Springer Handbook of Auditory Research. Series Editors: Richard R. Fay and Arthur N. Popper

Transcription

1 Springer Handbook of Auditory Research Series Editors: Richard R. Fay and Arthur N. Popper

2 Matthew W. Kelley Doris K. Wu Arthur N. Popper Richard R. Fay Editors Development of the Inner Ear With 29 illustrations and 4 color illustrations

3 Matthew W. Kelley Section on Developmental Neuroscience Porter Neuroscience Center NIDCD, National Institutes of Health Bethesda, MD Arthur N. Popper Department of Biology University of Maryland College Park, MD Series Editors: Richard R. Fay Parmly Hearing Institute and Department of Psychology Loyola University of Chicago Chicago, IL Doris K. Wu Section on Hair Cell Development and Regeneration NIDCD, National Institutes of Health Rockville, MD Richard R. Fay Parmly Hearing Institute and Department of Psychology Loyola University of Chicago Chicago, IL Arthur N. Popper Department of Biology University of Maryland College Park, MD Cover illustration: Paint-fills of the developing otocyst in mouse (top row), chick (second row), frog (third row), and zebrafish (bottom row) (see Fig. 3.2A from Mansour and Schoenwolf ). Paint-fill figures compiled courtesy of M. Bever and D. Fekete. Mouse paint-fills were originally published in Morsli et al. (1998, reprinted with permission of the Society for Neuroscience 1998), chick paint-fills in Bissonnette and Fekete (1996, reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons 1996), frog paint-fills in Bever et al. (2003, reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons 2003), and zebrafish paintfills in Bever and Fekete (2002, reprinted with permission of Wiley-Liss, Inc., a subsidiary of John Wiley & Sons 2002). Library of Congress Control Number: ISBN 10: ISBN 13: Printed on acid-free paper Springer Science Business Media, Inc. All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science Business Media, Inc., 233 Spring Street, New York, NY 10013, ), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. Printed in the United States of America. (MP) springeronline.com

4 Series Preface The Springer Handbook of Auditory Research presents a series of comprehensive and synthetic reviews of the fundamental topics in modern auditory research. The volumes are aimed at all individuals with interests in hearing research including advanced graduate students, postdoctoral researchers, and clinical investigators. The volumes are intended to introduce new investigators to important aspects of hearing science and to help established investigators to better understand the fundamental theories and data in fields of hearing that they may not normally follow closely. Each volume presents a particular topic comprehensively, and each serves as a synthetic overview and guide to the literature. As such, the chapters present neither exhaustive data reviews nor original research that has not yet appeared in peer-reviewed journals. The volumes focus on topics that have developed a solid data and conceptual foundation rather than on those for which a literature is only beginning to develop. New research areas will be covered on a timely basis in the series as they begin to mature. Each volume in the series consists of a few substantial chapters on a particular topic. In some cases, the topics will be ones of traditional interest for which there is a substantial body of data and theory, such as auditory neuroanatomy (Vol. 1) and neurophysiology (Vol. 2). Other volumes in the series deal with topics that have begun to mature more recently, such as development, plasticity, and computational models of neural processing. In many cases, the series editors are joined by a co-editor having special expertise in the topic of the volume. Richard R. Fay, Chicago, Illinois Arthur N. Popper, College Park, Maryland v

5 Volume Preface The last century ended with a renewed interest in the developmental biology of the mammalian inner ear. This arose as a result of the emergence of molecular biological techniques that allowed investigators to work with one of the smallest organs in the mammalian body. These new investigations, many of which are summarized in this volume, have resulted in a striking increase in the pace of discovery and remarkable progress in our understanding of the developmental biology of this organ. Indeed, as a result of the many new discoveries on inner ear biology, the development of the inner ear has been referred to as one of the most striking examples of cellular morphogenesis in any biological system. This volume provides a detailed overview of the development of the inner ear, particularly as our understanding has increased in the last decade of the twentieth century and the first five years of the twenty-first. In the first chapter of this volume, Kelley and Wu provide an overview of these recent discoveries as well as an overview of the volume. They complete their chapter with suggestions for areas of future research and discovery. In Chapter 2, Groves concisely describes the classic experiments of the past century and then provides a critical interpretation of these experiments in light of the emerging molecular data regarding the same developmental process. In Chapter 3, Mansour and Schoenwolf describe the ongoing assembly of a series of genetic cascades, both in surrounding tissues and in the otocyst itself, that play a role in these crucial developmental events. This chapter also highlights the power of mouse genetics as a tool for the study of early developmental events in ear formation. One of the most striking events that occurs during the initial formation of the otocyst is the specification and delamination of a group of neuroblasts from its ventral region. These interactions, as well as stimulating new hypotheses regarding the specification of the initial neuroblast population and its relationship with other cell types in the ear, are described in Chapter 4 by Pauley, Matei, Beisel, and Fritzsch. The Notch pathway is a nearly ubiquitously expressed signaling cascade that is used in multiple developing and mature systems to sort homogeneous progenitor cells into different cell fates (reviewed in Schweisguth 2004). In Chapter vii

6 viii Volume Preface 5, Lanford and Kelley examine the role of Notch in the ear in light of expression and functional data and recent progress in our understanding of the different cofactors and signaling events that mediate this intriguing signaling pathway. The final two chapters in this volume examine an exciting emerging field in inner ear development, the development of the stereociliary bundle located on all mechanosensory hair cells. In Chapter 6, Bryant, Forge, and Richardson describe the morphological process of hair cell differentiation, including the development of the stereociliary bundle, while in Chapter 7, Hertzano and Avraham review insights into the development of the inner ear that have been obtained through the identification of genetic mutations that underlie human nonsyndromic and syndromic deafness. Development of the inner ear, particularly at the molecular level, has not heretofore been considered in this series. However, development of other aspects of the auditory system has been of considerable interest in earlier volumes and these complement the chapters in this volume. Indeed, many chapters in Volume 15 (Development and Plasticity of the Central Auditory System) consider development of the auditory portions of the central nervous system as well as plasticity during development. Similarly, Volume 9 (Development of the Auditory System) has chapters that consider the overall embryology and development of the cochlea and central nervous system, including behavioral and functional data. Martthew W. Kelley, Bethesda, Maryland Doris K. Wu, Rockville, Maryland Arthur N. Popper, College Park, Maryland Richard R. Fay, Chicago, Illinois

7 Contents Series Preface... Volume Preface... Contributors... v vii xi Chapter 1 Developmental Neurobiology of the Ear: Current Status and Future Directions... 1 Matthew W. Kelley and Doris K. Wu Chapter 2 The Induction of the Otic Placode Andrew K. Groves Chapter 3 Morphogenesis of the Inner Ear Suzanne L. Mansour and Gary C. Schoenwolf Chapter 4 Chapter 5 Wiring the Ear to the Brain: The Molecular Basis of Neurosensory Development, Differentiation, and Survival Sarah Pauley, Veronica Matei, Kirk W. Beisel, and Bernd Fritzsch Notch Signaling and Cell Fate Determination in the Vertebrate Inner Ear Pamela J. Lanford and Matthew W. Kelley Chapter 6 The Differentiation of Hair Cells Jane E. Bryant, Andrew Forge, and Guy P. Richardson Chapter 7 Developmental Genes Associated with Human Hearing Loss Ronna Hertzano and Karen B. Avraham Index ix

8 Contributors karen b. avraham Department of Human Genetics and Molecular Medicine, Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel kirk w. beisel Department of Biomedical Sciences, Creighton University, Omaha, NE 68178, jane e. bryant School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QR, United Kingdom andrew forge UCL Center for Auditory Research, University College London 322, London WC1X 8EE, United Kingdom bernd fritzsch Department of Biomedical Sciences, Creighton University, Omaha, NE 68178, andrew k. groves House Ear Institute, Gonda Department of Cell and Molecular Biology, Los Angeles, CA 90057, ronna hertzano Department of Human Genetics and Molecular Medicine, Sackler School of Medicine, Tel Aviv University, Ramat Aviv, Tel Aviv 69978, Israel matthew w. kelley Section on Developmental Neuroscience, Porter Neuroscience Center, NIDCD, National Institutes of Health, Bethesda, MD 20892, xi

9 xii Contributors pamela j. lanford Biological Sciences Program, University of Maryland, College Park, MD 20742, suzanne l. mansour Department of Human Genetics, University of Utah, Salt Lake City, UT 84112, veronica matei Department of Biomedical Sciences, Creighton University, Omaha, NE 68178, sarah pauley Department of Biomedical Sciences, Creighton University, Omaha, NE 68178, guy p. richardson School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QR, United Kingdom gary c. schoenwolf Department of Neurobiology and Anaotmy, University of Utah School of Medicine, Salt Lake City, UT 84132, doris k. wu Section on Hair Cell Development and Regeneration, NIDCD, National Institutes of Health, Rockville, MD 20850,