Table Of ContentResearch Reports in Physics
Research Reports in Physics
Nuclear Structure of the Zirconium Region
Editors: J. Eberth, R. A. Meyer, and K. Sistemich
Ecodynamics Contributions to Theoretical Ecology
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Nonlinear Waves 1 Dynamics and Evolution
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Editors: A. V. Gaponov-Grekhov, M. I. Rabinovich, and J. Engelbrecht
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Editors: A. V. Gaponov-Grekhov, M. I. Rabinovich, and J. Engelbrecht
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Optimized LCAO Method and the Electronic Structure of Extended Systems
By H. Eschrig
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Problems of Modem Quantum Field Theory
Editors: A. A. Belavin, A. U. Klimyk, and A. B. Zamolodchikov
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Nonlinear Waves in Waveguides with Stratification By S. B. Leble
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Symmetries and Singularity Structures
Integrability and Chaos in Nonlinear Dynamical Systems
Editors: M. Lakshmanan and M. Daniel
Modeling Air-Lake Interaction Physical Background
Editor: S. S. Zilitinkevich
Nonlinear Evolution Equations and Dynamical Systems NEEDS '90
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Solitons and Chaos
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Electron-Electron Correlation Effects in Low-Dimensional Conductors
and Superconductors Editors: A. A. Ovchinnikov and 1.1. Ukrainskii
Signal Transduction in Photoreceptor Cells
Editors: P. A. Hargrave, K. P. Hofmann, and U. B. Kaupp
P. A. Hargrave K. P. Hofmann
V.B. Kaupp (Eds.)
Signal Transduction
in Photoreceptor Cells
Proceedings of an International Workshop
Held at the Research Centre lillich,
Jillich, Fed. Rep. of Germany, 8-11 August 1990
With 92 Figures
Springer-Verlag
Berlin Heidelberg New York London Paris
Tokyo Hong Kong Barcelona Budapest
Professor Dr. Paul A. Hargrave
Department of Ophthalmology and Department of Biochemistry and Molecular Biology,
University of Florida, Gainesville, Florida 32610, USA
Professor Dr. Klaus Peter Hofmann
Institut flir Biophysik und Strahlenbiologie, Universitat Freiburg,
AlbertstraBe 23, W-7800 Freiburg, Fed. Rep. of Germany
Professor Dr. U. Benjamin Kaupp
Institut fiir Biologische Informationsverarbeitung, KFA Jiilich,
Postfach 1913, W-5170 Jiilich, Fed. Rep. of Germany
ISBN-13: 978-3-540-53765-6 e-ISBN-13: 978-3-642-76482-0
DOl: 10.1007/978-3-642-76482-0
Library of Congress Cataloging-in-Publication Data Signal transduction in photoreceptor cells: proceedings of
an international workshop, held at the Research Centre Jiilich, Jiilich, Fed. Rep. of Germany, 8-11 August 19901
P. A. Hargrave, K. P. Hofmann, UB. Kaupp (eds.). p. cm. - (Research reports in physics) Contains edited
papers presented at the International Symposium on Signal Transduction in Photoreceptor Cells. Includes biblio-
graphical references and index.
ISBN-13:978-3-540-53765-6 (Springer-Verlag New York Berlin Heidelberg: acid-free paper) 1. Photorecep-
tors-Congresses. 2. Cellular signal transduction-Congresses. 3. Visual pigments-Congresses. I. Hargrave, P. A.
(Paul A.), 1938-. II. Hofmann, K. P. (Klaus Peter), 1943 -. III. Kaupp, 0. B. (0. Benjamin), 1949-. IV. Interna-
tional Symposium on Signal Transduction in Photoreceptor Cells (1990: Forschungszentrum Jiilich) V. Series.
QP 475.S564 1991 591.1'823-dc20 91-38290
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Preface
This volume contains manuscripts based upon talks presented at the International
Symposium on Signal Transduction in Photoreceptor Cells which was held at the
Forschungszentrum Jiilich August 8-11, 1990.* The meeting was dedicated to
the memory of Hermann Kuhn who made major contributions to our understand-
ing of transduction pathways in visual cells. Presentations at the meeting were
organized around the following topics: (1) Rhodopsin Structure and Function, (2)
Transducin and Phosphodiesterase, (3) Arrestin and Kinase, (4) The cGMP-gated
channel, (5) Role of Ca2+ in Photoreceptors, and (6) Transduction in Inverte-
brates.
In a Plenary Lecture, D. Oesterhelt (Martinsried, FRG) described the sen-
sory transduction system of the halobacteria. These primitive organisms employ
several retinal-containing pigments for sensory and ion-translocation purposes.
Their study is intrinsically interesting as well as serving as potential models for
the understanding of more complex systems.
Study of the structure and function of rhodopsin has been greatly aided by
use of the methods of molecular biology. T. Sakmar (Cambridge, MA, USA)
described his use of site specific mutagenesis to make systematic substitutions
of charged residues in the transmembrane helices of rhodopsin, leading to iden-
tification of the particular glutamic acid residue that serves as a counterion for
the protonated Schiff base. Vertebrate rhodopsin has also been cloned and ex-
pressed in the baculovirus system, (W. DeGrip, Nijmegen, The Netherlands)
which should facilitate production of sufficient quantities of mutant rhodopsin to
allow biophysical studies. An invertebrate rhodopsin, from octopus, has been
cloned and expressed (N. Abdulaev, Moscow, USSR). Although homologous to
vertebrate rhodopsins, this pigment also contains an unusual carboxyl-terminal
tail rich in prolines and glutamines. P. Hargrave and J.H. McDowell (Gainesville,
FL, USA) described their calorimetric studies on rhodopsin that show that the
transmembrane retinal-binding domain of the protein imparts most of its structural
stability.
Details of the mechanism of visual transduction are now better understood
than for any other sensory system. K.P. Hofmann (Freiburg, FRG) presented his
studies on the interaction of transducin and rhodopsin that identify those sites
involved in binding of transducin as distinguished from its activation. The steps
in the formation of the complex between photoexcited rhodopsin and transducin
* The complete material had reached Springer-Verlag by October 1991.
VII
Israel) presented his findings on the biochemical basis for retinal degeneration
in the Drosophila rdgB mutant. The defect in the mutant appears to increase
Ca2+ influx to the cell, which may represent a more general mechanism lead-
ing to photoreceptor cell death. Analysis of the ninaA Drosophila mutant has
led us to the unexpected finding that its gene product, the prolyl cis-trans iso-
merase cyclophilin, is required for normal expression of rhodopsin (B.-J. Shieh
and C. Zuker, La Jolla, CA, USA). This suggests that rhodopsin may need this
helper protein in order to achieve its proper folded structure. Finally, R. Paulsen
(Karlsruhe, FRG) presented the complete sequence of Calliphora rhodopsin and
described his unexpected observation that the early protein product is initially
glycosylated but the mature protein becomes deglycosylated.
The papers in this volume present a current and timely view of our state of
knowledge of visual transduction as we enter the last decade of the 20th century.
Our understanding of the molecular basis of vision has progressed exponentially
in the recent past, from the time of the entry of Hermann Kuhn to the area of
vision research in 1972. The exciting discoveries we have described here should
serve to pave the way for even greater advances in the future.
Jiilich, U.B. Kaupp
August 1991
Contents
Hennann Kuhn - In Memoriam
By P.A. Hargrave and M. Chabre (With 4 Figures) 1
Plenary Lecture
The Eyes of Halobacteria
By D. Oesterhelt .................................. 13
Part I Rhodopsin - Structure and Function
Mutagenesis Studies of Rhodopsin Phototransduction
By T.P. Sakmar, R.R. Franke, and H.G. Khorana
(With 5 Figures) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 21
Structural Stability of Rhodopsin and Opsin Studied
by Differential Scanning Calorimetry
By J.H. McDowell, S.M.A. Khan, D.W. Bolen, M.M. Santoro,
and P.A. Hargrave (With 2 Figures) ..................... 31
Molecular Analysis of Photoreceptor Protein Function
By W.J. de Grip, J.J.M. Janssen, R.G. Foster, H.-W. Korf,
K.J. Rothschild, E. Nevo, and G.LJ. de Caluwe
(With 7 Figures) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 42
Octopus Rhodopsin
By N.G. Abdulaev, I.D. Artamonov, and D.V. Zubov
(With 1 Figure) ................................... 60
Part II Transducin and Phosphodiesterase
The Activation of Transducin: Studies on its Mechanism
and Modulation
By K.P. Hofmann and M. Kahlert (With 10 Figures) .......... 71
x
The Transitory Complexes. Between Photoexcited Rhodopsin
and Transducin. Biochemical and Spectroscopic Studies
By F. Bornancin and C. Pfister (With 8 Figures) ............. 103
The Rate of GTP Hydrolysis by Transducin and the Termination
of the cGMP Cascade in Retinal Rods
By T.M. Vuong, F. Pages, P. Deterre, and M. Chabre
(With 5 Figures) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 119
The Molecular Biology of the Rod Photoreceptor cOMP
Phosphodiesterase a- and ,a-Subunits
By W. Baehr and SJ. Pittler (With 7 Figures) .............. 132
Part ill Deactivation Mechanisms
The Phosphorylation of Rhodopsin
By K. Palczewski and P.A. Hargrave .................... 151
Mechanisms of ,a-Adrenergic Receptor Desensitization
By MJ. Lohse .................................... 160
Part IV The cGMP-gated Channel
Gating Kinetics of the cGMP-Activated Conductance
of Retinal Cones
By K.-W. Yau and L.W. Haynes ....................... 175
Molecular Properties of the cGMP-gated Cation Channel
of Rod Photoreceptor Cells as Probed with Monoclonal Antibodies
By R.S. Molday, D.M. Reid, O. Connell, and L.L. Molday
(With 7 Figures) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 180
Cyclic Nucleotide-gated Channels - A Family of Proteins Involved
in Vertebrate Photoreception and Olfaction
By U.B. Kaupp, M. Vingron, W. Altenhofen, W. Bonigk,
E. Eismann, and 1. Ludwig (With 5 Figures) . . . . . . . . . . . . . . .. 195
Part V Ca2+ Metabolism and Light Adaptation
Interactions Between Calcium and cGMP
in Dialyzed Detached Retinal Rod Outer Segments
By G. Rispoli and P.B. Detwiler (With 5 Figures) . . . . . . . . . . .. 217
XI
The Role of Cytoplasmic Calcium Concentration
in Photoreceptor Light Adaptation
By T.D. Lamb (With 8 Figures) ........................ 236
Photoreceptor Guanylate Cyclase and Its Regulation by Calcium
By K.-W. Koch and H.-G. Lambrecht (With 5 Figures) ........ 259
Part VI Transduction in Invertebrates
Cyc1ic-GMP Phosphodiesterase in Photoreceptor Cells
in Limulus Ventral Eye
By M. Inoue, K. Ackermann, and 1.E. Brown (With 2 Figures) 271
The Molecular Mechanism of Retinal Degeneration
in the Retinal Degeneration B (rdgB) Mutant of Drosophila
By B. Minke, C.T. Rubinstein, I. Sahly, S. Bar-Nachum, E. Suss,
1. Kleiman, T. Byk, and Z. Selinger (With 6 Figures) ......... 281
Glycosylation of Dipteran Opsins During Membrane Biogenesis
By A. Huber and R. Paulsen (With 5 Figures) .............. 299
Molecular Genetics of Visual Transduction in Drosophila
By B.-H. Shieh and C.S. Zuker ........................ 308
Index of Contributors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 315
Subject Index .................................... 317
Hermann Kuhn - In Memoriam
P.A. Hargrave and M. Chabre
Hermann Kuhn was 49 years old when he died tragically in a mountaineering
accident on March 29th, 1988. We, in the visual sciences research community, mourn his
passing. As a visible expression of the high regard we had for Hermann, we have
gathered together for a meeting in his honor and to publish this collected volume
dedicated to his memory. Hermann's life touched all of us, and our lives are richer
because he lived. Hermann led a life rich both in experiences and in contributions. Each
of us was privileged to share a different part and a unique part of that life. Many of us,
his scientific colleagues, were influenced by his scientific accomplishments. Some of us
shared his music. Some of us were touched by his enthusiasm for the outdoors. All of us
admired the quiet and unassuming demeanor that accompanied his many talents. He
was a generous friend.
Hermann was born in 1939, and grew up in what we would all agree were difficult
times. As a youth he showed many accomplishments; in music and sports as well as in his
academic work. Hermann studied chemistry at the Universities of Munich and
Heidelberg, and received his Ph.D. in 1967. He continued research at Heidelberg, and
then in 1970, came to the United States, to California, with his wife Annie and their
young son Christoph. At CalTech he studied membrane biochemistry with Bill Dreyer.
At that period of time there were other postdoctoral fellows working in the laboratory;
David Papermaster, Paul Hargrave, and later, Bob Molday. Hermann began the study of
muscle ATPase, while Papermaster and Hargrave worked on rhodopsin. Hermann did a
comparative experiment using rod cell outer segments, and the rest is history. He found
that rhodopsin became phosphorylated in the presence of light. This finding shaped the
rest of his scientific career and propelled him into the area of vision research.
