Transduction in Biological Systems978-1-4684-5736...Library of Congress Cataloging-in-Publication...
Transcript of Transduction in Biological Systems978-1-4684-5736...Library of Congress Cataloging-in-Publication...
Transduction in Biological Systems
Series of the Centro de Estudios Cientificos de Santiago
Series Editor: Claudio Teitelboim Centro de Estudios Cientfjicos de Santiago, Santiago, Chile and Institute/or Advanced Study Princeton, New Jersey, USA
IONIC CHANNELS IN CELLS AND MODEL SYSTEMS Edited by Ramon Latorre
PHYSICAL PROPERTIES OF BIOLOGICAL MEMBRANES AND THEIR FUNCTIONAL IMPLICATIONS Edited by Cecilia Hidalgo
PRINCIPLES OF STRING THEORY Lars Brink and Marc Henneaux
QUANTUM MECHANICS OF FUNDAMENTAL SYSTEMS 1 Edited by Claudio Teitelboim
QUANTUM MECHANICS OF FUNDAMENTAL SYSTEMS 2 Edited by Claudio Teitelboim and Jorge Zanelli
TRANSDUCTION IN BIOLOGICAL SYSTEMS Edited by Cecilia Hidalgo, Juan Bacigalupo, Enrique Jaimovich, and Julio Vergara
Transduction in Biological Systems
Edited by
Cecilia Hidalgo Centro de Estudios Cient{jicos de Santiago
and Universidad de Chile Santiago, Chile
Juan Bacigalupo Universidad de Chile
Santiago, Chile
Enrique Jaimovich Centro de Estudios Cient{jicos de Santiago
and Universidad de Chile Santiago, Chile
and
Julio Vergara University of California at Los Angeles
Los Angeles, California
PLENUM PRESS. NEW YORK AND LONDON
Library of Congress Cataloging-in-Publication Data
Transduction in biological systems I edited by Cecilia Hidalgo •.. ret a 1. l.
p. c~. -- (Series of the Centro des Estudios Cientlficos de Santiago)
Originated from the Workshop "Transduction in Biological Syste~s", held May 23-30, 1988, at the Marine Biological Station of the Universidad de Valparaiso, Montemar, Chile, and contains contributions from most of the participants.
Includes bibliographical references.
ISBN-13: 978-1-4684-5738-4 001: 10.1007/978-1-4684-5736-0
e-ISBN-13: 978-1-4684-5736-0
1. Cellular signal transduction--Congresses. I. Hidalgo, Cecilia. II. Workshop "Transduction in Biological Systems" Marine Biological Station of the Universidad de Valparaiso) III. Ser i es. QP517.C45T7 1990 591 . 1 . 8--dc20
© 1990 Plenum Press, New York Softcover reprint of the hardcover 15t edition 1990 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013
All rights reserved
(1988 ,
90-35639 CIP
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, microfilming, recording, or otherwise, without written permission from the Publisher
Contributors
Barbara H. Alderson, Department of Physiology and Biophysics, The University of Texas Medical Branch, Galveston, Texas 77550
Bojena Antoniu, Department of Muscle Research, Boston Biomedical Research Institute, Boston, Massachusetts 02114
Illani Atwater, Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
Juan Bacigalupo, Departamento de Biologia, Facultad de Ciencias, Universidad de Chile, Santiago, Chile
Nelly Bennett, Laboratoire Biophysique Moleculaire et Cellulaire, Centre d'Etudes Nucleaires de Grenoble, 38041 Grenoble Cedex, France
Michael V. L. Bennett, Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461
Barbara Block, Departments of Biology and Anatomy, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018. Present address: Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois 60637
Neil R. Brandt, Department of Pharmacology, University of Miami School of Medicine, Miami, Florida 33101
v
vi Contributors
Mariange/Q Bravin, Centro di Studio per la Fisiologia dei Mitocondri del CNR, Istituto di Patologia Generale dell'Universita di Padova, 35131 Padua, Italy
Gustavo Brum, Departamento de Biofisica, Facultad de Medicina, Universidad de la Republica, Montevideo, Uruguay
Donald Brunder, Department of Physiology and Biophysics, The University of Texas Medical Branch, Galveston, Texas 77550
Ricardo BuU, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
A. Lee Bums, Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
M. Angelica Carrasco, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Patricia CarroU, Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
Anthony H. Caswell, Department of Phannacology, University of Miami School of Medicine, Miami, Florida 33101
Kevin J. Catt, Endocrinology and Reproduction Research Branch, National Institute of Child and Human Development, National Institutes of Health, Bethesda, Maryland 20892
Armel Clerc, Laboratoire Biophysique Moleculaire et Cellulaire, Centre d'Etudes Nucleaires de Grenoble, 38041 Grenoble Cedex, France
Deida Compagnon, Department of Physiology, University of California-Los Angeles, Los Angeles, California 90024
Serge Crouz;y, Laboratoire Biophysique Moleculaire et Cellulaire, Centre d'Etudes Nucleaires de Grenoble, 38041 Grenoble Cedex, France
Yves Chapron, Laboratoire Biophysique Moleculaire et Cellulaire, Centre d'Etudes Nucleaires de Grenoble, 38041 Grenoble Cedex, France
Pien-e Deslongcluunps, Laboratory of Organic Synthesis, Department of Chemistry, Faculty of Science, University of Sherbrooke, Sherbrooke, Quebec JIK 2R1, Canada
Christine Dettbam, Department of Physiology and Biophysics, The University of Texas Medical Branch, Galveston, Texas 77550
Francesco Di Virgilio, Centro di Studio per la Fisiologia dei Mitocondri del CNR, Istituto di Patologia Generale dell'Universita di Padova, 35131 Padua, Italy
Donald G. Ferguson, Department of Physiology and Biophysics, University of Cincinnati, Cincinnati, Ohio 45267
Contributors vII
Robert Fitts, Department of Physiology, Rush University, Chicago, Illinois 60612. Permanent address: Departmennt of Biology, Marquette University, Milwaukee, Wisconsin 53233.
Clara Franzini-Armstrong, Department of Anatomy, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018
W. Hanke, Universitat Osnabrock, FB Biologie, Biophysik, D-45oo Osnabrock, Federal Republic of Germany
Lawrence W. Haynes, Howard Hughes Medical Institute, and Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205. Present address: Department of Medical Physiology, University of Calgary. Alberta T2N 4Nl, Canada
Cecilia Hidalgo, Departamento de Fisiologfa y Bioffsica, Facultad de Medicina, Universidad de Chile, and Centro de Estudios Cientfficos de Santiago, Santiago, Chile
Noriaki lkemoto, Department of Muscle Research, Boston Biomedical Research Institute, Boston, Massachusetts, 02114, and Department of Neurology, Harvard Medical School, Boston, Massachusetts 02115
Michele lldefonse, Laboratoire Biophysique Moleculaire et Cellulaire, Centre d'Etudes Nucleaires de Grenoble, 38041 Grenoble Cedex, France
Veronica lrribarra, Departamento de Fisiologfa y Bioffsica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Vincent Jacquemond, Laboratoire de Physiologie des Elements Excitables, Universite Claude Bernard, F-69622 Villeurbanne Cedex, France
Enrique Jaimovich, Departamento de Fisiologia y Bioffsica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Edwin Johnson, Marshall University School of Medicine, Huntington, West Virginia 25704
Kyung Sook Kim, Department of Pharmacology, University of Miami School of Medicine, Miami, Florida 33101
Nestor Lagos, Department of Physiology, University of California-Los Angeles, Los Angeles, California 90024
Frank A. LatUlnzio, Jr., Department of Pharmacology, University of Nevada School of Medicine, Reno, Nevada 89557
Daniel P. Lew, Division des Maladies Infectieuses, Hopital Cantonal Universitaire, 1211 Geneva 4, Switzerland
John E. Lisman, Department of Biology, Brandeis University, Waltham, Massachusetts 02254
viii Contributors
Maria V. Lobo, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Ch.ile
Mario Luxoro, Laboratorio de Fisiologia Celular, Facultad de Ciencias y Facultad de Medicina, Universidad de Chile, Santiago, Chile
Juan Jose Marengo, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Elisa T. Marusic, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Gerhard Meissner, Departments of Biochemistry and Physiology, School of Medicine, University of North Carolina, Chapel Hill, North Carolina 27599-7260
Jacopo Meldolesi, Dipartimento di Farmacologia dell'Universita di Milano, Centro di Studio, di Cito Farmacologia del CNR, Istituto Scientifico San Raffaele, 20132 Milan, Italy
Veronica Nassar-Gentina, Laboratorio de Fisiologia Celular, Facultad de Ciencias y Facultad de Medicina, Universidad de Chile, Santiago, Chile
Philip Palade, Department of Physiology and Biophysics, The University of Texas Medical Branch, Galveston, Texas 77550
Richard Payne, Department of Zoology, University of Maryland, College Park, Maryland 20742
Gonzalo Perez, Unidad de Inmunologia Celular, Instituto de Nutrici6n y Tecnologia de los Alimentos, Universidad de Chile, Santiago, Chile
Gonzalo Pizarro, Department of Physiology, Rush University, Chicago, Illinois 60612
Harvey B. Pollard Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
Tullio Pozzan, Centro di Studio per la Fisiologia dei Mitocondri del CNR, Istituto di Patologia Generale dell'Universita di Padova, 35131 Padua, Italy
Evelyn Reilley, Department of Muscle Research, Boston Biomedical Research Institute, Boston, Massachusetts 02114
Eduardo Rios, Department of Physiology, Rush University, Chicago, Illinois 60612
Esther Robinson, Department of Pharmacology, University of Nevada School of Medicine, Reno, Nevada 89557
Phyllis Robinson, Department of Biology, Brandeis University, Waltham, Massachusetts 02254
Luis Robles, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Contributors ix
Cecilia Rojas, Departamento de Fisiologfa y Biofisica, Facultad de Medicina, Universidad de Chile, ~antiago, Chile
Eduardo Rojas, Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
Mario S. Rosemblatt, Unidad de Immunologia Celular, Instituto de Nutrici6n y Tecnologia de los Alimentos, Universidad de Chile, Santiago, Chile, and Department of Muscle Research, Boston Biomedical Research Institute, Boston, Massachusetts 02114
Oger Rougier, Laboratoire de Physiologie des Elements Excitables, Universite Claude Bernard, F-69622 Villeurbanne Cedex, France
Luc Ruest, Laboratory of Organic Synthesis, Department of Chemistry, Faculty of Science, University of Sherbrooke, Sherbrooke, Quebec 11K 2Rl, Canada
Juan C. Saez, Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461
Ximena Sanchez, Departamento de Fisiologia y Biofisica, Facultad de Medicina, Universidad de Chile, Santiago, Chile
Rosa Santos, Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
Robert G. Schlatterer, Department of Pharmacology, University of Nevada School of Medicine, Reno, Nevada 89557
Arthur Sherman, Mathematics Research Branch,National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892
R. Simmoteit, Universitiit Osnabriick, FB Biologie, Biophysik, D-4500 Osnabriick, Federal Republic of Germany
David C. Spray, Department of Neuroscience, Albert Einstein College of Medicine, Bronx, New York 10461
Philip Stein, Department of Physiology and Biophysics, The University of Texas Medical Branch, Galveston, Texas 77550
Stanko S. Stojilkovic, Endocrinology and Reproduction Research Branch, National Institute of Child and Human Development, National Institutes of Health, Bethesda, Maryland 20892
Andres Stutzin, Laboratory of Cell Biology and Genetics, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland 20892. Present address: Laboratorio de Fisiopatologia Molecular, Departamento de Medicina Experimental, Facultad de Medicina, Universidad de Chile, Santiago, Chile
x Contributors
Benjamin A. Suarez-Isla, Departamento de Fisiologia y Biofisica, FacuItad de Medicina, Universidad de Chile, and Centro de Estudios Cientificos de Santiago, Santiago, Chile
John L. SUlko, Department of Pharmacology, University of Nevada School of Medicine, Reno, Nevada 89557
Jane A. Talvenheimo, Department of Pharmacology, University of Miami School of Medicine, Miami, Rorida 33101
Ismael Uribe, Department of Physiology, Rush University, Chicago, Illinois 60612. Present address: Centro de Investigaci6n del Instituto Politecnico Nacional, Mexico City, Mexico
R. A. Venosa, Catedra de Fisiologia y Biofisica, FacuItad de Ciencias Medicas, Universidad Nacional de La Plata, 1900 La Plata, Argentina
Pedro Verdugo, Center for Bioengineering, University of Washington, Seattle, Washington 98195
Julio Vergara, Department of Physiology, University of California-Los Angeles, Los Angeles, California 90024
Manuel Villalon, Center for Bioengineerin~, University of Washington, Seattle, Washington 98195
Pompeo Volpe, Department of Physiology and Biophysics, The University of Texas Medical Branch, Galveston, Texas 77550
Richard E. Weiss, Department of Pediatrics, Division of Cardiology, University of California-Los Angeles, Los Angeles, California 90024-1743
Shu-Rong Wen, Department of Pharmacology, University of Miami School of Medicine, Miami, Rorida 33101; and Department of Pharmacology, Beijing Medical University, Beijing, People's Republic of China
King-Wai Yau, Howard Hughes Medical Institute, and Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Maryland 21205
Patricio Zapata, Laboratorio de Neurobiologia, Universidad Cat6lica de Chile, Santiago, Chile
Preface
The present volume originated from the workshop "Transduction in Biological Systems," held at the Marine Biological Station of the Universidad de Valparaiso, Montemar, Chile, May 23-30, 1988, and contains contributions from most of the participants in the workshop.
The title of both the workshop and the book reflects accurately the central theme discussed during several days of intense debate and profound intellectual exchange in the peaceful environment offered by the central coast of Chile. It was apparent that the workshop was a great success-a sentiment expressed by many seasoned attendees, some of whom dared opinions as strong as "It was the best ever."
There is no single reason to explain why this workshop was so successful. Certainly instrumental was the incredible effort displayed by the Chilean Organizing Committee in selecting adequate facilities and in organizing social events that supplemented the scientific sessions and provided an authentic fraternal environment for the participants. Equally important were the foreign participants, who enthusiastically gave of their time to take part in the event, and the students, who came from Chile as well as from several other Latin American countries, and who applied the necessary pressure in their repeated demands for scientific clarity, accuracy, and sincerity.
Transduction processes are of fundamental importance in biological systems. In spite of their diversity, several similarities can be distinguished among them. Thus, the discussions in the chapters that compose this book are oriented toward the definition of common features in this field. We believe that this heterogeneous group of contributors, with widely different backgrounds ranging from classical electrophysiology to highly
xl
xii Preface
specialized biochemistry, and working in dissimilar biological systems, constituted an excellent group to discuss the general principles underlying biological transduction mechanisms. It is our hope that the outcome of these interdisciplinary interactions, crystallized in this book, will provide the reader with a unifying perspective on the role of second messengers in biological systems, and that this book will transmit to the scientific community the unique spirit of integration attained during the workshop.
We would like to thank the National Science Foundation, U.S.A., for their grant NSF !NT 87-15069, which provided travel support for most of the scientists from the U.S. who participated in the workshop. We also thank the Chilean sponsors, Fundacion Andes, CONICYT, and the Universidad de Chile, for providing funds for the organization of the workshop. Our special thanks go to the Chilean Organizing Committee, the tireless efforts of whose members (I. Behrens, R. Bull, A. Carrasco, P. Donoso, M. E. Fernandez, V. Nassar-Gentina, C. Rojas, and C. Vergara) made this workshop, and hence this book, possible.
The Editors Santiago and Los Angeles
Contents
Introduction ...................................................... .
I. STIMULUS-RESPONSE COUPLING
A. Transduction in Sensory Cells
Chapter 1
Dynamics of the Release of Calcium by Light and Inositol I,4,S-Trisphosphate in Limulus Ventral Photoreceptors .................................... 9
Richard Payne
Chapter 2
Second Messengers in Invertebrate Phototransduction
Juan Bacigalupo, Edwin Johnson, Phyllis Robinson, and John E. Lisman
Chapter 3
The cGMP-Gated Channels of Rod and Cone Photoreceptors
Lawrence W. Haynes and King-Wai fau
xiii
27
47
xlv Contents
Chapter 4
Functional Aspects of the cGMP-Activated Channel from Bovine Rod Outer Segments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 59
w. Hanke and R. Simmoteit
Chapter 5
A Complex Regulation of the cGMP-Dependent Channels of Retinal Rod Membranes by the cGMP Phosphodiesterase ............................ 75
Michele Ildefonse, Nelly Bennet, Serge Crouzy, Yves Chapron, and Armel Clerc
Chapter 6
Transduction, Signal Transference, and Encoding in Composite Chemoreceptors: A Comparison between Gustatory and Arterial Chemoreceptors .................................................... 87
Patricio Zapata
B. Excitation-Secretion Coupling
Chapter 7
Role of Membrane Receptors in Stimulus-Secretion Coupling . ............. 101
Illani Atwater, Eduardo Rojas, and Rosa M. Santos
Chapter 8
Glucose Dose Response of Pancreatic ~CeUs: Experimental and Theoretical Results .................................................. 123
Arthur Sherman, Patricia Carroll, Rosa M. Santos, and Illan; Atwater
Chapter 9
Electrical and Secretory Response to Cholinergic Stimulation in Mouse and Human Adrenal Medullary Chromaffin CeUs ............................ 143
Veronica Nassar-Gentina, Harvey B. Pollard, and Eduardo Rojas
Chapter 10
Calcium Currents and Hormone Secretion in the Rat Pituitary Gonadotroph . 163
Andres Stutzin, Stanko S. Stojilkovic, Kevin J. Catt, and Eduardo Rojas
Chapter 11
Synexin-Driven Membrane Fusion: Molecular Basis for Exocytosis ......... 175
Eduardo Rojas, A. Lee Burns, and Harvey B. Pollard
Contents xv
Chapter 12
Signal Transduction and Ion Permeability in Adrenal Glomerulosa Cells . .... 195
Elisa T. Marusic and Maria V. Lobo
C. Other Transduction Mechanisms
Chapter 13
The Target of InositoII,4,5-Trisphosphate in Nonmuscle Cells: Calciosome or Endoplasmic Reticulum? ............................................. 209
Pompeo Volpe, Mariangela Bravin, Barbara H. Alderson, Daniel P. Lew, Jacopo Meldolesi, and Tullio Pozzan
Chapter 14
Stimulus-Response Coupling in Mammalian Ciliated Cells: The Role of Ca2 +
in Prostaglandin Stimulation .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 221
Manuel Villalon and Pedro Verdugo
Chapter 15
Hepatocyte Gap Junctions: Metabolic Regulation and Possible Role in Liver Metabolism ........................................................ 231
Juan C. Saez, Michael V. L. Bennett, and David C. Spray
Chapter 16
Mechanisms of Frequency Tuning in the Internal Ear .................... 245
Luis Robles
II. EXCITATION-CONTRACTION COUPLING IN STRIATED MUSCLE
A. Sodium Channels and Sodium Pump
Chapter 17
Coexistence of Different Types of Sodium Channels in Striated Muscle and Nerve ............................................................. 261
Richard E. Weiss
Chapter 18
Sodium Pump in T-Tubules of Frog Muscle Fibers .. . . . . . . . . . . . . . . . . . . . .. 275
R. A. Venosa
xvi Contents
B. Calcium Channels in T-Tubule
Chapter 19
Excitation-Contraction Coupling in Barnacle Muscle Fibers: Does Calcium Entry Trigger Contraction Directly? .................................... 289
Mario Luxoro, Veronica Nassar-Gentina, and Eduardo Rojas
Chapter 20
Biochemical Structure of the Dihydropyridine Receptor
Jane A. Talvenheimo, Shu-Rong Wen, Kyung Sook Kim, and Anthony H. Caswell
Chapter 21
301
Role of Slow Inward Calcium Current in Excitation-Contraction Coupling .. 321
Vincent Jacquemond and Ogier Rougier
C. Molecular Architecture of the Triad
Chapter 22
Molecular Architecture of T-SR Junctions: Evidence for a Junctional Complex That Directly Connects the Two Membrane Systems ...................... 339
Clara Franzini-Armstrong, Barbara Block, and Donald G. Ferguson
Chapter 23
Proteins of the Triad Junction of Skeletal Muscle ........................ 361
Anthony H. Caswell, Neil R. Brandt, Shu-Rong Wen, and Jane A. Talvenheimo
Chapter 24
Monoclonal Antibodies as Probes of Triad Structure and Excitation-Contraction Coupling in Skeletal Muscle ............................... 371
Mario S. Rosemblatt, Gonzalo Perez, Bojena Antoniu, Evelyn Reilley, and Noriaki Ikemoto
D. Transduction at the Triad
Chapter 25
A Third Role for Calcium in Excitation-Contraction Coupling ............. 385
Eduardo Rios, Robert Fitts, Ismael Uribe, Gonzalo Pizarro, and Gustavo Brum
Chapter 26
A Pharmacological Approach to the Physiological Mechanism of Excitation-Contraction Coupling . ............................................... 401
Philip Palade, Donald Brunder, Christine Dettbarn, and Philip Stein
Contents xvII
Chapter 27
A Chemical Mechanism for Excitation-Contraction Coupling in Skeletal Muscle ............................................................ 415
Julio Vergara, Nestor Lagos, and Deida Compagnon
Chapter 28
What We Know and What We Would Like to Know about the Role of Inositol I,4,5-Trisphosphate in Skeletal Muscle . ................................ 429
Pompeo Volpe, Francesco Di Virgilio, and Tullio Pozzan
Chapter 29
Calcium Release in Skinned Muscle Fibers: Effect of Inositol 1,4,5-Trisphosphate ...................................................... 439
Enrique Jaimovich, Cecilia Rojas, and Eduardo Rojas
Chapter 30
Metabolism of Phosphoinositides in Skeletal Muscle Membranes . ........... 449
Cecilia Hidalgo, Ximena Sanchez, and M. Angelica Carrasco
E. Calcium Release
Chapter 31
Pharmacology of the Ryania Alkaloids: The Ester A, a Ryanodine Analog That Only Increases Sarcoplasmic Reticulum Calcium Permeability ......... 465
John L. Sutko, Esther Robinson, Frank A. Lattanzio, Jr., Robert G. Schlatterer, Pierre Deslongchamps, and Luc Ruest
Chapter 32
Ca2 + Release Channel of Sarcoplasmic Reticulum: Characterization of the Regulatory Sites .................................................... 475
Gerhard Meissner
Chapter 33
Calcium Channels in Sarcoplasmic Reticulum Membranes Isolated from Skeletal Muscle ..................................................... 487
Benjamin A. Suarez-Isla, Juan Jose Marengo, Veronica Irribarra, and Ricardo Bull
Index ............................................................. 501