Mechanism of Myofilament Sliding in Muscle Contraction

822 Pages·1993·26.974 MB·English

by  A. F. Huxley (auth.), Haruo Sugi, Gerald H. Pollack (eds.)

MECHANISM
OF MYOFILAMENT
SLIDING IN MUSCLE
CONTRACTION
ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY
Editorial Board:
NATHAN BACK. State University of New York at Buffalo
IRUN 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
Recent Volumes in this Series
Volume 325
RECOVERY FROM BRAIN DAMAGE: Reflections and Directions
Edited by F. D. Rose and D. A. Johnson
Volume 326
THE USE OF RESEALED ERYTHROCYTES AS CARRlERS AND BIOREACTORS
Edited by Mauro Magnani and John R. DeLoach
Volume 327
GENETICALLY ENGINEERED VACCINES
Edited by Joseph E. Ciardi. Jerry R. McGhee. and Jerry M. Keith
Volume 328
ENZYMOLOGY AND MOLECULAR BIOLOGY OF CARBONYL METABOLISM 4
Edited by Henry Weiner. David W. Crabb. and T. Geoffrey Flynn
Volume 329
DENDRITIC CELLS IN FUNDAMENTAL AND CLINICAL IMMUNOLOGY
Edited by Eduard W. A. Kamperdijk, Paul Nieuwenhuis. and Elisabeth C. M. Hoefsmit
Volume 330
THE UNDERLYING MOLECULAR. CELLULAR. AND IMMUNOLOGICAL FACTORS IN
CANCER AND AGING
Edited by Stringner Sue Yang and Huber R. Warner
Volume 331
FRONTIERS IN CEREBRAL VASCULAR BIOLOGY: Transport and Its Regulation
Edited by Lester R. Drewes and A. Lorris Betz
Volume 332
MECHANISM OF MYOFlLAMENT SLIDING IN MUSCLE CONTRACTION
Edited by Haruo Sugi and Gerald H. Pollack
Volume 333
OPTICAL IMAGING OF BRAIN FUNCTION AND METABOLISM
Edited by Ulrich Dimagl, Amo Villringer. and Karl M. Einhliupl
A Continuation Order Plan is available for Ibis 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.
MECHANISM
OF MYOFILAMENT
SLIDING IN MUSCLE
CONTRACTION
Edited by
Haruo Sugi
Teikyo University
Tokyo. Japan
and
Gerald H. Pollack
University of Washington
Seattle. Washington
SPRINGER SCIENCE+BUSINESS MEDIA, LLC
Llbrary of Congress Cataloglng-ln-Publication Oata
Mechanlsm of myofl1ament sllding In muscle contractlon I edlted by
Haruo Sugl and Gerald H. Pollack.
p. cm. -- (Advances in experImental medlclne and bl0logy ; v.
332)
Includes blbllographical references and Index.
ISBN 978-1-4613-6245-6 ISBN 978-1-4615-2872-2 (eBook)
DOI 10.1007/978-1-4615-2872-2
1. Muscle contraction--Congresses. 2. Cytoplasmlc fllaments
-Congresses. 3. Actln--Congresses. 4. Myosln--Congresses.
I. Sugl. Haruo. 1933- 11. Pollack. Gerald H. 111. Serles.
OP321.M3385 1993
591.1·852--dc20 93-22795
CIP
Proceedings of a symposium on Mechanism of Myofilament Sliding in Muscle Contraction. held
November 11-15. 1991, in Hakone, Japan
© 1993 by Springer Science+Business Media New York
Originally published by Plenum Press, New York in 1993
All rights reserved
No part of this book may be reproduced, stored in 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 entire proceedings of the symposium organized by one
of us (H.S.) on November 11 to 15, 1991 at Hakone, Japan, under the title of
"Mechanism of Myofllament Sliding in Muscle Contraction."
Among various kinds of energy transduction mechanisms in biological systems,
the mechanism of muscle contraction has been studied most intensively and
extensively over many years. Since the monumental discovery by the two Huxleys
and coworkers that muscle contraction results from relative sliding between the
thick and thin myofilaments, attention of muscle investigators has been focused on
the question, what makes the fllaments slide past one another. In response to the
above question, A.F. Huxley and Simmons put forward a contraction model in 1971,
in which globular heads of myosin (cross-bridges) extending from the thick fllament
first attach to actin on the thin fllament, and then change their angle of attachment to
actin (power stroke) leading to force generation or myofilament sliding until they
detach from the thin fllament. The rocking cross-bridge contraction model seemed
to be entirely consistent with the kinetic scheme of actomyosin ATPase published by
Lymn and Taylor at the same time, thus giving a strong impression to the people
concerned that the muscle contraction mechanism would soon be sorted out. In his
review lecture in 1974, however, A.F. Huxley warned against such optimism by
stating "The whole history of theories of muscular contraction during the last half
century shows that even when a set of ideas seems to be well established, there is a
large chance that it will be overthrown by some unexpected discovery."
Nearly twenty years has passed since Huxley gave the above review lecture.
Despite the accumulation of our knowledge about structural changes during muscle
contraction and the relation between the actomyosin ATPase cycle and mechanical
events, derived from a number of new experimental techniques, we are still unable
to answer the question, what makes the myofilaments slide past one another. In our
feeling, it is uncertain whether the mechanism of muscle contraction will eventually
be solved along the lines drawn in the early 1970's, or in a completely different way
based on unexpected discoveries in the future.
Whichever the truth may be, the editors agree in that, for uncovering the
mechanism of muscle contraction, it is necessary to pay attention to phenomena that
appear inconsistent with the genera1lines of thinking, and to place more emphasis on
experiments with intact or demembranated muscle fibers in which three
dimensional myofilament-lattice structures are preserved. Based on the above ideas,
we have already published proceedings of three muscle symposia organized by us (in
v
vi preface
1984) or one of us (H.S.) (in 1979 and 1988). It is our great pleasure that the above
proceedings have been highly evaluated by readers, not only for the quality of
papers contained, but also for the extensive discussions which constituted a most
stimulating and informative part of the proceedings. This volume also contains a lot
of such discussions which are, regrettably, always extremely time-consuming for us
to edit. Thus, as with our previous publications, this volume is published after a
delay of more than one year. Nevertheless, we believe that this volume will be useful
and stimulating for readers, if the recent rather slow progress in the field of muscle
research is taken into consideration.
Finally, we would like to express our hearty thanks to President Okinaga of
Teikyo University, without whose generous support and encouragement the present
symposium as well as the past three symposia could not have been held.
HaruoSugi
Gerald H. Pollack
OBITUARY
William F. Harrington (1920 - 1992)
William F. Harrington, Professor of Biology at the Johns Hopkins University,
died on October 31, 1992 after a heart attack at the age of 72. He was born in Seattle,
earned his undergraduate and graduate degrees at the University of California at
Berkeley, and finished his postgraduate work at Cambridge University and at the
Carlsberg Laboratory in Copenhagen. After working at Iowa State University and at
the National Heart Institute in Bethesda, Professor Harrington came to the Johns
Hopkins University in 1960 and was chairman of the Biology department and
director of the McCollum-Pratt Institute from 1973 to 1983.
As a distinguished muscle biochemist, he published more than 125 scientific
papers, and had received a National Institute of Health Merit award for 10 years of
research. He was visiting professor at Oxford University and at the University of
Washington, and was director of the Institute for Biophysical Research on
Macromolecular Assemblies at the Johns Hopkins University. As a member of the
National Academy of Sciences and a fellow of the American Academy of Arts and
Sciences, he served on the editorial boards of scientific journals.
Based on experimental results obtained in his laboratory, Professor Harrington
has raised the possibility that the length of the subfragment-2 moiety of the myosin
molecule shortens when it moves away from the thick filament backbone on muscle
activation to contribute to muscle force generation. This unique hypothesis, quite
different from the general view that the myosin subfragment-2 only serves as an
elastic link connecting the myosin head (subfragment 1) to the thick filament, has
stimulated the interest of muscle investigators and has evoked a great deal of
discussion at many scientific meetings. Personally, I worked with him recently on
the above topic, and was very much impressed with his enthusiasm in research work
as well as his modest and friendly character. Besides his scientific activities, he loved
chamber music and was a founding member and on the board of the concert series at
the Johns Hopkins University.
As with everyone who knew him, I shall gravely miss Professor Harrington, a
great investigator and a true gentleman in every sense.
HaruoSugi
vii
ACKNOWLEDGEMENT
The editors express their sincere thanks to Dr. Shoichi Okinaga, President of
Teikyo University, for his interest, encouragement and generous financial support,
which made this symposium possible as well as the previous three symposia held in
1978 (Tokyo), 1982 (Seattle) and 1986 (Hakone).
Our thanks are also due to Mr. Takashi Takeuchi, President of Japan Electron
Optics Laboratory (JEOL) Co., Ltd. for their generous additional financial support.
We owe a debt of gratitude to Ms. Therese Grisham and Ms. Tiffany Jones at the
University of Washington, who made enormous efforts in transcribing the tapes of
the discussions, and to Dr. Hiroyuki Iwamoto and Miss Naoko Itagaki at Teikyo
University for their help in preparing the text for camera-ready duplication, and to
Drs. Teizo Tsuchiya, Takenori Yamada, Suechika Suzuki, Takakazu Kobayashi,
Hiroyuki Iwamoto and Kazuhiro Oiwa in compiling the indices.
viii
CONTENTS
Introductory lecture on muscle contraction
A.F. Huxley .......................................................................................... 1
I. STRUCTURAL BASIS OF MYOFll..AMENT SLIDING
Introduction ................................................................................................ 13
A comparison of the atomic model of F-actin with cryo-electron micrographs of
actin and decorated actin
K.C. Holmes, M. Tirion, D. Popp, M. Lorenz, W. Kabsch and R.A. Milligan
........................................................................................................ 15
Discussion ................................................................................................ 22
A new crystal form of tropomyosin
A. Miegel, L. Lee, Z. Dauter and Y. Maeda .............................................. 25
Discussion ................................................................................................ 32
Experiments on rigor crossbridge actin and filament sliding in insect flight muscle
M.K. Reedy, C. Lucaveche, M.C. Reedy and B. Somasundaram ................... 33
Discussion ................................................................................................ 44
Gross structural features of myosin head during sliding movement of actin as studied
by quick-freeze deep-etch electron microscopy
E. Katayama ......................................................................................... 47
Discussion ................................................................................................ 54
Cross-bridge angle distribution and thin filament stiffness in frog skeletal muscle
fibers as studied by quick-freeze deep-etch electron microscopy
S. Suzuki, Y. Oshimi and H. Sugi ............................................................. 57
Discussion ................................................................................................ 68
Elastic properties of connecting filaments along the sarcomere
K. Trombitis and G.H. Pollack ............................................................... 71
Discussion ................................................................................................ 79
Structural studies on the conformations of myosin
A.R. Faruqi, R.A. Cross and J. Kendrick-Jones ......................................... 81
Discussion ................................................................................................ 89
ix
Contents
x
n.
REGULATORY MECHANISMS OF CONTRACTION
Introduction ....... '" .................. '" ., ............................................................... 95
Activation and relaxation mechanisms in single muscle fibres
e.e. Ashley, T.J. Lea, I.P. Milligan, R.E., Palmer and SJ. Simnett. ............. 97
Discussion .............................................................................................. 114
The molecular switch in troponin C
J. Gergely, Z. Grabareck and T. Tao ...................................................... 117
Discussion .............................................................................................. 123
The mechanism of Ca2+ -coordination in the EF-hand of TnC, by cassette
mutagenesis
A. Babu, H. Su and J. Gulati .................................................................. 125
Discussion .............................................................................................. 131
The strength of binding of the weakly-binding crossbridge created by sulfhydryl
modification has very low calcium sensitivity
V.A. Barnett and M. Schoenberg ........................................................... 133
Discussion .............................................................................................. 138
Role of parvalbumin in relaxation in relaxation of frog skeletal muscle
T. Hou, J.D. Johnson and J.A. RaIl ......................................................... 141
Discussion .............................................................................................. 151
Evidence for the existence of endothelial factors regulating contractility in rat heart
S. Winegrad ....................................................................................... 155
Discussion .............................................................................................. 163
Effects of tropomyosin deficiency in flight muscle of Drosophila melanogaster
J. Molloy, A. Kreuz, R. Miller, T. Tansey and D. Maughan ....................... 165
Discussion .............................................................................................. 171
Effect of myosin heavy chain peptides on contractile activation of skinned cardiac
muscle fibres
J.e. Ruegg, J.D. Strauss, e. Zeugner and I. Trayer .................................. 173
Discussion .............................................................................................. 180
Cross-bridges affect both TnC structure and calcium affinity in muscle fibers
A.M. Gordon and E.B. Ridgway ........................................................... 183
Discussion .............................................................................................. 192
Phosphorylation-contraction coupling in smooth muscle: Role of caldesmon
G. Pfitzer, W. Fischer and J.M. Chalovich .............................................. 195
Discussion .............................................................................................. 202
[nfluence of Ca-activated brevin on the mechanical properties of skinned smooth
muscle
Ph. Gailly, J.M. Gillis and J.P. Capony .................................................. 205
Discussion .............................................................................................. 210
m.
BIOCHEMICAL ASPECTS OF ACTIN-MYOSIN INTERACTION
Introduction, Obituary: Ken Hotta ................................................................ 215