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Comparison of cross-bridge cycling kinetics in neonatal vs. adult rat ventricular muscle

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Abstract

The developmental shift in contractile protein isoform expression in the rodent heart likely affects actin-myosin cross-bridge interactions. We compared the Ca2+ sensitivity for force generation and cross-bridge cycling kinetics in neonatal (postnatal days 0–3) and adult (day 84) rats. The force-pCa relationship was determined in Triton-X skinned muscle bundles activated at pCa 9.0 to 4.0. In strips maximally activated at pCa 4.0, the following parameters of cross-bridge cycling were measured: (1) rate of force redevelopment following rapid shortening and restretching (ktr); and (2) isometric stiffness at maximal activation and in rigor. The fraction of attached cross-bridges (αfs) and apparent rate constants for cross-bridge attachment (fapp) and detachment (gapp) were derived assuming a two-state model for cross-bridge cycling. Compared to the adult, the force-pCa curve for neonatal cardiac muscle was significantly shifted to the left. Neonatal cardiac muscle also displayed significantly smaller αfs, slower ktr and fapp; however, gapp was not significantly different between age groups. These data indicate that weaker force production in neonatal cardiac muscle involves, at least in part, less efficient cross-bridge cycling kinetics.

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References

  • Ausoni S, De-Nardi C, Moretti P, Gorza L and Schiaffino S (1991) Developmental expression of rat cardiac troponin I mRNA. Development 112: 1041–1051.

    Google Scholar 

  • Barany M (1967) ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 50: 197–216.

    Google Scholar 

  • Brenner B (1983) Technique for stabilizing the striation pattern in maximally calcium-activated skinned rabbit psoas fibers. Biophys J 41: 99–102.

    Google Scholar 

  • Brenner B (1986a) The cross-bridge cycle in muscle. Mechanical, biochemical, and structural studies on single skinned rabbit psoas fibers to characterize cross-bridge kinetics in muscle for correlation with the actomyosin-ATPase in solution. Basic Res Cardiol 81: 1–15.

    Google Scholar 

  • Brenner B (1986b) Kinetics of the crossbridge cycle derived from measurements of force, rate of force development and isometric ATPase. J Muscle Res Cell Motil 7: 75–76.

    Google Scholar 

  • de Tombe PP and ter Keurs HEDJ (1991) Lack of effect of isoproterenol on unloaded velocity of sarcomere shortening in rat cardiac trabeculae. Circ Res 68: 382–391.

    Google Scholar 

  • Fabiato A (1982) Calcium release in skinned cardiac cells: varations with species tissues and development. Fed Proc 41: 2238–2244.

    Google Scholar 

  • Fabiato A and Fabiato F (1975) Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol 249: 469–495.

    Google Scholar 

  • Fabiato A and Fabiato F (1976) Dependence of calcium release, tension generation and restoring forces on sarcomere length in skinned cardiac cells. Eur J Cardiol 4: 13–27.

    Google Scholar 

  • Ford LE, Huxley AF and Simmons RM (1981) The relation between stiffness and filament overlap in stimulated frog muscle fibres. J Physiol 311: 219–429.

    Google Scholar 

  • Friedman WF (1972) The intrinsic physiologic properties of the developing heart. Prog Cardiovasc Dis 15: 87–111.

    Google Scholar 

  • Godt RE and Lindley BD (1982) Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol 80: 279–297.

    Google Scholar 

  • Harris DE, Work SS, Wright RK, Alpert NR and Warshaw DM (1994) Smooth, cardiac and skeletal muscle myosin force and motion generation assessed by cross-bridge mechanical interactions in vitro. J Muscle Res Cell Motil 15: 11–19.

    Google Scholar 

  • Hassenfuss G, Mulieri LA, Blanchard EM, Holubarsch C, Leavitt BJ, Ittleman F and Alpert NR (1991) Energetics of isometric force development in control and volume-overload human myocardium: comparison with animal species. Circ Res 68: 836–846.

    Google Scholar 

  • Hibberd MG and Jewell BR (1982) Calcium-and length-dependent force production in rat ventricular muscle. J Physiol (Lond) 329: 527–540.

    Google Scholar 

  • Hill AV (1938) The heat of shortening and the dynamic constants of muscle. Proc R Soc Lond 126: 136–195.

    Google Scholar 

  • Hoh JF, McGrath PA and Hale PT (1978) Electrophoretic analysis of multiple forms of rat cardiac myosin: effects of hypophysectomy and thyroxine replacement. J Mol Cell Cardiol 10: 1053–1076.

    Google Scholar 

  • Huxley AF (1957) Muscle structure and theories of contraction. Prog Biophysics Biophys Chem 7: 255–318.

    Google Scholar 

  • Huxley AF and Simmons RM (1971) Proposed mechanism of force generation in striated muscle. Nature 233: 533–538.

    Google Scholar 

  • Julian FJ, Sollins KR and Sollins MR (1974) A model for the transient and steady-state mechanical behavior of contracting muscle. Biophys J 14: 546–562.

    Google Scholar 

  • Kawai M and 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.

    Google Scholar 

  • Kentish JC, Ter Keurs HEDJ, Ricciardi L, Bucx JJJ and Noble MIM (1986) Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle: Influence of calcium on these relations. Circ Res 58: 755–768.

    Google Scholar 

  • Krane EJ and Su JY (1989) Comparison of the effects of halothane on skinned myocardial fibers from newborn and adult rabbit. II. Effects on sarcoplasmic reticulum. Anesthesiology 71: 103–109.

    Google Scholar 

  • Linari M, Dobbie I, Reconditi M, Koubassova N, Irving M, Piazzesi G and Lombardi V (1998) The stiffness of skeletal muscle in isometric contraction and rigor: the fraction of myosin heads bound to actin. Biophys J 74: 2459–2473.

    Google Scholar 

  • Mahdavi V, Periasamy M and Nadal-Ginard B (1982) Molecular characterization of two myosin heavy chain genes expressed in the adult heart. Nature 297: 659–664.

    Google Scholar 

  • Martin AF, Ball K, Gao L, Kumar P and Solaro RJ (1991) Identification and functional significance of troponin isoforms in neonatal rat heart myofibrils. Circ. Res. 69: 1244–1252.

    Google Scholar 

  • Moss RL (1992) Ca2+ regulation of mechanical properties of striated muscle: mechanistic studies using extraction and replacement of regulatory proteins. Circ Res 70: 865–884.

    Google Scholar 

  • Murat I, Hoerter J and Ventura-Clapier R (1990) Developmental changes in effects of halothane and isoflurane on contractile properties of rabbit cardiac skinned fibers. Anesthesiology 73: 137–145.

    Google Scholar 

  • Murphy AM (1996) Contractile protein phenotypic variation during development. Cardiovasc Res 31: E25–E33.

    Google Scholar 

  • O'Brien TX, Lee KJ and Chien KR (1993) Positional specification of ventricular myosin light chain 2 gene: nucleotide sequence of full length cDNA and expression in normal and hypertensive rat. Proc Natl Acad Sci USA 90: 5157–5160.

    Google Scholar 

  • Pope B, Hoh JF and Weeds A (1980) The ATPase activites of rat cardiac myosin isoenzymes. FEBS Lett 118: 205–208.

    Google Scholar 

  • Reiser PJ, Westfall MV, Schiaffino S and Solaro RJ (1994) Tension production and thin-filament protein isoforms in developing rat myocardium. Am J Physiol 267: H1589–H1596.

    Google Scholar 

  • Rossmanith GH, Hamilton AM and Hoh JF (1995) Influence of myosin isoforms on tension cost and crossbridge kinetics in skinned rat cardiac muscle. Clin Exp Pharmacol Physiol 22: 423–429.

    Google Scholar 

  • Saggin L, Ausoni S, Gorza L, Sartore S and Schiaffino S (1988) Troponin T switching in the developing rat heart. J Biol Chem 263: 18488–18492.

    Google Scholar 

  • Saggin L, Gorza L, Ausoni S and Schiaffino S (1989) Troponin I switching in the developing heart. J Biol Chem 264: 16299–16302.

    Google Scholar 

  • Schwartz K, Lecarpentier Y, Martin JL, Lompre AM, Mercadier JJ and Swynghedauw B (1981) Myosin isoenzymic distribution correlates with speed of myocardial contraction. J Mol Cell Cardiol 13: 1071–1075.

    Google Scholar 

  • Sieck GC, Han YS, Prakash YS and Jones KA (1998) Cross-bridge cycling kinetics, actomyosin ATPase activity and myosin heavy chain isoforms in skeletal and smooth respiratory muscles. Comp Biochem Physiol 119: 435–450.

    Google Scholar 

  • Solaro RJ (1991) Regulation of Ca2+-signaling in cardiac myofilaments. Med Sci Sports Exerc 23: 1145–1148.

    Google Scholar 

  • Solaro RJ, Kumar P, Blanchard EM and Martin AF (1986) Differential effects of pH on calcium activation of myofilaments of adult and perinatal dog hearts: evidence for developmental differences in thin filament regulation. Circ Res 58: 721–729.

    Google Scholar 

  • Solaro RJ, Lee JA, Kentish JC and Allen DG (1988) Effects of acidosis on ventricular muscle from adult and neonatal rats. Circ Res 63: 779–787.

    Google Scholar 

  • Stein RB and Gordon T (1986) Nonlinear stiffness-force relationships in whole mammalian skeletal muscles. Can J Physiol Pharmacol 64: 1236–1244.

    Google Scholar 

  • Sweeney HL, Bowman BF and Stull JT (1993) Myosin light chain phosphorylation in vertebrate striated muscle: regulation and function [Review]. Am J Physiol 264: C1085–C1095.

    Google Scholar 

  • Sweeney HL, Corteselli SA and Kushmerick MJ (1987) Measurements on permeabilized skeletal muscle fibers during continuous activation. Am J Physiol 252: C575–C580.

    Google Scholar 

  • Swynghedauw B (1999) Molecular mechanisms of myocardial remodeling. Physiol Rev 79: 216–262.

    Google Scholar 

  • VanBuren P, Harris DE, Alpert NR and Warshaw DM (1995) Cardiac V1 and V3 myosins differ in their hydrolytic and mechanical activities in vitro. Circ Res 77: 439–444.

    Google Scholar 

Download references

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Prakash, Y.S., Cody, M.J., Housmans, P.R. et al. Comparison of cross-bridge cycling kinetics in neonatal vs. adult rat ventricular muscle. J Muscle Res Cell Motil 20, 717–723 (1999). https://doi.org/10.1023/A:1005585807179

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  • DOI: https://doi.org/10.1023/A:1005585807179

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