Skip to main content

Advertisement

Log in

Role of sarco/endoplasmic reticulum calcium content and calcium ATPase activity in the control of cell growth and proliferation

  • Cell and Molecular Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

Ca2+, the main second messenger, is central to the regulation of cellular growth. There is increasing evidence that cellular growth and proliferation are supported by a continuous store-operated Ca2+ influx. By controlling store refilling, the sarco/endoplasmic reticulum Ca2+ ATPase (SERCA) also controls store-operated calcium entry and, thus, cell growth. In this review, we discuss data showing the involvement of SERCA in the regulation of proliferation and hypertrophy. First, we describe the Ca2+-related signaling pathways involved in cell growth. Then, we present evidence that SERCA controls proliferation of differentiated cells and hypertrophic growth of cardiomyocytes, and discuss the role of SERCA isoforms. Last, we consider the potential therapeutic applications of increasing SERCA activity for the treatment of cardiovascular diseases and of modulating SERCA and SR content for the treatment of cancer.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

ATP:

adenosine triphosphate

Ca2+ :

ion calcium

CCE:

capacitative Ca2+ entry

CDK4:

cyclin-dependent kinase 4

CRAC:

calcium-release activated channel

CRACM1:

calcium-release activated channel molecule 1

IP3:

inositol-1,4,5-trisphosphate

IP3R:

inositol-1,4,5-trisphosphate receptor

NFAT:

nuclear factor of activated T-lymphocytes

PDGF:

platelet derived growth factor

PKC:

protein kinase C

Rb:

retinoblastoma protein

ROC:

receptor operated calcium channels

RyR:

ryanodine receptor

SR/ER:

sarco/endoplasmic reticulum

SERCA:

sarco/endoplasmic reticulum Ca2+ ATPase

SOC:

store-operated calcium channels

SRF:

serum response factor

STIM1:

stromal interaction molecule 1

TRPC:

transient receptor potential channels

VOCC:

voltage operated calcium channels

WT:

wild type

References

  1. Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schoneich C, Cohen RA (2004) S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 10:1200–1207

    Article  PubMed  CAS  Google Scholar 

  2. Armoundas AA, Rose J, Aggarwal R, Stuyvers BD, O’Rourke B, Kass DA, Marban E, Shorofsky SR, Tomaselli GF, William Balke C (2007) Cellular and molecular determinants of altered Ca2+ handling in the failing rabbit heart: primary defects in SR Ca2+ uptake and release mechanisms. Am J Physiol Heart Circ Physiol 292:H1607–18

    Article  PubMed  CAS  Google Scholar 

  3. Baker DL, Hashimoto K, Grupp IL, Ji Y, Reed T, Loukianov E, Grupp G, Bhagwhat A, Hoit B, Walsh R, Marban E, Periasamy M (1998) Targeted overexpression of the sarcoplasmic reticulum Ca2+-ATPase increases cardiac contractility in transgenic mouse hearts. Circ Res 83:1205–1214

    PubMed  CAS  Google Scholar 

  4. Baksh S, Widlund HR, Frazer-Abel AA, Du J, Fosmire S, Fisher DE, DeCaprio JA, Modiano JF, Burakoff SJ (2002) NFATc2-mediated repression of cyclin-dependent kinase 4 expression. Mol Cell 10:1071–1081

    Article  PubMed  CAS  Google Scholar 

  5. Bert AG, Johnson BV, Baxter EW, Cockerill PN (2007) A modular enhancer is differentially regulated by GATA and NFAT elements that direct different tissue-specific patterns of nucleosome positioning and inducible chromatin remodeling. Mol Cell Biol 27:2870–2885

    Article  PubMed  CAS  Google Scholar 

  6. Bobe R, Bredoux R, Corvazier E, Lacabaratz-Porret C, Martin V, Kovacs T, Enouf J (2005) How many Ca(2)+ ATPase isoforms are expressed in a cell type? A growing family of membrane proteins illustrated by studies in platelets. Platelets 16:133–150

    Article  PubMed  CAS  Google Scholar 

  7. Brilakis ES, Banerjee S, Berger PB (2007) The risk of drug-eluting stent thrombosis with noncardiac surgery. Curr Cardiol Rep 9:406–411

    Article  PubMed  Google Scholar 

  8. Brouland JP, Gelebart P, Kovacs T, Enouf J, Grossmann J, Papp B (2005) The loss of sarco/endoplasmic reticulum calcium transport ATPase 3 expression is an early event during the multistep process of colon carcinogenesis. Am J Pathol 167:233–242

    PubMed  CAS  Google Scholar 

  9. Buchholz M, Ellenrieder V (2007) An emerging role for Ca2+/calcineurin/NFAT signaling in cancerogenesis. Cell Cycle 6:16–9

    PubMed  CAS  Google Scholar 

  10. Buchholz M, Schatz A, Wagner M, Michl P, Linhart T, Adler G, Gress TM, Ellenrieder V (2006) Overexpression of c-myc in pancreatic cancer caused by ectopic activation of NFATc1 and the Ca2+/calcineurin signaling pathway. EMBO J 25:3714–3724

    Article  PubMed  CAS  Google Scholar 

  11. Byrne CR (2006) The focal nature of Darier’s disease lesions: calcium pumps, stress, and mutation? J Invest Dermatol 126:702–703

    Article  PubMed  CAS  Google Scholar 

  12. Caetano MS, Vieira-de-Abreu A, Teixeira LK, Werneck MB, Barcinski MA, Viola JP (2002) NFATC2 transcription factor regulates cell cycle progression during lymphocyte activation: evidence of its involvement in the control of cyclin gene expression. FASEB J 16:1940–1942

    PubMed  CAS  Google Scholar 

  13. Cahalan MD, Zhang SL, Yeromin AV, Ohlsen K, Roos J, Stauderman KA (2007) Molecular basis of the CRAC channel. Cell Calcium 42:133–144

    Article  PubMed  CAS  Google Scholar 

  14. Camacho P, Lechleiter JD (1993) Increased frequency of calcium waves in Xenopus laevis oocytes that express a calcium-ATPase. Science 260:226–229

    Article  PubMed  CAS  Google Scholar 

  15. Chaabane C, Corvazier E, Bredoux R, Dally S, Raies A, Villemain A, Dupuy E, Enouf J, Bobe R (2006) Sarco/endoplasmic reticulum Ca2+ATPase type 3 isoforms (SERCA3b and SERCA3f): distinct roles in cell adhesion and ER stress. Biochem Biophys Res Commun 345:1377–1385

    Article  PubMed  CAS  Google Scholar 

  16. Chen Y, Escoubet B, Prunier F, Amour J, Simonides WS, Vivien B, Lenoir C, Heimburger M, Choqueux C, Gellen B, Riou B, Michel JB, Franz WM, Mercadier JJ (2004) Constitutive cardiac overexpression of sarcoplasmic/endoplasmic reticulum Ca2+-ATPase delays myocardial failure after myocardial infarction in rats at a cost of increased acute arrhythmias. Circulation 109:1898–1903

    Article  PubMed  CAS  Google Scholar 

  17. Chung FY, Lin SR, Lu CY, Yeh CS, Chen FM, Hsieh JS, Huang TJ, Wang JY (2006) Sarco/endoplasmic reticulum calcium-ATPase 2 expression as a tumor marker in colorectal cancer. Am J Surg Pathol 30:969–974

    Article  PubMed  Google Scholar 

  18. Crepin A, Bidaux G, Vanden-Abeele F, Dewailly E, Goffin V, Prevarskaya N, Slomianny C (2007) Prolactin stimulates prostate cell proliferation by increasing endoplasmic reticulum content due to SERCA 2b over-expression. Biochem J 401:49–55

    Article  PubMed  CAS  Google Scholar 

  19. Davia K, Bernobich E, Ranu HK, del Monte F, Terracciano CM, MacLeod KT, Adamson DL, Chaudhri B, Hajjar RJ, Harding SE (2001) SERCA2A overexpression decreases the incidence of aftercontractions in adult rabbit ventricular myocytes. J Mol Cell Cardiol 33:1005–1015

    Article  PubMed  CAS  Google Scholar 

  20. Davies CH, Davia K, Bennett JG, Pepper JR, Poole-Wilson PA, Harding SE (1995) Reduced contraction and altered frequency response of isolated ventricular myocytes from patients with heart failure. Circulation 92:2540–2549

    PubMed  CAS  Google Scholar 

  21. De Jaegere S, Wuytack F, De Smedt H, Van den Bosch L, Casteels R (1993) Alternative processing of the gene transcripts encoding a plasma-membrane and a sarco/endoplasmic reticulum Ca2+ pump during differentiation of BC3H1 muscle cells. Biochim Biophys Acta 1173:188–194

    PubMed  Google Scholar 

  22. de la Bastie D, Levitsky D, Rappaport L, Mercadier JJ, Marotte F, Wisnewsky C, Brovkovich V, Schwartz K, Lompre AM (1990) Function of the sarcoplasmic reticulum and expression of its Ca2(+)-ATPase gene in pressure overload-induced cardiac hypertrophy in the rat. Circ Res 66:554–64

    PubMed  Google Scholar 

  23. del Monte F, Harding SE, Schmidt U, Matsui T, Kang ZB, Dec GW, Gwathmey JK, Rosenzweig A, Hajjar RJ (1999) Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation 100:2308–2311

    CAS  Google Scholar 

  24. del Monte F, Lebeche D, Guerrero JL, Tsuji T, Doye AA, Gwathmey JK, Hajjar RJ (2004) Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Natl Acad Sci USA 101:5622–5627

    Article  PubMed  CAS  Google Scholar 

  25. del Monte F, Williams E, Lebeche D, Schmidt U, Rosenzweig A, Gwathmey JK, Lewandowski ED, Hajjar RJ (2001) Improvement in survival and cardiac metabolism after gene transfer of sarcoplasmic reticulum Ca(2+)-ATPase in a rat model of heart failure. Circulation 104:1424–1429

    Article  PubMed  CAS  Google Scholar 

  26. Denmeade SR, Isaacs JT (2005) The SERCA pump as a therapeutic target: making a “smart bomb” for prostate cancer. Cancer Biol Ther 4:14–22

    Article  PubMed  CAS  Google Scholar 

  27. Dhitavat J, Dode L, Leslie N, Sakuntabhai A, Lorette G, Hovnanian A (2003) Mutations in the sarcoplasmic/endoplasmic reticulum Ca2+ATPase isoform cause Darier’s disease. J Invest Dermatol 121:486–489

    Article  PubMed  CAS  Google Scholar 

  28. Dolmetsch RE, Lewis RS, Goodnow CC, Healy JI (1997) Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature 386:855–858

    Article  PubMed  CAS  Google Scholar 

  29. Endo Y, Uzawa K, Mochida Y, Shiiba M, Bukawa H, Yokoe H, Tanzawa H (2004) Sarcoendoplasmic reticulum Ca(2+) ATPase type 2 downregulated in human oral squamous cell carcinoma. Int J Cancer 110:225–231

    Article  PubMed  CAS  Google Scholar 

  30. Fantozzi I, Zhang S, Platoshyn O, Remillard CV, Cowling RT, Yuan JX (2003) Hypoxia increases AP-1 binding activity by enhancing capacitative Ca2+ entry in human pulmonary artery endothelial cells. Am J Physiol Lung Cell Mol Physiol 285:L1233–45

    PubMed  CAS  Google Scholar 

  31. Feske S, Gwack Y, Prakriya M, Srikanth S, Puppel SH, Tanasa B, Hogan PG, Lewis RS, Daly M, Rao A (2006) A mutation in Orai1 causes immune deficiency by abrogating CRAC channel function. Nature 441:179–185

    Article  PubMed  CAS  Google Scholar 

  32. Frank KF, Bolck B, Brixius K, Kranias EG, Schwinger RH (2002) Modulation of SERCA: implications for the failing human heart. Basic Res Cardiol 97(Suppl 1):I72–8

    PubMed  Google Scholar 

  33. Freeman K, Lerman I, Kranias EG, Bohlmeyer T, Bristow MR, Lefkowitz RJ, Iaccarino G, Koch WJ, Leinwand LA (2001) Alterations in cardiac adrenergic signaling and calcium cycling differentially affect the progression of cardiomyopathy. J Clin Invest 107:967–74

    Article  PubMed  CAS  Google Scholar 

  34. Gackiere F, Bidaux G, Lory P, Prevarskaya N, Mariot P (2006) A role for voltage gated T-type calcium channels in mediating “capacitative” calcium entry? Cell Calcium 39:357–366

    Article  PubMed  CAS  Google Scholar 

  35. Garg P, Mauri L (2007) The conundrum of late and very late stent thrombosis following drug-eluting stent implantation. Curr Opin Cardiol 22:565–571

    PubMed  Google Scholar 

  36. Gelebart P, Kovacs T, Brouland JP, van Gorp R, Grossmann J, Rivard N, Panis Y, Martin V, Bredoux R, Enouf J, Papp B (2002) Expression of endomembrane calcium pumps in colon and gastric cancer cells. Induction of SERCA3 expression during differentiation. J Biol Chem 277:26310–26320

    Article  PubMed  CAS  Google Scholar 

  37. Gianni D, Chan J, Gwathmey JK, del Monte F, Hajjar RJ (2005) SERCA2a in heart failure: role and therapeutic prospects. J Bioenerg Biomembr 37:375–380

    Article  PubMed  CAS  Google Scholar 

  38. Golovina VA (1999) Cell proliferation is associated with enhanced capacitative Ca(2+) entry in human arterial myocytes. Am J Physiol 277:C343–9

    PubMed  CAS  Google Scholar 

  39. Golovina VA, Platoshyn O, Bailey CL, Wang J, Limsuwan A, Sweeney M, Rubin LJ, Yuan JX (2001) Upregulated TRP and enhanced capacitative Ca(2+) entry in human pulmonary artery myocytes during proliferation. Am J Physiol Heart Circ Physiol 280:H746–55

    PubMed  CAS  Google Scholar 

  40. Gomez MF, Stevenson AS, Bonev AD, Hill-Eubanks DC, Nelson MT (2002) Opposing actions of inositol 1,4,5-trisphosphate and ryanodine receptors on nuclear factor of activated T-cells regulation in smooth muscle. J Biol Chem 277:37756–37764

    Article  PubMed  CAS  Google Scholar 

  41. Gonzalez Bosc LV, Layne JJ, Nelson MT, Hill-Eubanks DC (2005) Nuclear factor of activated T cells and serum response factor cooperatively regulate the activity of an alpha-actin intronic enhancer. J Biol Chem 280:26113–26120

    Article  PubMed  CAS  Google Scholar 

  42. Gwathmey JK, Copelas L, MacKinnon R, Schoen FJ, Feldman MD, Grossman W, Morgan JP (1987) Abnormal intracellular calcium handling in myocardium from patients with end-stage heart failure. Circ Res 61:70–76

    PubMed  CAS  Google Scholar 

  43. Gwathmey JK, Morgan JP (1985) Altered calcium handling in experimental pressure-overload hypertrophy in the ferret. Circ Res 57:836–843

    PubMed  CAS  Google Scholar 

  44. Haghighi K, Kolokathis F, Gramolini AO, Waggoner JR, Pater L, Lynch RA, Fan GC, Tsiapras D, Parekh RR, Dorn GW II, MacLennan DH, Kremastinos DT, Kranias EG (2006) A mutation in the human phospholamban gene, deleting arginine 14, results in lethal, hereditary cardiomyopathy. Proc Natl Acad Sci USA 103:1388–1393

    Article  PubMed  CAS  Google Scholar 

  45. Heineke J, Molkentin JD (2006) Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol 7:589–600

    Article  PubMed  CAS  Google Scholar 

  46. Heit JJ, Apelqvist AA, Gu X, Winslow MM, Neilson JR, Crabtree GR, Kim SK (2006) Calcineurin/NFAT signalling regulates pancreatic beta-cell growth and function. Nature 443:345–349

    Article  PubMed  CAS  Google Scholar 

  47. Horsley V, Pavlath GK (2002) NFAT: ubiquitous regulator of cell differentiation and adaptation. J Cell Biol 156:771–774

    Article  PubMed  CAS  Google Scholar 

  48. Hoshijima M (2005) Gene therapy targeted at calcium handling as an approach to the treatment of heart failure. Pharmacol Ther 105:211–228

    Article  PubMed  CAS  Google Scholar 

  49. Hoshijima M, Ikeda Y, Iwanaga Y, Minamisawa S, Date MO, Gu Y, Iwatate M, Li M, Wang L, Wilson JM, Wang Y, Ross Jr J, Chien KR (2002) Chronic suppression of heart-failure progression by a pseudophosphorylated mutant of phospholamban via in vivo cardiac rAAV gene delivery. Nat Med 8:864–871

    PubMed  CAS  Google Scholar 

  50. Humez S, Legrand G, Vanden-Abeele F, Monet M, Marchetti P, Lepage G, Crepin A, Dewailly E, Wuytack F, Prevarskaya N (2004) Role of endoplasmic reticulum calcium content in prostate cancer cell growth regulation by IGF and TNFalpha. J Cell Physiol 201:201–213

    Article  PubMed  CAS  Google Scholar 

  51. Ito K, Yan X, Feng X, Manning WJ, Dillmann WH, Lorell BH (2001) Transgenic expression of sarcoplasmic reticulum Ca(2+) atpase modifies the transition from hypertrophy to early heart failure. Circ Res 89:422–429

    Article  PubMed  CAS  Google Scholar 

  52. Iwanaga Y, Hoshijima M, Gu Y, Iwatate M, Dieterle T, Ikeda Y, Date MO, Chrast J, Matsuzaki M, Peterson KL, Chien KR, Ross J Jr. (2004) Chronic phospholamban inhibition prevents progressive cardiac dysfunction and pathological remodeling after infarction in rats. J Clin Invest 113:727–736

    PubMed  CAS  Google Scholar 

  53. Jaggar JH, Nelson MT (2000) Differential regulation of Ca(2+) sparks and Ca(2+) waves by UTP in rat cerebral artery smooth muscle cells. Am J Physiol Cell Physiol 279:C1528–39

    PubMed  CAS  Google Scholar 

  54. Jauliac S, Lopez-Rodriguez C, Shaw LM, Brown LF, Rao A, Toker A (2002) The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat Cell Biol. 4:540–544

    Article  PubMed  CAS  Google Scholar 

  55. John LM, Lechleiter JD, Camacho P (1998) Differential modulation of SERCA2 isoforms by calreticulin. J Cell Biol 142:963–973

    Article  PubMed  CAS  Google Scholar 

  56. Jousset H, Frieden M, Demaurex N (2007) STIM1 knockdown reveals that store-operated Ca2+ channels located close to sarco/endoplasmic Ca2+ ATPases (SERCA) pumps silently refill the endoplasmic reticulum. J Biol Chem 282:11456–11464

    Article  PubMed  CAS  Google Scholar 

  57. Kaprielian R, del Monte F, Hajjar RJ (2002) Targeting Ca2+ cycling proteins and the action potential in heart failure by gene transfer. Basic Res Cardiol 97(Suppl 1):I136–45

    PubMed  Google Scholar 

  58. Kaye DM, Preovolos A, Marshall T, Byrne M, Hoshijima M, Hajjar R, Mariani JA, Pepe S, Chien KR, Power JM (2007) Percutaneous cardiac recirculation-mediated gene transfer of an inhibitory phospholamban peptide reverses advanced heart failure in large animals. J Am Coll Cardiol 50:253–260

    Article  PubMed  CAS  Google Scholar 

  59. Kohn EC, Felder CC, Jacobs W, Holmes KA, Day A, Freer R, Liotta LA (1994) Structure-function analysis of signal and growth inhibition by carboxyamido-triazole, CAI. Cancer Res 54:935–942

    PubMed  CAS  Google Scholar 

  60. Komuro I, Kurabayashi M, Shibazaki Y, Takaku F, Yazaki Y (1989) Molecular cloning and characterization of a Ca2+ + Mg2+-dependent adenosine triphosphatase from rat cardiac sarcoplasmic reticulum. Regulation of its expression by pressure overload and developmental stage. J Clin Invest 83:1102–1108

    Article  PubMed  CAS  Google Scholar 

  61. Korosec B, Glavac D, Rott T, Ravnik-Glavac M (2006) Alterations in the ATP2A2 gene in correlation with colon and lung cancer. Cancer Genet Cytogenet 171:105–111

    Article  PubMed  CAS  Google Scholar 

  62. Kuga T, Kobayashi S, Hirakawa Y, Kanaide H, Takeshita A (1996) Cell cycle-dependent expression of L- and T-type Ca2+ currents in rat aortic smooth muscle cells in primary culture. Circ Res 79:14–19

    PubMed  CAS  Google Scholar 

  63. Kuwahara K, Wang Y, McAnally J, Richardson JA, Bassel-Duby R, Hill JA, Olson EN (2006) TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest 116:3114–3126

    Article  PubMed  CAS  Google Scholar 

  64. Launay S, Bobe R, Lacabaratz-Porret C, Bredoux R, Kovacs T, Enouf J, Papp B (1997) Modulation of endoplasmic reticulum calcium pump expression during T lymphocyte activation. J Biol Chem 272:10746–10750

    Article  PubMed  CAS  Google Scholar 

  65. Lipskaia L, del Monte F, Capiod T, Yacoubi S, Hadri L, Hours M, Hajjar RJ, Lompre AM (2005) Sarco/endoplasmic reticulum Ca2+-ATPase gene transfer reduces vascular smooth muscle cell proliferation and neointima formation in the rat. Circ Res 97:488–495

    Article  PubMed  CAS  Google Scholar 

  66. Lipskaia L, Lompre AM (2004) Alteration in temporal kinetics of Ca2+ signaling and control of growth and proliferation. Biol Cell 96:55–68

    Article  PubMed  CAS  Google Scholar 

  67. Lipskaia L, Ly H, Kawase Y, Hajjar R, Lompre AM (2007) Treatment of heart failure by calcium cycling gene therapy. Future Cardiol 3:413–423

    Article  CAS  PubMed  Google Scholar 

  68. Lipskaia L, Pinet C, Fromes Y, Hatem S, Cantaloube I, Coulombe A, Lompre AM (2007) Mutation of delta-sarcoglycan is associated with Ca(2+)-dependent vascular remodeling in the Syrian hamster. Am J Pathol 171:162–171

    Article  PubMed  CAS  Google Scholar 

  69. Lipskaia L, Pourci ML, Delomenie C, Combettes L, Goudouneche D, Paul JL, Capiod T, Lompre AM (2003) Phosphatidylinositol 3-kinase and calcium-activated transcription pathways are required for VLDL-induced smooth muscle cell proliferation. Circ Res 92:1115–1122

    Article  PubMed  CAS  Google Scholar 

  70. Liu LH, Boivin GP, Prasad V, Periasamy M, Shull GE (2001) Squamous cell tumors in mice heterozygous for a null allele of Atp2a2, encoding the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 Ca2+ pump. J Biol Chem 276:26737–26740

    Article  PubMed  CAS  Google Scholar 

  71. Liu Z, Dronadula N, Rao GN (2004) A novel role for nuclear factor of activated T cells in receptor tyrosine kinase and G protein-coupled receptor agonist-induced vascular smooth muscle cell motility. J Biol Chem 279:41218–41226

    Article  PubMed  CAS  Google Scholar 

  72. Liu Z, Zhang C, Dronadula N, Li Q, Rao GN (2005) Blockade of nuclear factor of activated T cells activation signaling suppresses balloon injury-induced neointima formation in a rat carotid artery model. J Biol Chem 280:14700–14708

    Article  PubMed  CAS  Google Scholar 

  73. Lytton J, Westlin M, Burk SE, Shull GE, MacLennan DH (1992) Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J Biol Chem 267:14483–14489

    PubMed  CAS  Google Scholar 

  74. Macian F, Garcia-Rodriguez C, Rao A (2000) Gene expression elicited by NFAT in the presence or absence of cooperative recruitment of Fos and Jun. Embo J 19:4783–95

    Article  PubMed  CAS  Google Scholar 

  75. Massaeli H, Austria JA, Pierce GN (2000) Lesions in ryanodine channels in smooth muscle cells exposed to oxidized low density lipoprotein. Arterioscler Thromb Vasc Biol 20:328–334

    PubMed  CAS  Google Scholar 

  76. Mayosi BM, Kardos A, Davies CH, Gumedze F, Hovnanian A, Burge S, Watkins H (2006) Heterozygous disruption of SERCA2a is not associated with impairment of cardiac performance in humans: implications for SERCA2a as a therapeutic target in heart failure. Heart 92:105–109

    Article  PubMed  CAS  Google Scholar 

  77. Mercadier JJ, Lompre AM, Duc P, Boheler KR, Fraysse JB, Wisnewsky C, Allen PD, Komajda M, Schwartz K (1990) Altered sarcoplasmic reticulum Ca2(+)-ATPase gene expression in the human ventricle during end-stage heart failure. J Clin Invest 85:305–309

    Article  PubMed  CAS  Google Scholar 

  78. Minamisawa S, Hoshijima M, Chu G, Ward CA, Frank K, Gu Y, Martone ME, Wang Y, Ross J Jr, Kranias EG, Giles WR, Chien KR (1999) Chronic phospholamban-sarcoplasmic reticulum calcium ATPase interaction is the critical calcium cycling defect in dilated cardiomyopathy. Cell 99:313–322

    Article  PubMed  CAS  Google Scholar 

  79. Miyamoto MI, del Monte F, Schmidt U, DiSalvo TS, Kang ZB, Matsui T, Guerrero JL, Gwathmey JK, Rosenzweig A, Hajjar RJ (2000) Adenoviral gene transfer of SERCA2a improves left-ventricular function in aortic-banded rats in transition to heart failure. Proc Natl Acad Sci USA 97:793–798

    Article  PubMed  CAS  Google Scholar 

  80. Moccia F, Berra-Romani R, Tritto S, Signorelli S, Taglietti V, Tanzi F (2003) Epidermal growth factor induces intracellular Ca2+ oscillations in microvascular endothelial cells. J Cell Physiol 194:139–150

    Article  PubMed  CAS  Google Scholar 

  81. Molkentin JD, Lu JR, Antos CL, Markham B, Richardson J, Robbins J, Grant SR, Olson EN (1998) A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215–228

    Article  PubMed  CAS  Google Scholar 

  82. Monteith GR, McAndrew D, Faddy HM, Roberts-Thomson SJ (2007) Calcium and cancer: targeting Ca2+ transport. Nat Rev Cancer 7:519–530

    Article  PubMed  CAS  Google Scholar 

  83. Mountian I, Manolopoulos VG, De Smedt H, Parys JB, Missiaen L, Wuytack F (1999) Expression patterns of sarco/endoplasmic reticulum Ca(2+)-ATPase and inositol 1,4,5-trisphosphate receptor isoforms in vascular endothelial cells. Cell Calcium 25:371–380

    Article  PubMed  CAS  Google Scholar 

  84. Muller OJ, Lange M, Rattunde H, Lorenzen HP, Muller M, Frey N, Bittner C, Simonides W, Katus HA, Franz WM (2003) Transgenic rat hearts overexpressing SERCA2a show improved contractility under baseline conditions and pressure overload. Cardiovasc Res 59:380–389

    Article  PubMed  CAS  Google Scholar 

  85. Musaro A, McCullagh KJ, Naya FJ, Olson EN, Rosenthal N (1999) IGF-1 induces skeletal myocyte hypertrophy through calcineurin in association with GATA-2 and NF-ATc1. Nature 400:581–585

    Article  PubMed  CAS  Google Scholar 

  86. Nagai R, Zarain-Herzberg A, Brandl CJ, Fujii J, Tada M, MacLennan DH, Alpert NR, Periasamy M (1989) Regulation of myocardial Ca2+-ATPase and phospholamban mRNA expression in response to pressure overload and thyroid hormone. Proc Natl Acad Sci USA 86:2966–2970

    Article  PubMed  CAS  Google Scholar 

  87. Nakayama H, Otsu K, Yamaguchi O, Nishida K, Date MO, Hongo K, Kusakari Y, Toyofuku T, Hikoso S, Kashiwase K, Takeda T, Matsumura Y, Kurihara S, Hori M, Tada M (2003) Cardiac-specific overexpression of a high Ca2+ affinity mutant of SERCA2a attenuates in vivo pressure overload cardiac hypertrophy. FASEB J 17:61–3

    PubMed  CAS  Google Scholar 

  88. Nakayama H, Wilkin BJ, Bodi I, Molkentin JD (2006) Calcineurin-dependent cardiomyopathy is activated by TRPC in the adult mouse heart. FASEB J 20:1660–1670

    Article  PubMed  CAS  Google Scholar 

  89. Neal JW, Clipstone NA (2003) A constitutively active NFATc1 mutant induces a transformed phenotype in 3T3-L1 fibroblasts. J Biol Chem 278:17246–17254

    Article  PubMed  CAS  Google Scholar 

  90. Nilsson LM, Sun ZW, Nilsson J, Nordstrom I, Chen YW, Molkentin JD, Wide-Swensson D, Hellstrand P, Lydrup ML, Gomez MF (2007) Novel blocker of NFAT activation inhibits IL-6 production in human myometrial arteries and reduces vascular smooth muscle cell proliferation. Am J Physiol Cell Physiol 292:C1167–C1178

    Article  PubMed  CAS  Google Scholar 

  91. O’Neill JP, Velalar CN, Lee DI, Zhang B, Nakanishi T, Tang Y, Selaru F, Ross D, Meltzer SJ, Hussain A (2006) Thapsigargin resistance in human prostate cancer cells. Cancer 107:649–659

    Article  PubMed  CAS  Google Scholar 

  92. Owens GK, Kumar MS, Wamhoff BR (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 84:767–801

    Article  PubMed  CAS  Google Scholar 

  93. Pacifico F, Ulianich L, De Micheli S, Treglia S, Leonardi A, Vito P, Formisano S, Consiglio E, Di Jeso B (2003) The expression of the sarco/endoplasmic reticulum Ca2+-ATPases in thyroid and its down-regulation following neoplastic transformation. J Mol Endocrinol 30:399–409

    Article  PubMed  CAS  Google Scholar 

  94. Pani B, Cornatzer E, Cornatzer W, Shin DM, Pittelkow MR, Hovnanian A, Ambudkar IS, Singh BB (2006) Up-regulation of transient receptor potential canonical 1 (TRPC1) following sarco(endo)plasmic reticulum Ca2+ ATPase 2 gene silencing promotes cell survival: a potential role for TRPC1 in Darier’s disease. Mol Biol Cell 17:4446–4458

    Article  PubMed  CAS  Google Scholar 

  95. Periasamy M, Huke S (2001) SERCA pump level is a critical determinant of Ca(2+)homeostasis and cardiac contractility. J Mol Cell Cardiol 33:1053–1063

    Article  PubMed  CAS  Google Scholar 

  96. Periasamy M, Kalyanasundaram A (2007) SERCA pump isoforms: their role in calcium transport and disease. Muscle Nerve 35:430–442

    Article  PubMed  CAS  Google Scholar 

  97. Periasamy M, Reed TD, Liu LH, Ji Y, Loukianov E, Paul RJ, Nieman ML, Riddle T, Duffy JJ, Doetschman T, Lorenz JN, Shull GE (1999) Impaired cardiac performance in heterozygous mice with a null mutation in the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 (SERCA2) gene. J Biol Chem 274:2556–2562

    Article  PubMed  CAS  Google Scholar 

  98. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG (2006) Orai1 is an essential pore subunit of the CRAC channel. Nature 443:230–233

    Article  PubMed  CAS  Google Scholar 

  99. Prasad AM, Ma H, Sumbilla C, Lee DI, Klein MG, Inesi G (2007) Phenylephrine hypertrophy, Ca2+-ATPase (SERCA2), and Ca2+ signaling in neonatal rat cardiac myocytes. Am J Physiol Cell Physiol 292:C2269–C2275

    Article  PubMed  CAS  Google Scholar 

  100. Prasad V, Boivin GP, Miller ML, Liu LH, Erwin CR, Warner BW, Shull GE (2005) Haploinsufficiency of Atp2a2, encoding the sarco(endo)plasmic reticulum Ca2+-ATPase isoform 2 Ca2+ pump, predisposes mice to squamous cell tumors via a novel mode of cancer susceptibility. Cancer Res 65:8655–8661

    Article  PubMed  CAS  Google Scholar 

  101. Ranger AM, Hodge MR, Gravallese EM, Oukka M, Davidson L, Alt FW, de la Brousse FC, Hoey T, Grusby M, Glimcher LH (1998) Delayed lymphoid repopulation with defects in IL-4-driven responses produced by inactivation of NF-ATc. Immunity 8:125–134

    Article  PubMed  CAS  Google Scholar 

  102. Rao A, Luo C, Hogan PG (1997) Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15:707–747

    Article  PubMed  CAS  Google Scholar 

  103. Richard S, Neveu D, Carnac G, Bodin P, Travo P, Nargeot J (1992) Differential expression of voltage-gated Ca(2+)-currents in cultivated aortic myocytes. Biochim Biophys Acta 1160:95–104

    PubMed  CAS  Google Scholar 

  104. Roderick HL, Lechleiter JD, Camacho P (2000) Cytosolic phosphorylation of calnexin controls intracellular Ca(2+) oscillations via an interaction with SERCA2b. J Cell Biol 149:1235–1248

    Article  PubMed  CAS  Google Scholar 

  105. Rodman DM, Reese K, Harral J, Fouty B, Wu S, West J, Hoedt-Miller M, Tada Y, Li KX, Cool C, Fagan K, Cribbs L (2005) Low-voltage-activated (T-type) calcium channels control proliferation of human pulmonary artery myocytes. Circ Res 96:864–872

    Article  PubMed  CAS  Google Scholar 

  106. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Velicelebi G, Stauderman KA (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol 169:435–445

    Article  PubMed  CAS  Google Scholar 

  107. Sato Y, Kiriazis H, Yatani A, Schmidt AG, Hahn H, Ferguson DG, Sako H, Mitarai S, Honda R, Mesnard-Rouiller L, Frank KF, Beyermann B, Wu G, Fujimori K, Dorn GW II, Kranias EG (2001) Rescue of contractile parameters and myocyte hypertrophy in calsequestrin overexpressing myocardium by phospholamban ablation. J Biol Chem 276:9392–9399

    Article  PubMed  CAS  Google Scholar 

  108. Schabbauer G, Schweighofer B, Mechtcheriakova D, Lucerna M, Binder BR, Hofer E (2007) Nuclear factor of activated T cells and early growth response-1 cooperate to mediate tissue factor gene induction by vascular endothelial growth factor in endothelial cells. Thromb Haemost 97:988–997

    PubMed  CAS  Google Scholar 

  109. Schmitt JP, Kamisago M, Asahi M, Li GH, Ahmad F, Mende U, Kranias EG, MacLennan DH, Seidman JG, Seidman CE (2003) Dilated cardiomyopathy and heart failure caused by a mutation in phospholamban. Science 299:1410–1413

    Article  PubMed  CAS  Google Scholar 

  110. Schmitt R, Clozel JP, Iberg N, Buhler FR (1995) Mibefradil prevents neointima formation after vascular injury in rats. Possible role of the blockade of the T-type voltage-operated calcium channel. Arterioscler Thromb Vasc Biol 15:1161–1165

    PubMed  CAS  Google Scholar 

  111. Schultz Jel J, Glascock BJ, Witt SA, Nieman ML, Nattamai KJ, Liu LH, Lorenz JN, Shull GE, Kimball TR, Periasamy M (2004) Accelerated onset of heart failure in mice during pressure overload with chronically decreased SERCA2 calcium pump activity. Am J Physiol Heart Circ Physiol 286:H1146–53

    Article  PubMed  Google Scholar 

  112. Schwinger RH, Bohm M, Schmidt U, Karczewski P, Bavendiek U, Flesch M, Krause EG, Erdmann E (1995) Unchanged protein levels of SERCA II and phospholamban but reduced Ca2+ uptake and Ca(2+)-ATPase activity of cardiac sarcoplasmic reticulum from dilated cardiomyopathy patients compared with patients with nonfailing hearts. Circulation 92:3220–3228

    PubMed  CAS  Google Scholar 

  113. Seth M, Sumbilla C, Mullen SP, Lewis D, Klein MG, Hussain A, Soboloff J, Gill DL, Inesi G (2004) Sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA) gene silencing and remodeling of the Ca2+ signaling mechanism in cardiac myocytes. Proc Natl Acad Sci USA 101:16683–16688

    Article  PubMed  CAS  Google Scholar 

  114. Song Q, Schmidt AG, Hahn HS, Carr AN, Frank B, Pater L, Gerst M, Young K, Hoit BD, McConnell BK, Haghighi K, Seidman CE, Seidman JG, Dorn GW 2nd, Kranias EG (2003) Rescue of cardiomyocyte dysfunction by phospholamban ablation does not prevent ventricular failure in genetic hypertrophy. J Clin Invest 111:859–867

    PubMed  CAS  Google Scholar 

  115. Spassova MA, Soboloff J, He LP, Xu W, Dziadek MA, Gill DL (2006) STIM1 has a plasma membrane role in the activation of store-operated Ca(2+) channels. Proc Natl Acad Sci USA 103:4040–4045

    Article  PubMed  CAS  Google Scholar 

  116. Stathopulos PB, Li GY, Plevin MJ, Ames JB, Ikura M (2006) Stored Ca2+ depletion-induced oligomerization of stromal interaction molecule 1 (STIM1) via the EF-SAM region: An initiation mechanism for capacitive Ca2+ entry. J Biol Chem 281:35855–35862

    Article  PubMed  CAS  Google Scholar 

  117. Suzuki E, Nishimatsu H, Satonaka H, Walsh K, Goto A, Omata M, Fujita T, Nagai R, Hirata Y (2002) Angiotensin II induces myocyte enhancer factor 2- and calcineurin/nuclear factor of activated T cell-dependent transcriptional activation in vascular myocytes. Circ Res 90:1004–1011

    Article  PubMed  CAS  Google Scholar 

  118. Takahashi Y, Watanabe H, Murakami M, Ohba T, Radovanovic M, Ono K, Iijima T, Ito H (2007) Involvement of transient receptor potential canonical 1 (TRPC1) in angiotensin II-induced vascular smooth muscle cell hypertrophy. Atherosclerosis 195(2):287–296

    Article  PubMed  CAS  Google Scholar 

  119. Takahashi Y, Watanabe H, Murakami M, Ono K, Munehisa Y, Koyama T, Nobori K, Iijima T, Ito H (2007) Functional role of stromal interaction molecule 1 (STIM1) in vascular smooth muscle cells. Biochem Biophys Res Commun 361:934–940

    Article  PubMed  CAS  Google Scholar 

  120. Talukder MA, Kalyanasundaram A, Zhao X, Zuo L, Bhupathy P, Babu GJ, Cardounel AJ, Periasamy M, Zweier JL (2007) Expression of SERCA isoform with faster Ca2+ transport properties improves postischemic cardiac function and Ca2+ handling and decreases myocardial infarction. Am J Physiol Heart Circ Physiol 293:H2418–28

    Article  PubMed  CAS  Google Scholar 

  121. Tavadia S, Authi KS, Hodgins MB, Munro CS (2004) Expression of the sarco/endoplasmic reticulum calcium ATPase type 2 and 3 isoforms in normal skin and Darier’s disease. Br J Dermatol 151:440–445

    Article  PubMed  CAS  Google Scholar 

  122. Tavadia S, Tait RC, McDonagh TA, Munro CS (2001) Platelet and cardiac function in Darier’s disease. Clin Exp Dermatol 26:696–699

    Article  PubMed  CAS  Google Scholar 

  123. Thebault S, Flourakis M, Vanoverberghe K, Vandermoere F, Roudbaraki M, Lehen’kyi V, Slomianny C, Beck B, Mariot P, Bonnal JL, Mauroy B, Shuba Y, Capiod T, Skryma R, Prevarskaya N (2006) Differential role of transient receptor potential channels in Ca2+ entry and proliferation of prostate cancer epithelial cells. Cancer Res 66:2038–2047

    Article  PubMed  CAS  Google Scholar 

  124. Trost SU, Belke DD, Bluhm WF, Meyer M, Swanson E, Dillmann WH (2002) Overexpression of the sarcoplasmic reticulum Ca(2+)-ATPase improves myocardial contractility in diabetic cardiomyopathy. Diabetes 51:1166–1171

    Article  PubMed  CAS  Google Scholar 

  125. Vallot O, Combettes L, Jourdon P, Inamo J, Marty I, Claret M, Lompre AM (2000) Intracellular Ca(2+) handling in vascular smooth muscle cells is affected by proliferation. Arterioscler Thromb Vasc Biol 20:1225–1235

    PubMed  CAS  Google Scholar 

  126. Van Belle E, Susen S, Jude B, Bertrand ME (2007) Drug-eluting stents: trading restenosis for thrombosis? J Thromb Haemost 5(Suppl 1):238–245

    Article  PubMed  Google Scholar 

  127. Vangheluwe P, Schuermans M, Raeymaekers L, Wuytack F (2007) Tight interplay between the Ca2+ affinity of the cardiac SERCA2 Ca2+ pump and the SERCA2 expression level. Cell Calcium 42:281–289

    Article  PubMed  CAS  Google Scholar 

  128. Vangheluwe P, Tjwa M, Van Den Bergh A, Louch WE, Beullens M, Dode L, Carmeliet P, Kranias E, Herijgers P, Sipido KR, Raeymaekers L, Wuytack F (2006) A SERCA2 pump with an increased Ca2+ affinity can lead to severe cardiac hypertrophy, stress intolerance and reduced life span. J Mol Cell Cardiol 41:308–317

    Article  PubMed  CAS  Google Scholar 

  129. Ver Heyen M, Heymans S, Antoons G, Reed T, Periasamy M, Awede B, Lebacq J, Vangheluwe P, Dewerchin M, Collen D, Sipido K, Carmeliet P, Wuytack F (2001) Replacement of the muscle-specific sarcoplasmic reticulum Ca(2+)-ATPase isoform SERCA2a by the nonmuscle SERCA2b homologue causes mild concentric hypertrophy and impairs contraction-relaxation of the heart. Circ Res 89:838–846

    Article  Google Scholar 

  130. Verboomen H, Wuytack F, De Smedt H, Himpens B, Casteels R (1992) Functional difference between SERCA2a and SERCA2b Ca2+ pumps and their modulation by phospholamban. Biochem J 286(Pt 2):591–595

    PubMed  CAS  Google Scholar 

  131. Wang J, Wang N, Xie J, Walton SC, McKown RL, Raab RW, Ma P, Beck SL, Coffman GL, Hussaini IM, Laurie GW (2006) Restricted epithelial proliferation by lacritin via PKCalpha-dependent NFAT and mTOR pathways. J Cell Biol 174:689–700

    Article  PubMed  CAS  Google Scholar 

  132. Wilkins BJ, De Windt LJ, Bueno OF, Braz JC, Glascock BJ, Kimball TF, Molkentin JD (2002) Targeted disruption of NFATc3, but not NFATc4, reveals an intrinsic defect in calcineurin-mediated cardiac hypertrophic growth. Mol Cell Biol 22:7603–7613

    Article  PubMed  CAS  Google Scholar 

  133. Yellaturu CR, Ghosh SK, Rao RK, Jennings LK, Hassid A, Rao GN (2002) A potential role for nuclear factor of activated T-cells in receptor tyrosine kinase and G-protein-coupled receptor agonist-induced cell proliferation. Biochem J 368:183–190

    Article  PubMed  CAS  Google Scholar 

  134. Yeromin AV, Zhang SL, Jiang W, Yu Y, Safrina O, Cahalan MD (2006) Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai. Nature 443:226–229

    Article  PubMed  CAS  Google Scholar 

  135. Ying J, Tong X, Pimentel DR, Weisbrod RM, Trucillo MP, Adachi T, Cohen RA (2007) Cysteine-674 of the sarco/endoplasmic reticulum calcium ATPase is required for the inhibition of cell migration by nitric oxide. Arterioscler Thromb Vasc Biol 27:783–790

    Article  PubMed  CAS  Google Scholar 

  136. Yoshida H, Nishina H, Takimoto H, Marengere LE, Wakeham AC, Bouchard D, Kong YY, Ohteki T, Shahinian A, Bachmann M, Ohashi PS, Penninger JM, Crabtree GR, Mak TW (1998) The transcription factor NF-ATc1 regulates lymphocyte proliferation and Th2 cytokine production. Immunity 8:115–124

    Article  PubMed  CAS  Google Scholar 

  137. Yu H, Sliedregt-Bol K, Overkleeft H, van der Marel GA, van Berkel TJ, Biessen EA (2006) Therapeutic potential of a synthetic peptide inhibitor of nuclear factor of activated T cells as antirestenotic agent. Arterioscler Thromb Vasc Biol 26:1531–1537

    Article  PubMed  CAS  Google Scholar 

  138. Yu Y, Sweeney M, Zhang S, Platoshyn O, Landsberg J, Rothman A, Yuan JX (2003) PDGF stimulates pulmonary vascular smooth muscle cell proliferation by upregulating TRPC6 expression. Am J Physiol Cell Physiol 284:C316–30

    PubMed  CAS  Google Scholar 

  139. Zhang SL, Yeromin AV, Zhang XH, Yu Y, Safrina O, Penna A, Roos J, Stauderman KA, Cahalan MD (2006) Genome-wide RNAi screen of Ca(2+) influx identifies genes that regulate Ca(2+) release-activated Ca(2+) channel activity. Proc Natl Acad Sci USA 103:9357–9362

    Article  PubMed  CAS  Google Scholar 

  140. Zhang SL, Yu Y, Roos J, Kozak JA, Deerinck TJ, Ellisman MH, Stauderman KA, Cahalan MD (2005) STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature 437:902–905

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anne-Marie Lompré.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lipskaia, L., Hulot, JS. & Lompré, AM. Role of sarco/endoplasmic reticulum calcium content and calcium ATPase activity in the control of cell growth and proliferation. Pflugers Arch - Eur J Physiol 457, 673–685 (2009). https://doi.org/10.1007/s00424-007-0428-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-007-0428-7

Keywords

Navigation