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The Retina: A Model for Cell Biology Studies PDF

369 Pages·1986·26.177 MB·English
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CELLULAR NEUROBIOLOGY: A SERIES EDITED BY SERGEY FEDOROFF THE NODE OF RANVIER Edited by JOY C. ZAGOREN AND SERGEY FEDOROFF THE RETINA: A MODEL FOR CELL BIOLOGY STUDIES, PART I Edited by RUBEN ADLER AND DEBORA FARBER THE RETINA: A MODEL FOR CELL BIOLOGY STUDIES, PART II Edited by RUBEN ADLER AND DEBORA FARBER THE RETINA A Model for Cell Biology Studies Part I EDITED BY RUBEN ADLER DEBORA FARBER The Michael M. Wynn Center for the Jules Stein Eye Institute Study of Retinal Degenerations UCLA School of Medicine The Wilmer Ophthalmological Institute Los Angeles, California The Johns Hopkins University School of Medicine Baltimore, Maryland 1986 < $> ACADEMIC PRESS, INC. Harcourt Brace Jovanovich, Publishers Orlando San Diego New York Austin London Montreal Sydney Tokyo Toronto COPYRIGHT © 1986 BY ACADEMIC PRESS, INC. ALL RIGHTS RESERVED. NO PART OF THIS PUBLICATION MAY BE REPRODUCED OR TRANSMITTED IN ANY FORM OR BY ANY MEANS ELECTRONIC OR MECHANICAL, INCLUDING PHOTOCOPY, RECORDING. OR ANY INFORMATION STORAGE AND RETRIEVAL SYSTEM, WITHOUT PERMISSION IN WRITING FROM THE PUBLISHER. ACADEMIC PRESS, INC. Orlando, Florida 32887 United Kingdom Edition published b\ ACADEMIC PRESS INC. (LONDON) LTD. 24-28 Oval Road, London NWI 7DX Library of Congress Cataloging in Publication Data Main entry under title: The Retina : a model for cell biology studies. Includes bibliographies and index. 1. Retina-Cytology. I. Adler, Ruben. II. Farber, Debora. [DNLM: 1. Retina-cytology. 2. Retina- physiology. WW 270 R43804] QP479.R468 1986 599\01823 85-23005 ISBN 0-12-044275-2 (Pt. I : alk. paper) PRINTHD IN THH UNITHD STATUS OF AMHRICA 86 87 88 89 9 8 7 6 5 4 3 2 1 This book is dedicated to Alfred J. ("Chris") Coulombre, a pioneer of the field of retinal cell biology and an outstanding human being CONTRIBUTORS Numbers in parentheses indicate the pages on which the authors' contributions begin. Ruben Adler (1, 111), The Michael M. Wynn Center for the Study of Retinal Degenerations, The Wilmer Ophthalmological Institute, The Johns Hopkins University, School of Medicine, Baltimore, Maryland 21205 Joseph C. Besharse (297), Department of Anatomy and Cell Biology, Emory University School of Medicine, Atlanta, Georgia 30322 Beth Burnside (151), Department of Physiology-Anatomy, University of Cal- ifornia, Berkeley, Berkeley, California 94720 Allen Dearry (151), Department of Physiology-Anatomy, University of Cal- ifornia, Berkeley, Berkeley, California 94720 Debora B. Farber (1, 239), Jules Stein Eye Institute, UCLA School of Medi- cine, Los Angeles, California 90024 Christopher C. Getch (67), Department of Biology, Princeton University, Princeton, New Jersey 08544 Paul A. Hargrave (207), Department of Ophthalmology and Department of Biochemistry and Molecular Biology, College of Medicine, University of Flor- ida, Gainesville, Florida 32610 Robert E. Marc (17), Sensory Sciences Center, University of Texas Graduate School of Biomedical Sciences, Houston, Texas 77030 Terrence A. Shuster (239), Jules Stein Eye Institute, UCLA School of Medi- cine, Los Angeles, California 90024 Malcolm S. Steinberg (67), Department of Biology, Princeton University, Princeton, New Jersey 08544 xi PREFACE Retinal Cell Biology: Past, Present, and Future It is difficult at times to define the field of cell biology. One need only attend the annual meeting of the American Society for Cell Biology to experience the enormous breadth of this field. Nonetheless, many would define cell biology in a very general way as a combination of microscopic anatomy, biochemistry, phys- iology, and pathology. The confluence of these disciplines into a unifying field did not really occur until the 1950s, but we can trace the ancestry of the discipline to Matthias Schleiden, Theodor Schwann, and Rudolf Virchow, the botanist, histologist, and pathologist, respectively, who are generally credited with the development of the cell theory in 1839. Somewhat later in that century the study of retinal cells was initiated. Ultimately, Max Schultze (1867) set forth the duplicity theory for photoreceptor function through his observation that cones are the receptors for bright light and color and that rods function in dim light. Subsequently Franz Boll (1877) observed that the photochemical event underlying light detection was the bleaching of ' 'visual purple" now known as rhodopsin. He also suggested that a carotenoid might be a precursor for this photopigment. His contemporary, Willy Kuhne (1878) was the first to solubilize photopigments in bile salts thereby demonstrating their hydrophobic nature. Santiago Ramon y Cajal (1894) soon thereafter modified methods shared by fellow Nobel laureate Camillo Golgi and displayed the neuronal network of the retina in such breathtaking detail that his work serves as the standard even to this day. Therefore, by the turn of the century, the study of retinal cells by representatives of the separate disciplines of microscopic anatomy, biochemistry, and physiology was well established. Retinal research was graced by investigators of equivalent intuition and creativity during the first half of this century. The disciplines of electrophysiolo- gy and biochemistry, exemplified by Ragnar Granit, Haldane Hartline, and George Wald, produced insights into retinal electrical activity, cell interactions, and photochemistry worthy of the Nobel Prize so appropriately bestowed upon them. The contributions of these gifted scientists and their contemporaries drew xiii XIV PREFACE into the field a new generation of capable scientists armed with new and powerful techniques. Fritiof Sjostrand, Eichi Yamada, Adolph Cohen, Brian Boycott, John Dowling, and many others began the systematic examination of retinal cells by electron microscopy. The application of tissue autoradiographic technique to retinal studies by Richard Sidman, Richard Young, and Bernard Droz in the early to mid 1960s added a dynamic component to microscopy. It was possible for the first time to mark retinal birth dates and to study the metabolism of individual cell types. Particularly suitable for autoradiographic studies were the photoreceptors with their highly compartmentalized structure and their prodigious biosynthesis and assembly of membranes. By virtue of this technique, an entirely new role was discovered for retinal pigment epithelial cells, the phagocytosis and photorecep- tor outer segment membranes. Furthermore, a new research strategy began to emerge. Whereas scientists of the past had adhered rather strictly to their chosen disciplines each of which drew upon a rather limited constellation of methods, the new approach was to combine the methods of multiple disciplines in order to address problems of ever-increasing complexity. This is the essence of cell biology and, with the advent of this approach, retinal cell biology came into full bloom. A subject that benefited greatly from this philosophy was the study of mem- brane biosynthesis in photoreceptors. Michael Hall and I combined radio- biochemical and autoradiographic methods in the study of rhodopsin bio- synthesis and assembly into outer segment disk membranes, and David Papermaster and Barbara Schneider applied high-resolution immunocytochemi- cal methods to plot membrane trafficking from sites of synthesis to sites of assembly within the cell. Another area that was aided tremendously by this combined approach was that of retinal neurotransmitter studies. Relatively little progress was made on this subject until the introduction of autoradiographic and immunocytochemical tech- niques. Autoradiographic analysis of high-affinity-uptake sites for neurotrans- mitters as initiated by Berndt Ehinger and Dominic Lam combined with immu- nocytochemical localization of enzymes involved in neurotransmitter synthesis have been very illuminating as have studies introduced by Harvey Karten and Nicholas Brecha on the localization of the myriad of peptides that are now known to exist either as neurotransmitters or neuromodulators in the amacrine cells of the retina. Immunocytochemical techniques are now employed by a growing number of retinal cell biologists and, when applied at high resolution in particu- lar, will add significantly to our understanding of the molecular division of labor among retinal organelles. Research during the 1970s has featured another group of exciting topics. The subject of photoreceptor transduction has been hotly debated among proponents who favor the hypothesis that calcium serves as the internal messenger during PREFACE xv signal amplification, as first proposed by William Hagins and Shuko Yoshikami, and the adherents of cyclic guanosine monophosphate, as initially suggested from the work of Mark Bitensky and collaborators. Whatever the outcome, it appears likely that the photoreceptors will be the first sensory cells in which the mystery of transduction is solved. Furthermore, the contributions of Debora Farber and Richard Lolley and their collaborators have shown how cyclic nu- cleotide metabolism, when perturbed, can lead to photoreceptor degeneration of the type observed in some animal models for retinitis pigmentosa. Rhythmic phenomena in the retina, pioneered by Matthew LaVail through his observations on cyclic outer segment disk shedding, have also been a subject of intense investigation resulting in the discovery by several laboratories that these activities are controlled intraocularly rather than by remote tissues such as the pineal gland. The development of an in vitro preparation by Joseph Besharse for the study of the molecular basis of rhythmic activity has already moved us significantly toward an understanding of these processes. Superimposed upon these metabolic studies has been exciting progress in our understanding of the role of extracellular adhesion and matrix molecules in retinal development and trophic interactions. The recent work of Ruben Adler and associates now pro- vides us with the capability to study the differentiation of photoreceptors in culture. Another informational leap is now occurring in retinal cell biology, spawned by the technology that has impacted so favorably on other tissues as well, namely, recombinant DNA research. Some of the most exciting observations are so new that they have not yet appeared in print. The first application of recombi- nant DNA methods to retinal research has involved the amino acid sequencing of proteins involved in phototransduction. The sequencing of bovine rhodopsin by conventional methods was initiated by Paul Hargrave and his colleagues shortly after this protein was purified by Joram Heller in 1968. About 15 years of intensive work were required before the primary structure of this hydrophobic membrane protein was solved. Utilizing this important se- quence information, the fact that the vertebrate photopigments are well con- served, and rapid nucleotide sequencing developed independently by the labora- tories of Frederick Sanger and Walter Gilbert, Jeremy Nathans and David Hogness have sequenced human rhodopsin and all of the human cone opsins in the space of just a few years. Additionally, the primary sequences of all of the subunits of the G protein and light-activated cyclic nucleotide phosphodiesterase thought to be involved in phototransduction will probably be solved in several laboratories by the time that these books (Parts I and II) appear in print. With this information in hand we will have, for the first time, the opportunity to determine the molecular basis of several forms of inherited photoreceptor degeneration that are thought to involve one or more of these proteins. We are currently experiencing a fast-moving and exciting period for the retinal XVI PREFACE cell biologist and the opportunities appear almost limitless at this time. It is therefore most fitting that a two-part series entitled The Retina: A Model for Cell Biology Studies should be made available to those who already have an interest in this subject and to others who may be inspired to join us. We hope that you find the subject as inviting and rewarding as we have during the past two decades. DEAN BOK THE RETINA, PART I ISSUES AND QUESTIONS IN CELL BIOLOGY OF THE RETINA DEBORA FARBER Jules Stein Eye Institute UCLA School of Medicine Los Angeles, California RUBEN ADLER The Michael M. Wynn Center for the Study of Retinal Degenerations The Wilmer Ophthalmological Institute The Johns Hopkins University School of Medicine Baltimore, Maryland I. Introduction 2 II. The Adult Retina 3 A. Localization within the Eye 3 B. Cell Layers and Neuronal Networks 4 C. Glia 8 III. The Developing Retina 9 IV. The Pathological Retina 14 V. Concluding Remarks 15 References 16 Most investigations of enzymes and other chemical constituents of the developing chick retina are of recent date. . . . thus far inadequate attention has been given to chemical dif- ferences between the pigmented epithelium and the neural retina. ... it seemed reasonable to trace in more detail the histogenesis of this tissue and to make correlation of the findings with the data on retinal chemistry. [Coulombre, 1955] 1 Copyright © 1986 by Academic Press, Inc. All rights of reproduction in any form reserved.

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