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Rigor and contracture: the role of phosphorus compounds and cytosolic Ca2+

  • G. J. M. Stienen
  • G. Elzinga
Part of the Developments in Cardiovascular Medicine book series (DICM, volume 104)

Abstract

Since in the intact myocardium the effects of ischemia lead to changes in the composition of the sarcoplasm, the sarcoplasmic factors which affect mechanical performance in ischemia cannot effectively be studied at the level of complexity found in the intact cell. Much has been learned in this respect from skinned muscle preparations, i.e. preparations where the cellular membrane is made permeable so that the ‘intracellular’ composition can be controlled by the composition of the bathing solution. These studies show that the contractile apparatus is not only sensitive to calcium, which is essential for contraction, but also to pH, inorganic phosphate, ATP, and ADP amongst others.

Phosphate and acidification have a depressive effect on force production, which is more pronounced at the calcium levels, normally found in the beating heart, which do not cause maximum force production. ADP has a potentiating effect on force but it depresses shortening velocity, probably by acting as a competitive inhibitor of ATP induced crossbridge detachment. A decrease of ATP, in the presence of calcium, increases force until a concentration of about 100 μM is reached. When ATP drops even below this level, force decreases but never disappears as rigor develops at these low levels. Shortening velocity decreases when ATP falls. The ATPase activity related to contraction varies with Ca2+ concentration in proportion to force production. It is depressed by ADP at larger concentrations, and by ATP at low concentrations.

Keywords

ATPase Activity Cardiac Muscle Force Production Myosin Head Actomyosin ATPase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Fabiato A, Fabiato F (1975a) Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol 249: 469–495PubMedGoogle Scholar
  2. 2.
    Fabiato A, Fabiato F (1975b) Effects of magnesium on contractile activation of skinned cardiac cells. J Physiol 249: 497–517PubMedGoogle Scholar
  3. 3.
    Stephenson EW (1981) Activation of fast skeletal muscle: contributions of studies on skinned fibers. Am J Physiol 240: C1–C19PubMedGoogle Scholar
  4. 4.
    Allen DG, Orchard CH (1987) Myocardial contractile function during ischemia and hypoxia. Circ Res 60: 153–168PubMedGoogle Scholar
  5. 5.
    Gibbs CL (1978) Cardiac energetics. Physiol Rev 58: 174–254PubMedGoogle Scholar
  6. 6.
    Hibberd MG, Trentham DR (1986) Relationships between chemical and mechanical events during muscular contraction. Ann Rev Biophys Biophys Chem 15: 119–161CrossRefGoogle Scholar
  7. 7.
    Woledge RC, Curtin NA, Homsher E (1985) Energetic aspects of muscle contraction. Monographs of the Physiological Society. London: Academic PressGoogle Scholar
  8. 8.
    Lymn RW, Taylor EW (1971) Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10: 4617–4624PubMedCrossRefGoogle Scholar
  9. 9.
    Taylor EW (1979) Mechanism of actomyosin ATPase and the problem of muscle contraction. CRC Crit Rev Biochem 6: 103–164PubMedCrossRefGoogle Scholar
  10. 10.
    Siemankowski RF, White HD (1984) Kinetics of the interaction between actin, ADP, and cardiac myosin-S1. J Biol Chem 259: 5045–5053PubMedGoogle Scholar
  11. 11.
    Siemankowski RF, Wisemann MO, White HD (1985) ADP dissociation from actomyosin subfragment 1 is sufficiently slow to limit the unload shortening velocity in vertebrate muscle. Proc Natl Acad Sc 82: 658–662CrossRefGoogle Scholar
  12. 12.
    Smith SJ, White HD (1985) Kinetic mechanisms of l-N6-etheno-2-aza-ATP and 1-N6-ethano-2-aza-ADP binding to bovine ventricular actomyosin-S1 and myofibrils. J Biol Chem 260: 15156–15162PubMedGoogle Scholar
  13. 13.
    Marston SB, Taylor EW (1980) Comparison of the myosin and actomyosin ATPase mechanisms of four types of vertebrate muscles. Biochim Biophys Acta 1: 573–600Google Scholar
  14. 14.
    Fenn WO (1923) A quantitative comparison between the energy liberated and the work performed by the isolated sartorius of the frog. J Physiol 58: 175–203PubMedGoogle Scholar
  15. 15.
    Yanagida T, Arata T, Oosawa F (1985) Sliding distance of actin filament induced by a myosin crossbridge during one ATP hydrolysis cycle. Nature 316: 366–369PubMedCrossRefGoogle Scholar
  16. 16.
    Goldman YE, Hibberd MG, McCray JA, Trentham DR (1982) Relaxation of muscle fibres by photolysis of caged ATP. Nature 300: 701–705PubMedCrossRefGoogle Scholar
  17. 17.
    Balaban RS, Kantor HL, Katz LA, Briggs RW (1986) Relation between work and phosphate metabolite in the in vivo paced mammalian heart. Science 232: 1121–1123PubMedCrossRefGoogle Scholar
  18. 18.
    Bittl JA, Balschi JA, Ingwall JS (1987) Contractile failure and high-energy phosphate turnover during hypoxia: 31P-NMR surface coil studies in living rat. Circ Res 60: 871–878PubMedGoogle Scholar
  19. 19.
    Blackledge MJ, Rajagopalan B, Oberhaensli RD, Bolas NM, Styles P, Radda GK (1987) Quantitative studies of human cardiac metabolism by 31P rotating-frame NMR. Proc Natl Acad Sc 84: 4283–4387CrossRefGoogle Scholar
  20. 20.
    Mattews PM, Bland JL, Gadian DG, Radda GK (1982) A 31P-NMR saturation transfer study of the regulation of creatine kinase in the rat heart. Biochim Biophys Acta 721: 312–320CrossRefGoogle Scholar
  21. 21.
    Clarke K, O’Connor AJ, Willis RJ (1987) Temporal relation between energy metabolism and myocardial function during ischemia and reperfusion. Am J Physiol 253: H412–H421PubMedGoogle Scholar
  22. 22.
    Katz LA, Swain JA, Portman MA, Balaban RS (1988) Intracellular pH and inorganic phosphate content of heart in vivo: a 31P-NMR study. Am J Physiol 255: H189–H196PubMedGoogle Scholar
  23. 23.
    Steenbergen C, Murphy E, Levy L, London RE (1987) Elevation in cytosolic free calcium concentration early in myocardial ischemia in perfused rat heart. Circ Res 60: 700–707PubMedGoogle Scholar
  24. 24.
    Fabiato A, Fabiato F (1978) Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiac and skeletal muscles. J Physiol 276: 233–255PubMedGoogle Scholar
  25. 25.
    Kentish JC, Jewell BR (1984) Some characteristics of Ca2+-regulated force production in EGTA-treated muscles from rat heart. J Gen Physiol 84: 83–99PubMedCrossRefGoogle Scholar
  26. 26.
    Godt RE, Lindley BD (1982) Influence of temperature upon contractile and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol 80: 279–297PubMedCrossRefGoogle Scholar
  27. 27.
    Fink RHA, Stephenson DG, Williams DA (1986) Potassium and ionic strength effects on isometric force of skinned twitch muscle fibres of rat and toad. J Physiol 370: 317–337PubMedGoogle Scholar
  28. 28.
    Kentish JC, ter Keurs HEDJ, Ricciardi L, Bucx JJJ, Noble MIM (1986) Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Circ Res 58: 755–768PubMedGoogle Scholar
  29. 29.
    Kentish JC (1984) The inhibitory effects of monovalent ions on force development in detergent-skinned ventricular muscle from the guinea pig. J Physiol 352: 353–374PubMedGoogle Scholar
  30. 30.
    Kentish JC (1986) The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricle. J Physiol 370: 585–604PubMedGoogle Scholar
  31. 31.
    Kentish JC (1987) The inhibitory action of acidosis and inorganic phosphate on the Ca2+-regulated force production of rat cardiac myofibrils. J Physiol 390: 59PGoogle Scholar
  32. 32.
    Brandt PW (1984) The thin filament of vertebrate skeletal muscle cooperatively activates as a unit. J Mol Biol 180: 379–384PubMedCrossRefGoogle Scholar
  33. 33.
    Babu A, Scordilis SP, Sonneblick EH, Gulati J (1989) The control of myocardial contraction with skeletal fast muscle troponin C. J Biol Chem 262,12: 5815–5822Google Scholar
  34. 34.
    Babu A, Sonnenblick E, Gulati J (1988) Molecular basis for the influence of muscle length on myocardial performance. Science 240: 74–76PubMedCrossRefGoogle Scholar
  35. 35.
    Moss RL (1986) Effects on shortening velocity of rabbit skeletal muscle due to variations in the level of thin-filament activation. J Physiol 377: 487–505PubMedGoogle Scholar
  36. 36.
    Brandt PW, Cox RN, Kawai M, Robinson T (1982) Regulation of tension in skinned muscle fibers. Effect of cross-bridge kinetics on apparent Ca2+ sensitivity. J Gen Physiol 79: 997–1016PubMedCrossRefGoogle Scholar
  37. 37.
    Julian FJ (1971) The effect of calcium on the force-velocity relation of briefly glycerinated frog muscle fibres. J Physiol 218: 117–145PubMedGoogle Scholar
  38. 38.
    Podolsky RJ, Teichholtz LE (1970) The relation between calcium and contraction kinetics in skinned muscle fibres. J Physiol 211: 19–35PubMedGoogle Scholar
  39. 39.
    Chalovich JM, Eisenberg E (1986) The effect of troponin-tropomyosin on the binding of heavy meromyosin to actin in the presence of ATP. J Biol Chem 261: 5088–5093PubMedGoogle Scholar
  40. 40.
    Gibbs CL, Loiselle D (1978) Energy output of tetanized cardiac muscle: species differences. Pflügers Arch 373: 31–38PubMedCrossRefGoogle Scholar
  41. 41.
    Cooper G (1976) The myocardial energetic active state. I. Oxygen consumption during tetanus of cat papillary muscle. Circ Res 39: 695–704PubMedGoogle Scholar
  42. 42.
    Spencer RGS, Balschi JA, Leigh Jr JS, Ingwall JS (1988) ATP synthesis and degradation rates in the perfused heart. Biophys J 54: 921–929PubMedCrossRefGoogle Scholar
  43. 43.
    Bhatnagar GM, Walford GD, Beard ES, Humphreys S, Lakatta EG (1984) ATPase activity and force production in myofibrils and twitch characteristics in intact muscle from neonatal, adult, and senescent rat myocardium. J Mol Cell Cardiol 16: 203–218PubMedCrossRefGoogle Scholar
  44. 44.
    Portzehl H, Zaolarek P, Gaudin J (1969) The activation by Ca2+ of the ATPase of extracted muscle fibrils with variation of ionic strength, pH and concentration of Mg ATP. Biochim Biophys Acta 189: 440–448PubMedCrossRefGoogle Scholar
  45. 45.
    Saeki Y, Kato C, Totsuka T, Yanagisawa K (1987) Mechanical properties and ATPase activity in glycerinated cardiac muscle of hyperthyroid rabbit. Pflügers Arch 408: 578–583PubMedCrossRefGoogle Scholar
  46. 46.
    van den Berg C, Elzinga G, Stienen GJM (1989) Relation between ATPase activity and force development in chemically skinned cardiac trabeculae of rat. J Physiol 415: 114PGoogle Scholar
  47. 47.
    Barsotti RJ, Ferenczi MA (1988) Kinetics of ATP hydrolysis and tension production in skinned cardiac muscle of the guinea pig. J Biol Chem 263,32: 16750–16756PubMedGoogle Scholar
  48. 48.
    Bremel RD, Weber A (1972) Cooperation within actin filament in vertebrate skeletal muscle. Nature (Lond) New Biol 238: 91–101CrossRefGoogle Scholar
  49. 49.
    Ferenczi MA, Simmons RM, Sleep JA (1982) General considerations of cross-bridge models in relation to the dependence on MgATP concentration of mechanical parameters of skinned fibers from frog muscle. In: Twarog BM, Levine RJC, Dewey MM (eds) Basic Research of Muscles: A Comparative Approach. New York: Raven Press, pp 91–107Google Scholar
  50. 50.
    Ferenczi MA, Goldman YE, Simmons RM (1984) The dependence of force and shortening velocity on substrate concentration in skinned muscle fibres from Rana temporaria. J Physiol 350: 519–543PubMedGoogle Scholar
  51. 51.
    Cooke R, Bialek W (1979) Contraction of glycerinated muscle fibers as a function of the ATP concentration. Biophys J 28: 241–258PubMedCrossRefGoogle Scholar
  52. 52.
    Chaen S, Kometani K, Yamada T, Shimizu H (1981) Substate-concentration dependence of tension, shortening velocity and ATPase activity of glycerinated single muscle fibers. J Biochem 90: 1611–1621PubMedGoogle Scholar
  53. 53.
    Stienen GJM, van der Laarse WJ, Elzinga G (1988) Dependency of the force velocity relationships on MgATP in different types of muscle fibers from Xenopus laevis. Biophys J 53: 849–855PubMedCrossRefGoogle Scholar
  54. 54.
    Glyn H, Sleep JA (1985) Dependence of adenosine triphosphatase activity of rabbit psoas muscle fibres and myofibrils on substrate concentration. J Physiol 365: 259–276PubMedGoogle Scholar
  55. 55.
    Rüegg JCM, Schadler GJ, Steiger, Muller G (1971) Effects of inorganic phosphate on the contractile mechanism. Pflügers Arch 325: 359–364PubMedCrossRefGoogle Scholar
  56. 56.
    Nosek TM, Fender KY, Godt RE (1987) It is the dipronated inorganic phosphate that depresses force in skinned skeletal muscle fibers. Science 236: 77–97CrossRefGoogle Scholar
  57. 57.
    Cooke R, Franks K, Luciani GB, Pate E (1988) The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J Physiol 395: 77–97PubMedGoogle Scholar
  58. 58.
    Dawson MJ, Smith S, Wilkie DR (1986) The [H2PO4 -1] may determine cross-bridge cycling rate and force reduction in fatiguing muscle. Biophys J 49: 268aGoogle Scholar
  59. 59.
    Hibberd MG, Dantzig JA, Trentham DR, Goldman YE (1985) Phosphate release and force generation in skeletal muscle fibers. Science 228: 1317–1319PubMedCrossRefGoogle Scholar
  60. 60.
    Cooke R, Pate E (1985) The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J 48: 789–798PubMedCrossRefGoogle Scholar
  61. 61.
    Elzinga G, Stienen GJM, Versteeg PGA (1989) Effect of inorganic phosphate on length responses to changes in load in skinned rabbit psoas fibres. J Physiol 415: 132PGoogle Scholar
  62. 62.
    Kawai M, Güth K, Winnekes K, Haist C, Rüegg JC (1987) The effect of inorganic phosphate on the ATP hydrolysis rate and tension development in chemically skinned rabbit psoas fibres. Pflügers Arch 408: 1–9PubMedCrossRefGoogle Scholar
  63. 63.
    Gagelman M, Güth K (1987) Effects of inorganic phosphate and Ca2+ sensitivity in skinned taenia coli smooth muscle fibers. Biophys J 51: 457–463CrossRefGoogle Scholar
  64. 64.
    Herzig JW, Peterson JW, Rüegg JC, Solaro RJ (1981) Vanadate and phosphate ions reduce tension and increase cross-bridge kinetics in chemically skinned heart muscle. Biochim Biophys Acta 672: 191–196PubMedGoogle Scholar
  65. 65.
    Chaen S, Shimada M, Sugi H (1986) Evidence for cooperative interactions of myosin heads with thin filament in the force generation of vertebrate skeletal muscle fibers. J Biol Chem 261: 13632–16636PubMedGoogle Scholar
  66. 66.
    Chase PB, Kushmerick MJ (1988) Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers. Biophys J 53: 935–946PubMedCrossRefGoogle Scholar
  67. 67.
    Hoar PE, Mahoney CW, Kerrick WGL (1987) MgADP increases maximum tension and Ca2+ sensitivity in skinned rabbit soleus fibers. Pflügers Arch 410: 30–36PubMedCrossRefGoogle Scholar
  68. 68.
    Schoenberg M, Eisenberg E (1987) ADP binding to myosin cross-bridges and its effect on the cross-bridge detachment rate constants. J Gen Physiol 89: 905–920PubMedCrossRefGoogle Scholar
  69. 69.
    Johnson RE, Adams PH (1984) ADP binds similarly to rigor muscle myofibrils and to actomyosin-subfragment one. FEBS Letters 174: 11–14PubMedCrossRefGoogle Scholar
  70. 70.
    Ventura-Clapier R, Mekhfi H, Vassort G (1987) Role of creatine kinase in force development in chemically skinned rat cardiac muscle. J Gen Physiol 89: 815–837PubMedCrossRefGoogle Scholar
  71. 71.
    Robertson SP, Kerrick WGL: The effects of pH on Ca2+-activated force in frog skeletal muscle fibers. Pflügers Arch 380: 41–45Google Scholar
  72. 72.
    Metzger JM, Moss RL (1988) Depression of Ca2+ insensitive tension due to reduced pH in partially troponin-extracted skinned skeletal muscle fibers. Biophys J 54: 1169–1173PubMedCrossRefGoogle Scholar
  73. 73.
    Metzger JM, Moss RL (1987) Greater hydrogen ion-induced depression of tension and velocity in skinned single fibres of rat fast than slow muscles. J Physiol 393: 727–742PubMedGoogle Scholar
  74. 74.
    Kammermeier H, Schmidt P, Jungling E (1982) Free energy change at ATP-hydrolysis: a causal factor of early hypoxic failure of the myocardium? J Mol and Cell Cardiol 14: 267–277CrossRefGoogle Scholar
  75. 75.
    Kammermeier H (1987) High energy phosphate of the myocardium: concentration versus free energy change. In: Jacob RHJ, Just, and Holubarsch CH (eds) Cardiac energetics. Darmstadt, Steinkopff Verlag, pp 31–36Google Scholar
  76. 76.
    Kushmerick MJ (1987) Energetics studies of muscles of different types. In: Jacob RHJ, Just, Holubarsch CH (eds) Cardiac energetics Darmstadt, Steinkopff Verlag pp 17–30Google Scholar
  77. 77.
    Dawson MJ, Gadian DG, Wilkie DR (1980) Mechanical relaxation rate and metabolism studied in fatiguing muscle by phosphorus nuclear magnetic resonance. J Physiol 299: 465–484PubMedGoogle Scholar
  78. 78.
    Eisenberg E, Hill TL, Chen Y (1980) Cross-bridge model of muscle contraction. Biophys J 29: 195–227PubMedCrossRefGoogle Scholar
  79. 79.
    Holubarsch C, Alpert NA, Goulette R, Mulieri LA (1982) Heat production during hypoxic contracture of rat myocardium. Circ Res 51: 777–786PubMedGoogle Scholar
  80. 80.
    Smith GL, Allen DG (1988) Effects of metabolic blockade on intracellular calcium concentration in isolated ferret ventricular muscle. Circ Res 62: 1223–1236PubMedGoogle Scholar
  81. 81.
    Jung DWG (1988) Dynamic properties of cross-bridges in frog skeletal muscle fibres. Thesis, AmsterdamGoogle Scholar
  82. 82.
    Goldman YE (1987) Special topic: molecular mechanism of muscle contraction. Ann Rev Physio 49: 629–654CrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1990

Authors and Affiliations

  • G. J. M. Stienen
    • 1
  • G. Elzinga
    • 1
  1. 1.The Laboratory for PhysiologyFree UniversityAmsterdamThe Netherlands

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