Abstract
Transport of Ca2+ across the membrane by the Ca2+-ATPase of skeletal muscle sarcoplasmic reticulum involves the transfer of two Ca2+ ions from a pair of cytoplasmic sites to a pair of luminal sites, driven by phosphorylation of the ATPase. The ATPase is inhibited by Mg2+ at alkaline pH values. Inhibition follows from a decrease in the rate of release of Ca2+ from the phosphorylated ATPase. Phosphorylation-induced release of Ca2+ from the ATPase is biphasic at alkaline pH, which is consistent with sequential release of Ca2+ from the phosphorylated ATPase; the rates of both components decrease with increasing Mg concentration. The effect of Mg2+ on the slow phase of release follows from the binding of Mg2+ at the empty outer luminal site, vacated by the release of the first Ca2+ ion. The effect of Mg2+ on the rate of release of the first Ca2+ ion could follow from binding to a gating site also affecting the binding of Ca2+ to the cytoplasmic sites.
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- Bishop J. E., Al-Shawi M. K. Inhibition of sarcoplasmic reticulum Ca2+-ATPase by Mg2+ at high pH. J Biol Chem. 1988 Feb 5;263(4):1886–1892. [PubMed] [Google Scholar]
- Brandl C. J., Green N. M., Korczak B., MacLennan D. H. Two Ca2+ ATPase genes: homologies and mechanistic implications of deduced amino acid sequences. Cell. 1986 Feb 28;44(4):597–607. doi: 10.1016/0092-8674(86)90269-2. [DOI] [PubMed] [Google Scholar]
- Champeil P., Guillain F. Rapid filtration study of the phosphorylation-dependent dissociation of calcium from transport sites of purified sarcoplasmic reticulum ATPase and ATP modulation of the catalytic cycle. Biochemistry. 1986 Nov 18;25(23):7623–7633. doi: 10.1021/bi00371a053. [DOI] [PubMed] [Google Scholar]
- Clarke D. M., Loo T. W., Inesi G., MacLennan D. H. Location of high affinity Ca2+-binding sites within the predicted transmembrane domain of the sarcoplasmic reticulum Ca2+-ATPase. Nature. 1989 Jun 8;339(6224):476–478. doi: 10.1038/339476a0. [DOI] [PubMed] [Google Scholar]
- Dalton K. A., East J. M., Mall S., Oliver S., Starling A. P., Lee A. G. Interaction of phosphatidic acid and phosphatidylserine with the Ca2+-ATPase of sarcoplasmic reticulum and the mechanism of inhibition. Biochem J. 1998 Feb 1;329(Pt 3):637–646. doi: 10.1042/bj3290637. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dupont Y. Low-temperature studies of the sarcoplasmic reticulum calcium pump. Mechanisms of calcium binding. Biochim Biophys Acta. 1982 May 21;688(1):75–87. doi: 10.1016/0005-2736(82)90580-6. [DOI] [PubMed] [Google Scholar]
- East J. M., Lee A. G. Lipid selectivity of the calcium and magnesium ion dependent adenosinetriphosphatase, studied with fluorescence quenching by a brominated phospholipid. Biochemistry. 1982 Aug 17;21(17):4144–4151. doi: 10.1021/bi00260a035. [DOI] [PubMed] [Google Scholar]
- Fabiato A., Fabiato F. Calculator programs for computing the composition of the solutions containing multiple metals and ligands used for experiments in skinned muscle cells. J Physiol (Paris) 1979;75(5):463–505. [PubMed] [Google Scholar]
- Forge V., Mintz E., Canet D., Guillain F. Lumenal Ca2+ dissociation from the phosphorylated Ca(2+)-ATPase of the sarcoplasmic reticulum is sequential. J Biol Chem. 1995 Aug 4;270(31):18271–18276. doi: 10.1074/jbc.270.31.18271. [DOI] [PubMed] [Google Scholar]
- Forge V., Mintz E., Guillain F. Ca2+ binding to sarcoplasmic reticulum ATPase revisited. II. Equilibrium and kinetic evidence for a two-route mechanism. J Biol Chem. 1993 May 25;268(15):10961–10968. [PubMed] [Google Scholar]
- 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]
- Hanel A. M., Jencks W. P. Dissociation of calcium from the phosphorylated calcium-transporting adenosine triphosphatase of sarcoplasmic reticulum: kinetic equivalence of the calcium ions bound to the phosphorylated enzyme. Biochemistry. 1991 Nov 26;30(47):11320–11330. doi: 10.1021/bi00111a019. [DOI] [PubMed] [Google Scholar]
- Hardwicke P. M., Green N. M. The effect of delipidation on the adenosine triphosphatase of sarcoplasmic reticulum. Electron microscopy and physical properties. Eur J Biochem. 1974 Feb 15;42(1):183–193. doi: 10.1111/j.1432-1033.1974.tb03328.x. [DOI] [PubMed] [Google Scholar]
- Henderson I. M., Starling A. P., Wictome M., East J. M., Lee A. G. Binding of Ca2+ to the (Ca(2+)-Mg2+)-ATPase of sarcoplasmic reticulum: kinetic studies. Biochem J. 1994 Feb 1;297(Pt 3):625–636. doi: 10.1042/bj2970625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes G., East J. M., Lee A. G. The hydrophilic domain of phospholamban inhibits the Ca2+ transport step of the Ca(2+)-ATPase. Biochem J. 1994 Oct 15;303(Pt 2):511–516. doi: 10.1042/bj3030511. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hughes G., Khan Y. M., East J. M., Lee A. G. Effects of polycations on Ca2+ binding to the Ca(2+)-ATPase. Biochem J. 1995 Jun 1;308(Pt 2):493–499. doi: 10.1042/bj3080493. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Inesi G. Sequential mechanism of calcium binding and translocation in sarcoplasmic reticulum adenosine triphosphatase. J Biol Chem. 1987 Dec 5;262(34):16338–16342. [PubMed] [Google Scholar]
- Jencks W. P., Yang T., Peisach D., Myung J. Calcium ATPase of sarcoplasmic reticulum has four binding sites for calcium. Biochemistry. 1993 Jul 13;32(27):7030–7034. doi: 10.1021/bi00078a031. [DOI] [PubMed] [Google Scholar]
- Lee A. G., Baker K., Khan Y. M., East J. M. Effects of K+ on the binding of Ca2+ to the Ca(2+)-ATPase of sarcoplasmic reticulum. Biochem J. 1995 Jan 1;305(Pt 1):225–231. doi: 10.1042/bj3050225. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MacLennan D. H., Rice W. J., Green N. M. The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. J Biol Chem. 1997 Nov 14;272(46):28815–28818. doi: 10.1074/jbc.272.46.28815. [DOI] [PubMed] [Google Scholar]
- Matthews I., Sharma R. P., Lee A. G., East J. M. Transmembranous organization of (Ca2(+)-Mg2+)-ATPase from sarcoplasmic reticulum. Evidence for lumenal location of residues 877-888. J Biol Chem. 1990 Nov 5;265(31):18737–18740. [PubMed] [Google Scholar]
- Moutin M. J., Dupont Y. Interaction of potassium and magnesium with the high affinity calcium-binding sites of the sarcoplasmic reticulum calcium-ATPase. J Biol Chem. 1991 Mar 25;266(9):5580–5586. [PubMed] [Google Scholar]
- Mészáros L. G., Bak J. Z. Coexistence of high- and low-affinity Ca2+ binding sites of the sarcoplasmic reticulum calcium pump. Biochemistry. 1993 Sep 28;32(38):10085–10088. doi: 10.1021/bi00089a025. [DOI] [PubMed] [Google Scholar]
- Mészáros L. G., Bak J. Simultaneous internalization and binding of calcium during the initial phase of calcium uptake by the sarcoplasmic reticulum Ca pump. Biochemistry. 1992 Feb 4;31(4):1195–1200. doi: 10.1021/bi00119a032. [DOI] [PubMed] [Google Scholar]
- Orlowski S., Champeil P. Kinetics of calcium dissociation from its high-affinity transport sites on sarcoplasmic reticulum ATPase. Biochemistry. 1991 Jan 15;30(2):352–361. doi: 10.1021/bi00216a007. [DOI] [PubMed] [Google Scholar]
- Orlowski S., Champeil P. The two calcium ions initially bound to nonphosphorylated sarcoplasmic reticulum Ca(2+)-ATPase can no longer be kinetically distinguished when they dissociate from phosphorylated ATPase toward the lumen. Biochemistry. 1991 Nov 26;30(47):11331–11342. doi: 10.1021/bi00111a020. [DOI] [PubMed] [Google Scholar]
- Petithory J. R., Jencks W. P. Sequential dissociation of Ca2+ from the calcium adenosinetriphosphatase of sarcoplasmic reticulum and the calcium requirement for its phosphorylation by ATP. Biochemistry. 1988 Jul 26;27(15):5553–5564. doi: 10.1021/bi00415a025. [DOI] [PubMed] [Google Scholar]
- Reed P. W., Lardy H. A. A23187: a divalent cation ionophore. J Biol Chem. 1972 Nov 10;247(21):6970–6977. [PubMed] [Google Scholar]
- Toyoshima C., Sasabe H., Stokes D. L. Three-dimensional cryo-electron microscopy of the calcium ion pump in the sarcoplasmic reticulum membrane. Nature. 1993 Apr 1;362(6419):467–471. doi: 10.1038/362469a0. [DOI] [PubMed] [Google Scholar]
- 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]
