Skip to main content
PMC home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1989 Mar 1;93(3):411–428. doi: 10.1085/jgp.93.3.411

Influence of temperature on the calcium sensitivity of the myofilaments of skinned ventricular muscle from the rabbit

PMCID: PMC2216215  PMID: 2703821

Abstract

The steady-state myofilament Ca sensitivity was determined in skinned cardiac trabeculae from the rabbit right ventricle (diameter, 0.13-0.34 mm) at 36, 29, 22, 15, 8, and 1 degree C. Muscles were stimulated to 0.5 Hz and stretched to a length at which maximum twitch tension was generated. The preparation was then skinned with 1% vol/vol Triton X- 100 in a relaxing medium (10 mM EGTA, pCa 9.0). Each preparation was exposed to a series of Ca-containing solutions (pCa 6.3-4.0) at two of the six temperatures studied (temperature was regulated to +/- 0.1 degree C). The pCa values (mean +/- SD, n = 6) corresponding to half maximal tension at 36, 29, 22, 15, 8, and 1 degree C were 5.47 +/- 0.07, 5.49 +/- 0.07, 5.34 +/- 0.05, 5.26 +/- 0.09, 4.93 +/- 0.06, and 4.73 +/- 0.04, respectively. Mean (+/- SD) maximum tension (Cmax) developed by the preparation as a percentage of that at 22 degrees C was 118 +/- 10, 108 +/- 5, 74 +/- 6, 57 +/- 7, and 29 +/- 5% at 36, 29, 15, 8, and 1 degree C, respectively. As cooling led to a shift of Ca sensitivity towards higher [Ca2+] and a reduction of Cmax, the Ca sensitivity curves over this range of temperatures do not cross over as has been described for canine Purkinje fibers (Fabiato 1985). Since tension is decreased by cooling at all levels of [Ca2+] it is unlikely that changes in myofilament Ca sensitivity play a role in the large hypothermic inotropy seen in rabbit ventricular muscle. The increase in sensitivity of the myofilaments to Ca on warming from 1 to 29 degrees C might be related to the increase in force seen on rewarming from a rapid cooling contracture in intact rabbit ventricular muscle.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. Ashley C. C., Moisescu D. G. Effect of changing the composition of the bathing solutions upon the isometric tension-pCa relationship in bundles of crustacean myofibrils. J Physiol. 1977 Sep;270(3):627–652. doi: 10.1113/jphysiol.1977.sp011972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bers D. M. A simple method for the accurate determination of free [Ca] in Ca-EGTA solutions. Am J Physiol. 1982 May;242(5):C404–C408. doi: 10.1152/ajpcell.1982.242.5.C404. [DOI] [PubMed] [Google Scholar]
  3. Bers D. M., Bridge J. H., MacLeod K. T. The mechanism of ryanodine action in rabbit ventricular muscle evaluated with Ca-selective microelectrodes and rapid cooling contractures. Can J Physiol Pharmacol. 1987 Apr;65(4):610–618. doi: 10.1139/y87-103. [DOI] [PubMed] [Google Scholar]
  4. Bers D. M. Mechanisms contributing to the cardiac inotropic effect of Na pump inhibition and reduction of extracellular Na. J Gen Physiol. 1987 Oct;90(4):479–504. doi: 10.1085/jgp.90.4.479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bers D. M., Philipson K. D., Langer G. A. Cardiac contractility and sarcolemmal calcium binding in several cardiac muscle preparations. Am J Physiol. 1981 Apr;240(4):H576–H583. doi: 10.1152/ajpheart.1981.240.4.H576. [DOI] [PubMed] [Google Scholar]
  6. Bers D. M. Ryanodine and the calcium content of cardiac SR assessed by caffeine and rapid cooling contractures. Am J Physiol. 1987 Sep;253(3 Pt 1):C408–C415. doi: 10.1152/ajpcell.1987.253.3.C408. [DOI] [PubMed] [Google Scholar]
  7. Bers D. M. SR Ca loading in cardiac muscle preparations based on rapid-cooling contractures. Am J Physiol. 1989 Jan;256(1 Pt 1):C109–C120. doi: 10.1152/ajpcell.1989.256.1.C109. [DOI] [PubMed] [Google Scholar]
  8. Bridge J. H. Relationships between the sarcoplasmic reticulum and sarcolemmal calcium transport revealed by rapidly cooling rabbit ventricular muscle. J Gen Physiol. 1986 Oct;88(4):437–473. doi: 10.1085/jgp.88.4.437. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cavalié A., McDonald T. F., Pelzer D., Trautwein W. Temperature-induced transitory and steady-state changes in the calcium current of guinea pig ventricular myocytes. Pflugers Arch. 1985 Oct;405(3):294–296. doi: 10.1007/BF00582574. [DOI] [PubMed] [Google Scholar]
  10. Chapman R. A. Sodium/calcium exchange and intracellular calcium buffering in ferret myocardium: an ion-sensitive micro-electrode study. J Physiol. 1986 Apr;373:163–179. doi: 10.1113/jphysiol.1986.sp016040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Crush K. G. Carnosine and related substances in animal tissues. Comp Biochem Physiol. 1970 May 1;34(1):3–30. doi: 10.1016/0010-406x(70)90049-6. [DOI] [PubMed] [Google Scholar]
  12. Eisner D. A., Lederer W. J. Characterization of the electrogenic sodium pump in cardiac Purkinje fibres. J Physiol. 1980 Jun;303:441–474. doi: 10.1113/jphysiol.1980.sp013298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ellis D., Thomas R. C. Direct measurement of the intracellular pH of mammalian cardiac muscle. J Physiol. 1976 Nov;262(3):755–771. doi: 10.1113/jphysiol.1976.sp011619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fabiato A., Fabiato F. Calcium-induced release of calcium from the sarcoplasmic reticulum of skinned cells from adult human, dog, cat, rabbit, rat, and frog hearts and from fetal and new-born rat ventricles. Ann N Y Acad Sci. 1978 Apr 28;307:491–522. doi: 10.1111/j.1749-6632.1978.tb41979.x. [DOI] [PubMed] [Google Scholar]
  15. Fabiato A., Fabiato F. Effects of pH on the myofilaments and the sarcoplasmic reticulum of skinned cells from cardiace and skeletal muscles. J Physiol. 1978 Mar;276:233–255. doi: 10.1113/jphysiol.1978.sp012231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Fabiato A. Myoplasmic free calcium concentration reached during the twitch of an intact isolated cardiac cell and during calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned cardiac cell from the adult rat or rabbit ventricle. J Gen Physiol. 1981 Nov;78(5):457–497. doi: 10.1085/jgp.78.5.457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Fabiato A. Time and calcium dependence of activation and inactivation of calcium-induced release of calcium from the sarcoplasmic reticulum of a skinned canine cardiac Purkinje cell. J Gen Physiol. 1985 Feb;85(2):247–289. doi: 10.1085/jgp.85.2.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ford L. E., Huxley A. F., Simmons R. M. Tension responses to sudden length change in stimulated frog muscle fibres near slack length. J Physiol. 1977 Jul;269(2):441–515. doi: 10.1113/jphysiol.1977.sp011911. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Godt R. E., Lindley B. D. Influence of temperature upon contractile activation and isometric force production in mechanically skinned muscle fibers of the frog. J Gen Physiol. 1982 Aug;80(2):279–297. doi: 10.1085/jgp.80.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Good N. E., Winget G. D., Winter W., Connolly T. N., Izawa S., Singh R. M. Hydrogen ion buffers for biological research. Biochemistry. 1966 Feb;5(2):467–477. doi: 10.1021/bi00866a011. [DOI] [PubMed] [Google Scholar]
  21. Gordon A. M., Pollack G. H. Effects of calcium on the sarcomere length-tension relation in rat cardiac muscle. Implications for the Frank-Starling mechanism. Circ Res. 1980 Oct;47(4):610–619. doi: 10.1161/01.res.47.4.610. [DOI] [PubMed] [Google Scholar]
  22. Harafuji H., Ogawa Y. Re-examination of the apparent binding constant of ethylene glycol bis(beta-aminoethyl ether)-N,N,N',N'-tetraacetic acid with calcium around neutral pH. J Biochem. 1980 May;87(5):1305–1312. doi: 10.1093/oxfordjournals.jbchem.a132868. [DOI] [PubMed] [Google Scholar]
  23. Harrison S. M., Bers D. M. The effect of temperature and ionic strength on the apparent Ca-affinity of EGTA and the analogous Ca-chelators BAPTA and dibromo-BAPTA. Biochim Biophys Acta. 1987 Aug 13;925(2):133–143. doi: 10.1016/0304-4165(87)90102-4. [DOI] [PubMed] [Google Scholar]
  24. Harrison S. M., Lamont C., Miller D. J. Hysteresis and the length dependence of calcium sensitivity in chemically skinned rat cardiac muscle. J Physiol. 1988 Jul;401:115–143. doi: 10.1113/jphysiol.1988.sp017154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Hibberd M. G., Jewell B. R. Calcium- and length-dependent force production in rat ventricular muscle. J Physiol. 1982 Aug;329:527–540. doi: 10.1113/jphysiol.1982.sp014317. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Illingworth J. A. A common source of error in pH measurements. Biochem J. 1981 Apr 1;195(1):259–262. doi: 10.1042/bj1950259. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Johnston I. A., Sidell B. D. Differences in temperature dependence of muscle contractile properties and myofibrillar ATPase activity in a cold-temperature fish. J Exp Biol. 1984 Jul;111:179–189. doi: 10.1242/jeb.111.1.179. [DOI] [PubMed] [Google Scholar]
  28. Kentish J. C. The effects of inorganic phosphate and creatine phosphate on force production in skinned muscles from rat ventricle. J Physiol. 1986 Jan;370:585–604. doi: 10.1113/jphysiol.1986.sp015952. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Kentish J. C. The inhibitory effects of monovalent ions on force development in detergent-skinned ventricular muscle from guinea-pig. J Physiol. 1984 Jul;352:353–374. doi: 10.1113/jphysiol.1984.sp015296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kentish J. C., ter Keurs H. E., Ricciardi L., Bucx J. J., Noble M. I. Comparison between the sarcomere length-force relations of intact and skinned trabeculae from rat right ventricle. Influence of calcium concentrations on these relations. Circ Res. 1986 Jun;58(6):755–768. doi: 10.1161/01.res.58.6.755. [DOI] [PubMed] [Google Scholar]
  31. Khan M. M., Martell A. E. Thermodynamic quantities associated with the interaction of adenosine triphosphate with metal ions. J Am Chem Soc. 1966 Feb 20;88(4):668–671. doi: 10.1021/ja00956a008. [DOI] [PubMed] [Google Scholar]
  32. Kuhn H. J., Güth K., Drexler B., Berberich W., Rüegg J. C. Investigation of the temperature dependence of the cross bridge parameters for attachment, force generation and detachment as deduced from mechano-chemical studies in glycerinated single fibres from the dorsal longitudinal muscle of Lethocerus maximus. Biophys Struct Mech. 1979 Dec;6(1):1–29. doi: 10.1007/BF00537592. [DOI] [PubMed] [Google Scholar]
  33. Kurihara S., Sakai T. Effects of rapid cooling on mechanical and electrical responses in ventricular muscle of guinea-pig. J Physiol. 1985 Apr;361:361–378. doi: 10.1113/jphysiol.1985.sp015650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Marini M. A., Evans W. J., Berger R. L. The determination of binding constants with a differential thermal and potentiometric titration apparatus. II. EDTA, EGTA and calcium. J Biochem Biophys Methods. 1986 Mar;12(3):135–146. doi: 10.1016/0165-022x(86)90028-x. [DOI] [PubMed] [Google Scholar]
  35. Micro-electrode measurement of the intracellular pH and buffering power of mouse soleus muscle fibres. J Physiol. 1977 Jun;267(3):791–810. doi: 10.1113/jphysiol.1977.sp011838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Miller D. J., Smith G. L. EGTA purity and the buffering of calcium ions in physiological solutions. Am J Physiol. 1984 Jan;246(1 Pt 1):C160–C166. doi: 10.1152/ajpcell.1984.246.1.C160. [DOI] [PubMed] [Google Scholar]
  37. Miller D. J., Smith G. L. The contractile behaviour of EGTA- and detergent-treated heart muscle. J Muscle Res Cell Motil. 1985 Oct;6(5):541–567. doi: 10.1007/BF00711914. [DOI] [PubMed] [Google Scholar]
  38. 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]
  39. Moisescu D. G., Thieleczek R. Calcium and strontium concentration changes within skinned muscle preparations following a change in the external bathing solution. J Physiol. 1978 Feb;275:241–262. doi: 10.1113/jphysiol.1978.sp012188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Orentlicher M., Brandt P. W., Reuben J. P. Regulation of tension in skinned muscle fibers: effect of high concentrations of Mg-ATP. Am J Physiol. 1977 Nov;233(5):C127–C134. doi: 10.1152/ajpcell.1977.233.5.C127. [DOI] [PubMed] [Google Scholar]
  41. Pagani E. D., Shemin R., Julian F. J. Tension-pCa relations of saponin-skinned rabbit and human heart muscle. J Mol Cell Cardiol. 1986 Jan;18(1):55–66. doi: 10.1016/s0022-2828(86)80982-8. [DOI] [PubMed] [Google Scholar]
  42. Phillips R. C., George P., Rutman R. J. Thermodynamic studies of the formation and ionization of the magnesium(II) complexes of ADP and ATP over the pH range 5 to 9. J Am Chem Soc. 1966 Jun 20;88(12):2631–2640. doi: 10.1021/ja00964a002. [DOI] [PubMed] [Google Scholar]
  43. Ranatunga K. W. Temperature-dependence of shortening velocity and rate of isometric tension development in rat skeletal muscle. J Physiol. 1982 Aug;329:465–483. doi: 10.1113/jphysiol.1982.sp014314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Saborowski F., Lang D., Albers C. Intracellular pH and buffer curves of cardiac muscle in rats as affected by temperature. Respir Physiol. 1973 Jul;18(2):161–170. doi: 10.1016/0034-5687(73)90046-7. [DOI] [PubMed] [Google Scholar]
  45. Saks V. A., Chernousova G. B., Vetter R., Smirnov V. N., Chazov E. I. Kinetic properties and the functional role of particulate MM-isoenzyme of creatine phosphokinase bound to heart muscle myofibrils. FEBS Lett. 1976 Mar 1;62(3):293–296. doi: 10.1016/0014-5793(76)80078-6. [DOI] [PubMed] [Google Scholar]
  46. Shattock M. J., Bers D. M. Inotropic response to hypothermia and the temperature-dependence of ryanodine action in isolated rabbit and rat ventricular muscle: implications for excitation-contraction coupling. Circ Res. 1987 Dec;61(6):761–771. doi: 10.1161/01.res.61.6.761. [DOI] [PubMed] [Google Scholar]
  47. Shiner J. S., Solaro R. J. The hill coefficient for the Ca2+-activation of striated muscle contraction. Biophys J. 1984 Oct;46(4):541–543. doi: 10.1016/S0006-3495(84)84051-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Smith G. L., Miller D. J. Potentiometric measurements of stoichiometric and apparent affinity constants of EGTA for protons and divalent ions including calcium. Biochim Biophys Acta. 1985 May 8;839(3):287–299. doi: 10.1016/0304-4165(85)90011-x. [DOI] [PubMed] [Google Scholar]
  49. Sonnenblick E. H., Skelton C. L. Reconsideration of the ultrastructural basis of cardiac length-tension relations. Circ Res. 1974 Oct;35(4):517–526. doi: 10.1161/01.res.35.4.517. [DOI] [PubMed] [Google Scholar]
  50. Stephenson D. G., Williams D. A. Calcium-activated force responses in fast- and slow-twitch skinned muscle fibres of the rat at different temperatures. J Physiol. 1981 Aug;317:281–302. doi: 10.1113/jphysiol.1981.sp013825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Stephenson D. G., Williams D. A. Temperature-dependent calcium sensitivity changes in skinned muscle fibres of rat and toad. J Physiol. 1985 Mar;360:1–12. doi: 10.1113/jphysiol.1985.sp015600. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Yue D. T., Marban E., Wier W. G. Relationship between force and intracellular [Ca2+] in tetanized mammalian heart muscle. J Gen Physiol. 1986 Feb;87(2):223–242. doi: 10.1085/jgp.87.2.223. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES