Advances in Anatomy Embryology and Cell Biology
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1 Advances in Anatomy Embryology and Cell Biology Vol. 150 Editors F. Beck, Melbourne D. Brown, Charlestown B. Christ, Freiburg W. -Kriz, Heidelberg E. Marani, Leiden R. Putz, Munchen Y. Sano, Kyoto T. H. Schiebler, Wurzburg K. Zilles, Dusseldorf
2 Springer Berlin Heidelberg New York Barcelona Budapest Hong Kong London Milan Paris Singapore Tokyo
3 c. Lambert de Rouvroit A. M. Goffinet The Reeler Mouse asa Model of Brain Development With 30 Figures and 3 Tables Springer
4 CATHERINE LAMBERT DE ROUVROIT, Ph. D. ANDRE M. GOFFINET, M. D, PH. D. Neurobiology Unit University ofnamur Medical School 61, Rue de Bruxelles 5000 Namur Belgium ISBN-13: Library of Congress-Cataloging-in-Publication-Data Lambert de Rouvroit, C. (Catherine), The reeler mouse as a model of brain development / C. Lambert de Rouvroit and A.M. Goffinet. p. cm. - (Advances in anatomy, embryology, and cellbiology, Vol. 150) Includes bibliographical references and index. ISBN -13: e-isbn -13: DOl: / Developmental neurobiology. 2. Neurogenetics. 3. Mice-Molecular genetics. 4. Developmental genetics. I. Goffinet, A. II. Series QL801.E67 Vol. 150 [QP363.5] 571 s-dc '61935] This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other way, and storage in data banks. Duplication of this publication or parts thereof is permitted only under the provisions of the German Copyright Law of September 9, 1965, in its current version, and permission for use must always be obtained from Springer-Verlag. Violations are liable for prosecution under the German Copyright Law. Springer-Verlag Berlin Heidelberg 1998 The use of general descriptive names, registered names, trademarks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. Product liability: The publishers cannot guarantee the accuracy of any information about dosage and application contained in this book. In every individual case the user must check such information by consulting the relevant literature. Production: PRO-EDIT GmbH, D Heidelberg SPIN: / Printed on acid-free paper
5 Preface Only five years ago, nobody in his right mind would have considered publishing a book on reeler as a model for brain development. Although this interesting mutation has been with us for half a century, it is fair to say that, in spite of a wave of enthusiasm in the late sixties and early seventies, generated primarily by Sidman, Caviness and colleagues, studies of reeler mice fell progressively out of fashion during the next two decades. All that changed almost overnight when the cloning of the reeler gene, dubbed reelin, was reported in Tom Curran's laboratory in The fact that the same gene was identified at the same time independently by two other groups using positional cloning suggested strongly that reelin was the right candidate. Although the key experiments of transgenic rescue have not been made (and perhaps will never be), the equation "reeler is reelin" has been established beyond reasonable doubt, as alterations of the reelin gene and/or its expression have been found in at least five alleles of reeler and in the mutation Shaking Rat Kawasaki (SRK), an ortholog of reeler. During the last four years, we have witnessed a renewed interest in reeler and robust attacks are now mounted on various fronts to understand better the action of reelin, to define the modifications or variants of the protein, to characterize other molecules interacting with reelin, either as receptors or reelin associated proteins, and to elucidate the putative reelin signaling pathway. Recently, several major findings were reported that broadly extend the perspective in which work on reeler can now be considered. First, a null mutation in the cyclin-dependent kinase 5 (Cdk5) gene was generated by gene targeting in mice, and displays developmental alterations in the cerebral cortex and cerebellum that are reminiscent of those in reeler, and in fact define a new stage of cortical development. A few months later, a mouse deficient in the p35 protein - a non kinase activator of Cdk5 - was also generated that replicates some features of the Cdk5 null phenotype, particularly laminar inversion in the cortex. Finally, two new mutations that generate a phenocopy of reeler, named scrambler and yotari were identified. Mice deficient in the mdabl gene, a probable adaptor of non-receptor v
6 tyrosine kinases, similar to Drosophila disabled, have a phenotype almost identical to reeler, and it was shown that scrambler and yotari are indeed recessive alleles ofmdabl. As in many other instances, this mind-boggling evolution comes as a fitting illustration of the highly nonlinear progress of science, characterized by alternating periods of slow work and sudden breakthrough. Also typical of modern biology is the fact that serendipity played a central role. Nobody could have predicted that insertion of a c-fos transgene in the reelin gene would allow the cloning of reelin, or that a mdabl knock out would generate a reeler-like phenotype. This state of affairs is intellectually quite frustrating, but a healthy reminder that our theories, particularly about the brain, are rudimentary to say the least, and should be dealt with accordingly. Thus far, studies of the reeler and related mouse models have benefited our understanding of human brain malformations mainly from a basic standpoint, by focusing our thinking on modern biological mechanisms of development. They did not yield any direct dividend in terms of medical output. Recent progress in the study of some human malformations and neuronal migration disorders suggests that this is about to change. We can reasonably hope that the views and theories on brain development generated from studies of mouse neurological mutations will soon prove useful for the understanding and perhaps the management of these debilitating diseases. In order to try and cover most aspects of research carried out on the reeler mouse and related models, a first chapter summarizes classical views on mouse brain development and reviews in some detail brain development in reeler mice. This is followed by a summary of current data on extracellular matrix components in cortical development. In a second chapter, we proceed with the genetics of reeler, including the experiments that led to the identification of reelin. The genomic organization of the reelin gene and the alterations that are found in the various reeler alleles are described, together with the alternative splicing events that have been defined thus far. The third chapter deals with the expression of reelin mrna during development, the production of antireelin antibodies and their use in studies of reelin protein expression, as well as with some experiments, still preliminary, carried out to define the action of the protein. A fourth chapter deals with some comparative aspects of cortical development that point to a possible role of reelin during brain evolution. In the last chapter, we discuss reelin in the context of other animal mutations and human malformations that produce related phenotypes. A preliminary model summarizing current data is presented. In this small monograph, extensive - some will perhaps say shameful- borrowing was made from works published by several colleagues; their contribution is clearly acknowledged in the text VI
7 and references. Some of the work reviewed in the various chapters was carried out in our laboratory and we would like to acknowledge particularly the contributions of I. Bar, M.e. Beckers, B. Bernier, V. de Bergeyck, T. Huynh-Thu and I. Royaux, as well as the expert technical assistance of C. Dernoncourt, D. Lannoy, B. Naerhuyzen, D. Ruelle and the secretarial aid of M. De Vos. Finally, we wish to thank Prof. E. Marani (Leiden University) for his valuable advice and help with the final edition of the manuscript. This review and discussion of past and recent studies of reeler is hopefully timely, but will serve its purpose only if it fosters new and original approaches to this old problem. Whether it succeeds in its task is left to the appreciation of the reader. VII
8 Contents 1 Brain Development in Normal and reeler Mice: The Phenotype Some Introductory Background The Early Development of the Normal Cerebral Cortex Orientation of Mitoses in the Ventricular Zone The Preplate The Early Marginal Zone The Appearance of the Cortical Plate Early Cortical Histogenesis in reeler Mutant Mice The reeler Cerebellum The reeler Inferior Olivary Complex The Facial Nerve Nucleus and Other Targets Other Targets of the reeler Gene ECM Components and Cortical Development ECM and Fiber Growth Integrins Genetics of reeler and Genomics of reelin Genetics and the Various Alleles of reeler Rat reeler-like Mutations Other Mouse Mutations with a reeler-like Phenotype Mapping of reeler and Cloning of reelin Mapping The reel in cdna... ; Genomic Organization of the reelin Gene Alternative Splicing of the reelin Gene l.l Alternative Use of a Six Base Pair Microexon Alternative Polyadenylation The Promoter Region Clues to the Possible Origin of the reelin Repeats? IX
9 3 Topography and Cellular Localization of reelin mrna and Protein Expression During Brain Development reelin mrna Expression During Development Study of Reelin Protein Expression Using Antibodies to Reelin Antireelin Antibodies Reelin Protein Expression During Mouse Brain and Human Cortical Development Studies of Reelin Function Using Antireelin Antibodies Is the Reelin Protein Processed in the Embryonic Mouse Brain? Some Questions Raised by the Studies of Reelin Expression Cajal-Retzius Cells and Other Reelin-positive Cells in the Developing Cortical Marginal Zone Does Reelin Act on Postmigratory Neurons, Radial Glia or Both? Reelin Expression is Poorly Correlated With the reeler Phenotype Reelin as a Repulsive, Extracellular Matrix-Expanding Molecule? Reelin and Axonal Growth The reeler Mutation and Brain Evolution The Evolution of Brain Development: ANew Theme? Comparative Data on Cell Migration, Maturation, Synaptogenesis And Neurogenesis Comparison of Cortical Plate Development in Emys and Lacerta Biological Mechanisms Involved in the Histogenesis of the Cortical Plate Evolutionary Considerations Reelin and a Model of Cortical Evolution A Model of Cortical Development Inspired by reeler: Facts and Hypotheses Early Hypotheses on the Actions of the reeler Gene on the Developing Brain Reeler and Cell Interaction/Adhesion x
10 5.1.2 The Action of the reeler Gene is Intrinsic to the Neuroepithelium Reeler Phenotype and Radial Glial Fibers Mouse Disabledl and the Scrambler/yotari Mutations Cydin-Dependent Protein Kinase 5 and its Activator p35: Definition of a New Step in Mammalian Cortical Development Reeler-Type Malformations and Human Neuropathology References Subject Index XI
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