Force transients and minimum cross-bridge models in muscular contraction

Springer Science and Business Media LLC - Tập 28 - Trang 371-395 - 2008
Masataka Kawai1, Herbert R. Halvorson2
1Department of Anatomy and Cell Biology, University of Iowa, Iowa City, USA
2Detroit, (USA)

Tóm tắt

Two- and three-state cross-bridge models are considered and examined with respect to their ability to predict three distinct phases of the force transients that occur in response to step change in muscle fiber length. Particular attention is paid to satisfying the Le Châtelier–Brown Principle. This analysis shows that the two-state model can account for phases 1 and 2 of a force transient, but is barely adequate to account for phase 3 (delayed force) unless a stretch results in a sudden increase in the number of cross-bridges in the detached state. The three-state model $$({\mathbf{A \rightarrow B\rightarrow C\rightarrow A}})$$ makes it possible to account for all three phases if we assume that the $${\mathbf{A\rightarrow B}}$$ transition is fast (corresponding to phase 2), the $${\mathbf{B \rightarrow C}}$$ transition is of intermediate speed (corresponding to phase 3), and the $${\mathbf{C \rightarrow A}}$$ transition is slow; in such a scenario, states A and C can support or generate force (high force states) but state B cannot (detached, or low-force state). This model involves at least one ratchet mechanism. In this model, force can be generated by either of two transitions: $${\mathbf{B\rightarrow A}}$$ or $${\mathbf{B\rightarrow C}}$$ . To determine which of these is the major force-generating step that consumes ATP and transduces energy, we examine the effects of ATP, ADP, and phosphate (Pi) on force transients. In doing so, we demonstrate that the fast transition (phase 2) is associated with the nucleotide-binding step, and that the intermediate-speed transition (phase 3) is associated with the Pi-release step. To account for all the effects of ligands, it is necessary to expand the three-state model into a six-state model that includes three ligand-bound states. The slowest phase of a force transient (phase 4) cannot be explained by any of the models described unless an additional mechanism is introduced. Here we suggest a role of series compliance to account for this phase, and propose a model that correlates the slowest step of the cross-bridge cycle (transition $${\mathbf{C\rightarrow A}}$$ ) to: phase 4 of step analysis, the rate constant k tr of the quick-release and restretch experiment, and the rate constant k act for force development time course following Ca2+ activation.

Tài liệu tham khảo

Abbott RH (1973) An interpretation of the effect of fiber length and calcium on the mechanical properties of insect flight muscle. Cold Spring Harb Symp Quant Biol 37:647–654 Abbott RH, Steiger GJ (1977) Temperature and amplitude dependence of tension transients in glycerinated skeletal and insect fibrillar muscle. J Physiol 266:13–42 Araujo A, Walker JW (1996) Phosphate release and force generation in cardiac myocytes investigated with caged phosphate and caged calcium. Biophys J 70:2316–2326 Bagni MA, Cecchi G, Colomo F and Poggesi C (1990) Tension and stiffness of frog muscle fibres at full filament overlap. J Muscle Res Cell Motil 11:371–377 Bagshaw CR, Eccleston JF, Eckstein F, Goody RS, Gutfreund H, Trentham DR (1974) The magnesium ion-dependent adenosine triphosphatase of myosin. Two-step processes of adenosine triphosphate association and adenosine diphosphate dissociation. Biochem J 141:351–364 Barsotti RJ, Ferenczi MA (1988) Kinetics of ATP hydrolysis and tension production in skinned cardiac muscle of the guinea pig. J Biol Chem 263:16750–16756 Bershitsky SY, Tsaturyan AK (1992) Tension responses to joule temperature jump in skinned rabbit muscle fibres. J Physiol 447:425–448 Brenner B (1988) Effect of Ca2+ on cross-bridge turnover kinetics in skinned single rabbit psoas fibers: implications for regulation of muscle contraction. Proc Natl Acad Sci USA 85:3265–3269 Brenner B, Schoenberg M, Chalovich JM, Greene LE, Eisenberg E (1982) Evidence for cross-bridge attachment in relaxed muscle at low ionic strength. Proc Natl Acad Sci USA 79:7288–7291 Burton K, Simmons RM, Sleep J (2006) Kinetics of force recovery following length changes in active skinned single fibres from rabbit psoas muscle. J Physiol 573(2):305–328 Campbell KB, Razumova MV, Kirkpatrick RD, Slinker BK (2001) Nonlinear myofilament regulatory processes affect frequency-dependent muscle fiber stiffness. Biophys J 81:2278–2296 Cooke R (2005) Milestone in physiology: the sliding filament model: 1972–2004. J Gen Physiol 123:643–656 Cooke R, Pate E (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J 48:789–798 Coupland ME, Puchert E, Ranatunga KW (2001) Temperature dependence of active tension in mammalian (rabbit psoas) muscle fibres: effect of inorganic phosphate. J Physiol 536:879–891 Dantzig J, Goldman Y, Millar NC, Lacktis J, Homsher E (1992). Reversal of the cross-bridge force-generating transition by the photogeneration of phosphate in rabbit psoas muscle fibers. J Physiol 451:247–278 Davis JS, Rodgers ME (1995) Force generation and temperature-jump and length-jump tension transients in muscle fibers. Biophys J 68:2032–2040 Davis JS, Satorius CL, Epstein ND (2002) Kinetic effects of myosin regulatory light chain phosphorylation on skeletal muscle contraction. Biophys J 83:359–370 Dickinson MH, Hyatt CJ, Lehmann F-O, Moore JR, Reedy MC, Simcox A, Tohtong R, Vigoreaux JO, Yamashita H, Maughan DW (1997) Phosphorylation-dependent power output of transgenic flies: an integrated study. Biophys J 73:3122–3134 Dobbie I, Linari M, Piazzesi G, Reconditi M, Koubassova N, Ferenczi M, Lombardi V, Irving M (1998) Elastic bending and active tilting of myosin heads during muscle contraction. Nature 396:383–387 Dominguez R, Freyzon Y, Trybus KM, Cohen C (1998) Crystal structure of a vertebrate smooth muscle myosin motor domain and its complex with the essential light chain: visualisation of the pre-power stroke state. Cell 94:559–571 Fenn WO (1923) A quantitative comparison between the energy liberated and the work performed by the isolated sartorius muscle of the frog. J Physiol 58:175–203 Finer JT, Simmons RM, Spudich JA (1994) Single myosin mechanics: piconewton forces and nanometre steps. Nature (Lond) 368:113–119 Ford LE, Huxley AF, Simmons RM (1977) Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol 269:441–515 Fortune NS, Geeves MA, Ranatunga KW (1991) Tension responses to rapid pressure release in glycerinated rabbit muscle fibers. Proc Natl Acad Sci USA 88:7323–7327 Fujita H, Sasaki D, Ishiwata S, Kawai M (2002) Elementary steps of the cross-bridge cycle in bovine myocardium with and without regulatory proteins. Biophys J 82:915–928 Galler S, Wang BG, Kawai M (2005) Elementary steps of the cross-bridge cycle in fast-twitch fiber types from rabbit skeletal muscles. Biophys J 89:3248–3260 Geeves MA, Holmes KC (1999) Structural mechanism of muscle contraction. Annu Rev Biochem 68:687–728 Geeves MA, Holmes KC (2005) The molecular mechanism of muscle contraction. Adv Protein Chem 71:161–193 Goldman YE, Hibberd MG, Trentham DR (1984) Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5’-triphosphate. J Physiol 354:577–604 Gordon AM, Homsher E, Regnier M (2000) Regulation of contraction in striated muscle. Physiol Rev 80:853–924 Guilford WH, Dupuis DE, Kennedy G, Wu J, Patlak JB, Warshaw DM (1997) Smooth muscle and skeletal muscle myosins produce similar unitary forces and displacements in the laser trap. Biophys J 72:1006–1021 Gutfreund H (1995) Kinetics for the life sciences. Receptors, transmitters and catalysts. Cambridge University Press Heinl P, Kuhn HJ, Rüegg JC (1974) Tension responses to quick length changes of glycerinated skeletal muscle fibres from the frog and tortoise. J Physiol 237:243–258 Herrmann C, Lionne C, Travers F, Barman T (1994) Correlation of ActoS1, myofibrillar, and muscle fiber ATPases. Biochemistry 33:4148–4154 Higuchi H, Yanagida T and Goldman YE (1995) Compliance of thin filaments in skinned fibers of rabbit skeletal muscle. Biophys J 69:1000–1010 Homsher W, Millar NC (1990) Caged compounds and striated muscle contraction. Annu Rev Physiol 52:875–896 Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophys Biophys Chem 7:255–318 Huxley AF (1974) Muscular contraction. J Physiol 243:1–43 Huxley AF (1980) Reflections on muscle. Princeton University Press, Princeton Huxley AF, Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233:533–538 Huxley HE, Stewart A, Sosa H, Irving T (1994). X-ray diffraction measurements of the extensibility of actin and myosin filaments in contracting muscle. Biophys J 67:2411–2421 Ishijima A, Kojima H, Higuchi H, Harada Y, Funatsu T, Yanagida T (1996) Multiple- and single-molecule analysis of the actomyosin motor by nanometer-piconewton manipulation with a microneedle: unitary steps and force. Biophys J 70:383–400 Julian FJ, Sollins KR, Sollins MR (1974) A model for the transient and steady-state mechanical behavior of contracting muscle. Biophys J 14:546–562 Kawai M (1978) Head rotation or dissociation? A study of exponential rate processes in chemically skinned rabbit muscle fibers when MgATP concentration is changed. Biophys J 22:97–103 Kawai M (1986) The role of orthophosphate in crossbridge kinetics in chemically skinned rabbit psoas fibers as detected with sinusoidal and step length alterations. J Muscle Res Cell Motil 7:421–434 Kawai M (2003) What do we learn by studying the temperature effect on isometric tension and tension transients in mammalian striated muscle fibres? J Muscle Res Cell Motil 24:127–138 Kawai M, Brandt PW (1980) Sinusoidal analysis: a high resolution method for correlating biochemical reactions with physiological processes in activated skeletal muscles of rabbit, frog and crayfish. J Muscle Res Cell Motil 1:279–303 Kawai M, Halvorson HR (1989) Role of MgATP and MgADP in the crossbridge kinetics in chemically skinned rabbit psoas fibers. Study of a fast exponential process (C). Biophys J 55:595–603 Kawai M, Halvorson HR (1991) Two step mechanism of phosphate release and the mechanism of force generation in chemically skinned rabbit psoas muscle. Biophys J 59:329–342 Kawai M, Schachat FH (1984) Differences in the transient response to fast and slow skeletal muscle fibers: correlations between complex modulus and myosin light chains. Biophys J 45:1145–1151 Kawai M, Zhao Y (1993) Cross-bridge scheme and force per cross-bridge state in skinned rabbit psoas muscle fibers. Biophys J 65:638–651 Kawai M, Saeki Y, Zhao Y (1993) Cross-bridge scheme and the kinetic constants of elementary steps deduced from chemically skinned papillary and trabecular muscles of the ferret. Circ Res 73:35–50 Kirkwood JG, Oppenheim I (1961) Chemical thermodynamics. McGraw-Hill Book Co. Inc., New York Kitamura K, Tokunaga M, Iwane AH, Yanagida T (1999) A single myosin head moves along an actin filament with regular steps of 5.3 nanometres. Nature 397(6715):129–134 Kojima H, Ishijima A, Yanagida T (1994). Direct measurement of stiffness of single actin filaments with and without tropomyosin by in vitro nanomanipulation. Proc Natl Acad Sci USA 91:12962–12966 Labeit D, Watanabe K, Witt C, Fujita H, Wu Y, Lahmers S, Funck T, Labeit S, Granzier H (2003) Calcium-dependent molecular spring elements in the giant protein titin. Proc Natl Acad Sci 100:13716–13721 Lu X, Bryant MK, Bryan KE, Rubenstein PA, Kawai M (2005) Role of the N-terminal negative charge of actin in cross-bridge kinetics and force generation in reconstituted bovine myocardium. J Physiol 564(1):65–82 Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–4624 Marcussen BL, Kawai M (1990) Role of MgATP and inorganic phosphate ions in crossbridge kinetics in insect (Lethocerus colossicus) flight muscle. In: Sperelakis N, Wood JD (eds) Frontiers in smooth muscle research. Wiley-Liss, New York, pp 805–813 Martin H, Barsotti RJ (1994) Relaxation from rigor of skinned trabeculae of the guinea pig induced by laser photolysis of caged ATP. Biophys J 66:1115–1128 Meyer RA, Brown TR, Kushmerick MJ (1985) Phosphorus nuclear magnetic resonance of fast- and slow-twitch muscle. Am J Physiol 248:C279–C287 Mijailovich SM, Fredberg JJ, Butler JP (1996) On the theory of muscle contraction: filament extensibility and the development of isometric force and stiffness. Biophys J 71:1475–1484 Millar NC, Geeves MA (1988) Protein fluorescence changes associated with ATP and adenosine 5’-[γ-thio]triphosphate binding to skeletal muscle myosin subfragment 1 and actomyosin subfragment 1. Biochem J 249:735–743 Millar NC, Homsher E (1992) Kinetics of force generation and phosphate release in skinned rabbit soleus muscle fibers. Am J Physiol 252(Cell Physiol 31):C1239–C1245 Miyata H, Yoshikawa H, Hakozaki H, Suzuki N, Furuno T, Ikegami A, Kinosita K Jr, Nishizaka T, Ishiwata S (1995) Mechanical measurements of single actomyosin motor force. Biophys J 68:286S–290S Molloy JE, Burns JE, Kendrick-Jones J, Tregear RT, White DCS (1995) Movement and force produced by a single myosin head. Nature (Lond) 378:209–212 Murase M, Tanaka H, Nishiyama K, Shimizu H (1986) A three-state model for oscillation in muscle: sinusoidal analysis. J Muscle Res Cell Motil 7:2–10 Palmer BM, Suzuki T, Wang Y, Barnes WD, Miller MS, Maughan DW (2007) Two-state model of acto-myosin attachment-detachment predicts C-process of sinusoidal analysis. Biophys J 93:760–769 Piazzesi G, Reconditi M, Linari M, Lucii L, Bianco P, Brunello E, Decostre V, Stewart A, Gore DB, Irving TC, Irving M, Lombardi V (2007) Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size. Cell 131:784–795 Piroddi N, Tesi C, Pellegrino MA, Tobacman LS, Homsher E, Poggesi C (2003) Contractile effects of the exchange of cardiac troponin for fast skeletal troponin in rabbit psoas single myofibrils. J Physiol 552.3:917–931 Preston LC, Lipscomb S, Robinson P, Mogensen J, McKenna WJ, Watkins H, Ashley CC, Redwood CS (2007) Functional effects of the DCM mutant Gly159Asp troponin C in skinned muscle fibres. Pflugers Arch 453:771–776 Pringle JWS (1978) Stretch activation of muscle: function and mechanism. Proc R Soc Lond B 201:107–130 Ranatunga KW (1999) Effects of inorganic phosphate on endothermic force generation in muscle. Proc Biol Sci 266:1381–1385 Rayment I, Rypniewski WR, Schmidt-Bäse K, Smith R, Tomchick DR, Benning MM, Winkelmann DA, Wesenberg G, Holden HM (1993) Three-dimensional structure of myosin subfragment-1: a molecular motor. Science 261:50–58 Regnier M, Morris C, Homsher E (1995) Regulation of the cross-bridge transition from a weakly to strongly bound state in skinned rabbit muscle fibers. Am J Physiol 269(6 Pt 1):C1532–C1539 Rosenfeld SS, Xing J, Whitaker M, Cheung HC, Brown F, Wells A, Milligan RA, Sweeney HL (2001) Kinetic and spectroscopic evidence for three actomyosin: ADP states in smooth muscle. J Biol Chem 275:25418–25426 Saeki Y, Kawai M, Zhao Y (1991) Comparison of crossbridge dynamics between intact and skinned myocardium from ferret right ventricles. Circ Res 68:772–781 Saeki Y, Sagawa K, Suga H (1978) Dynamic stiffness of cat heart muscle in Ba2+-induced contracture. Circ Res 42:324–333 Sleep JA, Hutton RL (1980) Exchange between inorganic phosphate and adenosine 5’-triphosphate in the medium by actomyosin subfragment 1. Biochemistry 19:1276–1283 Smith DA (1998) A strain-dependent ratchet model for [phosphate]- and [ATP]-dependent muscle contraction. J Muscle Res Cell Motil 19:189–211 Smith DA, Geeves MA (1995) Strain-dependent cross-bridge cycle for muscle. Biophys J 69:524–537 Spirito P, Seidman CE, McKenna WJ, Maron BJ (1997) The management of hypertrophic cardiomyopathy. N Engl J Med 336:775–785 Squire JM, Luther PK, Knupp C (2003) Structural evidence for the interaction of C-protein (MyBP-C) with actin and sequence identification of a possible actin-binding domain. J Mol Biol 331:713–724 Stehle R, Krüger M, Scherer P, Brixius K, Schwinger RH, Pfitzer G (2002) Isometric force kinetics upon rapid activation and relaxation of mouse, guinea pig and human heart muscle studied on the subcellular myofibrillar level. Basic Res Cardiol 97(Suppl 1):I127–I135 Steiger GJ, Abbott RH (1981) Biochemical interpretation of tension transients produced by a four-state mechanical model. J Muscle Res Cell Motil 2:245–260 Stein LA, Greene LE, Chock PB, Eisenberg E (1985) Rate-limiting step in the actomyosin adenosinetriphosphatase cycle: studies with myosin subfragment 1 cross-linked to actin. Biochemistry 24:1357–1363 Swank DM, Vishnudas VK, Maughan DW (2006) An exceptionally fast actomyosin reaction powers insect flight muscle. Proc Natl Acad Sci USA 103:17543–17547 Takagi Y, Shuman H, Goldman YE (2004) Coupling between phosphate release and force generation in muscle actomyosin. Philos Trans R Soc Lond B Biol Sci 359:1913–1920 Tanner BC, Daniel TL, Regnier M (2007) Sarcomere lattice geometry influences cooperative myosin binding in muscle. PLoS Comput Biol 3:1195–1211 Tawada K, Kawai M (1990) Covalent cross-linking of single muscle fibers from rabbit psoas increases oscillatory power. Biophys J 57:643–647 Taylor EW (1979) Mechanism of actomyosin ATPase and the problem of muscle contraction. CRC Crit Rev Biochem 6:103–164 Tesi C, Colomo F, Nencini S, Piroddi N, Poggesi C (2000) The effect of inorganic phosphate on force generation in single myofibrils from rabbit skeletal muscle. Biophys J 78:3081–3092 Tesi C, Colomo F, Piroddi N, Poggesi C (2002) Characterization of the cross-bridge force-generating step using inorganic phosphate and BDM in myofibrils from rabbit skeletal muscles. J Physiol 541(1):189–199 Thirlwell H, Sleep JA, Ferenczi MA (1995) Inhibition of unloaded shortening velocity in permeabilized muscle fibres by caged ATP compounds. J Muscle Res Cell Motil 16:131–137 Thorson J, White DC (1969) Distributed representations for actin-myosin interaction in the oscillatory contraction of muscle. Biophys J 9:360–390 Thorson J, White DC (1983) Role of cross-bridge distortion in the small-signal mechanical dynamics of insect and rabbit striated muscle. J Physiol 343:59–84 Tikunov BA, Sweeney HL, Rome LC (2000) Quantitative electrophoretic analysis of myosin heavy chains in single muscle fibers. J Appl Physiol 90:1927–1935 Vale RD, Oosawa F (1990) Protein motors and Maxwell’s demons: does mechanochemical transduction involve a thermal ratchet? Adv Biophys 26:97–134 Wakabayashi K, Sugimoto Y, Tanaka H, Ueno Y, Takezawa Y and Amemiya Y (1994) X-ray diffraction evidence for the extensibility of actin and myosin filaments during muscle contraction. Biophys J 67: 2422–2435 Walker JW, Lu Z, Moss RL (1992) Effects of Ca2+ on the kinetics of phosphate release in skeletal muscle. J Biol Chem 267:2459–2466 Wang G, Kawai M (1996) Effects of MgATP and MgADP on the cross-bridge kinetics of rabbit soleus slow-twitch muscle fibers. Biophys J 71:1450–1461 Wang G, Kawai M (1997) Force generation and phosphate release steps in skinned rabbit soleus slow-twitch muscle fibers. Biophys J 73:878–894 Wang G, Ding W, Kawai M (1999) Does thin filament compliance diminish the cross-bridge kinetics? A study in rabbit psoas fibers. Biophys J 76:978–984 Wannenburg T, Heijne GH, Geerdink JH, Van Den Dool HW, Janssen PM, De Tombe PP (2000) Cross-bridge kinetics in rat myocardium: effect of sarcomere length and calcium activation. Am J Physiol 279: H779–H790 Webb MR, Hibberd MG, Goldman YE, Trentham DR (1986) Oxygen exchange between Pi in the medium and water during ATP hydrolysis mediated by skinned fibers from rabbit skeletal muscle: evidence for Pi binding to a force-generating state. J Biol Chem 261:15557–15564 White DC (1983) The elasticity of relaxed insect fibrillar flight muscle. J Physiol 343:31–57 White HD, Taylor EW (1976) Energetics and mechanism of actomyosin adenosine triphosphatase. Biochemistry 15:5818–5826 Woledge RC, Curtin NA, Homsher E (1985) Energetic aspects of muscle contraction (Monographs of the Physiological Society, No. 41). Academic Press, New York Xu S, Offer G, Gu J, White HD, Yu LC (2003) Temperature and ligand dependence of conformation and helical order in myosin filaments. Biochemistry 42:390–401 Yates LD, Greaser ML (1983) Quantitative determination of myosin and actin in rabbit skeletal muscle. J Mol Biol 168:123–141 Yount RG, Lawson D, Rayment I (1995) Is myosin a “back door” enzyme? Biophys J 68:44S–47S Zhao Y, Kawai M (1993) The effect of the lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. II. Elementary steps affected by the spacing change. Biophys J 64:197–210 Zhao Y, Kawai M (1994) Kinetic and thermodynamic studies of the cross-bridge cycle in rabbit psoas muscle fibers. Biophys J 67:1655–1668 Zhao Y, Kawai M (1996) Inotropic agent EMD 53998 weakens nucleotide and phosphate binding to cross bridges in porcine myocardium. Am J Physiol 271(Heart Circ Physiol 40):H1394–H1406 Zhao Y, Swamy PMG, Humphries KA, Kawai M (1996) The effect of partial extraction of troponin C on the elementary steps of the cross-bridge cycle in rabbit psoas fibers. Biophys J 71:2759–2773