The ATP2B Plasma Membrane Ca2+ ATPase Family: Regulation in Response to Changing Demands of Cellular Calcium Transport

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Regulation of Ca2+-ATPases,V-ATPases and F-ATPases

Part of the book series: Advances in Biochemistry in Health and Disease ((ABHD,volume 14))

Abstract

The mammalian ATP2B family of plasma membrane calcium ATPases (PMCAs) consists of over 30 members generated from four genes and via complex alternative RNA splicing. Regulation occurs at the level of ATP2B gene transcription, splicing, translation, and posttranslational modification. PMCA isoforms and splice variants vary in their functional properties and are differentially regulated by intrinsic factors such as calmodulin and lipids, as well as by dynamic interaction with a large number of scaffolding and signaling proteins. A major emerging theme is the functional integration of different PMCAs in multiprotein complexes to allow reciprocal cross talk between localized PMCA-mediated Ca2+ control and the function of other members in the complex. The same PMCA isoform may be responsible for bulk calcium export in the cells of one tissue but control the local activity of a signaling microdomain in the cells of another. Regulation of the PMCAs must therefore be understood in the physiological context of the tissues and cells where they are expressed.

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References

  1. Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21

    Article  CAS  PubMed  Google Scholar 

  2. Brini M, Carafoli E (2000) Calcium signalling: a historical account, recent developments and future perspectives. Cell Mol Life Sci 57:354–370

    Article  CAS  PubMed  Google Scholar 

  3. Pedersen PL, Carafoli E (1987) Ion motive ATPases. I. Ubiquity, properties, and significance to cell function. Trends Biochem Sci 12:146–150

    Article  CAS  Google Scholar 

  4. Palmgren MG, Nissen P (2011) P-type ATPases. Annu Rev Biophys 40:243–266

    Article  CAS  PubMed  Google Scholar 

  5. Thever MD, Saier MH (2009) Bioinformatic characterization of P-type ATPases encoded within the fully sequenced genomes of 26 eukaryotes. J Membr Biol 229:115–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Strehler EE, Treiman M (2004) Calcium pumps of plasma membrane and cell interior. Curr Mol Med 4:323–335

    Article  CAS  PubMed  Google Scholar 

  7. Silverstein RS, Tempel BL (2006) Atp2b2, encoding plasma membrane Ca2+-ATPase type 2, (PMCA2) exhibits tissue-specific first exon usage in hair cells, neurons, and mammary glands of mice. Neuroscience 141:245–257

    Article  CAS  PubMed  Google Scholar 

  8. Carafoli E (1992) The Ca2+ pump of the plasma membrane. J Biol Chem 267:2115–2118

    CAS  PubMed  Google Scholar 

  9. Strehler EE, Zacharias DA (2001) Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol Rev 81:21–50

    CAS  PubMed  Google Scholar 

  10. Dumont RA, Lins U, Filoteo AG et al (2001) Plasma membrane Ca2+ ATPase isoform 2a is the PMCA of hair bundles. J Neurosci 21:5066–5078

    CAS  PubMed  Google Scholar 

  11. Bublitz M, Poulsen H, Morth JP, Nissen P (2010) In and out of the cation pumps: P-type ATPase structure revisited. Curr Opin Struct Biol 20:431–439

    Article  CAS  PubMed  Google Scholar 

  12. Brodin P, Falchetto R, Vorherr T, Carafoli E (1992) Identification of two domains which mediate the binding of activating phospholipids to the plasma-membrane Ca2+ pump. Eur J Biochem 204:939–946

    Article  CAS  PubMed  Google Scholar 

  13. Carafoli E (1994) Biogenesis: plasma membrane calcium ATPase: 15 years of work on the purified enzyme. FASEB J 8:993–1002

    CAS  PubMed  Google Scholar 

  14. Hilfiker H, Guerini D, Carafoli E (1994) Cloning and expression of isoform 2 of the human membrane Ca2+ ATPase. J Biol Chem 269:26178–26183

    CAS  PubMed  Google Scholar 

  15. Brini M, Di Leva F, Ortega CK et al (2010) Deletions and mutations in the acidic lipid-binding region of the plasma membrane Ca2+ pump. J Biol Chem 285:30779–30791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Chicka MC, Strehler EE (2003) Alternative splicing of the first intracellular loop of plasma membrane Ca2+-ATPase isoform 2 alters its membrane targeting. J Biol Chem 278:18464–18470

    Article  CAS  PubMed  Google Scholar 

  17. Penniston JT, Padányi R, Pászty K et al (2014) Apart from its known function, the plasma membrane Ca2+ ATPase can regulate Ca2+ signaling by controlling phosphatidylinositol 4,5-bisphosphate levels. J Cell Sci 127:72–84

    Article  CAS  PubMed  Google Scholar 

  18. Krebs J (2015) The plethora of PMCA isoforms: alternative splicing and differential expression. Biochim Biophys Acta 1853:2018-2024

    Google Scholar 

  19. Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89:1341–1378

    Article  CAS  PubMed  Google Scholar 

  20. Strehler EE, Filoteo AG, Penniston JT, Caride AJ (2007) Plasma-membrane Ca2+-pumps: structural diversity as the basis for functional versatility. Biochem Soc Trans 35:919–922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Strehler EE (2013) Plasma membrane calcium ATPases as novel candidates for therapeutic agent development. J Pharm Pharm Sci 16:190–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Giacomello M, De Mario A, Scarlatti C et al (2013) Plasma membrane calcium ATPases and related disorders. Int J Biochem Cell Biol 45:753–762

    Article  CAS  PubMed  Google Scholar 

  23. Ritchie MF, Zhou Y, Soboloff J (2011) Transcriptional mechanisms regulating Ca2+ homeostasis. Cell Calcium 49:314–321

    Article  CAS  PubMed  Google Scholar 

  24. Naranjo JR, Mellstrom B (2012) Ca2+-dependent transcriptional control of Ca2+ homeostasis. J Biol Chem 287:31674–31680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Yanagida E, Shoji S, Hirayama Y et al (2004) Functional expression of Ca2+ signaling pathways in mouse embryonic stem cells. Cell Calcium 36:135–146

    Article  CAS  PubMed  Google Scholar 

  26. Zacharias DA, Kappen C (1999) Developmental expression of the four plasma membrane calcium ATPase (Pmca) genes in the mouse. Biochim Biophys Acta 1428:397–405

    Article  CAS  PubMed  Google Scholar 

  27. Okunade GW, Miller ML, Pyne GJ et al (2004) Targeted ablation of plasma membrane Ca2+-ATPase (PMCA) 1 and 4 indicates a major housekee** function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4. J Biol Chem 279:33742–33750

    Article  CAS  PubMed  Google Scholar 

  28. Afroze T, Husain M (2000) c-myb-Binding sites mediate G1/S-associated repression of the plasma membrane Ca2+-ATPase-1 promoter. J Biol Chem 275:9062–9069

    Article  CAS  PubMed  Google Scholar 

  29. Habib T, Park H, Tsang M et al (2007) Myc stimulates B lymphocyte differentiation and amplifies calcium signaling. J Cell Biol 179:717–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Du Y, Carlock L, Kuo TH (1995) The mouse plasma membrane Ca2+ pump isoform 1 promoter: cloning and characterization. Arch Biochem Biophys 316:302–310

    Article  CAS  PubMed  Google Scholar 

  31. Kuo TH, Liu B-F, Diglio C, Tsang W (1993) Regulation of the plasma membrane calcium pump gene expression by two signal transduction pathways. Arch Biochem Biophys 305:428–433

    Article  CAS  PubMed  Google Scholar 

  32. Zelinski JM, Sykes DE, Weiser MW (1991) The effect of Vitamin D on rat intestinal plasma membrane Ca-pump mRNA. Biochem Biophys Res Commun 179:749–755

    Article  CAS  PubMed  Google Scholar 

  33. Cai Q, Chandler JS, Wasserman RH et al (1993) Vitamin D and adaptation to dietary calcium and phosphate deficiencies increase intestinal plasma membrane calcium pump expression. Proc Natl Acad Sci U S A 90:1345–1349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Pannabecker TL, Chandler JS, Wasserman RH (1995) Vitamin-D-dependent transcriptional regulation of the intestinal plasma membrane calcium pump. Biochem Biophys Res Commun 213:499–505

    Article  CAS  PubMed  Google Scholar 

  35. Glendenning P, Ratajczak T, Dick IM, Prince RL (2000) Calcitriol upregulates expression and activity of the 1b isoform of the plasma membrane calcium pump in immortalized distal kidney tubular cells. Arch Biochem Biophys 380:126–132

    Article  CAS  PubMed  Google Scholar 

  36. Glendenning P, Ratajczak T, Dick IM, Prince RL (2001) Regulation of the 1b isoform of the plasma membrane calcium pump by 1,25-dihydroxyvitamin D3 in rat osteoblast-like cells. J Bone Miner Res 16:525–534

    Article  CAS  PubMed  Google Scholar 

  37. Guerini D, Wang X, Li L, Genazzani A, Carafoli E (2000) Calcineurin controls the expression of isoform 4CII of the plasma membrane Ca2+ pump in neurons. J Biol Chem 275:3706–3712

    Article  CAS  PubMed  Google Scholar 

  38. Du X, Wang J, Zhu H et al (1999) Second cistron in CACNA1A gene encodes a transcription factor mediating cerebellar development and SCA6. Cell 154:118–133

    Article  CAS  Google Scholar 

  39. Reinhardt TA, Horst RL (1999) Ca2+-ATPases and their expression in the mammary gland of pregnant and lactating rats. Am J Physiol 276:C796–C802

    CAS  PubMed  Google Scholar 

  40. Reinhardt TA, Filoteo AG, Penniston JT, Horst RL (2000) Ca2+-ATPase protein expression in mammary tissue. Am J Physiol Cell Physiol 279:C1595–C1602

    CAS  PubMed  Google Scholar 

  41. Ayoubi TA, Van de Ven WJM (1995) Regulation of gene expression by alternative promoters. FASEB J 10:453–460

    Google Scholar 

  42. Hill JK, Williams DE, LeMasurier DE et al (2006) Splice-site A choice targets plasma-membrane Ca2+-ATPase isoform 2 to hair bundles. J Neurosci 26:6172–6180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kip SN, Gray NW, Burette A et al (2006) Changes in the expression of plasma membrane calcium extrusion systems during the maturation of hippocampal neurons. Hippocampus 16:20–34

    Article  CAS  PubMed  Google Scholar 

  44. Afroze T, Ge Y, Khoshbin A et al (2014) Calcium efflux activity of plasma membrane Ca2+ ATPase-4 (PMCA4) mediates cell cycle progression in vascular smooth muscle cells. J Biol Chem 289:7221–7231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zacharias DA, Strehler EE (1996) Change in plasma membrane Ca2+-ATPase splice-variant expression in response to a rise in intracellular Ca2+. Curr Biol 6:1642–1652

    Article  CAS  PubMed  Google Scholar 

  46. Grabowski PJ, Black DL (2001) Alternative RNA splicing in the nervous system. Prog Neurobiol 65:289–308

    Article  CAS  PubMed  Google Scholar 

  47. Li Q, Lee J-A, Black DL (2007) Neuronal regulation of alternative pre-mRNA splicing. Nat Rev Neurosci 8:819–831

    Article  CAS  PubMed  Google Scholar 

  48. **e J, Black DL (2001) A CaMK IV-responsive RNA element mediates depolarization-induced alternative splicing of potassium channels. Nature 410:936–939

    Article  CAS  PubMed  Google Scholar 

  49. Liu G, Razanau A, Hai Y et al (2012) A conserved serine of heterogeneous nuclear ribonucleoprotein L (hnRNPL) mediates depolarization-regulated alternative splicing of potassium channels. J Biol Chem 287:22709–22716

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Kosiorek M, Podszywalow-Bartnicka P, Zylinska L, Pikula S (2014) NFAT1 and NFAT3 cooperate with HDAC4 during regulation of alternative splicing of PMCA isoforms in PC12 cells. PLoS One 9:e99116

    Article  CAS  Google Scholar 

  51. Greeb J, Shull GE (1989) Molecular cloning of a third isoform of the calmodulin-sensitive plasma membrane Ca2+-transporting ATPase that is expressed predominantly in brain and skeletal muscle. J Biol Chem 264:18569–18576

    CAS  PubMed  Google Scholar 

  52. De Jaegere S, Wuytack F, Eggermont JA et al (1990) Molecular cloning and sequencing of the plasma-membrane Ca2+ pump of pig smooth muscle. Biochem J 271:655–660

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kuo TH, Wang KKW, Carlock L et al (1991) Phorbol ester induces both gene expression and phosphorylation of the plasma membrane Ca2+ pump. J Biol Chem 266:2520–2525

    CAS  PubMed  Google Scholar 

  54. Husain M, Jiang L, See V et al (1997) Regulation of vascular smooth muscle cell proliferation by plasma membrane Ca2+-ATPase. Am J Physiol 272:C1947–C1959

    CAS  PubMed  Google Scholar 

  55. Sasamura S, Furukawa K-I, Shiratori M et al (2002) Antisense-inhibition of plasma membrane Ca2+ pump induces apoptosis in vascular smooth muscle cells. Jpn J Pharmacol 90:164–172

    Article  CAS  PubMed  Google Scholar 

  56. Szemraj J, Kawecka I, Bartkowiak J, Zylinska L (2004) The effect of antisense oligonucleotide treatment of plasma membrane Ca2+-ATPase in PC12 cells. Cell Mol Biol Lett 9:451–464

    CAS  PubMed  Google Scholar 

  57. Kurnellas MP, Li H, Jain MR et al (2010) Reduced expression of plasma membrane calcium ATPase 2 and collapsin response mediator protein 1 promotes death of spinal cord neurons. Cell Death Differ 17:1501–1510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Curry MC, Luk NA, Kenny PA et al (2012) Distinct regulation of cytoplasmic calcium signals and cell death pathways by different plasma membrane calcium ATPase isoforms in MDA-MB-231 breast cancer cells. J Biol Chem 287:28598–28608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Jensen TP, Filoteo AG, Knöpfel T, Empson RM (2007) Presynaptic plasma membrane Ca2+ ATPase isoform 2a regulates excitatory synaptic transmission in rat hippocampal CA3. J Physiol 579(1):85–99

    Article  CAS  PubMed  Google Scholar 

  60. Burette AC, Strehler EE, Weinberg RJ (2009) “Fast” plasma membrane calcium pump PMCA2a concentrates in GABAergic terminals in the adult rat brain. J Comp Neurol 512:500–513

    Article  PubMed  PubMed Central  Google Scholar 

  61. Burette AC, Strehler EE, Weinberg RJ (2010) A plasma membrane Ca2+ ATPase isoform at the postsynaptic density. Neuroscience 169:987–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Guerini D, Pan B, Carafoli E (2003) Expression, purification, and characterization of isoform 1 of the plasma membrane Ca2+ pump. J Biol Chem 278:38141–38148

    Article  CAS  PubMed  Google Scholar 

  63. Brown CS, Dean W (2007) Regulation of plasma membrane Ca2+-ATPase in human platelets by calpain. Platelets 18:207–211

    Article  CAS  PubMed  Google Scholar 

  64. Lehotsky J, Kaplan P, Murin R, Raeymaekers L (2002) The role of plasma membrane Ca2+ pump (PMCA) in pathologies of mammalian cells. Front Biosci 7:d53–d84

    CAS  PubMed  Google Scholar 

  65. Pottorf WJ II, Johanns TM, Derrington SM et al (2006) Glutamate-induced protease-mediated loss of plasma membrane Ca2+ pump activity in rat hippocampal neurons. J Neurochem 98:1646–1656

    Article  CAS  PubMed  Google Scholar 

  66. Ferragamo MJ, Reinardy JL, Thayer SA (2009) Ca2+-dependent, stimulus-specific modulation of the plasma membrane Ca2+ pump in hippocampal neurons. J Neurophysiol 101:2563–2571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zaidi A, Michaelis ML (1999) Effects of reactive oxygen species on brain synaptic plasma membrane Ca2+-ATPase. Free Radic Biol Med 27:810–821

    Article  CAS  PubMed  Google Scholar 

  68. Jiang L, Bechtel MD, Galeva NA et al (2012) Decreases in plasma membrane Ca2+-ATPase in brain synaptic membrane rafts from aged rats. J Neurochem 123:689–699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Zaidi A (2010) Plasma membrane Ca2+-ATPases: targets of oxidative stress in brain aging and neurodegeneration. World J Biol Chem 1:271–280

    Article  PubMed  PubMed Central  Google Scholar 

  70. González Flecha FL, Castello PR, Gagliardino JJ, Rossi JP (1999) Molecular characterization of the glycated plasma membrane calcium pump. J Membr Biol 171:25–34

    Article  PubMed  Google Scholar 

  71. Horakova L, Strosova MK, Spickett CM, Blaskovic D (2013) Impairment of calcium ATPases by high glucose and potential pharmacological protection. Free Radic Res 47:81–92

    Article  CAS  PubMed  Google Scholar 

  72. Patel R, Al-Dossary AA, Stabley DL et al (2013) Plasma membrane Ca2+-ATPase 4 in murine epididymis: secretion of splice variants in the luminal fluid and a role in sperm maturation. Biol Reprod 89:1–11

    Article  CAS  Google Scholar 

  73. Al-Dossary AA, Strehler EE, Martin-DeLeon PA (2013) Expression and secretion of plasma membrane Ca2+-ATPase 4a (PMCA4a) during murine estrus: association with oviductal exosomes and uptake in sperm. PLoS One 8:e80181

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  74. James PH, Pruschy M, Vorherr T et al (1989) Primary structure of the cAMP-dependent phosphorylation site of the plasma membrane calcium pump. Biochemistry 28:4253–4258

    Article  CAS  PubMed  Google Scholar 

  75. Wang KKW, Wright LC, Machan C et al (1991) Protein kinase C phosphorylates the carboxyl terminus of the plasma membrane Ca2+-ATPase from human erythrocytes. J Biol Chem 266:9078–9085

    CAS  PubMed  Google Scholar 

  76. Hofmann F, Anagli J, Carafoli E, Vorherr T (1994) Phosphorylation of the calmodulin binding domain of the plasma membrane Ca2+ pump by protein kinase C reduces interaction with calmodulin and with its pump receptor site. J Biol Chem 269:24298–24303

    CAS  PubMed  Google Scholar 

  77. Enyedi A, Elwess NL, Filoteo AG et al (1997) Protein kinase C phosphorylates the “a” forms of plasma membrane Ca2+ pump isoforms 2 and 3 and prevents binding of calmodulin. J Biol Chem 272:27525–27528

    Article  CAS  PubMed  Google Scholar 

  78. Enyedi A, Verma AK, Filoteo AG, Penniston JT (1996) Protein kinase C activates the plasma membrane Ca2+ pump isoform 4b by phosphorylation of an inhibitory region downstream of the calmodulin-binding domain. J Biol Chem 271:32461–32467

    Article  CAS  PubMed  Google Scholar 

  79. Verma AK, Paszty K, Filoteo AG et al (1999) Protein kinase C phosphorylates plasma membrane Ca2+ pump isoform 4a at its calmodulin binding domain. J Biol Chem 274:527–531

    Article  CAS  PubMed  Google Scholar 

  80. Zylinska L, Guerini D, Gromadzinska E, Lachowicz L (1998) Protein kinases A and C phosphorylate purified Ca2+-ATPase from rat cortex, cerebellum and hippocampus. Biochim Biophys Acta 1448:99–108

    Article  CAS  PubMed  Google Scholar 

  81. Dean WL, Chen D, Brandt PC, Vanaman TC (1997) Regulation of platelet plasma membrane Ca2+-ATPase by cAMP-dependent and tyrosine phosphorylation. J Biol Chem 272:15113–15119

    Article  CAS  PubMed  Google Scholar 

  82. Wan TC, Zabe M, Dean WL (2003) Plasma membrane Ca2+-ATPase isoform 4b is phosphorylated on tyrosine 1176 in activated human platelets. Thromb Haemost 89:122–131

    CAS  PubMed  Google Scholar 

  83. Dean WL (2010) Role of platelet plasma membrane Ca2+-ATPase in health and disease. World J Biol Chem 1:265–270

    Article  PubMed  PubMed Central  Google Scholar 

  84. Wang KKW, Villalobo A, Roufogalis BD (1992) The plasma membrane calcium pump: a multiregulated transporter. Trends Cell Biol 2:46–52

    Article  CAS  PubMed  Google Scholar 

  85. Monteith GR, Roufogalis BD (1995) The plasma membrane calcium pump—a physiological perspective on its regulation. Cell Calcium 18:459–470

    Article  CAS  PubMed  Google Scholar 

  86. Penniston JT, Enyedi A (1998) Modulation of the plasma membrane Ca2+ pump. J Membr Biol 165:101–109

    Article  CAS  PubMed  Google Scholar 

  87. Schatzmann HJ (1982) The plasma membrane calcium pump of erythrocytes and other animal cells. In: Carafoli E (ed) Membrane transport of calcium. Academic, London, pp 41–108

    Google Scholar 

  88. Penniston JT (1983) Plasma membrane Ca2+-ATPases as active Ca2+ pumps. In: Cheung WY (ed) Calcium and cell function. Academic, New York, pp 99–147

    Google Scholar 

  89. Carafoli E (1991) Calcium pump of the plasma membrane. Physiol Rev 71:129–153

    CAS  PubMed  Google Scholar 

  90. Caride AJ, Filoteo AG, Penheiter AR et al (2001) Delayed activation of the plasma membrane calcium pump by a sudden increase in Ca2+: fast pumps reside in fast cells. Cell Calcium 30:49–57

    Article  CAS  PubMed  Google Scholar 

  91. Caride AJ, Penheiter AR, Filoteo AG et al (2001) The plasma membrane calcium pump displays memory of past calcium spikes. Differences between isoforms 2b and 4b. J Biol Chem 276:39797–39804

    Article  CAS  PubMed  Google Scholar 

  92. Caride AJ, Filoteo AG, Penniston JT, Strehler EE (2007) The plasma membrane Ca2+ pump isoform 4a differs from isoform 4b in the mechanism of calmodulin binding and activation kinetics. J Biol Chem 282:25640–25648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Niggli V, Adunyah ES, Carafoli E (1981) Acidic phospholipids, unsaturated fatty acids and proteolysis mimic the effect of calmodulin on the purified erythrocyte Ca2+-ATPase. J Biol Chem 256:8588–8592

    CAS  PubMed  Google Scholar 

  94. Missiaen L, Raeymaekers L, Wuytack F et al (1989) Phospholipid-protein interactions of the plasma-membrane Ca2+-transporting ATPase. Biochem J 263:287–294

    Article  Google Scholar 

  95. Rossi JP, Delfino JM, Caride AJ, Fernándes HN (1995) Interaction of unsaturated fatty acids with the red blood cell Ca2+-ATPase. Studies with a novel photoactivatable probe. Biochemistry 34:3802–3812

    Article  CAS  PubMed  Google Scholar 

  96. Tang D, Dean WL, Borchman D, Paterson CA (2006) The influence of membrane lipid structure on plasma membrane Ca2+-ATPase activity. Cell Calcium 39:209–216

    Article  CAS  PubMed  Google Scholar 

  97. Lehotsky J (1995) Plasma membrane Ca2+-pump functional specialization in the brain. Complex of isoform expression and regulation by effectors. Mol Chem Neuropathol 25:175–187

    Article  CAS  PubMed  Google Scholar 

  98. Duan J, Zhang J, Zhao Y et al (2006) Ganglioside GM2 modulates the erythrocyte Ca2+-ATPase through its binding to the calmodulin-binding domain and its “receptor”. Arch Biochem Biophys 434:155–159

    Article  CAS  Google Scholar 

  99. Perez-Gordones MC, Lugo MR, Winkler M et al (2009) Diacylglycerol regulates the plasma membrane calcium pump function from human erythrocytes by direct interaction. Arch Biochem Biophys 489:55–61

    Article  CAS  PubMed  Google Scholar 

  100. Mangialavori IC, Caride AJ, Rossi RC et al (2011) Diving into the lipid bilayer to investigate the transmembrane organization and conformational state transitions of P-type ion ATPases. Curr Chem Biol 5:118–129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Mangialavori I, Villamil Giraldo AM, Pignataro MF et al (2011) Plasma membrane calcium pump (PMCA) differential exposure of hydrophobic domains after calmodulin and phosphatidic acid activation. J Biol Chem 286:18397–18404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Lopreiato R, Giacomello M, Carafoli E (2014) The plasma membrane calcium pump: new ways to look at an old enzyme. J Biol Chem 289:10261–10268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Sepúlveda MR, Berrocal-Carrillo M, Gasset M, Mata AM (2006) The plasma membrane Ca2+-ATPase isoform 4 is localized in lipid rafts of cerebellum synaptic plasma membranes. J Biol Chem 281:447–453

    Article  PubMed  CAS  Google Scholar 

  104. Jiang L, Fernandes D, Mehta N et al (2007) Partitioning of the plasma membrane Ca2+-ATPase into lipid rafts in primary neurons: effects of cholesterol depletion. J Neurochem 102:378–388

    Article  CAS  PubMed  Google Scholar 

  105. Fujimoto T (1993) Calcium pump of the plasma membrane is localized in caveolae. J Cell Biol 120:1147–1157

    Article  CAS  PubMed  Google Scholar 

  106. Schnitzer JE, Oh P, Jacobson BS, Dvorak AM (1995) Caveolae from luminal plasmalemma of rat lung endothelium: microdomains enriched in caveolin, Ca2+-ATPase, and inositol triphosphate receptor. Proc Natl Acad Sci U S A 92:1759–1763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Tortelote GG, Valverde RHF, Lemos T et al (2004) The plasma membrane Ca2+ pump from proximal kidney tubules is exclusively localized and active in caveolae. FEBS Lett 576:31–35

    Article  CAS  PubMed  Google Scholar 

  108. Zhang J, **ao P, Zhang X (2009) Phosphatidylserine externalization in caveolae inhibits Ca2+ efflux through plasma membrane Ca2+-ATPase in ECV304. Cell Calcium 45:177–184

    Article  CAS  PubMed  Google Scholar 

  109. Kosk-Kosicka D, Bzdega T (1998) Activation of the erythrocyte Ca2+-ATPase by either self-association or interaction with calmodulin. J Biol Chem 263:18184–18189

    Google Scholar 

  110. Kosk-Kosicka D, Bzdega T, Wawrzynow A (1989) Fluorescence energy transfer studies of purified erythrocyte Ca2+-ATPase. Ca2+-regulated activation by oligomerization. J Biol Chem 264:19495–19499

    CAS  PubMed  Google Scholar 

  111. Vorherr T, Kessler T, Hofmann F, Carafoli E (1991) The calmodulin-binding domain mediates the self-association of the plasma membrane Ca2+ pump. J Biol Chem 266:22–27

    CAS  PubMed  Google Scholar 

  112. Levi V, Rossi JPFC, Castello PR et al (2002) Structural significance of the plasma membrane calcium pump oligomerization. Biophys J 82:437–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Strehler EE, Caride AJ, Filoteo AG et al (2007) Plasma membrane Ca2+ ATPases as dynamic regulators of cellular calcium handling. Ann N Y Acad Sci 1099:226–236

    Article  CAS  PubMed  Google Scholar 

  114. Holton ML, Wang W, Emerson M et al (2010) Plasma membrane calcium ATPases as novel regulators of signal transduction pathways. World J Biol Chem 1:201–208

    Article  PubMed  PubMed Central  Google Scholar 

  115. Di Leva F, Domi T, Fedrizzi L et al (2008) The plasma membrane Ca2+ ATPase of animal cells: structure, function and regulation. Arch Biochem Biophys 476:65–74

    Article  PubMed  CAS  Google Scholar 

  116. Oceandy D, Mohamed TM, Cartwright EJ, Neyses L (2011) Local signals with global impacts and clinical implications: lessons from the plasma membrane calcium pump (PMCA4). Biochim Biophys Acta 1813:974–978

    Article  CAS  PubMed  Google Scholar 

  117. Rimessi A, Coletto L, Pinton P et al (2005) Inhibitory interaction of the 14-3-3e protein with isoform 4 of the plasma membrane Ca2+-ATPase pump. J Biol Chem 280:37195–37203

    Article  CAS  PubMed  Google Scholar 

  118. Linde CI, Di Leva F, Domi T et al (2008) Inhibitory interaction of the 14-3-3 proteins with ubiquitous (PMCA1) and tissue-specific (PMCA3) isoforms of the plasma membrane Ca2+ pump. Cell Calcium 43:550–561

    Article  CAS  PubMed  Google Scholar 

  119. Yang Y-M, Lee J, Jo H et al (2014) Homer2 protein regulates plasma membrane Ca2+-ATPase-mediated Ca2+ signaling in mouse parotid gland acinar cells. J Biol Chem 289:24971–24979

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Post H, Gutberlet J, Wiche R et al (2008) The localization of PMCA1b in epithelial cells and aposomes of the rat coagulating gland is influenced by androgens. Prostate 68:1076–1085

    Article  CAS  PubMed  Google Scholar 

  121. Kruger WA, Yun CC, Monteith GR, Poronnik P (2009) Muscarinic-induced recruitment of plasma membrane Ca2+-ATPase involves PSD-95/Dlg/Zo-1-mediated interactions. J Biol Chem 284:1820–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Padányi R, **ong Y, Antalffy G et al (2011) Apical scaffolding protein NHERF2 modulates the localization of alternatively spliced plasma membrane Ca2+ pump 2b variants in polarized epithelial cells. J Biol Chem 285:31704–31712

    Article  CAS  Google Scholar 

  123. Enyedi A, Strehler EE (2011) Regulation of apical membrane enrichment and retention of plasma membrane Ca2+ ATPase splice variants by the PDZ-domain protein NHERF2. Commun Integr Biol 4:340–343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Rivas FV, O’Keefe JP, Alegre M-L, Gajewski TF (2004) Actin cytoskeleton regulates calcium dynamics and NFAT nuclear duration. Mol Cell Biol 24:1628–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Dalghi MG, Fernandez MM, Ferreira Gomes M et al (2013) Plasma membrane calcium ATPase activity is regulated by actin oligomers through direct interaction. J Biol Chem 288:23380–23393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Quintana A, Pasche M, Junker C et al (2011) Calcium microdomains at the immunological synapse: how ORAI channels, mitochondria and calcium pumps generate local calcium signals for efficient T-cell activation. EMBO J 30:3895–3912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Ritchie MF, Samakai E, Soboloff J (2012) STIM1 is required for attenuation of PMCA-mediated Ca2+ clearance during T-cell activation. EMBO J 31:1123–1133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Yang J, Pawlyk B, Wen X-H et al (2007) Mpp4 is required for proper localization of plasma membrane calcium ATPases and maintenance of calcium homeostasis at the rod photoreceptor synaptic terminals. Hum Mol Genet 16:1017–1029

    Article  CAS  PubMed  Google Scholar 

  129. Aartsen WM, Arsanto J-P, Chauvin J-P et al (2009) PSD95b regulates plasma membrane Ca(2+) pump localization at the photoreceptor synapse. Mol Cell Neurosci 41:156–165

    Article  CAS  PubMed  Google Scholar 

  130. deJuan-Sanz J, Nunez E, Zafra F et al (2014) Presynaptic control of glycine transporter 2 (GlyT2) by physical and functional association with plasma membrane Ca2+-ATPase (PMCA) and Na+-Ca2+ exchanger (NCX). J Biol Chem 289:34308–34324

    Article  CAS  Google Scholar 

  131. Tran Q-K, Ver Meer M, Burghard MA et al (2015) Hetero-oligomeric complex between the G protein-coupled estrogen receptor 1 and the plasma membrane Ca2+ ATPase 4b. J Biol Chem 290:13293–13307

    Google Scholar 

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Acknowledgements

I am grateful to M.-A. Strehler-Page for help with the preparation of Fig. 5.1. This work was supported in part by the Mayo Foundation for Medical Research.

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Correspondence to Emanuel E. Strehler .

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Strehler, E.E. (2016). The ATP2B Plasma Membrane Ca2+ ATPase Family: Regulation in Response to Changing Demands of Cellular Calcium Transport. In: Chakraborti, S., Dhalla, N. (eds) Regulation of Ca2+-ATPases,V-ATPases and F-ATPases. Advances in Biochemistry in Health and Disease, vol 14. Springer, Cham. https://doi.org/10.1007/978-3-319-24780-9_5

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