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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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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