RHODOPSINS AND PHOTOTRANSDUCTION The Norartis Foundation is an international scientific and educational charity (UK Registered Charity No. 313574). Known until September 1997 as the Ciba Foundation, it was established in 1947 by the CIRA company of Rasle, which merged with Sandoz in 1996, to form Novartis. The Foundation operates independently in London under English trust law. It was formally opened on 22 June 1949. ’The Foundation promotes the study and general knowledge of science and in particular encourages international co-operation in scientific research. To this end, it organizes internationally acclaimed meetings (typically eight symposia and allied open meetings, 15--20 discussion meetings, a public lecture and a public debate each year) and publishes eight books per year featuring the presented papers and discussions from the symposia. 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Singapore . Toronto Copyright 0 Novartis Foundation 1999 Published in 1999 by JohnWiley & Sons Ltd, Baffins Lane, Chichester, West Sussex PO19 IUD, England National 01243 779777 International (+44) 12437 79777 e-mail (for orders and customer service enquiries): [email protected] Visit our Home Page on http://www.wiley.co.uk or http://www.wiley.coni 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, recording, scanning or otherwise, except under the terms of the Copyright, Designs and Patents Act 1988 or under the terms of a licence issued by the Copyright Licensing Agency, 90 Tottenham Court Road, London,WlP 9HE, UK, without the permission in writing of the publisher. Other Wily Editorial Ofices John Wiley & Sons, Inc., 605 Third Avenue, NewYork, NY 10158-0012,U SA WILEY-VCH Verlag GmbH, Pappelallee 3, D-69469 Weinheim, Germany JacarandaWiley Ltd, 33 Park Road, Milton, Queensland 4064, Australia JohnWiley & Sons (Asia) Pte Ltd, 2 Clementi Loop #02-01, Jin Xing Distripark, Singapore 129809 JohnWiley & Sons (Canada) Ltd, 22 Worcester Road, Rexdale, Ontario M9W 1L1, Canada Novartis Foundation Symposium 224 ix+306 pages, 74 figures, 11 tables Library ofcongress Ca~aloging--in-PublicatiDona ta Rhodopsins and phototransduction. p. cm. - (Novartis Foundation symposium ; 224) Includes bibliographical references and index. ISBN 0-471-98827-8 (alk. paper) 1. Rhodopsin Congresses. I. Symposium on Rhodopsins and Phototransduction (1998: Kyoto, Japan). 11. Series. QP671.V5R48 1999 573.8'8459-dc21 99-37597 CIP British Librnry Cataloguing in Publication Data A catalogue record for this book is available from the British Library ISBN 0 471 98827 8 Typeset in 102 on 122 pt Garamond by DobbieTypesetting Limited, Tavistock, Devon. Printed and bound in Great Britain by Biddles Ltd, Guildford and King's Lynn. This book is printed on acid-free paper responsibly manufactured from sustainable forestry, in which at least two trees are planted for each one used for paper production. Contents The Novartis Foundation in collaboration with the Novartis Foundation (Japan)f or the Promotion of Science Jjmposium on Rhodopsins andphototransduction,h eld in Kyoto International Conference Hal/, Rjoto, Japan, 2628 October 1998 This gmposium is held in commemoration ojthe late Projessor George Wald, and is based on a proposalmade Ly Projessor?iiruyoshi~awa Editors: Ikuo Takeuchi and Gregovl Bock (O,yani&, andJamie A. Goode Toru Yoshizawa Chairman’s introduction 1 Ruth Hubbard and Elijah Wald George Wald memorial talk 5 Discussion 18 James K. Bowmaker The ecology of visual pigments 21 Discussion 31 General discussion I Vertebrate ancient (VA) opsin: a new vertebrate photopigment family 36 Fumio Tokunaga, Osamu Hisatomi, Takunori Satoh,Yuki Taniguchi, Shinji Matsuda,Yoshikazu Imanishi, Hanayo Honkawa,YusukeTakahashi, Yuko Kobayashi, MasaoYoshida and Yasuo Tsukahara Evolution of visual pigments and related molecules 44 Discussion 52 Gebhard F. X. Schertler Structure of rhodopsin 54 Discussion 66 Richard A. Mathies Photons, femtoseconds and dipolar interactions: a molecular pkture of the primary events in vision 70 Discussion 84 General discussion I1 90 Willem J. DeGrip, Frank DeLange, Corn6 H. W. Klaassen, Peter J. M.Verdegem, Stacie Wallace-Williams, Alain F. L. Creemers,Vladislav Bergo, Petra H. M. Bovee, Jan Raap, Kenneth J. Rothschild, Huub J. M. DeGroot and Johan Lugtenburg Photoactivation of rhodopsin: interplay between protein and chromophore 102 Discussion 11 8 V vi CONTENTS Steven W. Lin and Thomas P. Sakmar Colour tuning mechanism of visual pigments 124 Discussion 135 Yoshinori Shichida and Hiroo Imai Amino acid residues controlling properties and functions of rod and cone visual pigments 142 Discussion 153 Klaus Peter Hofmann Signalling states of photoactivated rhodopsin 158 Discussion 175 General discussion 111 181 Krzysztof Palczewski, Christophe L. M. J.Verlinde and Franqoise Haeseleer Molecular mechanism of visual transduction 191 Discussion 204 Satoru Kawamura Calcium-dependent regulation of rhodopsin phosphorylation 208 Discussion 21 8 Hiroyuki Matsumoto, Esther S. Kahn and Naoka Komori The emerging role of mass spectrometry in molecular biosciences: studies of protein phosphorylation in fly eyes as an example 225 Discmion 244 Robert S. Molday, Renk Warren, Chris Loewen and Laurie Molday Cyclic GMP-gated channel and peripherin/rds-rom-1 complex of rod cells 249 Discussion 261 Daisuke Kojima and Yoshitaka Fukada Non-visual photoreception by a variety of vertebrate opsins 265 Discussion 279 Final discussion 283 'EiruYoshizawa Chairman's summing-up 291 Index of contributors 297 Subject index 299 Participants James K. Bowmaker Department of Visual Science, Institute of Ophthalmology, University College London, Bath Street, London EClV OEL, UK Willem J. DeGrip Department of Biochemistry, FMW-160, Institute of Cellular Signalling, University of Nijmegen, PO Box 9101,6500 HB Nijmegen, The Netherlands John E. Dowling Department of Molecular and Cellular Biology, Harvard University Biological Laboratories, 16 Divinity Avenue, Cambridge, MA 02138, USA Russell Foster Sir Alexander Fleming Building, Department of Biology (Rm 549, Imperial College of Science, Technology and Medicine, London SW7 2A2, UK Yoshitaka Fukada Department of Biophysics and Biochemistry, Graduate School of Science, University of Tokyo, Hongo 7- 3-1, Bunkyo ku, Tokyo 113-0032, Japan Klaus Peter Hofmann Institut fur Medizinische Physick und Biophysik, Charite-Humboldt University, Schumannstrasse 20-21, D-10098 Berlin, Germany Ruth Hubbard Harvard University Biological Laboratories, 16 Divinity Avenue, Cambridge, MA 02138, USA Yasushi Imamoto (Nuvurtis Foundutiun Bursar) Graduate School of Materials Sciences, Nara Institute of Science and Technology, 8916-5, Takayama, Ikoma, Nara 630-0101, Japan Toshiaki Kakitani Department of Physics, Graduate School of Science, Nagoya University, Furoucho, Chigusaku, Nagoya 464-8602, Japan vii viii PARTICIPANTS Hideki Kandori Department of Biophysics, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan U. Benjamin Kaupp Forschungszentrum Jiilich, Institut fur Biologische Informationsverarbeitung, 52425 Jiilich, Germany Satoru Kawamura Department of Biology, Graduate School of Science, Osaka University, Toyonaka, Osaka 560-0043, Japan H. Gobind Khorana Department of Biology, Massachusetts Institute of Technology, 77 Massachusetts Ave., Cambridge, MA 02139-4307, USA Richard A. Mathies Department of Chemistry, University of California, Berkeley, CA 94720-1460, USA Hiroyuki Matsumoto Department of Biochemistry and Molecular Biology, University of Oklahoma Health Sciences Center, PO Box 26901, Oklahoma City, OK 73104, USA Robert S. Molday Department of Biochemistry and Molecular Biology, University of British Columbia, Faculty of Medicine, 2146 Health Sciences Mall, Vancouver BC, CanadaV6T 123 Tadashi Nakamura Department of Applied Physics and Chemistry, University of Electro-Communications, Chofu, Tokyo 182-8585, Japan Krzysztof Palczewski Depart,ment of Ophthalmology, University of Washington, PO Box 356485, Seattle,WA 98195-6485, USA Thomas P. Sakmar The Howard Hughes Medical Institute, Laboratory of Molecular Biology and Biochemistry, The Rockefeller University, New York, NY 10021, USA Gebhard F. X. Schertler MRC Laboratory of Molecular Biology, Hills Road, Cambridge CB2 2QH, UK Yoshinori Shichida Department of Biophysics, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto 606-8502, Japan IkuoTakeuchi Novartis Foundation (Japan) for the Promotion of Science, 10-66 Miyuki-Cho,Takarazuka 665, Japan PARTICIPANTS 1x FumioTokunaga Department of Earth and Space Science and Department of Biology, Graduate School of Science, Osaka University, Toyonaka, Osaka 560- 0043, Japan Elijah Wald 39 Burnham Street, Somerville, MA 02144, USA AkioYamazaki The Kresge Eye Institute, Departments of Ophthalmology and Pharmacology, Wayne State University, School of Medicine, 4717 St. Antoine Blvd, Detroit, MI 48202, USA ToruYoshizawa (Chairman) Osaka Sangyo University, 3-1-1 Nakagaito, Daito-shi, Osaka 574-8530, Japan Novartif Foundation Symposium Edited by Ikuo Takeuchi, GregoIy R. Bock, Jamie A. Goode Copyright 0 1999 by Novartis Foundation Chairman’s introduction T6ru Yoshizawa Osaka Sangyo University, 3- I- I Nakagaito, Daito-shi, Osaka 574-8530,]apun In October 1998, the Novartis Foundation (UK) in collaboration with the Novartis Foundation (Japan) for the Promotion of Science jointly organized a symposium on Rhodopsins and phototransduction. It was a great pleasure for me to introduce the symposium dedicated to the memory of Professor George Wald, with Ruth Hubbard Wald and their son Elijah Wald both present. I would like to briefly describe why the symposium was held at this time in Kyoto. It was in April 1997 that I heard the sad news of Professor Wald’s death. At the ARVO (Association for Research in Vision and Ophthalmology) meeting that May, I met Professor John Dowling of Harvard University and promised him that I would organize a memorial symposium in Japan, because the 8th International Conference of Retinal Protein had been scheduled to be held in June 1998 at Awaji island, close to Kansai Airport. Shortly after, I was informed by Professor Ikuo Takeuchi of the Novartis Foundation (Japan) that they wanted me to serve as the chairman of this symposium with the provisional title of ‘Rhodopsin and vision’ and, later, that the symposium was going to be held in the autumn in Kyoto. Since it may safely be said that all the research achievements in this field are based on the work of George Wald, and bearing in mind he had a great affection for Kyoto, an old capital of Japan, I thought it would be appropriate that this Novartis Foundation symposium should become the memorial symposium. As you may know, George Wald was awarded a Nobel Prize in 1967. Though his achievements will be described in detail by Professor Ruth Hubbard in the first paper of this book, I would like to touch on them briefly here. His accomplishments were summarized in the presentation speech by Professor C. G. Bernhard, a member of the Nobel Committee. Here are the last few sentences of his qeech, in italics, with my comments underneath. ‘Professor Wuld. Witha deep biologicalins@andagreat biochemicalskill . . ’ , In fact, he had a wide knowledge of science, from psychology to quantum chemistry, and studied mainly vision using various techniques (e.g. psychophysical, morphological, electrophysiological, biochemical and spectroscopical techniques) on the one hand, and on the other hand enunciated his scientific philosophy from origin of life to evolution of consciousness. 1