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. 1987 Jun;51(6):883–893. doi: 10.1016/S0006-3495(87)83416-1

Analysis of compartmentation of ATP in skeletal and cardiac muscle using 31P nuclear magnetic resonance saturation transfer.

R Zahler, J A Bittl, J S Ingwall
PMCID: PMC1330022  PMID: 3607210

Abstract

We have developed a model for the analysis of the forward creatine kinase reaction in muscle as measured by the nuclear magnetic resonance (NMR) technique of magnetization transfer. The model, accounting for the double-exponential behavior observed in some NMR magnetization transfer data, allows for the existence of two ATP pools, one that is NMR-visible (NMR-VIS) and another that is NMR-invisible (NMR-INVIS). We have applied the model to experimental data for the forward creatine kinase reaction in skeletal and cardiac muscles to study the dependence of the creatine kinase rate constants and fluxes on workload and to account for the differences between heart and skeletal muscle. The results suggest that an NMR-distinct ATP pool exists in both heart and skeletal muscles, and that phosphate exchange with this pool catalyzed by creatine kinase increases with increased workload. The results also agree with previously published estimates of the rates of mitochondrial translocase and net ATP synthesis obtained by traditional biochemical methods.

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Selected References

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

  1. Balaban R. S., Kantor H. L., Ferretti J. A. In vivo flux between phosphocreatine and adenosine triphosphate determined by two-dimensional phosphorous NMR. J Biol Chem. 1983 Nov 10;258(21):12787–12789. [PubMed] [Google Scholar]
  2. Bittl J. A., Ingwall J. S. Reaction rates of creatine kinase and ATP synthesis in the isolated rat heart. A 31P NMR magnetization transfer study. J Biol Chem. 1985 Mar 25;260(6):3512–3517. [PubMed] [Google Scholar]
  3. CHANCE B. THE ENERGY-LINKED REACTION OF CALCIUM WITH MITOCHONDRIA. J Biol Chem. 1965 Jun;240:2729–2748. [PubMed] [Google Scholar]
  4. Gadian D. G., Radda G. K., Brown T. R., Chance E. M., Dawson M. J., Wilkie D. R. The activity of creatine kinase in frog skeletal muscle studied by saturation-transfer nuclear magnetic resonance. Biochem J. 1981 Jan 15;194(1):215–228. doi: 10.1042/bj1940215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Jacobus W. E., Lehninger A. L. Creatine kinase of rat heart mitochondria. Coupling of creatine phosphorylation to electron transport. J Biol Chem. 1973 Jul 10;248(13):4803–4810. [PubMed] [Google Scholar]
  6. Jacobus W. E. Respiratory control and the integration of heart high-energy phosphate metabolism by mitochondrial creatine kinase. Annu Rev Physiol. 1985;47:707–725. doi: 10.1146/annurev.ph.47.030185.003423. [DOI] [PubMed] [Google Scholar]
  7. Kupriyanov V. V., Ya Steinschneider A., Ruuge E. K., Kapel'ko V. I., Yu Zueva M., Lakomkin V. L., Smirnov V. N., Saks V. A. Regulation of energy flux through the creatine kinase reaction in vitro and in perfused rat heart. 31P-NMR studies. Biochim Biophys Acta. 1984 Dec 11;805(4):319–331. doi: 10.1016/0167-4889(84)90014-4. [DOI] [PubMed] [Google Scholar]
  8. LaNoue K. F., Bryla J., Williamson J. R. Feedback interactions in the control of citric acid cycle activity in rat heart mitochondria. J Biol Chem. 1972 Feb 10;247(3):667–679. [PubMed] [Google Scholar]
  9. Matthews P. M., Bland J. L., Gadian D. G., Radda G. K. A 31P-NMR saturation transfer study of the regulation of creatine kinase in the rat heart. Biochim Biophys Acta. 1982 Nov 17;721(3):312–320. doi: 10.1016/0167-4889(82)90084-2. [DOI] [PubMed] [Google Scholar]
  10. Meyer R. A., Sweeney H. L., Kushmerick M. J. A simple analysis of the "phosphocreatine shuttle". Am J Physiol. 1984 May;246(5 Pt 1):C365–C377. doi: 10.1152/ajpcell.1984.246.5.C365. [DOI] [PubMed] [Google Scholar]
  11. Nunnally R. L., Hollis D. P. Adenosine triphosphate compartmentation in living hearts: a phosphorus nuclear magnetic resonance saturation transfer study. Biochemistry. 1979 Aug 7;18(16):3642–3646. doi: 10.1021/bi00583a032. [DOI] [PubMed] [Google Scholar]
  12. Saks V. A., Chernousova G. B., Gukovsky D. E., Smirnov V. N., Chazov E. I. Studies of energy transport in heart cells. Mitochondrial isoenzyme of creatine phosphokinase: kinetic properties and regulatory action of Mg2+ ions. Eur J Biochem. 1975 Sep 1;57(1):273–290. doi: 10.1111/j.1432-1033.1975.tb02299.x. [DOI] [PubMed] [Google Scholar]
  13. Turner D. C., Wallimann T., Eppenberger H. M. A protein that binds specifically to the M-line of skeletal muscle is identified as the muscle form of creatine kinase. Proc Natl Acad Sci U S A. 1973 Mar;70(3):702–705. doi: 10.1073/pnas.70.3.702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Veech R. L., Lawson J. W., Cornell N. W., Krebs H. A. Cytosolic phosphorylation potential. J Biol Chem. 1979 Jul 25;254(14):6538–6547. [PubMed] [Google Scholar]

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