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. 1989 Oct 15;263(2):547–552. doi: 10.1042/bj2630547

Further characterization of the plasma membrane- and intracellular membrane-associated platelet Ca2+ transport systems.

J Enouf 1, R Bredoux 1, N Bourdeau 1, B Sarkadi 1, S Levy-Toledano 1
PMCID: PMC1133462  PMID: 2532004

Abstract

Biochemical characterization of the Ca2+-ATPases isolated from human platelet intracellular and plasma membranes is reported. A comparative study of the previously partly described plasma membrane Ca2+-ATPase [Enouf, Bredoux, Bourdeau & Levy-Toledano (1987) J. Biol. Chem. 261, 9293-9297] and the intracellular membrane Ca2+-ATPase obtained simultaneously shows differences in the following parameters: (1) different kinetics of the two enzymes; (2) similar apparent affinity towards Ca2+ (10(-7) M), though the intracellular membrane enzyme was inhibited at Ca2+ concentrations above 10(-6) M; (3) different pH dependence with an activity maximum at pH 7 for the intracellular membrane Ca2+-ATPase and no detectable pH maximum for the plasma membrane Ca2+-ATPase; (4) a 10-fold difference in the ATP requirement of the two Ca2+-ATPases; (5) different patterns of inhibition by vanadate. Finally, the possible regulation of the Ca2+-ATPases was examined by studying the effect of chlorpromazine on the two Ca2+-ATPase activities, with only the plasma membrane enzyme being inhibited. It is concluded that the two platelet Ca2+ transport systems show biochemical differences in spite of the previously shown similarity in the molecular masses of their Ca2+-ATPases, thus conferring a definite specificity to the platelet system.

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Selected References

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  1. Adunyah S. E., Dean W. L. Ca2+ transport in human platelet membranes. Kinetics of active transport and passive release. J Biol Chem. 1986 Mar 5;261(7):3122–3127. [PubMed] [Google Scholar]
  2. Adunyah S. E., Dean W. L. Effects of sulfhydryl reagents and other inhibitors on Ca2+ transport and inositol trisphosphate-induced Ca2+ release from human platelet membranes. J Biol Chem. 1986 Oct 5;261(28):13071–13075. [PubMed] [Google Scholar]
  3. Authi K. S., Crawford N. Inositol 1,4,5-trisphosphate-induced release of sequestered Ca2+ from highly purified human platelet intracellular membranes. Biochem J. 1985 Aug 15;230(1):247–253. doi: 10.1042/bj2300247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brandl C. J., deLeon S., Martin D. R., MacLennan D. H. Adult forms of the Ca2+ATPase of sarcoplasmic reticulum. Expression in developing skeletal muscle. J Biol Chem. 1987 Mar 15;262(8):3768–3774. [PubMed] [Google Scholar]
  5. Brandt P., Zurini M., Neve R. L., Rhoads R. E., Vanaman T. C. A C-terminal, calmodulin-like regulatory domain from the plasma membrane Ca2+-pumping ATPase. Proc Natl Acad Sci U S A. 1988 May;85(9):2914–2918. doi: 10.1073/pnas.85.9.2914. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Brass L. F., Joseph S. K. A role for inositol triphosphate in intracellular Ca2+ mobilization and granule secretion in platelets. J Biol Chem. 1985 Dec 5;260(28):15172–15179. [PubMed] [Google Scholar]
  7. Brattin W. J., Waller R. L. Calcium inhibition of rat liver microsomal calcium-dependent ATPase. J Biol Chem. 1983 Jun 10;258(11):6724–6729. [PubMed] [Google Scholar]
  8. Cutler L. S., Feinstein M. B., Rodan G. A., Christian C. P. Cytochemical evidence for the segregation of adenylate cyclase, Ca2+-, Mg2+-ATPase, K+-dependent p-nitrophenyl phosphatase in separate membrane compartments in human platelets. Histochem J. 1981 Jul;13(4):547–554. doi: 10.1007/BF01002710. [DOI] [PubMed] [Google Scholar]
  9. De Metz M., Lebret M., Enouf J., Lévy-Tolédano S. The phospholipid requirement of the (Ca2+ + Mg2+)-ATPase from human platelets. Biochim Biophys Acta. 1984 Mar 14;770(2):159–165. doi: 10.1016/0005-2736(84)90125-1. [DOI] [PubMed] [Google Scholar]
  10. Dean W. L. Purification and reconstitution of a Ca2+ pump from human platelets. J Biol Chem. 1984 Jun 10;259(11):7343–7348. [PubMed] [Google Scholar]
  11. Dean W. L., Sullivan D. M. Structural and functional properties of a Ca2+-ATPase from human platelets. J Biol Chem. 1982 Dec 10;257(23):14390–14394. [PubMed] [Google Scholar]
  12. Enouf J., Bredoux R., Boizard B., Wautier J. L., Chap H., Thomas J., de Metz M., Levy-Toledano S. Simultaneous isolation of two platelet membrane fractions: biochemical, immunological and functional characterization. Biochem Biophys Res Commun. 1984 Aug 30;123(1):50–58. doi: 10.1016/0006-291x(84)90378-4. [DOI] [PubMed] [Google Scholar]
  13. Enouf J., Bredoux R., Bourdeau N., Levy-Toledano S. Two different Ca2+ transport systems are associated with plasma and intracellular human platelet membranes. J Biol Chem. 1987 Jul 5;262(19):9293–9297. [PubMed] [Google Scholar]
  14. Enouf J., Giraud F., Bredoux R., Bourdeau N., Levy-Toledano S. Possible role of a cAMP-dependent phosphorylation in the calcium release mediated by inositol 1,4,5-trisphosphate in human platelet membrane vesicles. Biochim Biophys Acta. 1987 Apr 2;928(1):76–82. doi: 10.1016/0167-4889(87)90087-5. [DOI] [PubMed] [Google Scholar]
  15. Enouf J., Lompré A. M., Bredoux R., Bourdeau N., de La Bastie D., Levy-Toledano S. Different sensitivity to trypsin of the human platelet plasma and intracellular membrane Ca2+ pumps. J Biol Chem. 1988 Sep 25;263(27):13922–13929. [PubMed] [Google Scholar]
  16. Enyedi A., Sarkadi B., Földes-Papp Z., Monostory S., Gárdos G. Demonstration of two distinct calcium pumps in human platelet membrane vesicles. J Biol Chem. 1986 Jul 15;261(20):9558–9563. [PubMed] [Google Scholar]
  17. 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]
  18. Fauvel J., Chap H., Roques V., Levy-Toledano S., Douste-Blazy L. Biochemical characterization of plasma membranes and intracellular membranes isolated from human platelets using Percoll gradients. Biochim Biophys Acta. 1986 Mar 27;856(1):155–164. doi: 10.1016/0005-2736(86)90022-2. [DOI] [PubMed] [Google Scholar]
  19. Fischer T. H., Campbell K. P., White G. C., 2nd Evidence that platelet and skeletal sarcoplasmic reticulum Ca2+-ATPase are structurally distinct. J Biol Chem. 1985 Jul 25;260(15):8996–9001. [PubMed] [Google Scholar]
  20. Graf E., Verma A. K., Gorski J. P., Lopaschuk G., Niggli V., Zurini M., Carafoli E., Penniston J. T. Molecular properties of calcium-pumping ATPase from human erythrocytes. Biochemistry. 1982 Aug 31;21(18):4511–4516. doi: 10.1021/bi00261a049. [DOI] [PubMed] [Google Scholar]
  21. Gunteski-Hamblin A. M., Greeb J., Shull G. E. A novel Ca2+ pump expressed in brain, kidney, and stomach is encoded by an alternative transcript of the slow-twitch muscle sarcoplasmic reticulum Ca-ATPase gene. Identification of cDNAs encoding Ca2+ and other cation-transporting ATPases using an oligonucleotide probe derived from the ATP-binding site. J Biol Chem. 1988 Oct 15;263(29):15032–15040. [PubMed] [Google Scholar]
  22. Hack N., Crawford N. Two-dimensional polyacrylamide-gel electrophoresis of the proteins and glycoproteins of purified human platelet surface and intracellular membranes. Biochem J. 1984 Aug 15;222(1):235–246. doi: 10.1042/bj2220235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hack N., Croset M., Crawford N. Studies on the bivalent-cation-activated ATPase activities of highly purified human platelet surface and intracellular membranes. Biochem J. 1986 Feb 1;233(3):661–668. doi: 10.1042/bj2330661. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Herbener G. H., Dean W. L. Immunocytochemical localization of the Ca2+-ATPase polypeptide in human platelets. Biochem Biophys Res Commun. 1988 Jun 16;153(2):848–854. doi: 10.1016/s0006-291x(88)81173-2. [DOI] [PubMed] [Google Scholar]
  25. Kallner A. Determination of phosphate in serum and urine by a single step malachite-green method. Clin Chim Acta. 1975 Feb 22;59(1):35–39. doi: 10.1016/0009-8981(75)90215-6. [DOI] [PubMed] [Google Scholar]
  26. Kraus-Friedmann N., Biber J., Murer H., Carafoli E. Calcium uptake in isolated hepatic plasma-membrane vesicles. Eur J Biochem. 1982 Dec;129(1):7–12. doi: 10.1111/j.1432-1033.1982.tb07014.x. [DOI] [PubMed] [Google Scholar]
  27. Käser-Glanzmann R., Jakäbovä M., George J. N., Lüscher E. F. Stimulation of calcium uptake in platelet membrane vesicles by adenosine 3',5'-cyclic monophosphate and protein kinase. Biochim Biophys Acta. 1977 May 2;466(3):429–440. doi: 10.1016/0005-2736(77)90336-4. [DOI] [PubMed] [Google Scholar]
  28. Lapetina E. G., Watson S. P., Cuatrecasas P. myo-Inositol 1,4,5-trisphosphate stimulates protein phosphorylation in saponin-permeabilized human platelets. Proc Natl Acad Sci U S A. 1984 Dec;81(23):7431–7435. doi: 10.1073/pnas.81.23.7431. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Le Peuch C. J., Le Peuch D. A., Katz S., Demaille J. G., Hincke M. T., Bredoux R., Enouf J., Levy-Toledano S., Caen J. Regulation of calcium accumulation and efflux from platelet vesicles. Possible role for cyclic-AMP-dependent phosphorylation and calmodulin. Biochim Biophys Acta. 1983 Jun 23;731(3):456–464. doi: 10.1016/0005-2736(83)90041-x. [DOI] [PubMed] [Google Scholar]
  30. Lytton J., MacLennan D. H. Molecular cloning of cDNAs from human kidney coding for two alternatively spliced products of the cardiac Ca2+-ATPase gene. J Biol Chem. 1988 Oct 15;263(29):15024–15031. [PubMed] [Google Scholar]
  31. Menashi S., Authi K. S., Carey F., Crawford N. Characterization of the calcium-sequestering process associated with human platelet intracellular membranes isolated by free-flow electrophoresis. Biochem J. 1984 Sep 1;222(2):413–417. doi: 10.1042/bj2220413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Menashi S., Weintroub H., Crawford N. Characterization of human platelet surface and intracellular membranes isolated by free flow electrophoresis. J Biol Chem. 1981 Apr 25;256(8):4095–4101. [PubMed] [Google Scholar]
  33. Michaelis E. K., Michaelis M. L., Chang H. H., Kitos T. E. High affinity Ca2+-stimulated Mg2+-dependent ATPase in rat brain synaptosomes, synaptic membranes, and microsomes. J Biol Chem. 1983 May 25;258(10):6101–6108. [PubMed] [Google Scholar]
  34. O'Rourke F. A., Halenda S. P., Zavoico G. B., Feinstein M. B. Inositol 1,4,5-trisphosphate releases Ca2+ from a Ca2+-transporting membrane vesicle fraction derived from human platelets. J Biol Chem. 1985 Jan 25;260(2):956–962. [PubMed] [Google Scholar]
  35. Robblee L. S., Shepro D., Belamarich F. A. Calcium uptake and associated adenosine triphosphatase activity of isolated platelet membranes. J Gen Physiol. 1973 Apr;61(4):462–481. doi: 10.1085/jgp.61.4.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Shull G. E., Greeb J. Molecular cloning of two isoforms of the plasma membrane Ca2+-transporting ATPase from rat brain. Structural and functional domains exhibit similarity to Na+,K+- and other cation transport ATPases. J Biol Chem. 1988 Jun 25;263(18):8646–8657. [PubMed] [Google Scholar]
  37. Steiner B., Lüscher E. F. Evidence that the platelet plasma membrane does not contain a (Ca2+ + Mg2+)-dependent ATPase. Biochim Biophys Acta. 1985 Sep 10;818(3):299–309. doi: 10.1016/0005-2736(85)90003-3. [DOI] [PubMed] [Google Scholar]
  38. Tada M., Yamamoto T., Tonomura Y. Molecular mechanism of active calcium transport by sarcoplasmic reticulum. Physiol Rev. 1978 Jan;58(1):1–79. doi: 10.1152/physrev.1978.58.1.1. [DOI] [PubMed] [Google Scholar]
  39. Wuytack F., Raeymaekers L., Casteels R. The Ca2+-transport ATPases in smooth muscle. Experientia. 1985 Jul 15;41(7):900–905. doi: 10.1007/BF01970008. [DOI] [PubMed] [Google Scholar]
  40. de la Bastie D., Wisnewsky C., Schwartz K., Lompré A. M. (Ca2+ + Mg2+)-dependent ATPase mRNA from smooth muscle sarcoplasmic reticulum differs from that in cardiac and fast skeletal muscles. FEBS Lett. 1988 Feb 29;229(1):45–48. doi: 10.1016/0014-5793(88)80794-4. [DOI] [PubMed] [Google Scholar]

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