has been realized.
R. Kevin Hunt
C H A P T E R 1
THE NEURAL CREST: WHAT CAN IT TELL US ABOUT
CELL MIGRATION AND DETERMINATION?
Marianne E. Bronner-Fraser”
THOMAS C. JENKINS DEPARTMENT OF BIOPHYSICS
THE JOHNS HOPKINS UNIVERSITY
BALTIMORE, MARYLAND
and Alan M. Cohen-i.
DEPARTMENT OF CELL BIOLOGY AND ANATOMY
THE JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE
BALTIMORE, MARYLAND
I. Introduction ............................................... .. ... 1
11. Control of Neural Crest Migration and Localization .......... .. ... 4
111. Neural Crest Differentiation ................................ ... .. 15
IV. Conclusion ................................................ ... .. 21
References ................................................ .. 23
1. Introduction
Of all vertebrate structures, the nervous system has perhaps the
greatest cellular diversification and complexity of organization. The
study of developmental neurobiology, therefore, sharply probes the
central issue of embryogenesis; i.e., how does a complex system arise
from a single cell? During development, ectodermal tissue becomes
determined along neuronal lines via contact or “primary induction”
from the roof of the archenteron (Mangold, 1933; Spemann, 1938).
A major problem is how the morphologically indistinguishable stem
cells of the neuroectoderm become progressively determined along
divergent developmental lines such that they give rise to a myriad
of cell types in the mature nervous system. Another question posed
by this system is how the cells migrate to their final locations and
become organized in precise spatial arrays. Once the pattern is com-
posed, what mechanisms govern the establishment of the proper con-
* Present address: Department of Physiology, California College of Medicine, Univer-
sity of California at Irvine, Irvine, California.
.i Present address: Department of Anatomy and Neurobiology, Washington Univer-
sity School of Medicine, St. Louis, Missouri.
1
CURRENT TOPICS IN Copyright 0 1980 by Academic Press, Inc
DEVELOPMENTAL BIOLOGY, Vd 1.5 All right- of reproduction in any form reserved
ISBN 0.12 -153 115-5
2 M. E. BRONNER-FRASER AND A. M. COHEN
nections between neurons and other neurons, as well as between
neurons and their target organs?
The vertebrate neural crest, which is the anlage of the peripheral
nervous system, has become a popular subset of neural development for
the analysis of these problems. The neural crest arises from the
neuroectoderm and migrates extensively along well-defined pathways.
The crest gives rise to diverse and numerous derivatives including
sensory and autonomic ganglia, Schwann sheath cells, chromaffi cells,
melanocytes, cranial cartilage, and many others (Weston, 1970). Un-
like most of the central nervous system, the neural crest is readily
accessible to surgical and biochemical manipulations during both ini-
tial and certain later stages in its development. Because of the tempor-
ally and spatially patterned movements which characterize neural
crest migration and the diversity of crest derivatives, this population of
cells affords a unique opportunity for the study of morphogenesis and
cytodifferentiation.
Like stem cells of the neuroectodenn, neural crest cells appear
morphologically similar at the onset of migration. In the trunk of the
avian embryo, the crest arises on the dorsal side of the embryo as the
neural folds close to form the neural tube. Shortly after formation, the
crest cells migrate away from the neural tube in two directions: either
dorsolaterally just under the ectoderm or ventrally along side the
neural tube (see Fig. 1).T he dorsolateral stream is composed primarily
FIG. 1. Diagram illustrating the normal routes of neural crest migration in the trunk
region of the avian embryo. Cells choosing the ventral (V)p athway localize in three main
areas: (1) the sensory ganglia; (2) the primary sympathetic chain; and (3) the adrenal
gland, aortic plexuses, and some cells of the metanephric mesenchyme. Crest cells follow-
ing the dorsolateral (D) pathway migrate under the ectoderm and become skin melano-
cytes. From Bronner and Cohen (1979).
1. THE NEURAL CREST 3
of presumptive melanocytes. The cells of the ventral stream migrate
between the neural tube and the somites, contributing to the sensory
ganglia, sympathetic ganglia, adrenal medulla, aortic plexus, and
some cells of the metanephric mesenchyme.
What then causes this outwardly homogeneous population of cells
to migrate extensively and give rise to cell types as divergent as
neurons and melanocytes? The neural crest cells may, in fact, be de-
termined prior to migration and undergo “directed’ movements to ap-
propriate final sites. Alternatively, the neural crest could be pluripo-
tent at the onset of migration, migrate in response to environmental
cues, and differentiate according to interactions experienced during or
at the conclusion of migration. Many mechanisms have been suggested
to play a role in crest migration; these include contact guidance and
contact inhibition, specific cell recognition, differential adhesion, and
chemotaxis. Which of these possible mechanisms influences the dis-
tribution and localization of crest cells remains unclear. These are
questions which may be answered using experimental embryological
and cell culture techniques.
We are studying questions of neural crest migration and determina-
tion using a combination of tissue culture and embryological methods
on avian embryos. When neural tubes are explanted in uitro, crest cells
migrate from the dorsal aspect of the neural tube similar to the crest
emigration in uiuo. Cohen and Konigsberg (1975) took advantage of the
natural tendency of crest cells to migrate and developed a technique for
isolating and cloning neural crest cells. After crest cells have migrated
from the neural tube, the tube is scraped away, leaving a monolayer of
mesenchymal crest cells. The cells, after a period of growth, are re-
plated at low densities to establish clones; that is, populations of sister
cells derived from a single precursor. Three types of clones arise under
these conditions: all pigmented cells, all unpigmented cells, and mixed
pigmented and unpigmented cells. To examine the migration and de-
velopmental potential of these cells we have developed a method for
injecting neural crest clones and other cell types back into chick em-
bryos (Bronner and Cohen, 1979). The injected cells are derived from
quail embryos and therefore can be distinguished from those of the
chick hosts (see Section 11). We find that cloned pigment cells and
unpigmented crest cells migrate along the ventral neural crest path-
way when injected in this manner. These clones undergo melanotic and
adrenergic differentiation in uitro (Sieber-Blum and Cohen, 1979) and
in uiuo (Bronner-Fraser et al., 1980). The following discussion reviews
recent data from our laboratory and others relating to migration and
determination of the avian neural crest.