Length‐dependent activation in three striated muscle types of the rat

The process whereby sarcomere length modulates the sensitivity of the myofilaments to Ca2+ is termed length‐dependent activation. Length‐dependent activation is a property of all striated muscles, yet the relative extent of length‐dependent activation between skeletal muscle and cardiac muscle is unclear. Although length‐dependent activation may be greater in fast skeletal muscle (FSM) than in slow skeletal muscle (SSM), there has not been a well controlled comparison of length‐dependent activation between skeletal muscle and cardiac muscle (CM). Accordingly, we measured sarcomere length‐dependent properties in skinned soleus (SSM), psoas (FSM) and ventricular trabeculae (CM) of the rat under carefully controlled conditions. The free Ca2+‐force relationship was determined at sarcomere lengths (SL) of 1.95 μm, 2.10 μm and 2.25 μm and fitted to a modified Hill equation. FSM and SSM were more sensitive to Ca2+ than CM. Length‐dependent activation was ordered as CM > FSM > SSM. Cooperativity as measured by the Hill coefficient of the Ca2+‐force relationship was not significantly different between CM and FSM, both of which exhibited greater cooperativity than SSM. SL did not significantly alter this parameter in each muscle type. To establish whether the observed differences can be explained by alterations in interfilament spacing, we measured myofilament lattice spacing (LS) by synchrotron X‐ray diffraction in relaxed, skinned muscle preparations. LS was inversely proportional to SL for each muscle type. The slope of the SL‐LS relationship, however, was not significantly different between striated muscle types. We conclude that (1) length‐dependent activation differs among the three types of striated muscle and (2) these differences in the length‐dependent properties among the striated muscle types may not solely be explained by the differences in the response of interfilament spacing to changes in muscle length in relaxed, skinned isolated muscle preparations.

[1]  S. Ishiwata,et al.  Effects of MgADP on length dependence of tension generation in skinned rat cardiac muscle. , 2000, Circulation research.

[2]  E. Rome,et al.  X-ray diffraction studies of the filament lattice of striated muscle in various bathing media. , 1968, Journal of molecular biology.

[3]  K S McDonald,et al.  Rate of tension development in cardiac muscle varies with level of activator calcium. , 1995, Circulation research.

[4]  R. Moss,et al.  Calcium-sensitive cross-bridge transitions in mammalian fast and slow skeletal muscle fibers. , 1990, Science.

[5]  R. Moss,et al.  Factors influencing the ascending limb of the sarcomere length‐tension relationship in rabbit skinned muscle fibres. , 1987, The Journal of physiology.

[6]  A. Fabiato,et al.  Dependence of the contractile activation of skinned cardiac cells on the sarcomere length , 1975, Nature.

[7]  F. Fuchs,et al.  Sarcomere length versus interfilament spacing as determinants of cardiac myofilament Ca2+ sensitivity and Ca2+ binding. , 1996, Journal of molecular and cellular cardiology.

[8]  E. Eisenberg,et al.  Evidence for cross-bridge attachment in relaxed muscle at low ionic strength. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[9]  G. Pollack,et al.  Sarcomere dynamics in intact cardiac muscle. , 1976, European journal of cardiology.

[10]  D. Allen,et al.  The effects of muscle length on intracellular calcium transients in mammalian cardiac muscle. , 1982, The Journal of physiology.

[11]  T. Irving,et al.  Myofilament Calcium Sensitivity in Skinned Rat Cardiac Trabeculae: Role of Interfilament Spacing , 2002, Circulation research.

[12]  R. Moss,et al.  Cross‐bridge interaction kinetics in rat myocardium are accelerated by strong binding of myosin to the thin filament , 2001, The Journal of physiology.

[13]  R. Solaro,et al.  The hill coefficient for the Ca2+-activation of striated muscle contraction. , 1984, Biophysical journal.

[14]  P. J. Griffiths,et al.  Lattice spacing changes accompanying isometric tension development in intact single muscle fibers. , 1994, Biophysical journal.

[15]  R. Gupta,et al.  M2-specific muscarinic cholinergic receptor-mediated inhibition of cardiac regulatory protein phosphorylation. , 1994, The American journal of physiology.

[16]  Siegfried Labeit,et al.  Cardiac titin: an adjustable multi‐functional spring , 2002, The Journal of physiology.

[17]  B. Millman,et al.  X-ray diffraction patterns from mammalian heart muscle. , 1973, The Journal of physiology.

[18]  T. Irving,et al.  Myofilament lattice spacing as a function of sarcomere length in isolated rat myocardium. , 2000, American journal of physiology. Heart and circulatory physiology.

[19]  J. Gulati,et al.  Diminished Ca2+ sensitivity of skinned cardiac muscle contractility coincident with troponin T-band shifts in the diabetic rat. , 1995, Circulation research.

[20]  D. A. Williams,et al.  Effects of sarcomere length on the force—pCa relation in fast‐ and slow‐twitch skinned muscle fibres from the rat , 1982, The Journal of physiology.

[21]  K S McDonald,et al.  Sarcomere length dependence of the rate of tension redevelopment and submaximal tension in rat and rabbit skinned skeletal muscle fibres , 1997, The Journal of physiology.

[22]  E. Marbán,et al.  Mechanism of force inhibition by 2,3‐butanedione monoxime in rat cardiac muscle: roles of [Ca2+]i and cross‐bridge kinetics. , 1994, The Journal of physiology.

[23]  Kenneth S. Campbell,et al.  Cooperative Mechanisms in the Activation Dependence of the Rate of Force Development in Rabbit Skinned Skeletal Muscle Fibers , 2001, The Journal of general physiology.

[24]  R. Solaro,et al.  Troponin and tropomyosin: proteins that switch on and tune in the activity of cardiac myofilaments. , 1998, Circulation research.

[25]  J. Potter,et al.  The calcium and magnesium binding sites on troponin and their role in the regulation of myofibrillar adenosine triphosphatase. , 1975, The Journal of biological chemistry.

[26]  P. D. de Tombe,et al.  Cooperative activation in cardiac muscle: impact of sarcomere length. , 2002, American journal of physiology. Heart and circulatory physiology.

[27]  T. Irving,et al.  Titin-Based Modulation of Calcium Sensitivity of Active Tension in Mouse Skinned Cardiac Myocytes , 2001, Circulation research.

[28]  P. D. de Tombe,et al.  Protein kinase A does not alter unloaded velocity of sarcomere shortening in skinned rat cardiac trabeculae. , 1997, American journal of physiology. Heart and circulatory physiology.

[29]  M. Greaser,et al.  Substitution of cardiac troponin C into rabbit muscle does not alter the length dependence of Ca2+ sensitivity of tension. , 1991, The Journal of physiology.

[30]  R. Moss,et al.  Influence of a strong-binding myosin analogue on calcium-sensitive mechanical properties of skinned skeletal muscle fibers. , 1992, The Journal of biological chemistry.

[31]  A. Fabiato,et al.  Myofilament-generated tension oscillations during partial calcium activation and activation dependence of the sarcomere length-tension relation of skinned cardiac cells , 1978, The Journal of general physiology.

[32]  K S McDonald,et al.  Osmotic compression of single cardiac myocytes eliminates the reduction in Ca2+ sensitivity of tension at short sarcomere length. , 1995, Circulation research.

[33]  B. R. Jewell,et al.  Calcium‐ and length‐dependent force production in rat ventricular muscle , 1982, The Journal of physiology.

[34]  Stephen H. Smith,et al.  Calcium, cross-bridges, and the Frank-Starling relationship. , 2001, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[35]  A. Huxley,et al.  Tension development in highly stretched vertebrate muscle fibres , 1966, The Journal of physiology.

[36]  J. Leiden,et al.  Attenuation of length dependence of calcium activation in myofilaments of transgenic mouse hearts expressing slow skeletal troponin I , 2000, The Journal of physiology.

[37]  J. Potter,et al.  The calcium and magnesium binding sites on cardiac troponin and their role in the regulation of myofibrillar adenosine triphosphatase. , 1980, The Journal of biological chemistry.

[38]  B. Brenner,et al.  Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[39]  K. Campbell,et al.  Rate constant of muscle force redevelopment reflects cooperative activation as well as cross-bridge kinetics. , 1997, Biophysical journal.

[40]  E. Sonnenblick,et al.  The role of troponin C in the length dependence of Ca(2+)‐sensitive force of mammalian skeletal and cardiac muscles. , 1991, The Journal of physiology.

[41]  E. Sonnenblick,et al.  Molecular basis for the influence of muscle length on myocardial performance. , 1988, Science.

[42]  J. Lowy,et al.  An X-ray and light-diffraction study of the filament lattice of striated muscle in the living state and in rigor , 1963 .

[43]  R. Moss,et al.  Strong binding of myosin modulates length-dependent Ca2+ activation of rat ventricular myocytes. , 1998, Circulation research.

[44]  H. T. ter Keurs,et al.  Tension Development and Sarcomere Length in Rat Cardiac Trabeculae: Evidence of Length‐Dependent Activation , 1980, Circulation research.

[45]  Stephen H. Smith,et al.  Effect of ionic strength on length-dependent Ca(2+) activation in skinned cardiac muscle. , 1999, Journal of molecular and cellular cardiology.

[46]  H. Keurs,et al.  Force and velocity of sarcomere shortening in trabeculae from rat heart. Effects of temperature. , 1990 .

[47]  G. Vassort,et al.  Is titin the length sensor in cardiac muscle? Physiological and physiopathological perspectives. , 2000, Advances in experimental medicine and biology.

[48]  S. Kurihara,et al.  Length dependence of Ca(2+)-tension relationship in aequorin-injected ferret papillary muscles. , 1997, The American journal of physiology.

[49]  G H Pollack,et al.  The sarcomere length-tension relation in skeletal muscle , 1978, The Journal of General Physiology.

[50]  H. T. ter Keurs,et al.  Comparison between the Sarcomere Length‐Force Relations of Intact and Skinned Trabeculae from Rat Right Ventricle: Influence of Calcium Concentrations on These Relations , 1986, Circulation research.

[51]  K. McDonald,et al.  Length dependence of Ca2+ sensitivity of tension in mouse cardiac myocytes expressing skeletal troponin C. , 1995, The Journal of physiology.

[52]  I. Ohtsuki,et al.  Effect of troponin I phosphorylation by protein kinase A on length-dependence of tension activation in skinned cardiac muscle fibers. , 2000, Biochemical and biophysical research communications.

[53]  B. Brenner,et al.  Equatorial x-ray diffraction from single skinned rabbit psoas fibers at various degrees of activation. Changes in intensities and lattice spacing. , 1985, Biophysical journal.

[54]  I. Ohtsuki,et al.  Role of troponin C in determining the Ca(2+)-sensitivity and cooperativity of the tension development in rabbit skeletal and cardiac muscles. , 1994, Journal of biochemistry.

[55]  M. Endo,et al.  Length Dependence of Activation of Skinned Muscle Fibers by Calcium , 1973 .

[56]  Pollack Gh,et al.  Sarcomere dynamics in intact cardiac muscle. , 1976 .

[57]  P. D. de Tombe,et al.  Cross-bridge kinetics in rat myocardium: effect of sarcomere length and calcium activation. , 2000, American journal of physiology. Heart and circulatory physiology.

[58]  A. Weber,et al.  Cooperation within actin filament in vertebrate skeletal muscle. , 1972, Nature: New biology.

[59]  S. Lehrer.  The regulatory switch of the muscle thin filament: Ca2+ or myosin heads? , 1994, Journal of Muscle Research & Cell Motility.

[60]  R. Moss.  Ca2+ regulation of mechanical properties of striated muscle. Mechanistic studies using extraction and replacement of regulatory proteins. , 1992, Circulation research.

[61]  P. D. de Tombe,et al.  Protein kinase A does not alter economy of force maintenance in skinned rat cardiac trabeculae. , 1995, Circulation research.

[62]  E. Marbán,et al.  Myofilament Ca2+ sensitivity in intact versus skinned rat ventricular muscle. , 1994, Circulation research.

[63]  D. Allen,et al.  The cellular basis of the length-tension relation in cardiac muscle. , 1985, Journal of molecular and cellular cardiology.

[64]  Y. Zhao,et al.  The effect of lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. I. Proportionality between the lattice spacing and the fiber width. , 1993, Biophysical journal.

[65]  I. Matsubara,et al.  X-ray diffraction studies on skinned single fibres of frog skeletal muscle. , 1972, Journal of molecular biology.