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Contractile and calcium regulating capacities of myocardia of different sized mammals scale with resting heart rate

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Abstract

The purpose of this study was to determine if selected biochemical parameters representing the contractile and calcium regulating systems of cardiac muscle scaled among mammals having inherently different resting heart rates (RHR). Eight mammalian species with RHR ranging from 51 to 475 beats per minute (bpm) were studied.

The oxidative capacity of the myocardium is highly correlated with the RHR. The hypothesis of the present study was that the capacities of the energy utilizing processes of contraction and calcium regulation would also be correlated to the functional demand imposed on the muscle as represented by the RHR.

Myosin (M) and myofibrillar (MF) ATPase activities, myosin isoenzyme distribution and sarcoplasmic reticulum (SR) ATPase activity were determined. Animals with RHR above 300 bpm express V1 myosin while animals with lower RHR express primarily V3. M and MF ATPase activities correlated with RHR, but the major difference in activities occurred at the ‘threshold’ RHR of about 300 bpm at which the switch from V3 to V1 appears to occur. SR ATPase activity per mg of microsomal protein was for the most part constant among different mammals, but the SR ATPase activity per g of heart tissue was significantly correlated with RHR as slower beating hearts tended to yield less SR protein per unit mass.

We conclude that both the contractile and calcium regulating systems are scaled to the functional parameter of RHR among different mammals. The contractile system uses a slow myosin ATPase isoform at low resting heart rates whereas above the postulated threshold RHR of about 300 bpm a switch in gene expression to a fast myosin ATPase isoform occurs. For the calcium regulating system, the heart does not seem to have the ‘choice’ of altering the quality of the SR ATPase isoform and thus calcium regulating capacity is set by alterations in the quantity of SR per unit of heart mass.

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References

  1. Blank S, Chen V, Hamilton N, Salerno T, Ianuzzo CD: Metabolic characteristics of mammalian myocardia. J Mol Cell Cardiol 21: 367–373, 1989

    Google Scholar 

  2. Coulson R, Hernandez T, Herbert J: Metabolic rate, enzyme kinetics in vivo. Comp Biochem Physiol 56A: 251–262, 1977

    Google Scholar 

  3. Henderson A, Craig R, Sonnenblick E, Urschel C: Species differences in intrinsic myocardial contractility. Proc Soc Exp Biol Med 134: 930–932, 1970

    Google Scholar 

  4. Holt J, Rhode E, Kines H: Ventricular volumes and body weights in mammals. Am J Physiol 215: 704–715, 1968

    Google Scholar 

  5. Hochachka PW, Emmett B, Suarez RK: Limits and constraints in the scaling of oxidative and glycolytic enzymes in homeotherms. Can J Zool 66: 1128–1138, 1988

    Google Scholar 

  6. Hoppeler H, Lindstedt SL, Claassen H, Taylor CR, Mathieu O, Weibel ER: Scaling mitochondrial volume in heart to body mass. Resp Physiol 55: 131–137, 1984

    Google Scholar 

  7. Ianuzzo CD, Blank S, Hamilton N, O'Brien P, Chen V, Brotherton S, Salerno T: The relationship of myocardial chronotropism to the biochemical capacities of mammalian hearts. In: AW Taylor, PD Gollnick, HJ Green, CD Ianuzzo, G Metivier, JR Sutton (eds.) Biochemistry of Exercise VII, International Series on Sport Sciences. Vol. 21 Human Kinetics Books, Champaign, IL, 1990

    Google Scholar 

  8. Biology Data Book, 2nd ed. Altman PL, Dittmer DS, eds. Vol. 3: 1688–1692, Bethesda, MD, 1979

  9. Canadian Council on Animal Care. Guide to the care and use of experimental animals. Vol. 1: 83–84, Ottawa, ON, 1980

  10. Baldwin KM, Cooke DA, Cheadle WG: Time course adaptations in normal and hypertrophied heart muscle. Fed Proc 41: 192–198, 1982

    Google Scholar 

  11. Solaro RJ, Pang DC, Briggs FN: Purification of cardiac myofibrils with Triton X-100. Biochim Biophys Acta 245: 259–262, 1971

    Google Scholar 

  12. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ: Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265–275, 1951

    CAS  PubMed  Google Scholar 

  13. Thomason DB, Baldwin KM, Herrick RE: Myosin isozyme distribution in rodent hindlimb skeletal muscle. J Appl Physiol 60(6): 1923–1931, 1986

    Google Scholar 

  14. Rockstein M, Herron PW: Colorimetric determination of inorganic phosphate in microgram quantities. Anal Chem 23: 1500–1501, 1951

    Google Scholar 

  15. Pagani ED, Solaro RJ: Swimming exercise, thyroid state, and the distribution of myosin isoenzymes in rat heart. Am J Physiol 245: H713-H720, 1983

    Google Scholar 

  16. Nakanishi T, Nagae M, Takao A: Developmental changes in contractile protein 5′-triphosphatase in rabbit heart. Circ Res 58: 890–895, 1982

    Google Scholar 

  17. Harigaya S, Schwartz A: Rate of calcium binding and uptake in normal animal and failing human cardiac muscle. Circ Res 25: 781–794, 1969

    Google Scholar 

  18. O'Brien PJ: Porcine malignant hyperthermia susceptibility: increased calcium sequestering activity of skeletal muscle sarcoplasmic reticulum. Can J Vet Res 50: 329–337, 1986

    Google Scholar 

  19. Laemmli UK: Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680–685, 1970

    PubMed  Google Scholar 

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

    Google Scholar 

  21. Wilson D, Nishiki K, Erecinska M: Energy metabolism in muscle and its regulation during individual contraction-relaxation cycles. TIBS 6: 16–19, 1981

    Google Scholar 

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

    Google Scholar 

  23. Barany M: ATP ase activity of myosin correlated with speed of muscle shortening. J Gen Physiol 40: 197–216, 1967

    Google Scholar 

  24. Delcayre C, Swynghedauw B: A comparative study of heart myosin. Pflugers Arch 355: 39–47, 1975

    Google Scholar 

  25. Hamrell B, Low R: The relationship of mechanical Vmax to myosin ATPase activity in rabbit and marmot ventricular muscle. Pflugers Arch 377: 119–124, 1978

    Google Scholar 

  26. Lompre AM, Mercadier J, Wesnewsky C, Bouveret P, Pantaloni C, D'Albis A, Schwartz K: Species- and age-dependent changes in relative amounts of cardiac myosin isozymes in mammals. Dev Biol 84: 286–290, 1981

    Google Scholar 

  27. Carafoli E: The homeostasis of calcium in heart cells. M Mol Cell Cardiol 17: 203–212, 1985

    Google Scholar 

  28. Rodgers R, Black S, Katz S, McNeill J: Thyroidectomy of SHR: effects on ventricular relaxation and on SR calcium uptake activity. Am J Physiol 250: H861-H865, 1986

    Google Scholar 

  29. Briggs FN, Cable MB, Geisow MG, Green NM: Primary structure of the nucleotide binding domain of the Ca, Mg-ATPase from cardiac sarcoplasmic reticulum. Biochem Biophys Res Commun 130: 732–738, 1986

    Google Scholar 

  30. Forbes M, Hawkey L, Jirge S, Sperelakis N: The sarcoplasmic reticulum of mouse heart: its divisions, configurations and distribution. J Ultrastr. Res 93: 1–16, 1985

    Google Scholar 

  31. Luff AR, Atwood HR: Changes in sarcoplasmic reticulum and transverse tubular system of fast and slow skeletal muscles of the mouse during postnatal development. J Cell Biol 51: 369–383, 1971

    Google Scholar 

  32. Lues I, Siegel R, Harting J: Effect of isomazole on the responsiveness to calcium of the contractile elements in skinned cardiac muscle fibres of various species. J Pharmacol 146: 145–153, 1988

    Google Scholar 

  33. Ruegg JC: Calcium in Muscle Activation. A Comparative Approach. Springer-Verlag, NY, 1988

    Google Scholar 

  34. Rall J: Energetic aspects of skeletal muscle contraction: implications of fiber types. Exer Sport Sci Rev 13: 33–74, 1985

    Google Scholar 

  35. Ianuzzo CD, Hamilton N, O'Brien PJ, Desrosiers C, Chiu R: Biochemical transformation of canine skeletal muscle for use in cardiac-assist devices. J Appl Physiol 68(4): 1481–1485, 1990

    Google Scholar 

  36. Alpert NR, Mulieri LA: 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 muscles. Circ Res 50: 491–500, 1982

    Google Scholar 

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Hamilton, N., Ianuzzo, C.D. Contractile and calcium regulating capacities of myocardia of different sized mammals scale with resting heart rate. Mol Cell Biochem 106, 133–141 (1991). https://doi.org/10.1007/BF00230179

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