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. 1982 Nov;79(22):6881–6884. doi: 10.1073/pnas.79.22.6881

Unifying concept for the coupling between ion pumping and ATP hydrolysis or synthesis.

G G Hammes
PMCID: PMC347237  PMID: 6129623

Abstract

A mechanism is proposed for the coupling between ion transport and enzyme catalysis. The basic concept is that enzymes associated with transport exist in two possible conformations. Each conformation has the potential of catalyzing the enzymatic reaction, and pumping is associated with the conversion of one conformational form to the other. The conformational transition is triggered by the kinetic blockage of specific mechanistic steps for each conformation. Such blockages can cause a cycling between the two conformations concomitant with catalysis. This mechanistic concept is consistent with a variety of results obtained with the Na+,K+-ATPase, the Ca2+,Mg2+-ATPase, and ATP synthesizing enzymes (coupling factors).

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Selected References

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

  1. Adelstein R. S., Eisenberg E. Regulation and kinetics of the actin-myosin-ATP interaction. Annu Rev Biochem. 1980;49:921–956. doi: 10.1146/annurev.bi.49.070180.004421. [DOI] [PubMed] [Google Scholar]
  2. Baird B. A., Hammes G. G. Structure of oxidative- and photo-phosphorylation coupling factor complexes. Biochim Biophys Acta. 1979 Jul 3;549(1):31–53. doi: 10.1016/0304-4173(79)90017-x. [DOI] [PubMed] [Google Scholar]
  3. Bruist M. F., Hammes G. G. Mechanism for catalysis and regulation of adenosine 5'-triphosphate hydrolysis by chloroplast coupling factor 1. Biochemistry. 1982 Jul 6;21(14):3370–3377. doi: 10.1021/bi00257a019. [DOI] [PubMed] [Google Scholar]
  4. Cantley L. C., Jr, Cantley L. G., Josephson L. A characterization of vanadate interactions with the (Na,K)-ATPase. Mechanistic and regulatory implications. J Biol Chem. 1978 Oct 25;253(20):7361–7368. [PubMed] [Google Scholar]
  5. Cantley L. C., Jr, Gelles J., Josephson L. Reaction of (Na-K)ATPase with 7-chloro-4-nitrobenzo-2-oxa-1,3-diazole: evidence for an essential tyrosine at the active site. Biochemistry. 1978 Feb 7;17(3):418–425. doi: 10.1021/bi00596a006. [DOI] [PubMed] [Google Scholar]
  6. Choate G. L., Hutton R. L., Boyer P. D. Occurrence and significance of oxygen exchange reactions catalyzed by mitochondrial adenosine triphosphatase preparations. J Biol Chem. 1979 Jan 25;254(2):286–290. [PubMed] [Google Scholar]
  7. Dewey T. G., Hammes G. G. Steady state kinetics of ATP synthesis and hydrolysis catalyzed by reconstituted chloroplast coupling factor. J Biol Chem. 1981 Sep 10;256(17):8941–8946. [PubMed] [Google Scholar]
  8. Dunn S. D., Heppel L. A. Properties and functions of the subunits of the Escherichia coli coupling factor ATPase. Arch Biochem Biophys. 1981 Sep;210(2):421–436. doi: 10.1016/0003-9861(81)90206-x. [DOI] [PubMed] [Google Scholar]
  9. Dupont Y. Kinetics and regulation of sarcoplasmic reticulum ATPase. Eur J Biochem. 1977 Jan 3;72(1):185–190. doi: 10.1111/j.1432-1033.1977.tb11238.x. [DOI] [PubMed] [Google Scholar]
  10. Epstein M., Kuriki Y., Biltonen R., Racker E. Calorimetric studies of ligand-induced modulation of calcium adenosine 5'-triphosphatase from sarcoplasmic reticulum. Biochemistry. 1980 Nov 25;19(24):5564–5568. doi: 10.1021/bi00565a016. [DOI] [PubMed] [Google Scholar]
  11. Fillingame R. H. The proton-translocating pumps of oxidative phosphorylation. Annu Rev Biochem. 1980;49:1079–1113. doi: 10.1146/annurev.bi.49.070180.005243. [DOI] [PubMed] [Google Scholar]
  12. Gresser M. J., Myers J. A., Boyer P. D. Catalytic site cooperativity of beef heart mitochondrial F1 adenosine triphosphatase. Correlations of initial velocity, bound intermediate, and oxygen exchange measurements with an alternating three-site model. J Biol Chem. 1982 Oct 25;257(20):12030–12038. [PubMed] [Google Scholar]
  13. Hastings D. F., Reynolds J. A. Molecular weight of (Na+,K+)ATPase from shark rectal gland. Biochemistry. 1979 Mar 6;18(5):817–821. doi: 10.1021/bi00572a012. [DOI] [PubMed] [Google Scholar]
  14. Hutton R. L., Boyer P. D. Subunit interaction during catalysis. Alternating site cooperativity of mitochondrial adenosine triphosphatase. J Biol Chem. 1979 Oct 25;254(20):9990–9993. [PubMed] [Google Scholar]
  15. Jardetzky O. Simple allosteric model for membrane pumps. Nature. 1966 Aug 27;211(5052):969–970. doi: 10.1038/211969a0. [DOI] [PubMed] [Google Scholar]
  16. Jencks W. P. The utilization of binding energy in coupled vectorial processes. Adv Enzymol Relat Areas Mol Biol. 1980;51:75–106. doi: 10.1002/9780470122969.ch2. [DOI] [PubMed] [Google Scholar]
  17. Jorgensen P. L. Purification and characterization of (Na+ plus K+ )-ATPase. IV. Estimation of the purity and of the molecular weight and polypeptide content per enzyme unit in preparations from the outer medulla of rabbit kidney. Biochim Biophys Acta. 1974 Jul 12;356(1):53–67. doi: 10.1016/0005-2736(74)90293-4. [DOI] [PubMed] [Google Scholar]
  18. Kagawa Y. Reconstitution of the energy transformer, gate and channel subunit reassembly, crystalline ATPase and ATP synthesis. Biochim Biophys Acta. 1978 Sep 21;505(1):45–93. doi: 10.1016/0304-4173(78)90008-3. [DOI] [PubMed] [Google Scholar]
  19. Kanike K., Lindenmayer G. E., Wallick E. T., Lane L. K., Schwartz A. Specific sodium-22 binding to a purified sodium + potassium adenosine triphosphatase. Inhibition by ouabain. J Biol Chem. 1976 Aug 10;251(15):4794–4795. [PubMed] [Google Scholar]
  20. MITCHELL P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature. 1961 Jul 8;191:144–148. doi: 10.1038/191144a0. [DOI] [PubMed] [Google Scholar]
  21. Martin D. W., Tanford C. Phosphorylation of calcium adenosinetriphosphatase by inorganic phosphate: van't Hoff analysis of enthalpy changes. Biochemistry. 1981 Aug 4;20(16):4597–4602. doi: 10.1021/bi00519a013. [DOI] [PubMed] [Google Scholar]
  22. Matsui H., Hayashi Y., Homareda H., Kimimura M. Ouabain-sensitive 42K binding to Na+, K+-ATPase purified from canine kidney outer medulla. Biochem Biophys Res Commun. 1977 Mar 21;75(2):373–380. doi: 10.1016/0006-291x(77)91052-x. [DOI] [PubMed] [Google Scholar]
  23. Moczydlowski E. G., Fortes P. A. Characterization of 2',3'-O-(2,4,6-trinitrocyclohexadienylidine)adenosine 5'-triphosphate as a fluorescent probe of the ATP site of sodium and potassium transport adenosine triphosphatase. Determination of nucleotide binding stoichiometry and ion-induced changes in affinity for ATP. J Biol Chem. 1981 Mar 10;256(5):2346–2356. [PubMed] [Google Scholar]
  24. Moczydlowski E. G., Fortes P. A. Inhibition of sodium and potassium adenosine triphosphatase by 2',3'-O-(2,4,6-trinitrocyclohexadienylidene) adenine nucleotides. Implications for the structure and mechanism of the Na:K pump. J Biol Chem. 1981 Mar 10;256(5):2357–2366. [PubMed] [Google Scholar]
  25. Neet K. E., Green N. M. Kinetics of the cooperativity of the Ca2+-transporting adenosine triphosphatase of sarcoplasmic reticulum and the mechanism of the ATP interaction. Arch Biochem Biophys. 1977 Jan 30;178(2):588–597. doi: 10.1016/0003-9861(77)90230-2. [DOI] [PubMed] [Google Scholar]
  26. Penefsky H. S. Mitochondrial ATPase. Adv Enzymol Relat Areas Mol Biol. 1979;49:223–280. doi: 10.1002/9780470122945.ch6. [DOI] [PubMed] [Google Scholar]
  27. Post R. L., Hegyvary C., Kume S. Activation by adenosine triphosphate in the phosphorylation kinetics of sodium and potassium ion transport adenosine triphosphatase. J Biol Chem. 1972 Oct 25;247(20):6530–6540. [PubMed] [Google Scholar]
  28. Post R. L., Kume S. Evidence for an aspartyl phosphate residue at the active site of sodium and potassium ion transport adenosine triphosphatase. J Biol Chem. 1973 Oct 25;248(20):6993–7000. [PubMed] [Google Scholar]
  29. Ribeiro J. M., Vianna A. L. Allosteric modification by K+ of the (Ca2+ + Mg2+)-dependent ATPase of sarcoplasmic reticulum. Interaction with Mg2+. J Biol Chem. 1978 May 10;253(9):3153–3157. [PubMed] [Google Scholar]
  30. Rizzolo L. J., Maire M., Reynolds J. A., Tanford C. Molecular weights and hydrophobicity of the polypeptide chain of sarcoplasmic reticulum calcium(II) adenosine triphosphatase and of its primary tryptic fragments. Biochemistry. 1976 Aug 10;15(16):3433–3437. doi: 10.1021/bi00661a006. [DOI] [PubMed] [Google Scholar]
  31. Robinson J. D., Flashner M. S. The (Na+ + K+)-activated ATPase. Enzymatic and transport properties. Biochim Biophys Acta. 1979 Aug 17;549(2):145–176. doi: 10.1016/0304-4173(79)90013-2. [DOI] [PubMed] [Google Scholar]
  32. Shigekawa M., Dougherty J. P., Katz A. M. Reaction mechanism of Ca2+-dependent ATP hydrolysis by skeletal muscle sarcoplasmic reticulum in the absence of added alkali metal salts. I. Characterization of steady state ATP hydrolysis and comparison with that in the presence of KCl. J Biol Chem. 1978 Mar 10;253(5):1442–1450. [PubMed] [Google Scholar]
  33. Slater E. C. Mechanism of oxidative phosphorylation. Annu Rev Biochem. 1977;46:1015–1026. doi: 10.1146/annurev.bi.46.070177.005055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Smith R. L., Zinn K., Cantley L. C. A study of the vanadate-trapped state of the (Na,K)-ATPase. Evidence against interacting nucleotide site models. J Biol Chem. 1980 Oct 25;255(20):9852–9859. [PubMed] [Google Scholar]
  35. WHITTAM R. The asymmetrical stimulation of a membrane adenosine triphosphatase in relation to active cation transport. Biochem J. 1962 Jul;84:110–118. doi: 10.1042/bj0840110. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Yamamoto T., Tonomura Y. Reaction mechanism of the Ca++ -dependent ATPase of sarcoplasmic reticulum from skeletal muscle. II. Intermediate formation of phosphoryl protein. J Biochem. 1968 Aug;64(2):137–145. doi: 10.1093/oxfordjournals.jbchem.a128873. [DOI] [PubMed] [Google Scholar]
  37. de Meis L., Boyer P. D. Induction by nucleotide triphosphate hydrolysis of a form of sarcoplasmic reticulum ATPase capable of medium phosphate-oxygen exchange in presence of calcium. J Biol Chem. 1978 Mar 10;253(5):1556–1559. [PubMed] [Google Scholar]
  38. de Meis L., Inesi G. ATP synthesis by sarcoplasmic reticulum ATPase following Ca2+, PH, temperature, and water activity jumps. J Biol Chem. 1982 Feb 10;257(3):1289–1294. [PubMed] [Google Scholar]
  39. de Meis L., Vianna A. L. Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum. Annu Rev Biochem. 1979;48:275–292. doi: 10.1146/annurev.bi.48.070179.001423. [DOI] [PubMed] [Google Scholar]

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