Age-dependent Changes in Myosin Composition Correlate with Enhanced Economy of Contraction in Guinea-pig Hearts

Overview

Journal J Physiol

Specialty Physiology

Date 1998 Mar 31

PMID 9518708

Citations 21

Authors

J van der Velden

A F Moorman

G J Stienen

Affiliations

Soon will be listed here.

Abstract

1. The composition of myosin heavy chains (MHCs) was investigated in young (1- to 8-week-old) and mature (9- to 26-week-old) guinea-pigs using two monoclonal antibodies directed specifically against alpha-MHC and beta-MHC. In addition, maximum force and the rate of ATP consumption during isometric contraction were measured in chemically skinned trabeculae taken from the same hearts. 2. An age-dependent shift in the MHC composition was found. The alpha-MHC fraction decreased from 0.17 +/- 0.02 (mean +/- S.E.M.; n = 24) in young to 0.04 +/- 0.01 (n = 43) in mature hearts. This shift was correlated with a decrease in tension cost (i.e. ATP consumption per second per trabecula volume/force per cross-sectional area) from 4.1 +/- 0.2 mmol kN-1 m-1 s-1 (n = 23) in young to 2.5 +/- 0.1 mmol kN-1 m-1 s-1 (n = 57) in mature hearts. 3. From the results it follows that the slow beta-MHC isoform, which predominates in hearts of mature guinea-pigs, is about 5 times more economical than the fast alpha-MHC isoform. Calcium sensitivity of force and ATP consumption decreased with age, but stabilized within a few weeks after birth. The pronounced dependence of cardiac energetics on MHC composition should be taken into account in long-term studies of cardiac overload.

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References

Gorza L, Pauletto P, Pessina A, Sartore S, Schiaffino S . Isomyosin distribution in normal and pressure-overloaded rat ventricular myocardium. An immunohistochemical study. Circ Res. 1981; 49(4):1003-9. DOI: 10.1161/01.res.49.4.1003. View

Mercadier J, Lompre A, Wisnewsky C, Samuel J, Bercovici J, Swynghedauw B . Myosin isoenzyme changes in several models of rat cardiac hypertrophy. Circ Res. 1981; 49(2):525-32. DOI: 10.1161/01.res.49.2.525. View

Martin A, Pagani E, Solaro R . Thyroxine-induced redistribution of isoenzymes of rabbit ventricular myosin. Circ Res. 1982; 50(1):117-24. DOI: 10.1161/01.res.50.1.117. View

WATRAS J . Changes in rat cardiac myosin during development and in culture. J Mol Cell Cardiol. 1981; 13(11):1011-21. DOI: 10.1016/0022-2828(81)90476-4. View

Schwartz K, Lecarpentier Y, Martin J, Lompre A, Mercadier J, Swynghedauw B . Myosin isoenzymic distribution correlates with speed of myocardial contraction. J Mol Cell Cardiol. 1981; 13(12):1071-5. DOI: 10.1016/0022-2828(81)90297-2. View

ALPERT N, MULIERI L . Increased myothermal economy of isometric force generation in compensated cardiac hypertrophy induced by pulmonary artery constriction in the rabbit. A characterization of heat liberation in normal and hypertrophied right ventricular papillary.... Circ Res. 1982; 50(4):491-500. DOI: 10.1161/01.res.50.4.491. View

Ebrecht G, Rupp H, Jacob R . Alterations of mechanical parameters in chemically skinned preparations of rat myocardium as a function of isoenzyme pattern of myosin. Basic Res Cardiol. 1982; 77(2):220-34. DOI: 10.1007/BF01908175. View

Giulian G, Moss R, Greaser M . Improved methodology for analysis and quantitation of proteins on one-dimensional silver-stained slab gels. Anal Biochem. 1983; 129(2):277-87. DOI: 10.1016/0003-2697(83)90551-1. View

Mercadier J, Bouveret P, Gorza L, Schiaffino S, Clark W, Zak R . Myosin isoenzymes in normal and hypertrophied human ventricular myocardium. Circ Res. 1983; 53(1):52-62. DOI: 10.1161/01.res.53.1.52. View

10.

BHATNAGAR G, Walford G, Beard E, Humphreys S, Lakatta E . ATPase activity and force production in myofibrils and twitch characteristics in intact muscle from neonatal, adult, and senescent rat myocardium. J Mol Cell Cardiol. 1984; 16(3):203-18. DOI: 10.1016/s0022-2828(84)80587-8. View

11.

Hirzel H, Tuchschmid C, Schneider J, KRAYENBUEHL H, Schaub M . Relationship between myosin isoenzyme composition, hemodynamics, and myocardial structure in various forms of human cardiac hypertrophy. Circ Res. 1985; 57(5):729-40. DOI: 10.1161/01.res.57.5.729. View

12.

Swynghedauw B . Developmental and functional adaptation of contractile proteins in cardiac and skeletal muscles. Physiol Rev. 1986; 66(3):710-71. DOI: 10.1152/physrev.1986.66.3.710. View

13.

Effron M, BHATNAGAR G, Spurgeon H, Lakatta E . Changes in myosin isoenzymes, ATPase activity, and contraction duration in rat cardiac muscle with aging can be modulated by thyroxine. Circ Res. 1987; 60(2):238-45. DOI: 10.1161/01.res.60.2.238. View

14.

Leijendekker W, van Hardeveld C, Elzinga G . Heat production during contraction in skeletal muscle of hypothyroid mice. Am J Physiol. 1987; 253(2 Pt 1):E214-20. DOI: 10.1152/ajpendo.1987.253.2.E214. View

15.

Ventura-Clapier R, Mekhfi H, Oliviero P, Swynghedauw B . Pressure overload changes cardiac skinned-fiber mechanics in rats, not in guinea pigs. Am J Physiol. 1988; 254(3 Pt 2):H517-24. DOI: 10.1152/ajpheart.1988.254.3.H517. View

16.

Barsotti R, Ferenczi M . Kinetics of ATP hydrolysis and tension production in skinned cardiac muscle of the guinea pig. J Biol Chem. 1988; 263(32):16750-6. View

17.

Henkel R, Vandeberg J, Shade R, Leger J, Walsh R . Cardiac beta myosin heavy chain diversity in normal and chronically hypertensive baboons. J Clin Invest. 1989; 83(5):1487-93. PMC: 303851. DOI: 10.1172/JCI114042. View

18.

de Groot I, Lamers W, Moorman A . Isomyosin expression patterns during rat heart morphogenesis: an immunohistochemical study. Anat Rec. 1989; 224(3):365-73. DOI: 10.1002/ar.1092240305. View

19.

Morano I, Rosch J, Arner A, Ruegg J . Phosphorylation and thiophosphorylation by myosin light chain kinase: different effects on mechanical properties of chemically skinned ventricular fibers from the pig. J Mol Cell Cardiol. 1990; 22(7):805-13. DOI: 10.1016/0022-2828(90)90091-f. View

20.

ALOUSI A, Grant A, Etzler J, Cofer B, Melvin D . Reduced cardiac myofibrillar Mg-ATPase activity without changes in myosin isozymes in patients with end-stage heart failure. Mol Cell Biochem. 1990; 96(1):79-88. DOI: 10.1007/BF00228455. View