How many Ca²+ATPase isoforms are expressed in a cell type? A growing family of membrane proteins illustrated by studies in platelets

References

• Carafoli E, Brini M. Calcium pumps: structural basis for and mechanism of calcium transmembrane transport. Curr Opin Chem Biol 2000;4:152–61.
   PubMed Web of Science ®Google Scholar
• Strehler EE, Zacharias DA. Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 2001;81:21–50.
   PubMed Web of Science ®Google Scholar
• Wuytack F, Raeymaekers L, Missiaen L. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium 2002;32:279–05.
   PubMed Web of Science ®Google Scholar
• Strehler EE, Treiman M. Calcium pumps of plasma membrane and cell interior. Curr Mol Med 2004;4:323–35.
   PubMedGoogle Scholar
• Lipskaia L, Lompre´ AM. Alteration in temporal kinetics of Ca2þ signaling and control of growth and proliferation. Biol Cell 2004;96:55–68.
   PubMed Web of Science ®Google Scholar
• Moller J, Juul B, Le Maire M. Structural organization, ion transport, and energy transduction of P-type ATPases. Biochim Biophys Acta 1996;1286:1–51.
   PubMed Web of Science ®Google Scholar
• Andersen JP. Dissection of the functional domains of the sarcoplasmic reticulum Ca2þ-ATPase by site-directed mutagenesis. Biosci Rep 1995;15:243–61.
   PubMedGoogle Scholar
• Martonosi AN. The structure and interactions of Ca2þ-ATPase. Biosci Rep 1995;15:263–81.
   PubMedGoogle Scholar
• MacLennan DH, Rice WJ, Green NM. The mechanism of Ca2þ transport by sarco(endo)plasmic reticulum Ca2þ-ATPases. J Biol Chem 1997;272:28815–18.
   PubMed Web of Science ®Google Scholar
• Toyoshima C, Nakasako M, Nomura H, Ogawa H. Crystal structure of the calcium pump of sarcoplasmic reticulum at 2.6 A resolution. Nature 2000;405:647–55.
   Google Scholar
• Toyoshima C, Nomura H. Structural changes in the calcium pump accompanying the dissociation of calcium. Nature 2002;418:605–11.
   PubMed Web of Science ®Google Scholar
• Lee AG, East JM. What the structure of a calcium pump tells us about its mechanism. Biochem J 2001;356:665–683.
   PubMedGoogle Scholar
• Xu C, Rice WJ, He W, Stokes DL. A structural model for the catalytic cycle of Ca2þ-ATPase. J Mol Biol 2002;316:201–11.
   PubMedGoogle Scholar
• Young HS, Stokes DL. The mechanics of calcium transport. J Membr Biol 2004;198:55–63.
   PubMedGoogle Scholar
• Borke JL, Minami J, Verma A, Penniston JT, Kumar R. Monoclonal antibodies to human erythrocyte membrane Ca2þ-Mg2þ adenosine triphosphatase pump recognize an epitope in the basolateral membrane of human kidney distal tubule cells. J Clin Invest 1987;80:1225–31.
   PubMed Web of Science ®Google Scholar
• Caride AJ, Filoteo AG, Enyedi A, Verma AK, Penniston JT. Detection of isoform 4 of the plasma membrane calcium pump in human tissues by using isoform-specific monoclonal antibodies. Biochem J 1996;316:353–59.
   PubMed Web of Science ®Google Scholar
• Ge´le´bart P, Martin V, Enouf J, Papp B. Identification of a new SERCA2 splice variant regulated during mono-cytic differentiation. Biochem Biophys Res Commun 2003;303:676–84.
   PubMedGoogle Scholar
• Jorgensen AO, Arnold W, Pepper DR, Kahl SD, Mandel F, Campbell KP. A monoclonal antibody to the Ca2þ-ATPase of cardiac sarcoplasmic reticulum cross-reacts with slow type I but not with fast type II canine skeletal muscle fibers: an immunocytochemical and immunochemical study. Cell Motil Cytoskeleton 1988;9:164–74.
   PubMedGoogle Scholar
• Wuytack F, Kanmura Y, Eggermont J A, Raeymaekers L, Verbist J, Hartweg D, Gietzen K, Casteels R. Smooth muscle expresses a cardiac/slow muscle isoform of the Ca2þ-transport ATPase in its endoplasmic reticulum. Biochem J 1989;257:117–23.
   PubMedGoogle Scholar
• Wuytack F, Eggermont JA, Raeymaekers L, Plessers L, Casteels R. Antibodies against the non-muscle isoform of the endoplasmic reticulum Ca2þ-transport ATPase. Biochem J 1989;264:765–69.
   PubMedGoogle Scholar
• Hack N, Wilkinson JM, Crawford N. A monoclonal antibody (PL/IM430) to human platelet intracellular membranes which inhibits the uptake of Ca2þ without affecting the Ca2þþMg2þ-ATPase. Biochem J 1988;250:355–61.
   PubMedGoogle Scholar
• Wuytack F, Papp B, Verboomen H, Raeymaekers L, Dode L, Bobe R, Enouf J, Bokkala S, Authi KS, Casteels R. A sarco/ endoplasmic reticulum Ca2þATPase 3-type Ca2þ pump is expressed in platelets, in lymphoid cells, and in mast cells. J Biol Chem 1994;269:1410–16.
   PubMed Web of Science ®Google Scholar
• Bobe R, Bredoux R, Wuytack F, Quarck R, Kovacs T, Papp B, Corvazier E, Magnier C, Enouf J. The rat platelet 97-kDa Ca +ATPase isoform is the sarcoendoplasmic reticulum Ca +ATPase 3 protein. J Biol Chem 1994;269:1417–24.
   PubMed Web of Science ®Google Scholar
• Bokkala S, el-Daher SS, Kakkar VV, Wuytack F, Authi KS. Localization and identification of Ca +ATPases in highly purified human platelet plasma and intracellular membranes. Evidence that the monoclonal antibody PL/IM430 recognizes the SERCA3 Ca +ATPase in human platelets. Biochem J 1995;306:837–42.
   Google Scholar
• Dode L, Wuytack F, Kools PF, Baba-Aissa F, Raeymaekers L, Brike F, van de Ven WJ, Casteels R, Brik F. cDNA cloning, expression and chromosomal localization of the human sarco/ endoplasmic reticulum Ca2+-ATPase 3 gene. Biochem J 1996;318:689–99.
   PubMedGoogle Scholar
• Dode L, De Greef C, Mountian I, Attard M, Town MM, Casteels R, Wuytack F. Structure of the human sarco/ endoplasmic reticulum Ca +-ATPase 3 gene. Promoter analysis and alternative splicing of the SERCA3 pre-mRNA. J Biol Chem 1998;273:13982–94.
   Google Scholar
• Kova`cs T, Felfoldi F, Papp B, Pa`szty K, Bredoux R, Enyedi A, Enouf J. All three splice variants of the human sarco/endoplasmic reticulum Ca2+ATPase 3 gene are translated to proteins. A study of their co-expression in platelets and lymphoid cells. Biochem J 2001;358:559–68.
   Google Scholar
• Martin V, Bredoux R, Corvazier E, van Gorp R, Kova`cs T, Ge´le´bart P, Enouf J. Three novel sarco/endoplasmic reticulum Ca +ATPase (SERCA) 3 isoforms. Expression, regulation and function of the SERCA3 family. J Biol Chem 2002;277:24442–52.
   Google Scholar
• Chandrasekera CP, Lytton J. Inhibition of human SERCA3 by PL/IM430. Molecular analysis of the interaction. J Biol Chem 2003;278:12482–88.
   PubMedGoogle Scholar
• Bobe R, Bredoux R, Corvazier E, Andersen JP, Clausen JD, Dode L, Kova`cs T, Enouf J. Identification, expression, function and localization of a novel (sixth) isoform of the human sarco/endoplasmic reticulum Ca +ATPase 3 (SERCA3) gene. J Biol Chem 2004;279:24297–306.
   PubMed Web of Science ®Google Scholar
• Borge PD, Jr, Wolf BA. Insulin receptor substrate 1 regulation of sarco-endoplasmic reticulum calcium ATPase 3 in insulin-secreting /¡-cells. J Biol Chem 2003;278:11359–68.
   PubMed Web of Science ®Google Scholar
• Machuca I, Domenget C, Jurdic P. Identification of avian sarcoplasmic reticulum Ca2+-ATPase (SERCA3) as a novel 1,25(OH)(2)D(3) target gene in the monocytic lineage. Exp Cell Res 1999;250:364–75.
   PubMedGoogle Scholar
• Alvarez CE, Sutcliffe JG, Thomas EA. Novel isoform of insulin receptor substrate p53/p58 is generated by alternative splicing in the CRIB/SH3-binding site. J Biol Chem 2002;277:24728–34.
   PubMedGoogle Scholar
• Nurtdinov RN, Artamonova II, Mironov AA, Gelfand MS. Low conservation of alternative splicing patterns in the human and mouse genes. Hum Mol Genet 2003;12:1313–20.
   PubMed Web of Science ®Google Scholar
• Varadi A, Lebel L, Hashim Y, Mehta Z, Ashcroft SJ, Turner R. Sequence variants of the sarco(endo)plasmic reticulum Ca +-transport ATPase 3 gene (SERCA3) in Caucasian type II diabetic patients (UK Prospective Diabetes Study 48). Diabetologia 1999;42:1240–43.
   PubMedGoogle Scholar
• Liu LH, Paul RJ, Sutliff RL, Miller ML, Lorenz JN, Pun RY, Duffy JJ, Doetschman T, Kimura Y, MacLennan DH, Hoying JB, Shull GE. Defective endothelium-dependent relaxation of vascular smooth muscle and endothelial cell Ca + signaling in mice lacking sarco(endo)plasmic reticulum Ca2+-ATPase isoform 3. J Biol Chem 1997;272:30538–45.
   PubMedGoogle Scholar
• Kao J, Fortner CN, Liu LH, Shull GE, Paul RJ. Ablation of the SERCA3 gene alters epithelium-dependent relaxation in mouse tracheal smooth muscle. Am J Physiol 1999;277:L264–70.
   Google Scholar
• Burk SE, Lytton J, MacLennan DH, Shull GE. cDNA cloning, functional expression, and mRNA tissue distribution of a third organellar Ca + pump. J Biol Chem 1989; 264:18561–68.
   PubMedGoogle Scholar
• Anger M, Samuel J-L, Marotte F, Wuytack F, Rappaport L, Lompre´ A-M. The sarco(endo)plasmic reticulum Ca2+-ATPase mRNA isoform, SERCA3, is expressed in endothelial and epithelial cells in various organs. FEBS Lett 1993;334:45–48.
   PubMedGoogle Scholar
• Anger M, Samuel JL, Marotte F, Wuytack F, Rappaport L, Lompre´ AM. In situ mRNA distribution of sarco(endo)plas-mic reticulum Ca +ATPase isoforms during ontogeny in the rat. J Mol Cell Cardiol 1994;26:539–50.
   PubMedGoogle Scholar
• Magnier C, Bredoux R, Kova`cs T, Quarck R, Papp B, Corvazier E, de Gunzburg J, Enouf J. Correlated expression of the 97 kDa sarcoendoplasmic reticulum Ca +-ATPase and Rap1B in platelets and various cell lines. Biochem J 1994;297:343–50.
   PubMedGoogle Scholar
• Wu KD, Lee WS, Wey J, Bungard D, Lytton J. Localization and quantification of endoplasmic reticulum Ca +-ATPase isoform transcripts. Am J Physiol 1995;269:C775–84.
   PubMedGoogle Scholar
• Varadi A, Molnar E, Ashcroft SJH. Characterisation of endoplasmic reticulum and plasma membrane Ca +-ATPases in pancreatic /¡-cells and in islets of Langerhans. Biochim Biophys Acta 1996;1236:119–27.
   Google Scholar
• Rooney E, Meldolesi J. The endoplasmic reticulum in PC12 cells. Evidence for a mosaic of domains differently specialized in Ca <sup>+</sup> handling. J Biol Chem 1996;271:29304–11.
   Google Scholar
• Santiago-Garcia J, Mas-Oliva J, Saavedra D, Zarain-Herzberg A. Analysis of mRNA expression and cloning of a novel plasma membrane Ca +-ATPase splice variant in human heart. Mol Cell Biochem 1996;155:173–82.
   PubMedGoogle Scholar
• Baba-Aissa F, Raeymaekers L, Wuytack F, Callewaert G, Dode L, Missiaen L, Casteels R. Purkinje neurons express the SERCA3 isoform of the organellar type Ca +-transport ATPase. Mol Brain Res 1996;41:169–74.
   PubMedGoogle Scholar
• Lee MG, Xu X, Zeng W, Diaz J, Kuo TH, Wuytack F, Raeymaekers L, Muallem S. Polarized expression of Ca + pumps in pancreatic and salivary gland cells. Role in initiation and propagation of [Ca<sup>2+</sup>]i waves. J Biol Chem 1997;272:15771–76.
   Google Scholar
• Launay S, Bobe R, Lacabaratz-Porret C, Bredoux R, Kova`cs T, Enouf J, Papp B. Modulation of endoplasmic reticulum calcium pump expression during T lymphocyte activation. J Biol Chem 1997;272:10746–50.
   PubMedGoogle Scholar
• Vanlingen S, Parys JB, Missiaen L, De Smedt H, Wuytack F, Casteels R. Distribution of inositol 1,4,5-trisphosphate receptor isoforms, SERCA isoforms and Ca2+ binding proteins in RBL-2H3 rat basophilic leukemia cells. Cell Calcium 1997;22:475–86.
   PubMedGoogle Scholar
• Kuo TH, Liu BF, Yu Y, Wuytack F, Raeymaekers L, Tsang W. Co-ordinated regulation of the plasma membrane calcium pump and the sarco(endo)plasmic reticular calcium pump gene expression by Ca +. Cell Calcium 1997;21:399–08.
   PubMedGoogle Scholar
• Baba-Aissa F, Raeymaekers L, Wuytack F, Dode L, Casteels R. Distribution and isoform diversity of the organellar Ca + pumps in the brain. Mol Chem Neuropathol 1998;33:199–08.
   PubMedGoogle Scholar
• Ozog A, Pouzet B, Bobe R, Lompre´ AM. Characterization of the 3’ end of the mouse SERCA 3 gene and tissue distribution of mRNA spliced variants. FEBS Lett 1998;427:349–52.
   PubMed Web of Science ®Google Scholar
• Poch E, Leach S, Snape S, Cacic T, MacLennan DH, Lytton J. Functional characterization of alternatively spliced human SERCA3 transcripts. Am J Physiol 1998;275:C1449–58.
   Google Scholar
• Liu L, Bian L, Borchman D, Paterson CA. Expression of sarco/endoplasmic reticular Ca2+-ATPase in human lens epithelial cells and cultured human lens epithelial B-3 cells. Curr Eye Res 1999;19:389–94.
   PubMed Web of Science ®Google Scholar
• Launay S, Gianni M, Kova`cs T, Bredoux R, Bruel A, Ge´le´bart P, Zassadowski F, Chomienne C, Enouf J, Papp B. Lineage-specific modulation of calcium pump expression during myeloid differentiation. Blood 1999;93:4395–405.
   PubMed Web of Science ®Google Scholar
• Reinhardt TA, Horst RL. Ca2þ-ATPases and their expression in the mammary gland of pregnant and lactating rats. Am J Physiol 1999;276:C796–802.
   Google Scholar
• Mountian I, Manolopoulos VG, De Smedt H, Parys JB, Missiaen L, Wuytack F. Expression patterns of sarco/endoplasmic reticulum Ca2þ-ATPase and inositol 1,4,5-trisphosphate receptor isoforms in vascular endothelial cells. Cell Calcium 1999;25:371–80.
   PubMedGoogle Scholar
• Caspersen C, Pedersen PS, Treiman M. The sarco-endoplas-mic reticulum calcium-ATPase 2b is an endoplasmic reticulum stress-inducible protein. J Biol Chem 2000; 275:22363–72.
   PubMed Web of Science ®Google Scholar
• Khan I, Sandhu V, Misquitta CM, Grover AK. SERCA pump isoform expression in endothelium of veins and arteries: every endothelium is not the same. Mol Cell Biochem 2000; 203:11–15.
   PubMedGoogle Scholar
• Martin V, Bredoux R, Corvazier E, Papp B, Enouf J. Platelet Ca2þATPases: a plural, species-specific, and multiple hypertension-regulated expression system. Hypertension 2000;35:91–02.
   PubMed Web of Science ®Google Scholar
• Magnino F, St-Pierre M, Luthi M, Hilly M, Mauger JP, Dufour JF. Expression of intracellular calcium channels and pumps after partial hepatectomy in rat. Mol Cell Biol Res Commun 2000;3:374–79.
   PubMedGoogle Scholar
• Hughes PJ, McLellan H, Lowes DA, Kahn SZ, Bilmen JG, Tovey SC, Godfrey RE, Michell RH, Kirk CJ, Michelangeli F. Estrogenic alkylphenols induce cell death by inhibiting testis endoplasmic reticulum Ca2þ pumps. Biochem Biophys Res Commun 2000;277:568–74.
   PubMed Web of Science ®Google Scholar
• Pottorf WJ, De Leon DD, Hessinger DA, Buchholz JN. Function of SERCA mediated calcium uptake and expression of SERCA3 in cerebral cortex from young and old rats. Brain Res 2001;914:57–65.
   PubMedGoogle Scholar
• Ge´le´bart P, Kova`cs T, Brouland JP, van Gorp R, Grossmann J, Rivard N, Panis Y, Martin V, Bredoux R, Enouf J, Papp B. Expression of endomembrane calcium pumps in colon and gastric cancer cells. Induction of SERCA3 expression during differentiation. J Biol Chem 2002;277:26310–20.
   Google Scholar
• Liu L, Paterson CA, Borchman D. Regulation of sarco/ endoplasmic Ca2þ-ATPase expression by calcium in human lens cells. Exp Eye Res 2002;75:583–90.
   PubMedGoogle Scholar
• Pacifico F, Ulianich L, De Micheli S, Treglia S, Leonardi A, Vito P, Formisano S, Consiglio E, Di Jeso B. The expression of the sarco/endoplasmic reticulum Ca2þ-ATPases in thyroid and its down-regulation following neoplastic transformation. J Mol Endocrinol 2003;30:399–09.
   PubMedGoogle Scholar
• Pan Y, Zvaritch E, Tupling AR, Rice WJ, de Leon S, Rudnicki M, McKerlie C, Banwell BL, MacLennan DH. Targeted disruption of the ATP2A1 gene encoding the sarco(endo)plasmic reticulum Ca2þATPase isoform 1 (SERCA1) impairs diaphragm function and is lethal in neonate mice. J Biol Chem 2003;278:13367–75.
   PubMedGoogle Scholar
• Xu GG, Gao Z, Borge PD Jr, Jegier PA, Young RA, Wolf BA. Insulin regulation of beta-cell function involves a feedback loop on SERCA gene expression, Ca2þ homeostasis, and insulin expression and secretion. Biochemistry 2000;39:14912–19.
   PubMed Web of Science ®Google Scholar
• Goellner GM, DeMarco SJ, Strehler EE. Characterization of PISP, a novel single-PDZ protein that binds to all plasma membrane Ca2þ-ATPase b-splice variants. Ann NY Acad Sci 2003;986:461–71.
   PubMedGoogle Scholar
• Schuh K, Uldrijan S, Telkamp M, Rothlein N, Neyses L. The plasma membrane calmodulin-dependent calcium pump: a major regulator of nitric oxide synthase I. J Cell Biol 2001;155:201–05.
   PubMedGoogle Scholar
• Schuh K, Uldrijan S, Gambaryan S, Roethlein N, Neyses L. Interaction of the plasma membrane Ca2þ pump 4b/CI with the Ca2þ/calmodulin-dependent membrane-associated kinase CASK. J Biol Chem 2003;278:9778–83.
   PubMedGoogle Scholar
• DeMarco SJ, Chicka MC, Strehler EE. Plasma membrane Ca2þATPase isoform 2b interacts preferentially with Naþ/Hþ exchanger regulatory factor 2 in apical plasma membranes. J Biol Chem 2002;277:10506–11.
   PubMed Web of Science ®Google Scholar
• Chen J, McLean PA, Neel BG, Okunade G, Shull GE, Wortis HH. CD22 attenuates calcium signalling by potentiating plasma membrane calcium-ATPase activity. Nat Immunol 2004;5:651–57.
   PubMed Web of Science ®Google Scholar
• Armesilla AL, Williams JC, Buch MH, Pickard A, Emerson M, Cartwright EJ, Oceandy D, Vos MD, Gillies S, Clark GJ, Neyses L. Novel functional interaction between the plasma membrane Ca2þ pump 4b and the proapoptotic tumor suppressor Ras-associated factor 1 (RASSF1). J Biol Chem 2004;279:31318–28.
   PubMed Web of Science ®Google Scholar
• Papp B, Sarkadi B, Enyedi A, Caride AJ, Penniston JT, Ga`rdos G. Functional domains of the in situ red cell membrane calcium pump revealed by proteolysis and monoclonal antibodies. J Biol Chem 1989;264:4577–82.
   PubMedGoogle Scholar
• Schwab BL, Guerini D, Didszun C, Bano D, Ferrando-May E, Fava E, Tam J, Xu D, Xanthoudakis S, Nicholson DW, Carafoli E, Nicotera P. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ 2002;9:818–31
   PubMed Web of Science ®Google Scholar
• Chami M, Ferrari D, Nicotera P, Paterlini-Brechot P, Rizzuto R. Caspase-dependent alterations of Ca2þ signaling in the induction of apoptosis by hepatitis B virus X protein. J Biol Chem 2003;278:31745–55.
   PubMedGoogle Scholar
• Pa`szty K, Verma AK, Padanyi R, Filoteo AG, Penniston JT, Enyedi A. Plasma membrane Ca2þATPase isoform 4b is cleaved and activated by caspase-3 during the early phase of apoptosis. J Biol Chem 2002;277:6822–29.
   PubMedGoogle Scholar
• Stefanovic B, Stefanovic L, Schnabl B, Bataller R, Brenner DA. TRAM2 protein interacts with endoplasmic reticulum Ca2þ pump SERCA2b and is necessary for collagen type I synthesis. Mol Cell Biol 2004;24:1758–68.
   PubMedGoogle Scholar
• Dode L, Vilsen B, Van Baelen K, Wuytack F, Clausen JD, Andersen JP. Dissection of the functional differences between sarco(endo)plasmic reticulum Ca2þ-ATPase (SERCA) 1 and 3 isoforms by steady-state and transient kinetic analyses. J Biol Chem 2002;277:45579–91.
   PubMed Web of Science ®Google Scholar
• Kulkarni RN, Roper MG, Dahlgren G, Shih DQ, Kauri LM, Peters JL, Stoffel M, Kennedy RT. 1slet secretory defect in insulin receptor substrate 1 null mice is linked with reduced calcium signaling and expression of sarco(endo)plasmic reticulum Ca2þ-ATPase (SERCA)-2b and -3. Diabetes 2004;53:1517–25.
   PubMed Web of Science ®Google Scholar
• Papp B, Enyedi A, Kova`cs T, Sarkadi B, Wuytack F, Thastrup O, Ga`rdos G, Bredoux R, Le´vy-Tole´dano S, Enouf J. Demonstration of two forms of calcium pumps by thapsigargin inhibition and radioimmunoblotting in platelet membrane vesicles. J Biol Chem 1991;266:14593–96.
   PubMed Web of Science ®Google Scholar
• Papp B, Enyedi A, Pa`szty K, Kova`cs T, Sarkadi B, Ga`rdos G, Magnier C, Wuytack F, Enouf J. Simultaneous presence of two distinct endoplasmic-reticulum-type calcium-pump isoforms in human cells. Biochem J 1992;288:297–02.
   PubMedGoogle Scholar
• Enouf J, Bredoux R, Papp B, Djaffar I, Lompre´ AM, Kieffer N, Gayet O, Clemetson K, Wuytack F, Rosa JP. Human platelets express the SERCA2b isoform of Ca2þ-transport ATPase. Biochem J 1992;286:135–40.
   PubMed Web of Science ®Google Scholar
• Papp B, Corvazier E, Magnier C, Kova`cs T, Bourdeau N, Le´vy-Tole´dano S, Bredoux R, Le´vy B, Poitevin P, Lompre´ AM, Wuytack F, Enouf J. Spontaneously hypertensive rats and platelet Ca2þ-ATPases: specific up-regulation of the 97kDa isoform. Biochem J 1993;295:685–90.
   PubMed Web of Science ®Google Scholar
• Enouf J, Corvazier E, Papp B, Quarck R, Magnier C, Kova`cs T, Bredoux R, Le´vy-Tole´dano S, de Gunzburg J, Wuytack F, Caen J. Abnormal cAMP-induced phosphorylation of Rap 187. protein in grey platelet syndrome platelets. Br J Haematol 1994;86:338–46.
   Google Scholar
• Kova`cs T, Corvazier E, Papp B, Magnier C, Bredoux R, Enyedi A, Sarkadi B, Enouf J. Controlled proteolysis of Ca2þ-ATPases in human platelet and non-muscle cell membrane vesicles. J Biol Chem 1994;269:6177–84.
   PubMedGoogle Scholar
• Cheng HY, Magocsi M, Cooper RS, Penniston JT, Borke JL. Expression of plasma membrane Ca2þ-pump epitopes in human platelets and megakaryoblasts. Cell Physiol Biochem 1994;4:31–43.
   Google Scholar
• Magnier C, Corvazier E, Aumont MC, Le Jemtel TH, Enouf J. Relationship between Rap1 protein phosphorylation and regulation of Ca2þ transport in platelets: a new approach. Biochem J 1995;310:469–75.
   PubMedGoogle Scholar
• Dean WL, Quinton TM. Distribution of plasma membrane Ca2þ-ATPase and inositol 1,4,5-trisphosphate receptor in human platelet membranes. Cell Calcium 1995;17:65–70.
   PubMed Web of Science ®Google Scholar
• Kova`cs T, Berger G, Corvazier E, Pa`szty K, Brown A, Bobe R, Papp B, Wuytack F, Cramer EM, Enouf J. Immunolocalization of the multi-sarco/endoplasmic reticulum Ca2þATPase system in human platelets. Br J Haematol 1997;97:192–03.
   PubMedGoogle Scholar
• Dean WL, Chen D, Brandt PC, Vanaman TC. Regulation of platelet plasma membrane Ca2þ-ATPase by cAMP-dependent and tyrosine phosphorylation. J Biol Chem 1997;272:15113–19.
   PubMedGoogle Scholar
• Authi KS. Ca2þ Homeostasis in human platelets. In: von Bruchhhausen F, Walter U, editors. Handbook of experimental pharmacology. Vol. 126. Berlin Heidelberg, Germany: Springer-Verlag; 1997.
   Google Scholar
• Bobe R, Lacabaratz-Porret C, Bredoux R, Martin V, Ozog A, Launay S, Corvazier E, Kova`cs T, Papp B, Enouf J. Expression of two isoforms of the third sarco/endoplasmic reticulum Ca2þATPase (SERCA3) in platelets. Possible recognition of the SERCA3b isoform by the PL/IM430 monoclonal antibody. FEBS Lett 1998;423:259–64.
   Google Scholar
• Feijge MAH, Lacabaratz-Porret C, van Pampus ECM, Hamulya`k K, Le´vy-Tole´dano S, Enouf J, Heemskerk JWM. Contribution of thromboxane and endomembrane Ca2þ-ATPases to variability in Ca2þ signalling of platelets from healthy volunteers. Platelets 1998;9:179–83.
   PubMed Web of Science ®Google Scholar
• Feijge MAH, van Pampus ECM, Lacabaratz-Porret C, Hamulya`k K, Le´vy-Tole´dano S, Enouf J, Heemskerk JWM. Inter-individual variability in Ca2þ signalling in platelets from healthy volunteers: effects of aspirin and relationship with expression of endomembrane Ca2þ-ATPases. Br J Haematol 1998;102:850–59.
   PubMed Web of Science ®Google Scholar
• Pa`szty K, Kova`cs T, Lacabaratz-Porret C, Papp B, Enouf J, Filoteo AG, Penniston JT, Enyedi A. Expression of hPMCA4b, the major form of the plasma membrane calcium pump in megakaryoblastoid cells is greatly reduced in mature human platelets. Cell Calcium 1998;24:129–35.
   Google Scholar
• Lacabaratz-Porret C, Corvazier E, Kova`cs T, Bobe R, Bredoux R, Launay S, Papp B, Enouf J. Platelet sarco/ endoplasmic reticulum Ca +ATPase isoform 3b and Rap 1b: interrelation and regulation in physiopathology. Biochem J 1998;332:173–81.
   PubMedGoogle Scholar
• Lacabaratz-Porret C, Launay S, Corvazier E, Bredoux R, Papp B, Enouf J. Biogenesis of endoplasmic reticulum proteins involved in Ca + signalling during megakaryocytic differentiation: an in vitro study. Biochem J 2000;350:723–34.
   PubMed Web of Science ®Google Scholar
• Blankenship KA, Dawson CB, Aronoff GR, Dean WL. Tyrosine phosphorylation of human platelet plasma membrane Ca +-ATPase in hypertension. Hypertension 2000;35:103–07.
   PubMed Web of Science ®Google Scholar
• Zabe M, Dean WL. Plasma membrane Ca +-ATPase associates with the cytoskeleton in activated platelets through a PDZ-binding domain. J Biol Chem 2001;276:14704–09.
   PubMed Web of Science ®Google Scholar
• Wan TC, Zabe M, Dean WL. Plasma membrane Ca +-ATPase isoform 4b is phosphorylated on tyrosine 1176 in activated human platelets. Thromb Haemost 2003;89:122–31.
   PubMed Web of Science ®Google Scholar
• Dean WL, Whiteheart SW. Plasma membrane Ca +-ATPase (PMCA) translocates to filopodia during platelet activation. Thromb Haemost 2004;91:325–33.
   PubMed Web of Science ®Google Scholar
• Mountian I, Baba-Aissa F, Jonas JC, de Smedt H, Wuytack F, Parys JB. Expression of Ca + transport genes in platelets and endothelial cells in hypertension. Hypertension 2001;37:135–41.
   PubMedGoogle Scholar
• Inoue O, Suzuki-Inoue K, Dean WL, Frampton J, Watson SP. Integrin alpha2beta1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLCy2. J Cell Biol 2003;160:769–80.
   PubMed Web of Science ®Google Scholar
• Rosado JA, Sage SO. Regulation of plasma membrane Ca +-ATPase by small GTPases and phosphoinositides in human platelets. J Biol Chem 2000;275:19529–35.
   PubMed Web of Science ®Google Scholar
• Lacabaratz C, Corvazier E, Kova`cs T, Bobe R, Wuytack F, Papp B, Enouf J. The PL/IM 430 and the N 89 antibodies recognize two distinct 97 kDa sarco/endoplas-mic-reticulum Ca +-ATPase proteins. Biochem J 1996; 318:359–60.
   PubMed Web of Science ®Google Scholar
• Rosado JA, Lopez JJ, Harper AG, Harper MT, Redondo PC, Pariente JA, Sage SO, Salido GM. Two pathways for store-mediated calcium entry differentially dependent on the actin cytoskeleton in human platelets. J Biol Chem 2004;279:29231–35.
   PubMed Web of Science ®Google Scholar
• Wan TC, Dean WL. Decreased PMCA4b expression has no effect on calcium homeostasis in Meg-01 cells. Platelets 2003;14:295–03.
   PubMed Web of Science ®Google Scholar