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. 1988 Feb;53(2):127–135. doi: 10.1016/S0006-3495(88)83074-1

The dependence of isometric tension, isometric ATPase activity, and shortening velocity of limulus muscle on the MgATP concentration.

S Pferrer 1, R Kulik 1, T Hiller 1, H J Kuhn 1
PMCID: PMC1330133  PMID: 2964257

Abstract

The dependence of the isometric tension, the velocity of unloaded shortening, and the steady-state rate of MgATP hydrolysis on the MgATP concentration (range 0.01-5 mM MgATP) was studied in Ca-activated skinned Limulus muscle fibers. With increasing MgATP concentration the isometric tension increased to a peak at approximately 0.1 mM, and slightly decreased in the range up to 5 mM MgATP. The velocity of unloaded shortening depended on the MgATP concentration roughly according to the Michaelis-Menten law of saturation kinetics with a Michaelis-Menten constant Kv = 95 microM and a maximum shortening velocity of 0.07 muscle lengths s-1; the detachment rate of the cross-bridges during unloaded shortening was 24 s-1. The rate of MgATP splitting also depended hyperbolically on the MgATP concentration with a Michaelis-Menten constant Ka = 129 microM and a maximum turnover frequency of 0.5-1 s-1. The results are discussed in terms of a cross-bridge model based on a biochemical scheme of ATP hydrolysis by actin and myosin in solution.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Best P. M., Donaldson S. K., Kerrick W. G. Tension in mechanically disrupted mammalian cardiac cells: effects of magnesium adenosine triphosphate. J Physiol. 1977 Feb;265(1):1–17. doi: 10.1113/jphysiol.1977.sp011702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Brenner B. 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. 1986;81 (Suppl 1):1–15. doi: 10.1007/978-3-662-11374-5_1. [DOI] [PubMed] [Google Scholar]
  3. Bárány M. ATPase activity of myosin correlated with speed of muscle shortening. J Gen Physiol. 1967 Jul;50(6 Suppl):197–218. doi: 10.1085/jgp.50.6.197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cooke R., Bialek W. Contraction of glycerinated muscle fibers as a function of the ATP concentration. Biophys J. 1979 Nov;28(2):241–258. doi: 10.1016/S0006-3495(79)85174-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cox R. N., Kawai M. Alternate energy transduction routes in chemically skinned rabbit psoas muscle fibres: a further study of the effect of MgATP over a wide concentration range. J Muscle Res Cell Motil. 1981 Jun;2(2):203–214. doi: 10.1007/BF00711870. [DOI] [PubMed] [Google Scholar]
  6. Dewey M. M., Colflesh D., Brink P., Fan S., Gaylinn B., Gural N. Structural, functional, and chemical changes in the contractile apparatus of Limulus striated muscle as a function of sarcomere shortening and tension development. Soc Gen Physiol Ser. 1982;37:53–72. [PubMed] [Google Scholar]
  7. Edman K. A. The velocity of unloaded shortening and its relation to sarcomere length and isometric force in vertebrate muscle fibres. J Physiol. 1979 Jun;291:143–159. doi: 10.1113/jphysiol.1979.sp012804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eisenberg E., Greene L. E. The relation of muscle biochemistry to muscle physiology. Annu Rev Physiol. 1980;42:293–309. doi: 10.1146/annurev.ph.42.030180.001453. [DOI] [PubMed] [Google Scholar]
  9. Ferenczi M. A., Goldman Y. E., Simmons R. M. The dependence of force and shortening velocity on substrate concentration in skinned muscle fibres from Rana temporaria. J Physiol. 1984 May;350:519–543. doi: 10.1113/jphysiol.1984.sp015216. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ferenczi M. A., Homsher E., Simmons R. M., Trentham D. R. Reaction mechanism of the magnesium ion-dependent adenosine triphosphatase of frog muscle myosin and subfragment 1. Biochem J. 1978 Apr 1;171(1):165–175. doi: 10.1042/bj1710165. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ferenczi M. A., Homsher E., Trentham D. R., Weeds A. G. Preparation and characterization of frog muscle myosin subfragment 1 and actin. Biochem J. 1978 Apr 1;171(1):155–163. doi: 10.1042/bj1710155. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ferenczi M. A., Simmons R. M., Sleep J. A. General considerations of cross-bridge models in relation to the dependence on MgATP concentration of mechanical parameters of skinned fibers from frog muscles. Soc Gen Physiol Ser. 1982;37:91–107. [PubMed] [Google Scholar]
  13. Gagelmann M., Güth K. Force generated by non-cycling crossbridges at low ionic strength in skinned smooth muscle from Taenia coli. Pflugers Arch. 1985 Feb;403(2):210–214. doi: 10.1007/BF00584102. [DOI] [PubMed] [Google Scholar]
  14. Geeves M. A., Goody R. S., Gutfreund H. Kinetics of acto-S1 interaction as a guide to a model for the crossbridge cycle. J Muscle Res Cell Motil. 1984 Aug;5(4):351–361. doi: 10.1007/BF00818255. [DOI] [PubMed] [Google Scholar]
  15. Glyn H., Sleep J. Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibres and myofibrils on substrate concentration. J Physiol. 1985 Aug;365:259–276. doi: 10.1113/jphysiol.1985.sp015770. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Goldman Y. E., Hibberd M. G., McCray J. A., Trentham D. R. Relaxation of muscle fibres by photolysis of caged ATP. Nature. 1982 Dec 23;300(5894):701–705. doi: 10.1038/300701a0. [DOI] [PubMed] [Google Scholar]
  17. Güth K., Kuhn H. J., Drexler B., Berberich W., Rüegg J. C. Stiffness and tension during and after sudden length changes of glycerinated single insect fibrillar muscle fibres. Biophys Struct Mech. 1979 Aug;5(4):255–276. doi: 10.1007/BF02426662. [DOI] [PubMed] [Google Scholar]
  18. HUXLEY A. F. Muscle structure and theories of contraction. Prog Biophys Biophys Chem. 1957;7:255–318. [PubMed] [Google Scholar]
  19. Harrington W. F. A mechanochemical mechanism for muscle contraction. Proc Natl Acad Sci U S A. 1971 Mar;68(3):685–689. doi: 10.1073/pnas.68.3.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Huxley A. F., Simmons R. M. Proposed mechanism of force generation in striated muscle. Nature. 1971 Oct 22;233(5321):533–538. doi: 10.1038/233533a0. [DOI] [PubMed] [Google Scholar]
  21. Julian F. J., Rome L. C., Stephenson D. G., Striz S. The maximum speed of shortening in living and skinned frog muscle fibres. J Physiol. 1986 Jan;370:181–199. doi: 10.1113/jphysiol.1986.sp015929. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Julian F. J. The effect of calcium on the force-velocity relation of briefly glycerinated frog muscle fibres. J Physiol. 1971 Oct;218(1):117–145. doi: 10.1113/jphysiol.1971.sp009607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Kawai M. Head rotation or dissociation? A study of exponential rate processes in chemically skinned rabbit muscle fibers when MgATP concentration is changed. Biophys J. 1978 Apr;22(1):97–103. doi: 10.1016/S0006-3495(78)85473-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Kuhn H. J., Bletz C., Güth K., Rüegg J. C. The effect of MgATP on forming and breaking actin-myosin linkages in contracted skinned insect flight muscle fibres. J Muscle Res Cell Motil. 1985 Feb;6(1):5–27. doi: 10.1007/BF00712308. [DOI] [PubMed] [Google Scholar]
  25. Lehman W., Szent-Györgyi A. G. Regulation of muscular contraction. Distribution of actin control and myosin control in the animal kingdom. J Gen Physiol. 1975 Jul;66(1):1–30. doi: 10.1085/jgp.66.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Marston S. B., Taylor E. W. Comparison of the myosin and actomyosin ATPase mechanisms of the four types of vertebrate muscles. J Mol Biol. 1980 Jun 5;139(4):573–600. doi: 10.1016/0022-2836(80)90050-9. [DOI] [PubMed] [Google Scholar]
  27. Maughan D. W., Godt R. E. Stretch and radial compression studies on relaxed skinned muscle fibers of the frog. Biophys J. 1979 Dec;28(3):391–402. doi: 10.1016/S0006-3495(79)85188-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Siemankowski R. F., White H. D. Kinetics of the interaction between actin, ADP, and cardiac myosin-S1. J Biol Chem. 1984 Apr 25;259(8):5045–5053. [PubMed] [Google Scholar]
  29. Taylor E. W. Mechanism of actomyosin ATPase and the problem of muscle contraction. CRC Crit Rev Biochem. 1979;6(2):103–164. doi: 10.3109/10409237909102562. [DOI] [PubMed] [Google Scholar]
  30. Walcott B., Dewey M. M. Length-tension relation in Limulus striated muscle. J Cell Biol. 1980 Oct;87(1):204–208. doi: 10.1083/jcb.87.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wilson M. G., White D. C. The role of magnesium adenosine triphosphate in the contractile kinetics of insect fibrillar flight muscle. J Muscle Res Cell Motil. 1983 Jun;4(3):283–306. doi: 10.1007/BF00711997. [DOI] [PubMed] [Google Scholar]
  32. Wray J. S., Vibert P. J., Cohen C. Cross-bridge arrangements in Limulus muscle. J Mol Biol. 1974 Sep 15;88(2):343–348. doi: 10.1016/0022-2836(74)90486-0. [DOI] [PubMed] [Google Scholar]

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