Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles (original) (raw)

Abstract

1. The effects of decreasing pH from 7.40 to 6.20 on the tension developed by direct activation of the myofilaments and by Ca2+ release from the sarcoplasmic reticulum were studied comparatively in segments of single cells of skeletal muscle (frog semitendinosus) and cardiac muscle (rat ventricle) from which the sarcolemma had been removed by micro-dissection (skinned muscle cells). 2. The concentration of free Ca2+ in the solutions was buffered with ethylene glycol-bis (beta-aminoethylether N,N'-tetraacetic acid (EGTA). The change of the buffer capacity of a given [total EGTA] caused by varying pH and the uncertainty about the value of the equilibrium constant for Ca-EGTA have been taken into account in the interpretation of the results. 3. Decreasing pH from 7.40 to 6.20 produced an increase in the [free Ca2+] required for the myofilaments to develop 50% of the maximum tension by a factor of about 5 in skinned cardiac cells but of only 3 in skeletal muscle fibres. In addition, acidosis depressed the maximum tension developed in the presence of a saturating [free Ca2+] by approximately the same amount in the two tissues. 4. The pH optimum for loading the sarcoplasmic reticulum of skinned fibres from skeletal muscle decreased when the pCa (-log [free Ca2+]) in the loading solution decreased. The optimum was pH 7.40-7.00 for a loading at pCa 7.75, pH 7.00-6.60 at pCa 7.00 and pH 6.60-6.20 at pCa 6.00. 5. The pH optimum for loading the sarcoplasmic reticulum of skinned cardiac cells with a solution at pCa 7.75 was about pH 7.40 as in skeletal muscle fibres. But the cardiac sarcoplasmic reticulum could not be loaded with a [free Ca2+] much higher than pCa 7.75 because a higher [free Ca2+] triggered a Ca2+-induced release of Ca2+ from the sarcoplasmic reticulum. 6. The pH optimum of about 7.40 for the loading of the cardiac sarcoplasmic reticulum was also optimum for the Ca2+-induced release of Ca2+ from it. 7. It was concluded that the effects of acidosis on the cardiac sarcoplasmic reticulum accentuate the depressive action of decreasing pH on the myofilaments. This may explain the pronounced depression of contractility observed during acidosis in cardiac muscle. In contrast, a moderate acidosis causes an effect on skeletal muscle sarcoplasmic reticulum that could compensate for the depressive action on the myofilaments, which is, in addition, less pronounced than in cardiac muscle.

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Selected References

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  1. Abbott R. H. The effects of fibre length and calcium ion concentration on the dynamic response of glycerol extracted insect fibrillar muscle. J Physiol. 1973 Jun;231(2):195–208. doi: 10.1113/jphysiol.1973.sp010228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allen D. G., Blinks J. R., Prendergast F. G. Aequorin luminescence: relation of light emission to calcium concentration--a calcium-independent component. Science. 1977 Mar 11;195(4282):996–998. doi: 10.1126/science.841325. [DOI] [PubMed] [Google Scholar]
  3. Ashley C. C., Moisescu D. G. Proceedings: The influence of Mg2+ concentration and of pH upon the relationship between steady-state isometric tension and Ca2+ concentration in isolated bundles of barnacle myofibrils. J Physiol. 1974 Jun;239(2):112P–114P. [PubMed] [Google Scholar]
  4. Bailin G. Evidence for a role for cardiac myosin in regulating the contractile response. Arch Biochem Biophys. 1975 Nov;171(1):206–213. doi: 10.1016/0003-9861(75)90025-9. [DOI] [PubMed] [Google Scholar]
  5. Botts J., Chashin A., Schmidt L. Computation of metal binding in bi-metal--bi-chelate systems. Biochemistry. 1966 Apr;5(4):1360–1364. doi: 10.1021/bi00868a032. [DOI] [PubMed] [Google Scholar]
  6. Bozler E. Control of the contractile mechanism of smooth and cardiac muscle. Am J Physiol. 1968 Aug;215(2):509–512. doi: 10.1152/ajplegacy.1968.215.2.509. [DOI] [PubMed] [Google Scholar]
  7. Briggs F. N., Fleishman M. Calcium binding by particle-free supernatants of homogenates of skeletal muscle. J Gen Physiol. 1965 Sep;49(1):131–149. [PMC free article] [PubMed] [Google Scholar]
  8. Chesnais J. M., Coraboeuf E., Sauviat M. P., Vassas J. M. Sensitivity to H, Li and Mg ions of the slow inward sodium current in frog atrial fibres. J Mol Cell Cardiol. 1975 Sep;7(9):627–642. doi: 10.1016/0022-2828(75)90140-6. [DOI] [PubMed] [Google Scholar]
  9. Clancy R. L., Brown E. B., Jr In vivo CO-2 buffer curves of skeletal and cardiac muscle. Am J Physiol. 1966 Dec;211(6):1309–1312. doi: 10.1152/ajplegacy.1966.211.6.1309. [DOI] [PubMed] [Google Scholar]
  10. Dipolo R., Requena J., Brinley F. J., Jr, Mullins L. J., Scarpa A., Tiffert T. Ionized calcium concentrations in squid axons. J Gen Physiol. 1976 Apr;67(4):433–467. doi: 10.1085/jgp.67.4.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Duggan P. F., Martonosi A. Sarcoplasmic reticulum. IX. The permeability of sarcoplasmic reticulum membranes. J Gen Physiol. 1970 Aug;56(2):147–167. doi: 10.1085/jgp.56.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Endo M. Calcium release from the sarcoplasmic reticulum. Physiol Rev. 1977 Jan;57(1):71–108. doi: 10.1152/physrev.1977.57.1.71. [DOI] [PubMed] [Google Scholar]
  13. Fabiato A., Fabiato F. Calcium release from the sarcoplasmic reticulum. Circ Res. 1977 Feb;40(2):119–129. doi: 10.1161/01.res.40.2.119. [DOI] [PubMed] [Google Scholar]
  14. Fabiato A., Fabiato F. Contractions induced by a calcium-triggered release of calcium from the sarcoplasmic reticulum of single skinned cardiac cells. J Physiol. 1975 Aug;249(3):469–495. doi: 10.1113/jphysiol.1975.sp011026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Fabiato A., Fabiato F. Effects of magnesium on contractile activation of skinned cardiac cells. J Physiol. 1975 Aug;249(3):497–517. doi: 10.1113/jphysiol.1975.sp011027. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fuchs F., Reddy Y., Briggs F. N. The interaction of cations with the calcium-binding site of troponin. Biochim Biophys Acta. 1970 Nov 17;221(2):407–409. doi: 10.1016/0005-2795(70)90290-4. [DOI] [PubMed] [Google Scholar]
  17. Gaskell W. H. On the Tonicity of the Heart and Blood Vessels. J Physiol. 1880 Aug;3(1):48–92.16. doi: 10.1113/jphysiol.1880.sp000083. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Godt R. E. Calcium-activated tension of skinned muscle fibers of the frog. Dependence on magnesium adenosine triphosphate concentration. J Gen Physiol. 1974 Jun;63(6):722–739. doi: 10.1085/jgp.63.6.722. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Katz A. M., Hecht H. H. Editorial: the early "pump" failure of the ischemic heart. Am J Med. 1969 Oct;47(4):497–502. doi: 10.1016/0002-9343(69)90180-6. [DOI] [PubMed] [Google Scholar]
  20. Kentish J., Nayler W. G. Effect of pH on the Ca2+-dependent ATPase of rabbit cardiac and white skeletal myofibrils [proceedings]. J Physiol. 1977 Feb;265(1):18P–19P. [PubMed] [Google Scholar]
  21. Kohlhardt M., Haap K., Figulla H. R. Influence of low extracellular pH upon the Ca inward current and isometric contractile force in mammalian ventricular myocardium. Pflugers Arch. 1976 Oct 15;366(1):31–38. doi: 10.1007/BF02486557. [DOI] [PubMed] [Google Scholar]
  22. Moisescu D. G. Kinetics of reaction in calcium-activated skinned muscle fibres. Nature. 1976 Aug 12;262(5569):610–613. doi: 10.1038/262610a0. [DOI] [PubMed] [Google Scholar]
  23. NANNINGA L. B. The association constant of the complexes of adenosine triphosphate with magnesium, calcium, strontium, and barium ions. Biochim Biophys Acta. 1961 Dec 9;54:330–338. doi: 10.1016/0006-3002(61)90373-0. [DOI] [PubMed] [Google Scholar]
  24. Nakamaru Y., Schwartz A. Possible control of intracellular calcium metabolism by [H+]: sarcoplasmic reticulum of skeletal and cardiac muscle. Biochem Biophys Res Commun. 1970 Nov 25;41(4):830–836. doi: 10.1016/0006-291x(70)90157-9. [DOI] [PubMed] [Google Scholar]
  25. Nakamaru Y., Schwartz A. The influence of hydrogen ion concentration on calcium binding and release by skeletal muscle sarcoplasmic reticulum. J Gen Physiol. 1972 Jan;59(1):22–32. doi: 10.1085/jgp.59.1.22. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ogawa Y. The apparent binding constant of glycoletherdiaminetetraacetic acid for calcium at neutral pH. J Biochem. 1968 Aug;64(2):255–257. doi: 10.1093/oxfordjournals.jbchem.a128887. [DOI] [PubMed] [Google Scholar]
  27. Pannier J. L., Leusen I. Contraction characteristics of papillary muscle during changes in acid-base composition of the bathing-fluid. Arch Int Physiol Biochim. 1968 Sep;76(4):624–634. doi: 10.3109/13813456809058730. [DOI] [PubMed] [Google Scholar]
  28. Pannier J. L., Weyne J., Leusen I. Effects of PCO2, bicarbonate and lactate on the isometric contractions of isolated soleus muscle of the rat. Pflugers Arch. 1970;320(2):120–132. doi: 10.1007/BF00588547. [DOI] [PubMed] [Google Scholar]
  29. Poole-Wilson P. A., Langer G. A. Effect of pH on ionic exchange and function in rat and rabbit myocardium. Am J Physiol. 1975 Sep;229(3):570–581. doi: 10.1152/ajplegacy.1975.229.3.570. [DOI] [PubMed] [Google Scholar]
  30. Portzehl H., Zaoralek P., Gaudin J. The activation by Ca2+ of the ATPase of extracted muscle fibrilsith variation of ionic strength, pH and concentration of MgATP. Biochim Biophys Acta. 1969;189(3):440–448. doi: 10.1016/0005-2728(69)90175-3. [DOI] [PubMed] [Google Scholar]
  31. Scarpa A., Azzi A. Cation binding to submitochondrial particles. Biochim Biophys Acta. 1968 Apr 29;150(3):473–481. doi: 10.1016/0005-2736(68)90147-8. [DOI] [PubMed] [Google Scholar]
  32. Schädler M. Proportional Aktivierung von ATPase-Aktivität und Kontraktionsspannung durch Calciumionen in isolierten contractilen Strukturen verschiedener Muskelarten. Pflugers Arch Gesamte Physiol Menschen Tiere. 1967;296(1):70–90. [PubMed] [Google Scholar]
  33. Shigekawa M., Finegan J. A., Katz A. M. Calcium transport ATPase of canine cardiac sarcoplasmic reticulum. A comparison with that of rabbit fast skeletal muscle sarcoplasmic reticulum. J Biol Chem. 1976 Nov 25;251(22):6894–6900. [PubMed] [Google Scholar]
  34. Tyberg J. V., Yeatman L. A., Parmley W. W., Urschel C. W., Sonnenblick E. H. Effects of hypoxia on mechanics of cardiac contraction. Am J Physiol. 1970 Jun;218(6):1780–1788. doi: 10.1152/ajplegacy.1970.218.6.1780. [DOI] [PubMed] [Google Scholar]
  35. Waddell W. J., Bates R. G. Intracellular pH. Physiol Rev. 1969 Apr;49(2):285–329. doi: 10.1152/physrev.1969.49.2.285. [DOI] [PubMed] [Google Scholar]
  36. Weisfeldt M. L., Armstrong P., Scully H. E., Sanders C. A., Daggett W. M. Incomplete relaxation between beats after myocardial hypoxia and ischemia. J Clin Invest. 1974 Jun;53(6):1626–1636. doi: 10.1172/JCI107713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Williams G. J., Collins S., Muir J. R., Stephens M. R. Observations on the interaction of calcium and hydrogen ions on ATP hydrolysis by the contractile elements of cardiac muscle. Recent Adv Stud Cardiac Struct Metab. 1975;5:273–280. [PubMed] [Google Scholar]