CONTRACTILE MECHANISMS IN MUSCLE ADV ANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY Editorial Board: NATHAN BACK, State University of New York at Biiffalo NICHOLAS R. DI LUZIO, Tulane University School of Medicine EPHRAIM KATCHALSKI-KATZIR, The Weizmann Institute of Science DAVID KRITCHEVSKY, Wistar Institute ABEL LAJTHA, Rockland Research Institute ROOOLFO PAOLETTI, University of Milan Recent Volumes in this Series Volume 164 THROMBOSIS AND CARDIOVASCULAR DISEASES Edited by Antonio Strano Volume 165 PURINE METABOLISM IN MAN-IV Edited by Chris H. M. M. De Bruyn, H. Anne Simmonds, and Mathias M. Miiller Volume 166 BIOLOGICAL RESPONSE MODIFIERS IN HUMAN ONCOLOGY AND IMMUNOLOGY Edited by Thomas Klein, Steven Specter, Herman Friedman, and Andor Szentivanyi Volume 167 PROTEASES: Potential Role in Health and Disease Edited by Walter H. Horl and August Heidland Volume 168 THE HEALING AND SCARRING OF ATHEROMA Edited by Moshe Wolman Volume 169 OXYGEN TRANSPORT TO TISSUE-V Edited by D. W. Liibbers, H. Acker, E. Leniger-Follert, and T. K. Goldstick Volume 170 CONTRACTILE MECHANISMS IN MUSCLE Edited by Gerald H. Pollack and Haruo Sugi Volume 171 GLUCOCORTICOID EFFECTS AND THEIR BIOLOGICAL CONSEQUENCES Edited by Louis V. Avioli, Carlo Gennari, and Bruno Imbimbo Volume 172 EUKARYOTIC CELL CULTURES: Basics and Applications Edited by Ronald T. Acton and J. Daniel Lynn A Continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediately upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher. CONTRACTILE MECHANISMS IN MUSCLE Edited by Gerald H. Pollack University of Washington School of Medicine Seattle, Washington and Haruo Sugi Teikyo University School of Medicine Tokyo, Japan PLENUM PRESS • NEW YORK AND LONDON Library of Congress Cataloging in Publication Data Main entry under title: Contractile mechanisms in muscle. (Advances in experimental medicine and biology; v. 170) "Proceedings of the second international symposium on Cross-bridge mechanisms in muscle contraction, held in June of 1982, in Seattle, Washington" - Verso t.p. Includes bibliographical references and index. 1. Muscle contraction-Congresses. I. Pollack, Gerald H. II. Sugi, Haruo, 1933- III. Series. [DNLM: 1. Muscle contraction-Congresses. 2. Muscles-Physiology Congresses. WI AD559 v.170 / WE 500 1605 1982c] QP321.C73 1984 591.1'852 83-26950 ISBN 978-1-4684-4705-7 ISBN 978-1-4684-4703-3 (eBook) DOI 10.1007/978-1-4684-4703-3 Proceedings of the second international symposium on Cross-Bridge Mechanisms in Muscle Contraction, held in June of 1982, in Seattle, Washington ©1984 Plenum Press, New York Softcover reprint of the hardcover 1s t edition 1984 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013 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, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE Prior to the emergence of the sliding filament model, contraction theories had been in abundance. In the absence of the kinds of structural and biochemical information available today, it has been a simple matter to speculate about the possible ways in which tension generation and shortening might occur. The advent of the sliding filament model had an immediate impact on these theories; within several years they fell by the wayside, and attention was redirected towards mechanisms by which the filaments might be driven to slide by one another. In terms of identifying the driving mechanism, the pivotal observa tion was the electron micrographic indentification of cross-bridges extending from the thick filaments. It was quite naturally assumed that such bridges, which had the ability to split ATP, were the molecular motors, i.e., that they were the sites of mechanochemical transduction. Out of this presumption grew the cross-bridge model. in which filament sliding is presumed to be driven by the cyclic interaction of cross-bridges with complementary actin sites located along the thin filaments. Although some thirty years have elapsed since the sliding filament theory was first proposed, the cross-bridge mechanism of contraction remains a matter for debate and speculation. A variety of cross-bridge models has been proposed to account for contraction and there is a significant minority view that none of these models is satisfactory. Thus, the present status of the field is somewhat reminiscent of that just prior to the emergence of the sliding filament theory, where competing models formed the basis of considerable debate; except that at the present time the debate is more or less restrictt;d to which of the various cross-bridge models is most consistent with the data. Since most experiments on muscular contraction are currently designed, carried out and interpreted within the framework of Huxley and Huxley-Simmons type cross-bridge models. we felt it would be useful to consider the validity of the basic assumptions underlying these models. In 1978, one of us (H.S.) organized a symposium in Tokyo. at which time various results were rather thoroughly discussed on the above basis. and we published the proceedings under the title of "Cross-bridge Mechanisms in Muscle Contraction" (ed. H.E. Sugi and G.H. Pollack. University of Tokyo Press/University Park Press, 1979). The unusual interest in this volume encouraged us to organize the present symposium in Seattle in 1982, as a sequel to the Tokyo symposium. v vi Preface As in the earlier symposium. most papers describe experiments on intact. skinned or glycerinated muscles. where the three-dimensional filament-lattice structures have been preserved. Biochemical experi ments on actomyosin solution systems have been rather intentionally excluded to maintain this focus. This omission is not meant to imply that the organizers regard such experiments as unuseful; quite the contrary. We did feel. however that such work is well covered at various other sym posia. whereas much of the material contained herein is not. Thus we have attempted to emphasize the relationship between structure and function. The preceedings of the symposium have been divided into two parts. The first, entitled Structural Dynamics, focuses on structural aspects of the contractile process, particularly on dynamic structural changes in thick filaments and cross-bridges. Controversial areas are not only incor porated but emphasized. These include, for example. questions of whether thick filaments shorten during contraction and questions of whether there is indeed any significant rotation of cross-bridges during tension development. New methods are brought to bear on these and other questions. The second part. entitled Mechanics, Energetics, and Molecular Models. builds on the structural information in the first part in attempting to relate findings of mechanical and energetic experiments to molecular models. Again. the emphasis is on new and controversial topics. Both parts contain three types of presentation that have been woven into a cohesive framework. These are: full oral presentations. posters. and short, extemporaneous presentations that were later formalized into short communications. The organizational format is by topic. Thus, each section of the book may contain a number of topically related contribu tions of variable length. More than half the time of the symposium was devoted to discussion. Many participants came away from the meeting expressing the view that the discussions were among the most stimulating and informative of any symposium they had attended. Thus. we have endeavored to preserve the pristine nature of the interchanges as much as possible. Only repetitious or vague comments were deleted. and only minor reorganizations were required to preserve continuity. The short poster presentations also con tain discussion sections; these are summaries. prepared by the presen tor. of the most interesting and provocative comments surrounding their poster. This seminar was originally planned as one of the United States - Japan Cooperative Seminars, under the auspices of the National Science Foundation and the Japan Society for the Promotion of Science, for a lim ited number of U.S. and Japanese participants. Owing to generous addi tional support from Teikyo University, Rigaku Denki, Inc., the Center for Advanced Studies of the University of Washington, and the American Cyanamid Company. we were able to invite many additional participants. particularly Europeans. Although there were still others we would like to have been able to invite, the complement of scientists included many Preface vii distinguished scientists from around the world as well as younger investi gators who we felt had something significant to contribute. -Gerald H. Pollack -Haruo Sugi ACKNOWLEDGEMENTS The editors express their sincere thanks to the National Science Foundation and the Japan Society for the Promotion of Science for the basic financial support of this symposium. Our thanks are also due to Dr. Shoichi Okinaga, President of Teikyo University, to Mr Hikaru Shimura, President of Rigaku Denki, Inc. and to Professor Robert F. Rushmer, Director of the Center for Advanced Studies at the University of Washington as well as to the American Cyanamid Com pany, for their very generous additional financial support which enabled us to invite so many distinguished investigators from various countries. We owe a debt of gratitude to Toni Ameslav, Joanne Brubaker, Joy Crist and Eileen Swanberg who spent countless hours transcribing the tapes of the discussions and painstakingly retyping all the manuscripts. and especially to Kathy Altringham, our Editorial Assistant, who assumed major responsibility for preparing the text for camera-ready duplication. G.P. B.S. viii CONTENTS PART I: STRUCTURAL DYNAMICS STRUCTURE OF THE UYOFILAMENTS Introduct.ion 3 Symmet.ry and Self-Assembly in Vertebrat.e A-Filament.s 5 A..1. Rowe and )(.C. )(a.w Image Analysis of the Complex of Actin-Tropomyosin and 21 Myosin Subfragment 1 T. lrakabayubl. C. ToJOllhima and E. Iata.yama A-Band Mass Exceeds Mass of it.s Filament Component.s by 30-45% 29 )(.1(. Reedy and C. Lucaveche Myofilament. Diamet.ers: An Ultrast.ruct.ural Re-Evaluat.ion 47 TJ. Robinson and L. Cohen-Could DO THICK FILAMENTS SHORTEN? Int.roduction 65 Limulus St.riat.ed Muscle Provides an Unusual Model for 67 Muscle Cont.raction )(.J[. Dewey. P. BrInk, D..E. Colftellh. B. GayUnn. Sol'. Fan and 1'. Anapol Dynamic Laser Light. Scattering of Papain-Treat.ed Thick 89 Filaments from Limulus St.riat.ed Muscle in Suspension S-I'. Fan.)(JI. Dewey, D• .C ol1I.ellh, P. BriDk and B. Chu St.ructure of Limulus and Ot.her Invert.ebrat.e Thick Filament.s 93 lU.C. Lerine. R.W.Kensler.)(. Reedy. lr. Boftman. S. Dmdheiaer and R.E. Davies ix x Contents Cinematographic Studies on the A-Band Length Changes During 107 Ca-Activated Contraction in Horseshoe Crab Muscle Myofibrils B. Sugi and S. Gomi Contraction Bands: Differences Between Physiologically vs. 119 Maximally Activated Single Heart Muscle Cells J. Krueger and B • .London Structural Studies of Glycerinated Skeletal Muscle. A-Band 135 Length and Cross-Bridge Period in ATP-Contracted Fibers P. Dreizen,. L Berman and J.E. Berger X-RAY DIFFRACTION APPROACHES TO STRUCTURAL DYNAMICS Introduction 159 Time Resolved X-Ray Diffraction Studies of Cross-Bridge 161 Movement. and Their Interpretation B.E.Huxley On the Possibility of Interaction Between Neighbouring Crossbridges 177 R.T. Tregear and II. L Clarke Cross-Bridge States in Invertebrate Muscles 185 J.S.lrrq Factors Affecting the Equatorial X-Ray Diffraction Pattern from 193 Contracting Frog Skeletal Muscle B. Tanaka,. B. Hasbizume and H. Sug1 Effect of Stretch on the Equatorial X-Ray Diffraction Pattern 203 from Frog Skeletal Muscle in Rigor B. Tanaka,. B. Sugi and B. Basbizume Structural Studies of Muscle During Force Development in 207 Various States I.e. Yu. T. Arata" A.C. steftn. GAS. Naylor. B.C. Gamble and R.J. Podolaky Muscle Crossbridge Positions from Equatorial Diffraction Data: 221 An Approach Towards Solving the Phase Problem J. Squire and J. Harford Configurations of Myosin Heads in the Crab Striated Muscle 237 as Studied by X-Ray Diffraction K. lrakabqasbi. K. Namba and T. Mitsui