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