EXCITATION-CONTRACTION COUPLING AND CARDIAC CONTRACTILE FORCE
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1 EXCITATION-CONTRACTION COUPLING AND CARDIAC CONTRACTILE FORCE
2 Developments in Cardiovascular Medicine VOLUME 122 The titles published in this series are listed at the end of this volume.
3 EXCITATION -CONTRACTION COUPLING AND CARDIAC CONTRACTILE FORCE by DONALD M. BERS Professor and Chairman, Department of Physiology, Loyola University Medical School, Maywood, U.S.A. Introduction by W. J. Lederer SPRINGER-SCIENCE+BUSINESS MEDIA, B.V.
4 Library of Congress Cataloging-in-Publication Data Bers. D. M. Excitation-contraction coupling and cardiac contractile force I by Donald M. Bers : Introduction by W.J. Lederer. p. cm. -- (Developments In cardiovascular medicine: v. 122) Includes bibliographical references and Index. ISBN ISBN (ebook) DOI / Heart--Contractlon. 2. CalcluN--Physlologlcal effect. 3. Calcium channels. 4. Excitation (Physiology) 5. Action potentials (Electrophysiology) I. Title. II. Series. [ONLM: 1. Calclum--Netabollsm. 2. Myocardial Contractlon -physiology. 3. MyocardlulR--utabollsm. Wl DE997\1ME v. 122/ WG 280 B535cl OPl13.2.B dc20 OLC for Library of Congress ISBN First published 1991 Reprinted 1993 Printed on acid-free paper All Rights Reserved 1991, 1993 Springer Science+Business Media Dordrecht Originally published by Kluwer Academic Publishers in 1993 Softcover reprint of the hardcover 1st edition 1993 No part of the material protected by this copyright notice may be reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording or by any information storage and retrieval system, without written permission from the copyright owner.
5 This book is dedicated to Kathy, Brian & Becky
6 PREFACE The main aim of this monograph is to provide an overview of calcium regulation in cardiac muscle cells, particularly with respect to excitation-contraction coupling and the control of cardiac contractile force. It is my hope that this book will be useful to students of the cardiovascular system and muscle at all different levels and in different disciplines (such as physiology, biochemistry, pharmacology and pathophysiology). I also hope that it will find use for those studying developmental, comparative and disease processes as well as more integrative phenomenon. I kept several goals in mind in writing this monograph. First, it should be easily readable. Second, I chose to include numerous illustrations and tables to help integrate results from numerous investigators in practical formats and also present key figures from important papers. Thus, this monograph may serve as a resource of information for people working in the areas described herein. Third, the presentation is a very personal one, and I have necessarily drawn extensively on my personal experience in this field over the past 15 years. This, I think, helps maintain a certain continuity of thought from chapter to chapter. Fourth, I have made serious attempts to make each chapter "up to date", despite the breadth of topics covered. I have also tried to be equitable in choosing references while not intending to be comprehensive or exhaustive. Neither of these aims can be perfectly matched, and I apologize to the many investigators whose papers I have not cited, but should have. While I thank all of my colleagues who make this a stimulating area in which to work, I would especially like to thank those who contributed by helpful discussions, providing original figures, sending preprints of manuscripts, and by commenting on drafts of individual chapters. These individuals include: S. Baudet, E.P. Bean, J.R. Berlin, J.H.B. Bridge, A. Fabiato, S. Fleischer, J.S. Frank, e. Franzini-Armstrong, M.M. Hosey, L.V. Hryshko, N. Ikemoto, L.R. Jones, W.J. Lederer, D.H. MacLennan, G. Meissner, M. Morad, KD. Philipson, J.D. Potter, E. Rios, RJ. Solaro, J.R Sommer, J.G. Tidball, J. McD. Tormey, W.G. Wier, A. Williams, D.T. Yue. I also thank my many research collaborators over the years who have joined me in making some contributions to this field, including: G.A. Langer, KD. Philipson, D. Ellis, A. Peskoff, J.L. Sutko, e.o. Maiecot, KT. MacLeod, J.H.E. Bridge, J.G. Tidball, M.J. Shattock, S.M. Harrison, P. Hess, KW. Spitzer, L.v. Hryshko, W.J. Lederer, J.R Berlin. Finally, a very special thanks are due to my wife, Kathryn E. Bers, whose combination of patience and assistance have made this book possible. Donald M. Bers January 1991 vii
7 INTRODUCTION How is the heartbeat generated? What controls the strength of contraction of heart muscle? What are the links between cardiac structure and function? How does our understanding of movement in skeletal and smooth muscle and in non-muscle cells influence our thinking about the development of force in heart muscle? Are there important species differences in how contraction is regulated in the heart? While these important questions have been asked many times, exciting results in many areas of mammalian biology have set the stage for this refreshing new book on Excitation Contraction Coupling and Cardiac Contractile Force. This informative and quantitative book always remains readable. Don Bers explains how contraction arises in heart and how it is controlled. Furthermore, he presents insightful and stimulating discussions of apparently disparate results that will inform and delight both students and "experts". In many ways, Don paints a modern "portrait" of how the heart works and in this picture he shows a close-up of the structural, chemical and physiological links between excitation and contraction. The recent molecular investigations of excitation-contraction coupling in skeletal and heart muscle have brought together cell physiologists, molecular biologists and physicians in numerous research projects that form the background for this book. These new investigations have led to the explosion of information that would challenge the individual who only seeks to read the primary sources. Don simplifies our task by bringing much of this material together in a single coherent presentation. Exciting questions abound and this book introduces and/or lays the foundation for many of them. Some are stated explicitly by Don while others depend on Don's presentation and the reader's background. For example, the five questions below are among the ones that jump out at me. (1) In heart and skeletal muscle cells, the sarcolemma (SL) has been reported to have many more dihydropyridine receptors than functional calcium channels. Is this apparent excess real or an artifact? If it is real, what does this excess mean? (2) Another question also centers on the dihydropyridine receptor (DHP-R) which is the L-type calcium channel in heart and skeletal muscle. Recent cdna sequence information along with investigations of structure and function using DHP-R chimeras from heart and skeletal muscle have suggested that a specific cytoplasmic domain or loop of the DHP-R can confer important properties on this receptor/channel. With the skeletal muscle loop in place, E-C coupling in skeletal muscle is "normal" (SL voltage-sensor-dependent calcium release) but when the cardiac loop is in place, the E-C coupling resembles that normally seen in heart (calcium-induced calcium-release). This raises the question of how this particular cytoplasmic loop normally interacts with the SR calcium release channel (i.e. ryanodine ix
8 x receptor) in skeletal muscle. In heart muscle the question is whether there is any interaction at all between the cytoplasmic loop of the DHP-R and the SR calcium release channel. Furthermore, I must wonder if this interaction (if any exists) changes during calcium overload or during maneuvers that change the inotropic state of the heart muscle cell. (3) While calcium-induced calcium release (CICR) appears to be the dominant factor in explaining the link between excitation and contraction in heart muscle, a question lurks just below the surface. How is CICR modulated? What is the relationship between Ca influx and Ca release from the SR? It would appear that all elements of CICR can be modified by intracellular calcium, drugs and neurohormones -- including calcium channels, Na-Ca exchangers, Ca-ATPases, and calcium release channels. Furthermore the release process also seems subject to modulation by intra-sr calcium and may also involve calsequestrin. (4) Do the T-tubular membrane and the non-invaginated SL membrane participate in a similar manner in E-C coupling? Do they have similar densities of DHP Rs? Do they possess the same CICR elements? (5) How can one make use of our knowledge of E-C coupling and Cellular Ca regulation to develop improved inotropic agents? Many questions are raised by the book, and each reader will undoubtedly focus on different ones. Although Don does not answer or directly address all of our questions, he provides an improved vantage point for us to view the issues important to each of us and to the field in general. In his portrait of E-C coupling in heart, Don Bers presents many new findings commingled with "established" truth and paints a new picture of how contraction arises and is controlled in the heart. The picture is sharper and contains many new details. He assembles important measurements in new and useful tables, presents figures from recent and more classical publications and shows new figures to supplement his presentation. While integrating new observations with traditional "facts", Don is able to retain both the excitement of discovery and the inevitable controversy arising when important questions cannot be fully answered. This book, written by an active research scientist, therefore provides a critical state-of-the-art report on how the heart works as an electrically and chemically regulated contractile machine. W.J. Lederer Baltimore, Maryland January 1991
9 Chapter TABLE OF CONTENTS Page 1. Major cellular structures involved in E-C coupling... 1 Sarcolemma and transverse tubules The extracellular space Sarcoplasmic reticulum Mitochondria Myofilaments Other cellular constituents Myofilaments: The end effector of E-C Coupling Myofilament proteins Mechanism by which Ca activates contraction Acto-myosin ATPase The length-tension relationship The Ca sensitivity of the myofilaments Force-pCa relation in intact cardiac muscle Factors which influence the force-pca relationship Possible sources and sinks of activator calcium Ca requirements for the activation of contraction Ca transport across the sarcolemma Ca transport by the sarcoplasmic reticulum General scheme of Ca cycle in cardiac myocyte Mitochondrial Ca transport Ca at the inner sarcolemmal surface Intracellular Ca buffering Ca influx via sarcolemmal Ca channels Ca channel types Biochemical characterization of L-type Ca channels Ca channel selectivity and permeation Numbers of Ca channels Ca channel gating Amount of Ca entry via Ca channels Modulation of cardiac Ca channels by agonists and antagonists Modulation of cardiac Ca channels by adrenergic agents Na/Ca exchange and the sarcolemmal Ca-pump The sarcolemmal Ca-pump The Na/Ca exchange Fundamental characterizations in sarcolemmal vesicles... 72
10 xii Na/Ca exchange current in myocytes V max vs. Ca requirements and site density Ca entry via Na/Ca exchange and contraction Thermodynamic considerations Competition between Na/Ca exchange, the sarcolemmal Ca-pump and SR Ca-pump during relaxation and at rest Sarcoplasmic reticulum Ca uptake, content and release SR Ca-pump Regulation of the cardiac SR Ca-pump by phospholamban Regulation of the cardiac SR Ca-pump by Ca, ph, ATP and Mg SR Ca uptake capacity Calsequestrin SR Ca uptake rate and relaxation Assessment of SR Ca content in intact cardiac muscle Electron probe microanalysis Caffeine-induced contractures Rapid cooling contractures Cumulative extracellular Ca depletions Direct chemical and radiotracer techniques SR Ca release channel or ryanodine receptor Regulation of Ca release by the SR Other SR channels related to Ca release Excitation-Contraction Coupling Depolarization-induced Ca release or charge-coupled Ca release Murine muscular dysgenesis: a model system Does the dihydropyrine receptor contact the ryanodine receptor? Direct SR depolarization Does charge-coupled Ca release work in cardiac muscle? Ca-induced Ca-release Ca-induced Ca-release in skeletal muscle Ca-induced Ca-release in mechanically skinned cardiac muscle Ca-induced Ca-release: support from intact cardiac myocytes Challenges to Ca-induced Ca-release in cardiac muscle Spontaneous SR Ca release and cyclic contractions Ins(1,4,5)Ps-induced Ca release lns( 1,4,5)P s induced Ca release in smooth muscle Ins(1,4,5)P 3 induced Ca release in skeletal muscle Ins(1,4,5)Ps induced Ca release in cardiac muscle Other possible E-C coupling mechanisms Summary
11 xiii 8. Control of cardiac contraction by SR Ca release and sarcolemmal Ca fluxes Species, regional and developmental differences Biphasic contractions Rest decay and rest potentiation Early electrical and mechanical restitution Rest decay and SR Ca depletion in rabbit ventricle Post-rest recovery and SR refilling in rabbit ventricle Rest potentiation and post-rest recovery in rat ventricle Ca influx and efflux in rabbit and rat ventricle Potentiation of contraction without increasing SR Ca Force-frequency relationships Cardiac inotropy and Ca overload Cardiac inotropy ;9-adrenergic agents and cardiac inotropy a-adrenergic agents and cardiac inotropy Hypothermic inotropy Cardioactive steroids: Glycoside inotropy Ca mismangement and negative inotropy Ca overload: Spontaneous SR Ca release Afterdepolarizations and triggered arrhythmias Acidosis Hypoxia and ischemia Sites for induction of cardiac inotropy Modulation of myofilament sensitivity Na/Ca exchange modulation Ca current modulation Phosphodiesterase inhibition SR Ca uptake and release Conclusion References Index
12 xv Figure # TABLE OF FIGURES Page CHAPTER 1 ULTRASTRUCTURE 1 Schematic of skeletal muscle structure Schematic of cardiac muscle structure Extended junctional SR in bird heart Surface coat and extemallamina in mammalian heart Extracellular space in mammalian heart Skeletal muscle triads ("feet") Cardiac muscle triads ("feet") Foot proteinjryanodine receptor Schematic oft-tubulejsrjunction Sarcomere organization CHAPTER 2 MYOFILAMENTS 11 Myofilament proteins Ca-dependent regulation of acto-myosin Crossbridge mechanical model Crossbridge chemical cycle Length-tension relationship (cardiac & skeletal) Temperature effects on myofilament Ca sensitivity Species differences in myofilament Ca sensitivity Myofilament Ca sensitivity (in vivo vs."skinned") CHAPTER 3 SOURCES & SINKS OF ACTIVATOR Ca 19 Intracellular Ca buffering in cardiac muscle Total Ca requirements for myofilament activation Ca cycle in cardiac muscle cell Ca cycle in mitochondria Ca binding at inner sarcolemmal surface...44 CHAPTER 4 SARCOLEMMAL Ca CHANNELS 24 Ca channel current (T & L type channels) Schematic of Ca channel Ca channel permeation model Surface charge effects Ca current inactivation Ca current "staircase" Ca channel agonist Bay K 8644 and channel modes Voltage dependence of Ca channel antagonists Ca channel receptor interaction p-adrenergic modulation of Ca channel... 67
13 xvi CHAPTER 5 Na/Ca EXCHANGE AND SARCOLEMMAL Ca PUMP 34 Na/Ca exchange in cardiac sarcolemmal vesicles Schematic of Na/Ca exchanger Na/Ca exchange current in myocytes [Cat and Na/Ca exchange current Ca fluxes expected during the cardiac action potential Ca entry via Ca current and extrusion via Na/Ca exchange SR Ca-pump and Na/Ca exchange compete during relaxation Voltage dependence of relaxation SR Ca-pump and Na/Ca exchange competition: paired RCCs SR Ca-pump and Na/Ca exchange competition: voltage clamp Diastolic Ca efflux depends on Na/Ca exchange CHAPTER 6 SR Ca UPTAKE AND RELEASE 45 Schematic diagram of SR Ca-pump Model of Ca transport by the SR Ca-pump Caffeine-induced contractures Rapid cooling contractures (RCCs) Cai transients during RCCs and rest decay in myocytes Ryanodine accelerates loss of SR Ca during rest decay Extracellular Ca depletions are altered by ryanodine Ryanodine alters SR Ca release, channel gating and vesicle efflux Three-dimensional reconstruction of ryanodine receptor Ca and caffeine activate the SR Ca release channel CHAPTER 7 EXCITATION-CONTRACTION COUPLING 55 Contractions in zero Ca: Cardiac vs skeletal Voltage dependence of contraction in cardiac muscle Voltage dependence of contraction in skeletal muscle Intramembrane charge movement and SR Ca release Schematic of T-tubule/SR junction Ca-induced Ca-release in cardiac muscle "Trigger Cal! vs SR Ca release Hypothetical scheme for Ca-induced Ca-release Schematic of E-C coupling architecture Ca release activated by Ca-"tail" current Ca entry is required for Ca release in heart Duration dependence of Cai transients in heart No intrinsic voltage dependence in cardiac SR Ca release [Ca]i near the mouth of a Ca channel Ins(1,4,5)Ps induced Ca release in smooth muscle Ins(1,4,5)Ps induced Ca release in cardiac muscle
14 xvii 71 E-C coupling in cardiac vs skeletal muscle E-C coupling in smooth muscle CHAPTER 8 CONTROL OF CARDIAC CONTRACTION BY SR Ca RELEASE AND SARCOLEMMAL Ca FLUXES 73 Species differences in dependence on SR Ca release Post-rest recovery in different species (± ryanodine) Biphasic contractions with milrinone Early mechanical restitution Rest decay in rabbit ventricle Refilling of the SR in rabbit ventricle Rest potentiation and recovery in rat ventricle Ca influx and efflux in rabbit and rat ventricle Ca fluxes during action potentials "Staircase" direction depends on pulse duration Action potentials modified by Na/Ca exchange Paired-pulses and sarcolemmal Ca fluxes Rest decay in ferret ventricle Frequency changes in rabbit ventricle Force-frequency relationship in rabbit, rat and guinea-pig CHAPTER 9 CARDIAC INOTROPY AND Ca OVERLOAD 88,a-adrenergic effects on [Cali and contraction Isoproterenol can abolish force "staircase" a- vs,a-adrenergic effects on [Cali and contraction Hypothermic inotropy Quick temperature switch and hypothermic inotropy Na-pump inhibition, anaj and tension Diastolic [Cali and glycoside inotropy Na-pump inhibition, twitch tension and RCCs Caffeine does not prevent glycoside inotropy Ca influx via Na/Ca exchange can activate contraction Extracellular Ca depletion is altered by Na-pump inhibition Na-pump inhibition icreases Ca influx and efflux Spontaneous SR Ca release decreases stimulated contraction Aftercontractions and afterdepolarizations Spontaneous SR Ca release can trigger an action potential Acidosis decreases force, but increases Caj transients Acidosis decreases myofilament Ca sensitivity Acidosis increases anaj Sulmazole alters tension and Caj transients Myofilament Ca sensitization
15 xviii Table # TABLE OF TABLES Page 1 Cellular elements ( surface area/volume) Cellular elements (as percent of cell volume) Cardiac contractile proteins Ca and Mg binding to troponin C Temperature alters myofilament Ca sensitivity Factors that alter myofilament Ca sensitivity Passive intracellular Ca buffering Properties of cardiac L- and T-type Ca channels Biochemical characteristics of L-type Ca channel Selectivity of cardiac L-type Ca channel Sarcolemmal Ca-pump: kinetic properties Factors that alter Na/Ca exchange Factors that alter Ca release from the SR Hormone receptors and ion transporters in cardiac muscle Cardiac phosphodiesterase classes
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