Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 1995 Dec;69(6):2580–2589. doi: 10.1016/S0006-3495(95)80129-3

Influence of inorganic phosphate and pH on ATP utilization in fast and slow skeletal muscle fibers.

E J Potma 1, I A van Graas 1, G J Stienen 1
PMCID: PMC1236496  PMID: 8599665

Abstract

The influence of P(i) and pH was studied on myofibrillar ATP turnover and force development during maximally activated isometric contractions, in skinned single fibers from rabbit soleus and psoas muscle. ATP hydrolysis was coupled to the breakdown of NADH, which was monitored photometrically at 340 nm. In psoas the depression by phosphate of force is twice that of ATP turnover, but in soleus force and ATP turnover are depressed equally by P(i). Most, but not all, of the ATPase and force values observed for a combination of high P(i) and low pH could be explained by independent effects of P(i) and pH. The effects of P(i) and pH on ATP turnover can be understood by a three-state cross-bridge scheme. Mass action of phosphate on the reaction from the actomyosin(AM).ADP state to the AM.ADP.P(i) state may largely account for the phosphate dependencies of ATPase activity found. Protons affect cross-bridge detachment from the AM.ADP state and the rate of the AM.ADP.P(i)-to-AM.ADP transition. In this scheme, the effects of P(i) and pH on cross-bridge kinetics appeared to be largely independent.

Full text

PDF
2583

Selected References

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

  1. Altringham J. D., Johnston I. A. Effects of phosphate on the contractile properties of fast and slow muscle fibres from an Antarctic fish. J Physiol. 1985 Nov;368:491–500. doi: 10.1113/jphysiol.1985.sp015871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barclay C. J., Constable J. K., Gibbs C. L. Energetics of fast- and slow-twitch muscles of the mouse. J Physiol. 1993 Dec;472:61–80. doi: 10.1113/jphysiol.1993.sp019937. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bowater R., Sleep J. Demembranated muscle fibers catalyze a more rapid exchange between phosphate and adenosine triphosphate than actomyosin subfragment 1. Biochemistry. 1988 Jul 12;27(14):5314–5323. doi: 10.1021/bi00414a055. [DOI] [PubMed] [Google Scholar]
  4. Brandt P. W., Cox R. N., Kawai M., Robinson T. Effect of cross-bridge kinetics on apparent Ca2+ sensitivity. J Gen Physiol. 1982 Jun;79(6):997–1016. doi: 10.1085/jgp.79.6.997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Chase P. B., Kushmerick M. J. Effects of pH on contraction of rabbit fast and slow skeletal muscle fibers. Biophys J. 1988 Jun;53(6):935–946. doi: 10.1016/S0006-3495(88)83174-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cooke R., Franks K., Luciani G. B., Pate E. The inhibition of rabbit skeletal muscle contraction by hydrogen ions and phosphate. J Physiol. 1988 Jan;395:77–97. doi: 10.1113/jphysiol.1988.sp016909. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cooke R., Pate E. The effects of ADP and phosphate on the contraction of muscle fibers. Biophys J. 1985 Nov;48(5):789–798. doi: 10.1016/S0006-3495(85)83837-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Crow M. T., Kushmerick M. J. Chemical energetics of slow- and fast-twitch muscles of the mouse. J Gen Physiol. 1982 Jan;79(1):147–166. doi: 10.1085/jgp.79.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dantzig J. A., Goldman Y. E., Millar N. C., Lacktis J., Homsher E. Reversal of the cross-bridge force-generating transition by photogeneration of phosphate in rabbit psoas muscle fibres. J Physiol. 1992;451:247–278. doi: 10.1113/jphysiol.1992.sp019163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Dawson M. J., Gadian D. G., Wilkie D. R. Muscular fatigue investigated by phosphorus nuclear magnetic resonance. Nature. 1978 Aug 31;274(5674):861–866. doi: 10.1038/274861a0. [DOI] [PubMed] [Google Scholar]
  11. Ebus J. P., Stienen G. J., Elzinga G. Influence of phosphate and pH on myofibrillar ATPase activity and force in skinned cardiac trabeculae from rat. J Physiol. 1994 May 1;476(3):501–516. doi: 10.1113/jphysiol.1994.sp020150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Edman K. A., Mattiazzi A. R. Effects of fatigue and altered pH on isometric force and velocity of shortening at zero load in frog muscle fibres. J Muscle Res Cell Motil. 1981 Sep;2(3):321–334. doi: 10.1007/BF00713270. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Fryer M. W., Owen V. J., Lamb G. D., Stephenson D. G. Effects of creatine phosphate and P(i) on Ca2+ movements and tension development in rat skinned skeletal muscle fibres. J Physiol. 1995 Jan 1;482(Pt 1):123–140. doi: 10.1113/jphysiol.1995.sp020504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gibbs C. L., Gibson W. R. Energy production of rat soleus muscle. Am J Physiol. 1972 Oct;223(4):864–871. doi: 10.1152/ajplegacy.1972.223.4.864. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. Goldman Y. E., Hibberd M. G., Trentham D. R. Relaxation of rabbit psoas muscle fibres from rigor by photochemical generation of adenosine-5'-triphosphate. J Physiol. 1984 Sep;354:577–604. doi: 10.1113/jphysiol.1984.sp015394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Goldman Y. E., Simmons R. M. Control of sarcomere length in skinned muscle fibres of Rana temporaria during mechanical transients. J Physiol. 1984 May;350:497–518. doi: 10.1113/jphysiol.1984.sp015215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hibberd M. G., Dantzig J. A., Trentham D. R., Goldman Y. E. Phosphate release and force generation in skeletal muscle fibers. Science. 1985 Jun 14;228(4705):1317–1319. doi: 10.1126/science.3159090. [DOI] [PubMed] [Google Scholar]
  20. 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]
  21. Iwamoto H. Strain sensitivity and turnover rate of low force cross-bridges in contracting skeletal muscle fibers in the presence of phosphate. Biophys J. 1995 Jan;68(1):243–250. doi: 10.1016/S0006-3495(95)80180-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kawai M., Güth K., Winnikes K., Haist C., Rüegg J. C. The effect of inorganic phosphate on the ATP hydrolysis rate and the tension transients in chemically skinned rabbit psoas fibers. Pflugers Arch. 1987 Jan;408(1):1–9. doi: 10.1007/BF00581833. [DOI] [PubMed] [Google Scholar]
  23. Martyn D. A., Gordon A. M. Force and stiffness in glycerinated rabbit psoas fibers. Effects of calcium and elevated phosphate. J Gen Physiol. 1992 May;99(5):795–816. doi: 10.1085/jgp.99.5.795. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Metzger J. M., Moss R. L. Effects of tension and stiffness due to reduced pH in mammalian fast- and slow-twitch skinned skeletal muscle fibres. J Physiol. 1990 Sep;428:737–750. doi: 10.1113/jphysiol.1990.sp018238. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Metzger J. M., Moss R. L. pH modulation of the kinetics of a Ca2(+)-sensitive cross-bridge state transition in mammalian single skeletal muscle fibres. J Physiol. 1990 Sep;428:751–764. doi: 10.1113/jphysiol.1990.sp018239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Millar N. C., Homsher E. Kinetics of force generation and phosphate release in skinned rabbit soleus muscle fibers. Am J Physiol. 1992 May;262(5 Pt 1):C1239–C1245. doi: 10.1152/ajpcell.1992.262.5.C1239. [DOI] [PubMed] [Google Scholar]
  27. Millar N. C., Homsher E. The effect of phosphate and calcium on force generation in glycerinated rabbit skeletal muscle fibers. A steady-state and transient kinetic study. J Biol Chem. 1990 Nov 25;265(33):20234–20240. [PubMed] [Google Scholar]
  28. Nagesser A. S., van der Laarse W. J., Elzinga G. Metabolic changes with fatigue in different types of single muscle fibres of Xenopus laevis. J Physiol. 1992 Mar;448:511–523. doi: 10.1113/jphysiol.1992.sp019054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Nosek T. M., Fender K. Y., Godt R. E. It is diprotonated inorganic phosphate that depresses force in skinned skeletal muscle fibers. Science. 1987 Apr 10;236(4798):191–193. doi: 10.1126/science.3563496. [DOI] [PubMed] [Google Scholar]
  30. Nosek T. M., Leal-Cardoso J. H., McLaughlin M., Godt R. E. Inhibitory influence of phosphate and arsenate on contraction of skinned skeletal and cardiac muscle. Am J Physiol. 1990 Dec;259(6 Pt 1):C933–C939. doi: 10.1152/ajpcell.1990.259.6.C933. [DOI] [PubMed] [Google Scholar]
  31. Pate E., Cooke R. A model of crossbridge action: the effects of ATP, ADP and Pi. J Muscle Res Cell Motil. 1989 Jun;10(3):181–196. doi: 10.1007/BF01739809. [DOI] [PubMed] [Google Scholar]
  32. Pate E., Cooke R. Addition of phosphate to active muscle fibers probes actomyosin states within the powerstroke. Pflugers Arch. 1989 May;414(1):73–81. doi: 10.1007/BF00585629. [DOI] [PubMed] [Google Scholar]
  33. Potma E. J., Stienen G. J., Barends J. P., Elzinga G. Myofibrillar ATPase activity and mechanical performance of skinned fibres from rabbit psoas muscle. J Physiol. 1994 Jan 15;474(2):303–317. doi: 10.1113/jphysiol.1994.sp020023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Potma E. J., van Graas I. A., Stienen G. J. Effects of pH on myofibrillar ATPase activity in fast and slow skeletal muscle fibers of the rabbit. Biophys J. 1994 Dec;67(6):2404–2410. doi: 10.1016/S0006-3495(94)80727-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schramm M., Klieber H. G., Daut J. The energy expenditure of actomyosin-ATPase, Ca(2+)-ATPase and Na+,K(+)-ATPase in guinea-pig cardiac ventricular muscle. J Physiol. 1994 Dec 15;481(Pt 3):647–662. doi: 10.1113/jphysiol.1994.sp020471. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Stienen G. J., Roosemalen M. C., Wilson M. G., Elzinga G. Depression of force by phosphate in skinned skeletal muscle fibers of the frog. Am J Physiol. 1990 Aug;259(2 Pt 1):C349–C357. doi: 10.1152/ajpcell.1990.259.2.C349. [DOI] [PubMed] [Google Scholar]
  37. Stienen G. J., Versteeg P. G., Papp Z., Elzinga G. Mechanical properties of skinned rabbit psoas and soleus muscle fibres during lengthening: effects of phosphate and Ca2+. J Physiol. 1992;451:503–523. doi: 10.1113/jphysiol.1992.sp019176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Webb M. R., Hibberd M. G., Goldman Y. E., Trentham D. R. Oxygen exchange between Pi in the medium and water during ATP hydrolysis mediated by skinned fibers from rabbit skeletal muscle. Evidence for Pi binding to a force-generating state. J Biol Chem. 1986 Nov 25;261(33):15557–15564. [PubMed] [Google Scholar]
  39. Wendt I. R., Gibbs C. L. Energy production of rat extensor digitorum longus muscle. Am J Physiol. 1973 May;224(5):1081–1086. doi: 10.1152/ajplegacy.1973.224.5.1081. [DOI] [PubMed] [Google Scholar]
  40. Westerblad H., Lee J. A., Lännergren J., Allen D. G. Cellular mechanisms of fatigue in skeletal muscle. Am J Physiol. 1991 Aug;261(2 Pt 1):C195–C209. doi: 10.1152/ajpcell.1991.261.2.C195. [DOI] [PubMed] [Google Scholar]
  41. Wilson G. J., Shull S. E., Cooke R. Inhibition of muscle force by vanadate. Biophys J. 1995 Jan;68(1):216–226. doi: 10.1016/S0006-3495(95)80177-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yoshizaki K., Seo Y., Nishikawa H., Morimoto T. Application of pulsed-gradient 31P NMR on frog muscle to measure the diffusion rates of phosphorus compounds in cells. Biophys J. 1982 May;38(2):209–211. doi: 10.1016/S0006-3495(82)84549-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zhao Y., Kawai M. The effect of the lattice spacing change on cross-bridge kinetics in chemically skinned rabbit psoas muscle fibers. II. Elementary steps affected by the spacing change. Biophys J. 1993 Jan;64(1):197–210. doi: 10.1016/S0006-3495(93)81357-2. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES