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Calcium Signaling in Vascular Smooth Muscle Cells: From Physiology to Pathology

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Calcium Signaling

Abstract

Cyclic variations in calcium (Ca2+) concentrations, through a process called excitation-contraction coupling, allow regulation of vascular smooth muscle cells contractility and thus modulation of vascular tone and blood pressure. As a second messenger, Ca2+ also activates signaling cascades leading to transcription factors activation in a process called excitation-transcription coupling. Furthermore, recent evidences indicate an interaction between post-transcriptional regulation by microRNAs (miRNAs) and Ca2+ signaling. All these actors, which are frequently altered in vascular diseases, will be reviewed here.

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References

  1. Somlyo AP, Somlyo AV (2003) Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83:1325–1358

    PubMed  CAS  Google Scholar 

  2. House SJ, Potier M, Bisaillon J, Singer HA, Trebak M (2008) The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflugers Arch 456:769–785

    Article  PubMed  CAS  Google Scholar 

  3. Earley S, Straub SV, Brayden JE (2007) Protein kinase C regulates vascular myogenic tone through activation of TRPM4. Am J Physiol Heart Circ Physiol 292:H2613–H2622

    Article  PubMed  CAS  Google Scholar 

  4. Welsh DG, Morielli AD, Nelson MT, Brayden JE (2002) Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ Res 90:248–250

    Article  PubMed  CAS  Google Scholar 

  5. Benham CD, Bolton TB (1986) Spontaneous transient outward currents in single visceral and vascular smooth muscle cells of the rabbit. J Physiol 381:385–406

    PubMed  CAS  Google Scholar 

  6. Catterall WA (1995) Structure and function of voltage-gated ion channels. Annu Rev Biochem 64:493–531

    Article  PubMed  CAS  Google Scholar 

  7. Koch WJ, Ellinor PT, Schwartz A (1990) cDNA cloning of a dihydropyridine-sensitive calcium channel from rat aorta. Evidence for the existence of alternatively spliced forms. J Biol Chem 265:17786–17791

    PubMed  CAS  Google Scholar 

  8. Navedo MF, Amberg GC, Westenbroek RE, Sinnegger-Brauns MJ, Catterall WA, Striessnig J, Santana LF (2007) Ca(v)1.3 channels produce persistent calcium sparklets, but Ca(v)1.2 channels are responsible for sparklets in mouse arterial smooth muscle. Am J Physiol Heart Circ Physiol 293:H1359–H1370

    Article  PubMed  CAS  Google Scholar 

  9. Zhang J, Berra-Romani R, Sinnegger-Brauns MJ, Striessnig J, Blaustein MP, Matteson DR (2007) Role of Cav1.2 L-type Ca2+ channels in vascular tone: effects of nifedipine and Mg2+. Am J Physiol Heart Circ Physiol 292:H415–H425

    Article  PubMed  CAS  Google Scholar 

  10. Amberg GC, Navedo MF, Nieves-Cintron M, Molkentin JD, Santana LF (2007) Calcium sparklets regulate local and global calcium in murine arterial smooth muscle. J Physiol 579:187–201

    Article  PubMed  CAS  Google Scholar 

  11. Navedo MF, Amberg GC, Nieves M, Molkentin JD, Santana LF (2006) Mechanisms underlying heterogeneous Ca2+ sparklet activity in arterial smooth muscle. J Gen Physiol 127:611–622

    Article  PubMed  CAS  Google Scholar 

  12. Navedo MF, Amberg GC, Votaw VS, Santana LF (2005) Constitutively active L-type Ca2+ channels. Proc Natl Acad Sci USA 102:11112–11117

    Article  PubMed  CAS  Google Scholar 

  13. Navedo MF, Nieves-Cintron M, Amberg GC, Yuan C, Votaw VS, Lederer WJ, McKnight GS, Santana LF (2008) AKAP150 is required for stuttering persistent Ca2+ sparklets and angiotensin II-induced hypertension. Circ Res 102:e1–e11

    Article  PubMed  CAS  Google Scholar 

  14. Rubart M, Patlak JB, Nelson MT (1996) Ca2+ currents in cerebral artery smooth muscle cells of rat at physiological Ca2+ concentrations. J Gen Physiol 107:459–472

    Article  PubMed  CAS  Google Scholar 

  15. Robertson BE, Schubert R, Hescheler J, Nelson MT (1993) cGMP-dependent protein kinase activates Ca-activated K channels in cerebral artery smooth muscle cells. Am J Physiol 265:C299–C303

    PubMed  CAS  Google Scholar 

  16. Taguchi H, Heistad DD, Kitazono T, Faraci FM (1995) Dilatation of cerebral arterioles in response to activation of adenylate cyclase is dependent on activation of Ca(2+)-dependent K  +  channels. Circ Res 76:1057–1062

    PubMed  CAS  Google Scholar 

  17. Perez-Reyes E (2003) Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev 83:117–161

    PubMed  CAS  Google Scholar 

  18. Perez-Reyes E, Cribbs LL, Daud A, Lacerda AE, Barclay J, Williamson MP, Fox M, Rees M, Lee JH (1998) Molecular characterization of a neuronal low-voltage-activated T-type calcium channel. Nature 391:896–900

    Article  PubMed  CAS  Google Scholar 

  19. Chiang CS, Huang CH, Chieng H, Chang YT, Chang D, Chen JJ, Chen YC, Chen YH, Shin HS, Campbell KP, Chen CC (2009) The Ca(v)3.2 T-type Ca(2+) channel is required for pressure overload-induced cardiac hypertrophy in mice. Circ Res 104:522–530

    Article  PubMed  CAS  Google Scholar 

  20. Mangoni ME, Traboulsie A, Leoni AL, Couette B, Marger L, Le Quang K, Kupfer E, Cohen-Solal A, Vilar J, Shin HS, Escande D, Charpentier F, Nargeot J, Lory P (2006) Bradycardia and slowing of the atrioventricular conduction in mice lacking CaV3.1/alpha1G T-type calcium channels. Circ Res 98:1422–1430

    Article  PubMed  CAS  Google Scholar 

  21. Chen CC, Lamping KG, Nuno DW, Barresi R, Prouty SJ, Lavoie JL, Cribbs LL, England SK, Sigmund CD, Weiss RM, Williamson RA, Hill JA, Campbell KP (2003) Abnormal coronary function in mice deficient in alpha1H T-type Ca2+ channels. Science 302:1416–1418

    Article  PubMed  CAS  Google Scholar 

  22. Bitar KN, Bradford P, Putney JW Jr, Makhlouf GM (1986) Cytosolic calcium during contraction of isolated mammalian gastric muscle cells. Science 232:1143–1145

    Article  PubMed  CAS  Google Scholar 

  23. Leung FP, Yung LM, Yao X, Laher I, Huang Y (2008) Store-operated calcium entry in vascular smooth muscle. Br J Pharmacol 153:846–857

    Article  PubMed  CAS  Google Scholar 

  24. Kumar B, Dreja K, Shah SS, Cheong A, Xu SZ, Sukumar P, Naylor J, Forte A, Cipollaro M, McHugh D, Kingston PA, Heagerty AM, Munsch CM, Bergdahl A, Hultgardh-Nilsson A, Gomez MF, Porter KE, Hellstrand P, Beech DJ (2006) Upregulated TRPC1 channel in vascular injury in vivo and its role in human neointimal hyperplasia. Circ Res 98:557–563

    Article  PubMed  CAS  Google Scholar 

  25. Large WA (2002) Receptor-operated Ca2(+)-permeable nonselective cation channels in vascular smooth muscle: a physiologic perspective. J Cardiovasc Electrophysiol 13:493–501

    Article  PubMed  Google Scholar 

  26. 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 

  27. 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 

  28. Baryshnikov SG, Pulina MV, Zulian A, Linde CI, Golovina VA (2009) Orai1, a critical component of store-operated Ca2+ entry, is functionally associated with Na+/Ca2+ exchanger and plasma membrane Ca2+ pump in proliferating human arterial myocytes. Am J Physiol Cell Physiol 297:C1103–C1112

    Article  PubMed  CAS  Google Scholar 

  29. Potier M, Gonzalez JC, Motiani RK, Abdullaev IF, Bisaillon JM, Singer HA, Trebak M (2009) Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J 23:2425–2437

    Article  PubMed  CAS  Google Scholar 

  30. Mercer JC, Dehaven WI, Smyth JT, Wedel B, Boyles RR, Bird GS, Putney JW Jr (2006) Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem 281:24979–24990

    Article  PubMed  CAS  Google Scholar 

  31. Gross SA, Wissenbach U, Philipp SE, Freichel M, Cavalie A, Flockerzi V (2007) Murine ORAI2 splice variants form functional Ca2+ release-activated Ca2+ (CRAC) channels. J Biol Chem 282:19375–19384

    Article  PubMed  CAS  Google Scholar 

  32. Vig M, DeHaven WI, Bird GS, Billingsley JM, Wang H, Rao PE, Hutchings AB, Jouvin MH, Putney JW, Kinet JP (2008) Defective mast cell effector functions in mice lacking the CRACM1 pore subunit of store-operated calcium release-activated calcium channels. Nat Immunol 9:89–96

    Article  PubMed  CAS  Google Scholar 

  33. Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S (2007) STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol 9:636–645

    Article  PubMed  CAS  Google Scholar 

  34. Parekh AB, Putney JW Jr (2005) Store-operated calcium channels. Physiol Rev 85:757–810

    Article  PubMed  CAS  Google Scholar 

  35. Dietrich A, Kalwa H, Fuchs B, Grimminger F, Weissmann N, Gudermann T (2007) In vivo TRPC functions in the cardiopulmonary vasculature. Cell Calcium 42:233–244

    Article  PubMed  CAS  Google Scholar 

  36. 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–C330

    PubMed  CAS  Google Scholar 

  37. Sweeney M, Yu Y, Platoshyn O, Zhang S, McDaniel SS, Yuan JX (2002) Inhibition of endogenous TRP1 decreases capacitative Ca2+ entry and attenuates pulmonary artery smooth muscle cell proliferation. Am J Physiol Lung Cell Mol Physiol 283:L144–L155

    PubMed  CAS  Google Scholar 

  38. Liao Y, Plummer NW, George MD, Abramowitz J, Zhu MX, Birnbaumer L (2009) A role for Orai in TRPC-mediated Ca2+ entry suggests that a TRPC:Orai complex may mediate store and receptor operated Ca2+ entry. Proc Natl Acad Sci USA 106:3202–3206

    Article  PubMed  CAS  Google Scholar 

  39. DeHaven WI, Jones BF, Petranka JG, Smyth JT, Tomita T, Bird GS, Putney JW Jr (2009) TRPC channels function independently of STIM1 and Orai1. J Physiol 587:2275–2298

    Article  PubMed  CAS  Google Scholar 

  40. Arnon A, Hamlyn JM, Blaustein MP (2000) Na(+) entry via store-operated channels modulates Ca(2+) signaling in arterial myocytes. Am J Physiol Cell Physiol 278:C163–C173

    PubMed  CAS  Google Scholar 

  41. Dai J, Lee CH, Poburko D, Szado T, Kuo KH, van Breemen C (2007) Endothelin-1-mediated wave-like [Ca2+]i oscillations in intact rabbit inferior vena cava. J Vasc Res 44:495–503

    Article  PubMed  CAS  Google Scholar 

  42. Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, Tang XD, Gill DL (2010) The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330:105–109

    Article  PubMed  CAS  Google Scholar 

  43. Park CY, Shcheglovitov A, Dolmetsch R (2010) The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 330:101–105

    Article  PubMed  CAS  Google Scholar 

  44. Mignen O, Shuttleworth TJ (2000) I(ARC), a novel arachidonate-regulated, noncapacitative Ca(2+) entry channel. J Biol Chem 275:9114–9119

    Article  PubMed  CAS  Google Scholar 

  45. Mignen O, Thompson JL, Shuttleworth TJ (2007) STIM1 regulates Ca2+ entry via arachidonate-regulated Ca2+−selective (ARC) channels without store depletion or translocation to the plasma membrane. J Physiol 579:703–715

    Article  PubMed  CAS  Google Scholar 

  46. Mignen O, Thompson JL, Shuttleworth TJ (2009) The molecular architecture of the arachidonate-regulated Ca2+−selective ARC channel is a pentameric assembly of Orai1 and Orai3 subunits. J Physiol 587:4181–4197

    Article  PubMed  CAS  Google Scholar 

  47. Demuth DG, Gkoumassi E, Droge MJ, Dekkers BG, Esselink HJ, van Ree RM, Parsons ME, Zaagsma J, Molleman A, Nelemans SA (2005) Arachidonic acid mediates non-capacitative calcium entry evoked by CB1-cannabinoid receptor activation in DDT1 MF-2 smooth muscle cells. J Cell Physiol 205:58–67

    Article  PubMed  CAS  Google Scholar 

  48. Taylor CW, Moneer Z (2004) Regulation of capacitative and non-capacitative Ca2+ entry in A7r5 vascular smooth muscle cells. Biol Res 37:641–645

    Article  PubMed  Google Scholar 

  49. Trebak M (2011) Review of transient receptor potential channels. Channels (Austin) 5:188–190

    Article  Google Scholar 

  50. Earley S, Heppner TJ, Nelson MT, Brayden JE (2005) TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ Res 97:1270–1279

    Article  PubMed  CAS  Google Scholar 

  51. Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, Imaizumi Y (2003) TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93:829–838

    Article  PubMed  CAS  Google Scholar 

  52. Sharif-Naeini R, Folgering JH, Bichet D, Duprat F, Lauritzen I, Arhatte M, Jodar M, Dedman A, Chatelain FC, Schulte U, Retailleau K, Loufrani L, Patel A, Sachs F, Delmas P, Peters DJ, Honore E (2009) Polycystin-1 and −2 dosage regulates pressure sensing. Cell 139:587–596

    Article  PubMed  CAS  Google Scholar 

  53. 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

    Article  PubMed  CAS  Google Scholar 

  54. Husain M, Jiang L, See V, Bein K, Simons M, Alper SL, Rosenberg RD (1997) Regulation of vascular smooth muscle cell proliferation by plasma membrane Ca(2+)-ATPase. Am J Physiol 272:C1947–C1959

    PubMed  CAS  Google Scholar 

  55. Buch MH, Pickard A, Rodriguez A, Gillies S, Maass AH, Emerson M, Cartwright EJ, Williams JC, Oceandy D, Redondo JM, Neyses L, Armesilla AL (2005) The sarcolemmal calcium pump inhibits the calcineurin/nuclear factor of activated T-cell pathway via interaction with the calcineurin A catalytic subunit. J Biol Chem 280:29479–29487

    Article  PubMed  CAS  Google Scholar 

  56. Blaustein MP, Golovina VA, Song H, Choate J, Lencesova L, Robinson SW, Wier WG (2002) Organization of Ca2+ stores in vascular smooth muscle: functional implications. Novartis Found Symp 246:125–137, discussion 137–141, 221–127

    Article  PubMed  CAS  Google Scholar 

  57. Zhang J, Ren C, Chen L, Navedo MF, Antos LK, Kinsey SP, Iwamoto T, Philipson KD, Kotlikoff MI, Santana LF, Wier WG, Matteson DR, Blaustein MP (2010) Knockout of Na+/Ca2+ exchanger in smooth muscle attenuates vasoconstriction and L-type Ca2+ channel current and lowers blood pressure. Am J Physiol Heart Circ Physiol 298:H1472–H1483

    Article  PubMed  CAS  Google Scholar 

  58. Klemm DJ, Watson PA, Frid MG, Dempsey EC, Schaack J, Colton LA, Nesterova A, Stenmark KR, Reusch JE (2001) cAMP response element-binding protein content is a molecular determinant of smooth muscle cell proliferation and migration. J Biol Chem 276:46132–46141

    Article  PubMed  CAS  Google Scholar 

  59. Kamiya K, Sakakibara K, Ryer EJ, Hom RP, Leof EB, Kent KC, Liu B (2007) Phosphorylation of the cyclic AMP response element binding protein mediates transforming growth factor beta-induced downregulation of cyclin A in vascular smooth muscle cells. Mol Cell Biol 27:3489–3498

    Article  PubMed  CAS  Google Scholar 

  60. Deisseroth K, Heist EK, Tsien RW (1998) Translocation of calmodulin to the nucleus supports CREB phosphorylation in hippocampal neurons. Nature 392:198–202

    Article  PubMed  CAS  Google Scholar 

  61. Dolmetsch RE, Pajvani U, Fife K, Spotts JM, Greenberg ME (2001) Signaling to the nucleus by an L-type calcium channel-calmodulin complex through the MAP kinase pathway. Science 294:333–339

    Article  PubMed  CAS  Google Scholar 

  62. Cartin L, Lounsbury KM, Nelson MT (2000) Coupling of Ca(2+) to CREB activation and gene expression in intact cerebral arteries from mouse: roles of ryanodine receptors and voltage-dependent Ca(2+) channels. Circ Res 86:760–767

    PubMed  CAS  Google Scholar 

  63. Stevenson AS, Gomez MF, Hill-Eubanks DC, Nelson MT (2001) NFAT4 movement in native smooth muscle. A role for differential Ca(2+) signaling. J Biol Chem 276:15018–15024

    Article  PubMed  CAS  Google Scholar 

  64. Gwack Y, Feske S, Srikanth S, Hogan PG, Rao A (2007) Signalling to transcription: store-operated Ca2+ entry and NFAT activation in lymphocytes. Cell Calcium 42:145–156

    Article  PubMed  CAS  Google Scholar 

  65. 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 

  66. Ambros V (2004) The functions of animal microRNAs. Nature 431:350–355

    Article  PubMed  CAS  Google Scholar 

  67. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  PubMed  CAS  Google Scholar 

  68. Small EM, Olson EN (2011) Pervasive roles of microRNAs in cardiovascular biology. Nature 469:336–342

    Article  PubMed  CAS  Google Scholar 

  69. Song Z, Li G (2010) Role of specific microRNAs in regulation of vascular smooth muscle cell differentiation and the response to injury. J Cardiovasc Transl Res 3:246–250

    Article  PubMed  Google Scholar 

  70. Cordes KR, Sheehy NT, White MP, Berry EC, Morton SU, Muth AN, Lee TH, Miano JM, Ivey KN, Srivastava D (2009) miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460:705–710

    PubMed  CAS  Google Scholar 

  71. Quintavalle M, Elia L, Condorelli G, Courtneidge SA (2010) MicroRNA control of podosome formation in vascular smooth muscle cells in vivo and in vitro. J Cell Biol 189:13–22

    Article  PubMed  CAS  Google Scholar 

  72. Wang X, Hu G, Zhou J (2010) Repression of versican expression by microRNA-143. J Biol Chem 285:23241–23250

    Article  PubMed  CAS  Google Scholar 

  73. 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 

  74. 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 

  75. Quignard JF, Harricane MC, Menard C, Lory P, Nargeot J, Capron L, Mornet D, Richard S (2001) Transient down-regulation of L-type Ca(2+) channel and dystrophin expression after balloon injury in rat aortic cells. Cardiovasc Res 49:177–188

    Article  PubMed  CAS  Google Scholar 

  76. Nieves-Cintron M, Amberg GC, Navedo MF, Molkentin JD, Santana LF (2008) The control of Ca2+ influx and NFATc3 signaling in arterial smooth muscle during hypertension. Proc Natl Acad Sci USA 105:15623–15628

    Article  PubMed  CAS  Google Scholar 

  77. Golovina VA (1999) Cell proliferation is associated with enhanced capacitative Ca(2+) entry in human arterial myocytes. Am J Physiol 277:C343–C349

    PubMed  CAS  Google Scholar 

  78. Bisaillon JM, Motiani RK, Gonzalez-Cobos JC, Potier M, Halligan KE, Alzawahra WF, Barroso M, Singer HA, Jourd’heuil D, Trebak M (2010) Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration. Am J Physiol Cell Physiol 298:C993–C1005

    Article  PubMed  CAS  Google Scholar 

  79. Aubart FC, Sassi Y, Coulombe A, Mougenot N, Vrignaud C, Leprince P, Lechat P, Lompre AM, Hulot JS (2009) RNA interference targeting STIM1 suppresses vascular smooth muscle cell proliferation and neointima formation in the rat. Mol Ther 17:455–462

    Article  PubMed  CAS  Google Scholar 

  80. Guo RW, Wang H, Gao P, Li MQ, Zeng CY, Yu Y, Chen JF, Song MB, Shi YK, Huang L (2009) An essential role for stromal interaction molecule 1 in neointima formation following arterial injury. Cardiovasc Res 81:660–668

    Article  PubMed  CAS  Google Scholar 

  81. Berra-Romani R, Mazzocco-Spezzia A, Pulina MV, Golovina VA (2008) Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Cell Physiol 295:C779–C790

    Article  PubMed  CAS  Google Scholar 

  82. Kunichika N, Yu Y, Remillard CV, Platoshyn O, Zhang S, Yuan JX (2004) Overexpression of TRPC1 enhances pulmonary vasoconstriction induced by capacitative Ca2+ entry. Am J Physiol Lung Cell Mol Physiol 287:L962–L969

    Article  PubMed  CAS  Google Scholar 

  83. Sweeney M, McDaniel SS, Platoshyn O, Zhang S, Yu Y, Lapp BR, Zhao Y, Thistlethwaite PA, Yuan JX (2002) Role of capacitative Ca2+ entry in bronchial contraction and remodeling. J Appl Physiol 92:1594–1602

    PubMed  CAS  Google Scholar 

  84. Xu SZ, Muraki K, Zeng F, Li J, Sukumar P, Shah S, Dedman AM, Flemming PK, McHugh D, Naylor J, Cheong A, Bateson AN, Munsch CM, Porter KE, Beech DJ (2006) A sphingosine-1-phosphate-activated calcium channel controlling vascular smooth muscle cell motility. Circ Res 98:1381–1389

    Article  PubMed  CAS  Google Scholar 

  85. Zhang S, Remillard CV, Fantozzi I, Yuan JX (2004) ATP-induced mitogenesis is mediated by cyclic AMP response element-binding protein-enhanced TRPC4 expression and activity in human pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 287:C1192–C1201

    Article  PubMed  CAS  Google Scholar 

  86. Lin MJ, Leung GP, Zhang WM, Yang XR, Yip KP, Tse CM, Sham JS (2004) Chronic hypoxia-induced upregulation of store-operated and receptor-operated Ca2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ Res 95:496–505

    Article  PubMed  CAS  Google Scholar 

  87. Liu D, Yang D, He H, Chen X, Cao T, Feng X, Ma L, Luo Z, Wang L, Yan Z, Zhu Z, Tepel M (2009) Increased transient receptor potential canonical type 3 channels in vasculature from hypertensive rats. Hypertension 53:70–76

    Article  PubMed  CAS  Google Scholar 

  88. Pulina MV, Zulian A, Berra-Romani R, Beskina O, Mazzocco-Spezzia A, Baryshnikov SG, Papparella I, Hamlyn JM, Blaustein MP, Golovina VA (2010) Upregulation of Na+ and Ca2+ transporters in arterial smooth muscle from ouabain-induced hypertensive rats. Am J Physiol Heart Circ Physiol 298:H263–H274

    Article  PubMed  CAS  Google Scholar 

  89. 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 

  90. 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 

  91. Bobe R, Hadri L, Lopez JJ, Sassi Y, Atassi F, Karakikes I, Liang L, Limon I, Lompre AM, Hatem SN, Hajjar RJ, Lipskaia L (2011) SERCA2a controls the mode of agonist-induced intracellular Ca(2+) signal, transcription factor NFAT and proliferation in human vascular smooth muscle cells. J Mol Cell Cardiol 50:621–633

    Article  PubMed  CAS  Google Scholar 

  92. 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

    Article  PubMed  CAS  Google Scholar 

  93. Schauer IE, Knaub LA, Lloyd M, Watson PA, Gliwa C, Lewis KE, Chait A, Klemm DJ, Gunter JM, Bouchard R, McDonald TO, O’Brien KD, Reusch JE (2010) CREB downregulation in vascular disease: a common response to cardiovascular risk. Arterioscler Thromb Vasc Biol 30:733–741

    Article  PubMed  CAS  Google Scholar 

  94. Chava KR, Karpurapu M, Wang D, Bhanoori M, Kundumani-Sridharan V, Zhang Q, Ichiki T, Glasgow WC, Rao GN (2009) CREB-mediated IL-6 expression is required for 15(S)-hydroxyeicosatetraenoic acid-induced vascular smooth muscle cell migration. Arterioscler Thromb Vasc Biol 29:809–815

    Article  PubMed  CAS  Google Scholar 

  95. Ono H, Ichiki T, Fukuyama K, Iino N, Masuda S, Egashira K, Takeshita A (2004) cAMP-response element-binding protein mediates tumor necrosis factor-alpha-induced vascular smooth muscle cell migration. Arterioscler Thromb Vasc Biol 24:1634–1639

    Article  PubMed  CAS  Google Scholar 

  96. Tokunou T, Shibata R, Kai H, Ichiki T, Morisaki T, Fukuyama K, Ono H, Iino N, Masuda S, Shimokawa H, Egashira K, Imaizumi T, Takeshita A (2003) Apoptosis induced by inhibition of cyclic AMP response element-binding protein in vascular smooth muscle cells. Circulation 108:1246–1252

    Article  PubMed  CAS  Google Scholar 

  97. Chen J, Jiang H, Xu L, Zhu LH, Wang L, Wen HZ, Hu XR (2008) Dysregulation of CREB binding protein triggers thrombin-induced proliferation of vascular smooth muscle cells. Mol Cell Biochem 315:123–130

    Article  PubMed  CAS  Google Scholar 

  98. 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 

  99. 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 

  100. Karpurapu M, Wang D, Van Quyen D, Kim TK, Kundumani-Sridharan V, Pulusani S, Rao GN (2010) Cyclin D1 is a bona fide target gene of NFATc1 and is sufficient in the mediation of injury-induced vascular wall remodeling. J Biol Chem 285:3510–3523

    Article  PubMed  CAS  Google Scholar 

  101. House SJ, Ginnan RG, Armstrong SE, Singer HA (2007) Calcium/calmodulin-dependent protein kinase II-delta isoform regulation of vascular smooth muscle cell proliferation. Am J Physiol Cell Physiol 292:C2276–C2287

    Article  PubMed  CAS  Google Scholar 

  102. Ji R, Cheng Y, Yue J, Yang J, Liu X, Chen H, Dean DB, Zhang C (2007) MicroRNA expression signature and antisense-mediated depletion reveal an essential role of MicroRNA in vascular neointimal lesion formation. Circ Res 100:1579–1588

    Article  PubMed  CAS  Google Scholar 

  103. Liu X, Cheng Y, Zhang S, Lin Y, Yang J, Zhang C (2009) A necessary role of miR-221 and miR-222 in vascular smooth muscle cell proliferation and neointimal hyperplasia. Circ Res 104:476–487

    Article  PubMed  CAS  Google Scholar 

  104. Sun SG, Zheng B, Han M, Fang XM, Li HX, Miao SB, Su M, Han Y, Shi HJ, Wen JK (2011) miR-146a and Kruppel-like factor 4 form a feedback loop to participate in vascular smooth muscle cell proliferation. EMBO Rep 12:56–62

    Article  PubMed  CAS  Google Scholar 

  105. Ikeda S, He A, Kong SW, Lu J, Bejar R, Bodyak N, Lee KH, Ma Q, Kang PM, Golub TR, Pu WT (2009) MicroRNA-1 negatively regulates expression of the hypertrophy-associated calmodulin and Mef2a genes. Mol Cell Biol 29:2193–2204

    Article  PubMed  CAS  Google Scholar 

  106. Dong DL, Chen C, Huo R, Wang N, Li Z, Tu YJ, Hu JT, Chu X, Huang W, Yang BF (2010) Reciprocal repression between microRNA-133 and calcineurin regulates cardiac hypertrophy: a novel mechanism for progressive cardiac hypertrophy. Hypertension 55:946–952

    Article  PubMed  CAS  Google Scholar 

  107. Li Q, Lin X, Yang X, Chang J (2010) NFATc4 is negatively regulated in miR-133a-mediated cardiomyocyte hypertrophic repression. Am J Physiol Heart Circ Physiol 298:H1340–H1347

    Article  PubMed  CAS  Google Scholar 

  108. da Costa Martins PA, Salic K, Gladka MM, Armand AS, Leptidis S, el Azzouzi H, Hansen A, Coenen-de Roo CJ, Bierhuizen MF, van der Nagel R, van Kuik J, de Weger R, de Bruin A, Condorelli G, Arbones ML, Eschenhagen T, De Windt LJ (2010) MicroRNA-199b targets the nuclear kinase Dyrk1a in an auto-amplification loop promoting calcineurin/NFAT signalling. Nat Cell Biol 12:1220–1227

    Article  PubMed  CAS  Google Scholar 

  109. Lin Z, Murtaza I, Wang K, Jiao J, Gao J, Li PF (2009) miR-23a functions downstream of NFATc3 to regulate cardiac hypertrophy. Proc Natl Acad Sci USA 106:12103–12108

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Anne-Marie Lompré .

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Marchand, A., Abi-Gerges, A., Saliba, Y., Merlet, E., Lompré, AM. (2012). Calcium Signaling in Vascular Smooth Muscle Cells: From Physiology to Pathology. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 740. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-2888-2_35

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