Molecular and physiological mechanisms of muscle contraction

346 Pages·2016·8.95 MB·English

by  Morel, Jean Emile

Molecular and
Physiological
Mechanisms of
Muscle Contraction
© 2016 by Taylor & Francis Group, LLC
© 2016 by Taylor & Francis Group, LLC
Molecular and
Physiological
Mechanisms of
Muscle Contraction
Jean Emile Morel
Commissariat à l’Energie Atomique
(Direction des Sciences du Vivant)
Ecole Centrale de Paris &
Université (Pierre et Marie Curie)
Paris, France

© 2016 by Taylor & Francis Group, LLC
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© 2016 by Taylor & Francis Group, LLC
To my wife Marie-Hélène, my son Philippe, my former students and coworkers
To my dear brother Yves who died in July 2014 and will never read this book
This monograph was written in Plouescat, Brittany, France, between 2001 and 2014

© 2016 by Taylor & Francis Group, LLC
© 2016 by Taylor & Francis Group, LLC
CONTENTS
Preface / ix SEVEN • FATIGUE IN ONE ISOMETRICALLY
Acknowledgements / xiii CONTRACTING HALF-FIBRE FROM
A YOUNG ADULT FROG, AND IN
Author / xv
INTACT AND TRADITIONALLY
DEMEMBRANATED FIBRES OF
ONE • INTRODUCTION: HISTORICAL VARIOUS ORIGINS: DISCUSSION
ACCOUNT AND OVERVIEW / 1 BASED ESSENTIALLY ON THE
HYBRID MODEL / 219
TWO • MATERIALS AND METHODS / 11
EIGHT • PREDICTIVE AND EXPLANATORY
THREE • ANALYSIS AND CHARACTERISTICS POWER OF THE HYBRID MODEL:
OF SOME MAJOR BIOPHYSICAL, ANALYSIS OF VARIOUS PROBLEMS / 231
ENZYMOLOGICAL AND
PHYSIOLOGICAL PHENOMENA NINE • IN VITRO MOTILITY: ANALYSIS OF
IN AN INTACT UNIT CELL DURING EXPERIMENTAL DATA AND THEIR
CONTRACTION (ISOMETRIC AND INTERPRETATIONS. MOVEMENT OF
ISOTONIC) / 23 CELL ORGANELLES / 267
FOUR • NEW AND OLDER EXPERIMENTAL TEN • GENERAL CONCLUSION: FROM
RESULTS AND INTERPRETATIONS / 105 OLD CONCEPTS, OLD AND
RECENT EXPERIMENTAL DATA
FIVE • GENERAL FEATURES OF THE HYBRID AND REASONING AND NEW
MODEL / 169 EXPERIMENTAL RESULTS, TO
A HYBRID MODEL OF MUSCLE
SIX • QUANTITATIVE DATA AND CONTRACTION / 273
CALCULATIONS, CONCERNING
Addendum / 277
SHORT TETANI UNDER STEADY-
STATE ISOMETRIC CONTRACTION
References / 285
CONDITIONS, REQUIRED FOR
QUANTIFICATION OF THE HYBRID
Index / 325
MODEL / 191
vii
© 2016 by Taylor & Francis Group, LLC
© 2016 by Taylor & Francis Group, LLC
PREFACE
Frog and rabbit are the principal animal species slack length, increased very slightly when the
studied in this monograph. The passage from one bulk ionic strength was lowered from 180 mM
species to another may make it difficult to fol- to ~40 mM. Between ~40 mM and ~30 mM,
low the reasoning, but this passage is necessary the relative resting force increased very rapidly
because most of the experimental results con- with further decreases in ionic strength, peaking
cerning physiological properties (e.g. isometric at high levels, between ~30 mM and ~20 mM.
tetanic tension and velocity of shortening) were Below ~20 mM, the relative resting force
obtained with intact frog fibres, whereas most decreased sharply. The dependence of the relative
of the enzymatic results concerning MgATPase resting force on ionic strength, the existence of
activities were obtained with demembranated a maximum and the rapid decrease at very low
rabbit fibres. ionic strengths demonstrate that strong radial
This book comprises a long line of reasoning, repulsive electrostatic forces are exerted between
with many interdependent and complex sections. the myofilaments under resting conditions (see
I therefore recommend reading the titles of the below concerning the conversion of radial forces
most complicated chapters and sections carefully into axial forces). These radial repulsive electro-
to facilitate understanding. Consulting the Index static forces are also effective in half-fibres (and
could also be useful. all types of fibre, whether intact or demembra-
In addition to reviewing and reanalysing the nated), under isometric tetanic contraction con-
results of studies of my own and many other inde- ditions, and present qualitative characteristics
pendent groups, I also report unpublished results similar to those at rest (only some quantitative
for experiments with half-fibres (intact fibres features differ).
split lengthwise) from white skeletal muscles of In another set of experiments, myosin heads
young adult frogs and with permeabilised fibre were cleaved enzymatically (i.e. digested with
bundles from red skeletal muscles of young adult α-chymotrypsin) from the rest of the thick myo-
rats. From this many-faceted ‘treatise’, a hybrid sin filaments, in permeabilised fibre bundles from
model emerges, combining the swinging cross- red skeletal muscles (tibialis anterior) of young adult
bridge/lever-arm processes and lateral swelling rats (Wistar), held around the slack length, in a buf-
mechanisms. fer mimicking the physiological resting medium,
In these new experimental findings, the rela- at room temperature. Very small, sometimes tiny,
tive resting force, recorded at pH 7 and 10°C, in but detectable, transitory contractures resulted
half-fibres from white skeletal muscles (iliofibularis) from these enzymatic cleavages, demonstrating
of young adult frogs (Rana pipiens), held around the that thin actin and thick myosin filaments are
ix
© 2016 by Taylor & Francis Group, LLC
tethered by a small number of ‘resting’ (weakly In 2000, Cyranoski published a commentary
bound) cross-bridges, exerting strong radial teth- paper concerning the symposium held in Osaka
ering forces (together with weak radial a ttractive/ (Japan) on in vitro motility and its possible link to
compressive forces) that counterbalance the muscle contraction. The author provided a severe,
radial repulsive electrostatic forces, under resting but lucid, analysis of the approach of Yanagida
conditions. and his coworkers (see also Chapter 9 in this book
Based on these two series of experimental for supplementary arguments). Cyranoski also
observations, a hybrid model of muscle contrac- cited Molloy, who claimed, during the sympo-
tion is proposed, in which the radial tethering sium, that ‘The tightly coupled lever-arm idea is
forces decrease drastically once contraction is simple, predictive and inherently testable because
triggered, leading to net radial expansive forces of its more restrictive nature’ (as opposed to ‘the
between the myofilaments. Under both rest- loose-coupled thermal ratchet model’ defended
ing and contracting conditions, the net radial by Yanagida and his group). Thus, in 2000, the
repulsive (expansive) forces are turned into axial general view, expressed by Molloy, was appar-
forces. Indeed, in the 1970s, based on theoreti- ently clearcut. In this monograph, I demonstrate
cal and logical reasoning, mechanisms for this that the situation is much more complex than
conversion were proposed that are valid at rest previously thought by many specialists in muscle
and during contraction, regardless of volume contraction and in vitro motility.
variations. In this hybrid model, under standard The starting point for writing this book was
conditions (e.g. 10°C, slack fibre length, pH ~7, essentially the conclusion of Cyranoski (2000),
ionic strength ~180 mM), part of the isometric who cited A.F. Huxley: ‘I came here confused
tetanic tension (~40%) results from lateral swell- about actin and myosin. Now, I am still confused,
ing mechanisms (the usual name for mecha- but at a higher level’.
nisms involving radial expansive forces inducing The need to reopen the question of the univer-
axial contractile forces) and another part (~60%) sality of swinging cross-bridge/lever-arm theo-
results from swinging cross-bridge/lever-arm ries and to search for innovative ideas, based on
processes plus, possibly, the impulsive mecha- new experiments, has been expressed by Bryant
nism developed by Elliott and Worthington plus, et al. (2007), who wrote: ‘the basic actomyosin
possibly, the ‘step-wise’ mechanism developed by motor has been embellished, altered, and reused
Pollack’s group, and other models (e.g. ~30% of many times through the evolution of the myosin
swinging cross-bridge/lever-arm models, ~10% superfamily’. More recently, Grazi (2011) wrote:
of impulsive model, ~10% of Pollack’s model, and ‘With time clever hypotheses may be accepted as
~10% of other models). In this work, I neglect the “facts” without being supported by solid experi-
‘unconventional’ models and use only swinging mental evidence. In our opinion this happened
cross-bridge/lever-arm mechanisms, with a pro- with muscle contraction where pure suggestions
portion of ~60%. still occupy the scene and delay the progress of
The experimental findings, summarised here, the research’. In the last few years, many authors,
and the hybrid model developed and discussed in including Bryant et al. (2007), have focused on
this book provide the pretext for a long critical myosin VI and discovered unexpected properties
and constructive review and an analysis concern- of this motor protein, studied in vitro by brilliant
ing many well-known properties of contracting techniques. The titles of the articles by Spudich
muscle fibres, as well as complex phenomena and Sivaramakrishnan (2010) and Sweeney and
(including unexplained, forgotten, ignored, even Houdusse (2010) were particularly ‘explosive’:
‘mysterious’ experimental and semi-empirical ‘Myosin VI: an innovative motor that chal-
results). Most of the ‘forgotten’ observations were lenged the swinging lever arm hypothesis’ and
not accounted for by swinging cross-bridge/lever- ‘Myosin VI rewrites the rules for myosin motors’,
arm models and were, therefore, rarely taken into respectively.
account in the many discussions presented in I have made use of the time available to me
publications concerning muscle contraction and since my retirement to read as many papers as
its molecular basis. By contrast, I think that the possible in the domains of muscle contraction and
hybrid model answers many of these awkward in vitro motility, with the aim of resolving the
questions. confusion. I provide in this work my own analysis
x Morel
© 2016 by Taylor & Francis Group, LLC