Table Of ContentRHODOPSINS 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. Although
primarily an operational rather than a grant-making foundation,
it awards bursaries to young scientists to attend the symposia and
afterwards work for up to three months with one of the other
participants.
The Foundation’s headquarters at 41 Portland Place, London W1N 4BN,
provide library facilities, open every weekday, to graduates in science
and allied disciplines. The library is home to the Media Resource
Service which offers journalists access to expertise on any scientific
topic. Media relations are also strengthened by regular press
conferences and book launches, and by articles prepared by the
Foundation’s Science Writer in Residence. The Foundation offers
accommodation and meeting facilities to visiting scientists and
their societies.
Information on all Foundation activities can be found at
http://www.novartisfound.org.uk
Novartis Foundation Symposium 224
RHODOPSINS AND
PHOTOTRANSDUCTION
1999
JOHN WILEY & SONS, LTD
Chichester New York . Weinheim . Brisbane . 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
