MECHANISMS OF WORK PRODUCTION AND WORK ABSORPTION IN MUSCLE

ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY

Editorial Board:

NA THAN BACK, State University of New York at Buffalo

lRUN R. COHEN, The Weizmann Institute of Science

DAVID KRITCHEVSKY, Wistar Institute

ABEL LAJTHA, N. S. Kline Institute for Psychiatric Research

RODOLFO PAOLETTI, University of Milan

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MECHANISMS OF WORK PRODUCTION AND WORK ABSORPTION IN MUSCLE

Edited by

Haruo Sugi Teikyo University Tokyo, Japan

and

Gerald H. Pollack University of Washington Seattle, Washington

Prepared under the auspices of the International Union of Physiological Sciences

PLENUM PRESS • NEW YORK AND LONDON

Library of Congress Cataloging-in-Publication Data

Mechanisms of work production and work absorption in muscle I edited by Haruo Sugi and Gerald H, Pollack; prepared under the auspices of the International Union of Physiological Sciences.

p. cm. -- (Advances in experimental medicine and biology; v. 453)

"Proceedings of a Symposium on Mechanisms of Work Productionand Work Absorption in Muscle, held October 27-31, 1997, in Hakone, Japan"--T.p, verso.

Includes bibliographical references and indexes.

ISBN-13: 978-1-4684-6041-4 e-ISBN-13: 978-1-4684-6039-1 001: 10.1007/978-1-4684-6039-1

1. Muscle contraction--Congresses. 2. Muscles--Molecular aspects­-Congresses. 3. Actomyos 1 n--Congresses. I. Sug i, Haruo, 1933-II. Pollack, Gerald H. III. International Unlon of Physiological Sciences. IV. Symposium on Mechanisms of Work Production and Work Absorption in Muscle (1997 Hakone-machi, Japan) V. Series. QP321.M3395 1998 573.7'54--dc21 98-31319

CIP

Proceedings of a Symposium on Mechanisms of Work Production and Work Absorption in Muscle, held October 27 - 31, 1997, in Hakone, Japan

© 1998 Plenum Press, New York Softcover reprint ofthe hardcover I st edition 1998 A Division of Plenum Publishing Corporation 233 Spring Street, New York, N.Y. 10013

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1098765432 1

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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

This volume presents the proceedings ofa symposium organized by one of us (H.S.) that was held on October 27-31, 1997 in Hakone, Japan, under the title "Mechanisms of Work Production and Work Absorption in Muscle." We have already published similar proceedings four times in the past: in 1978 under the title, "Cross-bridge Mechanism in Muscle Contraction" (University of Tokyo Press); in 1984 under the title, "Contractile Mechanism in Muscle Contraction" (Plenum); in 1988 under the title, "Molecular Mecha­nism of Muscle Contraction" (Plenum); and in 1993 under the title, "Mechanism of Myofilament Sliding in Muscle Contraction" (Plenum). In contrast to common practice, we have always tried to include as many discussions held at the meeting in our proceed­ings as possible, so as to enable readers to properly evaluate each paper presented, as well as to learn of future prospects in this field of research. Although the policy of including discussions occasions a long publication delay, we believe that it is worth repeating in our future publications, as we have met a number of young investigators fascinated by the dis­cussions in our proceedings.

The 1997 Hakone Symposium was somewhat different from the previous ones. Since 1993, I have chaired the Commission on Muscle Physiology of the International Un­ion of Physiological Sciences (!uPS), and have participated in !UPS official meetings, re­alizing that the IUPS executive members' main concern is to take every opportunity to emphasize the importance of "classical" or "integrative" physiology. At the end of 1996, Dr. Erwin Neher, Vice-president of the IUPS, suggested to me that I make a proposal to organize an international symposium based on this IUPS policy. In response to his sugges­tion, I presented a proposal to organize a symposium on "Mechanisms of Work Production and Work Absorption in Muscle," in which I included several prominent cardiac physiolo­gists, so as to realize the general theme of the IUPS, "From Molecules to Humans." Fortu­nately, my proposal was approved and granted. This symposium is therefore organized under the auspices of the IUPS, and is partly supported by an IUPS grant.

In the concluding remarks in this volume, Dr. Hugh E. Huxley, a principal architect of the sliding filament mechanism of muscle contraction, states that the molecular mecha­nism of myofilament sliding remains mysterious to all of us. We hope that this volume will stimulate muscle investigators to design and perform novel experiments to clarify the mysteries in muscle contraction.

Haruo Sugi Gerald H. Pollack

ACKNOWLEDGMENTS

The editors would like to express their sincere thanks to the International Union of Physiological Sciences and Teikyo University (Dr. Shoichi, Okinaga, President) for gener­ous financial support, which made this symposium possible.

Our thanks are also due to Uehara Science Foundation and Kanagawa Science Acad­emy Foundation for their additional financial support.

We owe a debt of gratitude to Ms. Sarah Richards at the University of Washington and Ms. Naoko Itagaki at Teikyo University for their enormous efforts in preparing the discussion records, and to Drs. Teizo Tsuchiya, Takenori Yamada, Suechika Suzuki, Shig­eru Chaen, Yasutake Saeki, Takakazu Kobayashi, and Ms. Ibuki Shirakawa for compiling the indices.

vii

CONTENTS

1. Introductory Remarks Haruo Sugi

I. Molecular Mechanism of Actin-Myosin Interaction, Part I

2. Linear and Rotary Molecular Motors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5 Kazuhiko Kinosita, Jr.

3. Measurement of ATPase Activities of Myosin at the Level of Tracks and Single Molecules .. :................................................ 15

Paul B. Conibear, Philip A. Kuhlman, and Clive R. Bagshaw

4. Evanescent Excitation Microscopy: Its Application to the Study of Single Molecular Process Kinetics of Actomyosin Motor ................... 29

Hidetake Miyata, Shigeru Chaen, Seiryo Sugiura, and Haruo Sugi

5. Three-Dimensional Image Analysis of Myosin Head in Function as Captured by Quick-Freeze Deep-Etch Replica Electron Microscopy ............... 37

Eisaku Katayama, Gouki Ohmori, and Norio Baba

6. Fluctuation Correlation in the Sliding Movement Generated by Protein Motors in Vitro. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 47

K. Tawada, M. Toyoda, Y. Imafuku, and A. Yamada

7. ATP-Induced Axial Movement of Myosin Heads in Living Thick Filaments Recorded with a Gas Environmental Chamber Attached to the Electron Microscope .................................................. 53

Haruo Sugi, Tsuyoshi Akimoto, Shigeru Chaen, and Suechika Suzuki

8. Design Principles and Applications of a Cooled CCD Camera for Electron Microscopy .................................................. 63

A. R. Faru.qi

ix

x Contents

II. Molecular Mechanism of Actin-Myosin Interaction, Part II

9. Structure of the Monomeric Actin-Myosin Head Complex as Revealed by X-Ray Solution Scattering ...................................... 73

T. Arata, S. Kimura, Y. Sugimoto, Y. Takezawa, N. Iwasaki, and K. Wakabayashi

10. The Use of Fast Kinetic Systems for the Study ofng-Ilg Quantities of Purified Muscle Proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79

Michael A. Geeves and Igor Chizhov

ll. Inhibitory Actions of Synthetic Actin Peptides and 2,3-Butanedion Monoxime on Actomyosin System ......................................... 91

Yoh Okamoto, Akihisa Hobo, and Koichi Kamisawada

12. Smooth Muscle Myosin: Amino Acid Residues Responsible for the Hydrolysis of ATP ...................................................... 99

Hirofumi Onishi, Manuel F. Morales, Shin-ichiro Kojima, Kazuo Katoh, and Keigi Fujiwara

13. The Molecular Biology and Pathophysiology of Hypertrophic Cardiomyopathy Due to Mutations in the Beta Myosin Heavy Chains and the Essential and Regulatory Light Chains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 105

Neal D. Epstein

14. Cross-Bridge Dynamics in the Contracting Heart Jon N. Peterson and Norman R. Alpert

15. Distinct Kinetic Properties of Cardiac Myosin Isoforms Revealed by in Vitro

117

Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 Seiryo Sugiura, Naoshi Kobayakawa, Hideo Fujita, Shin-ichi Momomura,

Shigeru Chaen, and Haruo Sugi

16. Functional Characterization of Dictyostelium discoideum Mutant Myosins Equivalent to Human Familial Hypertrophic Cardiomyopathy . . . . . . . . . . 131

Hideo Fujita, Seiryo Sugiura, Shin-ichi Momomura, Haruo Sugi, and Kazuo Sutoh

17. Hydrodynamic Properties of Water in Contractile System Michihiko Ogata

18. IH-NMR Spectroscopy of the Intracellular Water of Resting and Rigor Frog

139

Skeletal Muscle. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 145 Takenori Yamada

Contents

III. Molecular Mechanism of Regulation of Actin-Myosin Interaction

19. The Crystal Structure ofTroponin C in Complex with N-Terminal Fragment of Troponin I: The Mechanism of How the Inhibitory Action of Troponin I Is

xi

Released by Ca2+-Binding to Troponin C ........................... 157 Dmitry G. Vassylyev, Soichi Takeda, Soichi Wakatsuki, Kayo Maeda, and

Yuichiro Maeda

20. Molecular Switches in Troponin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 169 John Gergely

21. Fluorescence ofNBD-Labelled Troponin-I as a Probe for the Kinetics of Thin Filament Activation in Skeletal Muscle Fibers. . . . . . . . . . . . . . . . . . . . . . . 177

B. Brenner, Th. Kraft, and 1. M. Chalovich

22. Skeletal Muscle Regulatory Proteins Enhance F-Actin in Vitro Motility ....... 187 A. M. Gordon, Y. Chen, B. Liang, M. LaMadrid, Z. Luo, and P. B. Chase

23. Signal Transmission and Transduction in Excitation-Contraction Coupling. . . . . 199 Noriaki Ikemoto and Roque EI-Hayek

24. Regulation of Contraction in Heart Muscle: A Ca2+ Gradient Model for the Ca2+-Induced Ca2+-Release of the Sarcoplasmic Reticulum ............ 209

Tsukasa Tameyasu

25. Role of Calcium and Crossbridges in Modulation of Rates of Force Development and Relaxation in Skinned Muscle Fibers ............... 219

Jack A. RaIl and Philip A. Wahr

26. Structure and Function of Smooth Muscle Myosin Light Chain Kinase. . . . . . .. 229 Hiroko Kishi, Li-Hong Ye, Akio Nakamura, Tsuyoshi Okagaki, Akiko Iwata,

Takeshi Tanaka, and Kazuhiro Kohama

27. Regulation of Scallop Myosin by Calcium: Cooperativity and the "Off' State 235 Vassilios N. Kalabokis and Andrew G. Szent-Gyorgyi

28. Modulatory Effect of MgATP on Smooth Muscle Myosin Phosphatase Activity 241 Yasuo Ogawa and Osamu- Sato

IV. X-Ray Diffraction Studies on the Structural Changes during Contraction

29. Studies on the l4.5NM Meridional X-Ray Diffraction Reflection during Length Changes ofIntact Frog Muscle Fibres ............................. 247

P. 1. Griffiths, H. Amenitsch, C. C. Ashley, M. A. Bagni, S. Bemstorff, G. Cecchi, B. Colombini, and G. Rapp

30. On the Working Stroke Elicited by Steps in Length and Temperature Gabriella Piazzesi, Natalia Koubassova, Malcolm Irving, and

Vincenzo Lombardi

259

xii Contents

31. Myosin Head Movements during Isometric Contraction Studied by X-Ray Diffraction of Single Frog Muscle Fibres . . . . . . . . . . . . . . . . . . . . . . . . . .. 265

Massimo Reconditi, Ian Dobbie, Malcolm Irving, Olivier Diat, Peter Boesecke, Marco Linari, Gabriella Piazzesi, and Vincenzo Lombardi

32. X-Ray Diffraction Studies of the Cross-Bridge Intermediate States. . . . . . . . . .. 271 S. Xu, S. Malinchik, S. Frisbie, 1. Gu, T. Kraft, G. Rapp, 1. M. Chalovich,

B. Brenner, and L. C. Yu

33. Spacing Changes in the Actin and Myosin Filaments during Activation, and Their Implications . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 281

Hugh E. Huxley, Alex Stewart, and Tom Irving

34. Structural Features of Force-Generating Cross-Bridges: A 2D-X-Ray Diffraction Study. . . . . . . . . . . . . . . . . . . . . . .. . . . . .. . . . . .. . . . . . . .. . . . . . . . . . .. 289

T. Kraft, T. Mattei, and B. Brenner

35. Myosin Crossbridge Configurations in Equilibrium States of Vertebrate Skeletal Muscle: Heads Swing Axially or Turn Upside-Down between Resting and Rigor. .. . . . . .. . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . .. 297

Jeff Harford, Marie Cantino, Michael Chew, Richard Denny, Liam Hudson, Pradeep Luther, Robert Mendelson, Ed Morris, and John Squire

36. Extensibility of the Actin and Myosin Filaments in Various States of Skeletal Muscle as Studied by X-Ray Diffraction ........................... 309

Yasunori Takezawa, Yasunobu Sugimoto, and Katsuzo Wakabayashi

V. Contraction Characteristics in Skeletal Muscle

37. Contractile Properties of Thin (Actin) Filament-Reconstituted Muscle Fibers. .. 319 Shin'ichi Ishiwata, Takashi Funtasu, and Hideaki Fujita

38. The ATPase Activity in Isometric and Shortening Skeletal Muscle Fibres 331 Zhen-He He, Rod K. Chillingworth, and Michael A. Ferenczi

39. Force Generation Simplified: Insights from Laser Temperature-Jump Experiments on Contracting Muscle Fibers ......................... 343

Julien S. Davis

40. Evidence for Two Distinct Cross-Bridge Populations in Tetanized Frog Muscle Fibers Stretched with Moderate Velocities . . . . . . . . . . . . . . . . . . . . . . . . .. 353

Takakazu Kobayashi, Shoichi Kosuge, and Haruo Sugi

41. Implications of Quantal Motor Action in Biological Systems . . . . . . . . . . . . . . .. 361 Gerald H. Pollack, Felix Blyakhman, Tatyana Shklyar, Anna Tourovskaya,

Tsukasa Tameyasu, and Paul Yang

42. Calcium Dependence of the Apparent Rate of Force Generation in Single Striated Muscle Myofibrils Activated by Rapid Solution Changes ... . . .. 373

F. Colomo, S. Nencini, N. Piroddi, C. Poggesi, and C. Tesi

Contents xiii

43. Myofilament Compliance and Sarcomere Tension-Stiffness Relation during the Tetanus Rise in Frog Muscle Fibres ............................... 383

M. A. Bagni, G. Cecchi, B. Colombini, and F. Colomo

44. Muscle Work Enhancement by Stretch: Passive Visco-Elasticity or Cross-Bridges? ............................................... 393

G. A. Cavagna, N. C. Heglund, and M. Mantovani

45. The Physiological Evaluation of Gene Therapies of Dystrophin-Deficient Muscles. . . . . . . .. . .. . . . . . .. . . . .. . .. . . . . . . . . . . . . . . . . . . . .. . . . .. 411

J. M. Gillis and N. Deconinck

46. Communications between the Nuclotide- and Actin-Binding Site of the Myosin Head in Muscle Fibers ......................................... 419

Kazuhiro Yamada and Suguru Fujita

47. Crossbridge Head Detachment Rate Constants Determined from a Model that Explains the Behavior of Both Weakly- and Strongly-Binding Crossbridges ................................................. 425

Mark Schoenberg

48. Bidirectional Functional Communication between Myosin Sub fragments 1 and 2 in Skeletal Muscle Fib~s . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 435

Takakazu Kobayashi, Shoichi Kosuge, and Haruo Sugi

VI. Contraction Characteristics in Cardiac Muscle

49. Reappraisal of the Multicellular Preparation for the in Vitro Physiopharmacological Evaluation of Myocardial Performance . . . . . . . .. 441

Stanislas U. Sys, Gilles W. De Keulenaer, and Dirk L. Brutsaert

50. Alterations of Myocardial Contraction Associated with a Structural Heart Defect in Embryonic Chicks. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 453

R. E. Godt, R. T. H. Foga<;a, and T. M. Nosek

51. Influences of Protein Kinase A and D-cAMP on Actin~Myosin Interaction and Energy Consumption of Cardiac Muscles .......................... 461

Yasutake Saeki, Takakazu Kobayashi, Kiyohiro Takigiku, and Haruo Sugi

52. Work Production and Work Absorption in Muscle Strips from Vertebrate Cardiac and Insect Flight Muscle Fibers ........................... 471

David Maughan, leffMoore, Jim Vigoreaux, Bill Barnes, and Louis A. Mulieri

53. Expression and Function of Atrial Myosin Light Chain I in the Porcine Right Ventricle of Normal and Pulmonary Hypertensive Animals ............ 481

M. Morano, P. Boe1s, S. G. Haworth, H. Haase, and I. Morano

xiv Contents

54. Ventricular Pressure-Volume Area (PVA) Accounts for Cardiac Energy Consumption of Work Production and Absorption ................... 491

Junichi Araki, Juichiro Shimizu, Takeshi Mikane, Satoshi Mohri, Hiromi Matsubara, Hiroki Yamaguchi, Shunji Sano, Tohru Ohe, Miyako Takaki, and Hiroyuki Suga

55. Oxygen Consumption and Motility of Mechanically Unloaded Myocardial Slices 499 Miyako Takaki, Hisaharu Kohzuki, Susumu Sakata, Yoshimi Ohga,

Satoshi Shimizu, Hiromi Ishidate, Haruo Ito, Takashi Kishi, and Hiroyuki Suga

56. Vascular Endothelial Cell-Cardiac Myocyte Crosstalk in Achieving a Balance between Energy Supply and Energy Use ........................... 507

Saul Winegrad, Daniel Henrion, Lydie Rappaport, and Jane-Lyse Samuel

57. Ramp-Rate Dependent External Work during Ramp-Load Release in Cardiac Muscle. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 515

Hiroshi Okuyama and Hiroko Toyota

VII. Factors Affecting Mechanical Efficiency in Skeletal and Cardiac Muscle

58. Efficiency of Skeletal and Cardiac Muscle C. L. Gibbs and C. J. Barclay

59. Muscle Energetics during Unfused Tetanic Contractions: Modelling the Effects

527

of Series Elasticity ............................................ 537 Roger C. Woledge

60. Shortening during Stimulation vs. during Relaxation: How Do the Costs Compare? ................................................... 545

Fang Lou, N. A. Curtin and R. C. Woledge

61. Load-Dependent Mechanical Efficiency oflndividual Myosin Heads in Skeletal Muscle Fibers Activated by Laser Flash Photolysis of Caged Calcium in the Presence of a Limited Amount of ATP .......................... 557

Haruo Sugi, Hiroyuki Iwamoto, Tsuyoshi Akimoto, and Hiroko Ushitani

62. Measurement of ATP Turnover during Shortening and Lengthening of Rabbit Psoas Myofibrils Using a Fluorescent ATP Analog ................... 569

Shigeru Chaen, Ibuki Shirakawa, Clive R. Bagshaw, and Haruo Sugi

General Discussion I . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 577 Chaired by B. Brenner, G. H. Pollack, and C. R. Bagshaw

General Discussion II ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 601 Chaired by H. Sugi and N. Epstein

General Discussion III ................................................... 619 Chaired by J. RaIl and R. C. Woledge

Contents

63. Concluding Remarks H. E. Huxley

xv

647

Participants Photos ...................................................... 651 Participants ............................................................ 655 Contributors Index ...................................................... 659 Subject Index .......................................................... 661