Neural Development and Stem Cells Contemporary Neuroscience Neural Development and Stem Cells, Gene Therapy for Neurological Disorders Second Edition, edited by Mahendra S. and Brain Tumors, edited by E. Antonio Rao, 2005 Chiocca and Xandra O. Breakefield, Neurobiology of Aggression: Understanding 1998 and Preventing Violence, edited by Cell Transplantation for Neurological Mark P. Mattson, 2003 Disorders: Towards Reconstruction of the Neuroinflammation: Mechanisms and Human Central Nervous System, edited Management, Second Edition, edited by byThomas B. Freeman and Hakan Paul L. Wood, 2003 Widner, 1998 Neural Stem Cells for Brain and Spinal Highly Selective Neurotoxins: Basic and Cord Repair, edited by Tanja Zigova, Clinical Applications, edited by Richard Evan Y. Snyder, and Paul R. Sanberg, M. Kostrzewa, 1998 2003 Neuroinflammation: Mechanisms and Neurotransmitter Transporters: Structure, Management,edited by Paul L. Wood, Function, and Regulation, Second 1998 Edition,edited by Maarten E. A. Reith, Antidepressants: New Pharmacological 2002 Strategies,edited by Phil Skolnick, 1997 The Neuronal Environment: Brain Homeostasis Neuroprotective Signal Transduction, edited in Health and Disease, edited by Wolfgang byMark P. Mattson, 1998 Walz,2002 Clinical Pharmacology of Cerebral Ischemia, Neuroglia in the Aging Brain, edited by edited by Gert J. Ter Horst andJakob Jean de Vellis, 2002 Korf,1997 Pathogenesis of Neurodegenerative Disorders, Molecular Mechanisms of Dementia, edited edited by Mark P. Mattson, 2001 byWilma Wasco and Rudolph E. Stem Cells and CNS Development, edited by Tanzi,1997 Mahendra S. Rao, 2001 Neurotransmitter Transporters: Structure, Function, and Regulation, edited by Neurobiology of Spinal Cord Injury, edited Maarten E. A. Reith, 1997 byRobert G. Kalb andStephen M. Motor Activity and Movement Disorders: Strittmatter, 2000 Research Issues and Applications, Cerebral Signal Transduction: From First edited byPaul R. Sanberg, Klaus-Peter to Fourth Messengers, edited by Ossenkopp, and Martin Kavaliers,1996 Maarten E. A. Reith, 2000 Neurotherapeutics: Emerging Strategies, Central Nervous System Diseases: Innovative edited by Linda M. Pullan and Jitendra Animal Models from Lab to Clinic, edited Patel, 1996 byDwaine F. Emerich,Reginald L. Dean, III, and Paul R. Sanberg,2000 Neuron–Glia Interrelations During Phylogeny: Mitochondrial Inhibitors and Neurodegenerative II. Plasticity and Regeneration, edited by Disorders,edited by Paul R. Sanberg, Antonia Vernadakis and Betty I. Roots, Hitoo Nishino, and Cesario V. 1995 Borlongan, 2000 Neuron–Glia Interrelations During Phylogeny: Cerebral Ischemia: Molecular and Cellular I. Phylogeny and Ontogeny of Glial Cells, Pathophysiology,edited by Wolfgang edited byAntonia VernadakisandBetty Walz, 1999 I. Roots, 1995 Cell Transplantation for Neurological The Biology of Neuropeptide Y and Related Disorders,edited by Thomas B. Freeman Peptides, edited by William F. Colmers and Håkan Widner,1998 andClaes Wahlestedt, 1993 Neural Development and Stem Cells Second Edition Edited by Mahendra S. Rao, , MBBS PhD National Institute on Aging, Baltimore, MD © 2006 Humana Press Inc. 999 Riverview Drive, Suite 208 Totowa, New Jersey 07512 www.humanapress.com 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. All papers, comments, opinions, conclusions, or recommendations are those of the author(s), and do not necessarily reflect the views of the publisher. For additional copies, pricing for bulk purchases, and/or information about other Humana titles, contact Humana at the above address or at any of the following numbers: Tel.: 973-256-1699; Fax: 973-256-8341; E-mail: [email protected], or visit our Website: www.humanapress.com This publication is printed on acid-free paper. ∞ ANSI Z39.48-1984 (American Standards Institute) Permanence of Paper for Printed Library Materials. Cover illustration: Figure 4 from Chapter 13, “Embryonic Stem Cells and Neurogenesis” by Robin L. Wesselschmidt and John W. McDonald Cover design by Patricia F. Cleary. Photocopy Authorization Policy: Authorization to photocopy items for internal or personal use, or the internal or personal use of specific clients, is granted by Humana Press Inc., provided that the base fee of US $30 is paid directly to the Copyright Clearance Center at 222 Rosewood Drive, Danvers, MA 01923. For those organizations that have been granted a photocopy license from the CCC, a separate system of payment has been arranged and is acceptable to Humana Press Inc. The fee code for users of the Transactional Reporting Service is: [1-58829-481-1/06 $30]. Printed in the United States of America. 10 9 8 7 6 5 4 3 2 1 Library of Congress Cataloging-in-Publication Data Neural development and stem cells / edited by Mahendra S. Rao.— 2nd ed. p. cm. — (Contemporary neuroscience) Includes bibliographical references and index. ISBN 1-58829-481-1 (alk. paper) EISBN 1-59259-914-1 1. Developmental neurobiology. 2. Stem cells. I. Rao, Mahendra S. II. Series. QP363.5.S75 2005 612.8—dc22 2004024052 Preface Developing the second edition of Neural Development and Stem Cellswas necessi- tated by the rapid increase in our knowledge of the development of the nervous system. It has become increasingly clear that stem cells are a heterogeneous population that changes extensively during development. Perhaps the most important advance in our understanding of stem cell behavior has been the realization that regionalization of stem cells occurs early in development and this bias toward differentiation in pheno- types of neurons or cells characteristic of a particular part of the brain appears to persist even after prolonged culture. We have therefore included additional chapters on olfac- tory epithelial stem cells and retinal stem cells, both of which differ in their properties from ventricular zone and subventricular zone–derived neural stem cells. It is also now clear from an analysis of mutants and transgenics where the death or self-renewal path- way is altered that cell death regulates stem cell number. As a consequence, this second edition includes a separate chapter on cell death that summarizes the important changes in the death pathway that occur as stem cells mature. The existing chapters in the book have also been extensively revised and updated by experts who have generously con- tributed their time and expertise. The chapters have been organized along the lines of our understanding of how the nervous system develops (Fig.1, on p. vi). Stem cells are present early in development, well before the onset of neurogenesis and gliogenesis. Stem cells proliferate and respond to extrinsic cues to mature as adult stem cells, undergo cell death, enter a state of quies- cence, or differentiate. Stem cells appear to become regionally specified and their differ- entiation potential depends on the region that they have been isolated from. I thank the authors for their efforts in ensuring that their manuscripts are as up to date as possible, and we all hope that this second edition of Neural Development and Stem Cellswill serve as a handy guide for a course on stem cell biology in the nervous system for the novice and expert alike. Mahendra S. Rao, MBBS,PhD v vi Preface Fig. 1.Multipotent stem cells (NSC) can undergo self-renewal, enter a quiescent state, mature into adult stem cells, die, or respond to signals to differentiate. Differentiation appears to occur via a progressive set of fate choices that include the generation of divid- ing precursors with a restricted set of fate choices. These precursor cells present during development and, in the adult, mature to generate fully differentiated neurons, astrocytes, and oligodendrocytes. A limited set of data suggest that mature cells or intermediate precursors can dedifferentiate to reenter the cell cycle and acquire the characteristics of NSC. Contents Preface...................................................................................................................v Contributors....................................................................................................... ix 1 Defining Neural Stem Cells and Their Role in Normal Development of the Nervous System Sally Temple.........................................................................................................1 2 Neural Stem Cells in the Adult Brain: Implications of Their Glial Characteristics Daniel A. Lim and Arturo Alvarez-Buylla ..................................................29 3 Cellular and Molecular Properties of Multipotent Neural Stem Cells Throughout Ontogeny Larysa Halyna Pevny.......................................................................................49 4 Multipotent Stem Cells in the Embryonic Nervous System Ali Jalali, Michael Bonaguidi, Caitilin Hamill, and John A. Kessler.......................................................................................67 5 Regulation of Neural Stem Cell Death Rizwan S. Akhtar and Kevin A. Roth...........................................................97 6 Neuronal Progenitor Cells of the Mammalian Neonatal Anterior Subventricular Zone Douglas L. Falls and Marla B. Luskin........................................................123 7 Glial Restricted Precursors Mark Noble and Margot Mayer-Pröschel..................................................143 8 PNS Precursor Cells in Development and Cancer Houman D. Hemmati, Tanya A. Moreno, and Marianne Bronner-Fraser..................................................................189 9 Stem Cells of the Adult Olfactory Epithelium James E. Schwob and Woochan Jang ..........................................................219 10 Retinal Stem Cells Ani V. Das, Jackson James, Sreekumaran Edakkot, and Iqbal Ahmad ........................................................................................235 11 Transdifferentiation in the Nervous System Ying Liu and Mahendra S. Rao.....................................................................249 12 Neural Progenitor Cells of the Adult Human Brain Steven A. Goldman .........................................................................................267 vii viii Contents 13 Embryonic Stem Cells and Neurogenesis Robin L. Wesselschmidt and John W. McDonald.....................................299 14 Mobilizing of Neural Precursors in the Adult Central Nervous System Theo D. Palmer and Fred H. Gage................................................................343 15 Neural Stem Cells and Transplant Therapy: Intrinsic Programs and Clinical Applications Jaime Imitola, Yang D. Teng, Vaclav Ourednik, Kook In Park, Richard L. Sidman, and Evan Y. Snyder.................................................371 Appendix A: Neural Stem Cell Companies.......................................................421 Appendix B: Stem Cells and Transplants...........................................................425 Appendix C: Patents and Stem Cells ..................................................................429 Appendix D: Stem Cells and US Federal Guidelines.......................................431 Index...................................................................................................................445 Contributors IQBAL AHMAD • Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, NE RIZWAN S. AKHTAR • Departments of Pathology and Neurobiology, Division of Neuropathology, University of Alabama at Birmingham, Birmingham, AL ARTURO ALVAREZ-BUYLLA • Program in Developmental and Stem Cell Biology, Department of Neurological Surgery, University of California, San Francisco, CA MICHAEL BONAGUIDI • Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL MARIANNE BRONNER-FRASER • Division of Biology, California Institute of Technology, Pasadena, CA ANIV. DAS • Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, NE SREEKUMARAN EDAKKOT • Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, NE DOUGLAS L. FALLS • Department of Cell Biology, Emory University School of Medicine, Atlanta, GA FRED H. GAGE • Laboratory of Genetics, The Salk Institute for Biological Studies, La Jolla, CA STEVENA. GOLDMAN • Department of Neurology, Division of Cell and Gene Therapy, University of Rochester Medical Center, Rochester, NY CAITILIN HAMILL • Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL HOUMAN D. HEMMATI • Division of Biology, California Institute of Technology, Pasadena, CA JAIME IMITOLA • Center for Neurologic Diseases, Brigham and Women’s Hospital, Harvard Medical School, Boston, MA ALI JALALI • Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL JACKSON JAMES • Department of Ophthalmology and Visual Sciences, University of Nebraska Medical Center, Omaha, NE WOOCHAN JANG • Department of Anatomy and Cellular Biology, Tufts University School of Medicine, Boston, MA JOHNA. KESSLER • Department of Neurology, Northwestern University Feinberg School of Medicine, Chicago, IL DANIELA. LIM • Program in Developmental and Stem Cell Biology, Department of Neurological Surgery, University of California, San Francisco, CA YING LIU • Laboratory of Neurosciences, National Institute on Aging, Baltimore, MD ix