SERCA2a controls the mode of agonist-induced intracellular Ca2+ signal, transcription factor NFAT and proliferation in human vascular smooth muscle cells

Journal of Molecular and Cellular Cardiology

Volumn 50, Issue 4, 2011, Pages 621-633

  Bobe, Regis ^a   Hadri, Lahouaria ^b   Lopez, Jose J ^a   Sassi, Yassine ^c   Atassi, Fabrice ^c   Karakikes, Ioannis ^b   Liang, Lifan ^b   Limon, Isabelle ^d   Lompré, Anne Marie ^c   Hatem, Stephane N ^c   Hajjar, Roger J ^b   Lipskaia, Larissa ^b,c  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c UPMC Paris 6 ^*  (France)

^d SORBONNE UNIVERSITÉ   (France)

Author keywords

Calcium oscillations; NFAT; Proliferation; SERCA; Signal transduction; Store operated calcium entry

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE 2A; STROMAL INTERACTION MOLECULE 1; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

ARTERY MUSCLE; ARTICLE; BLOOD VESSEL TONE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY ARTERY; GENE TRANSFER; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOPLASMIC RETICULUM; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

BLOTTING, WESTERN; CALCIUM; CALCIUM SIGNALING; CELL MOVEMENT; CELL PROLIFERATION; CELLS, CULTURED; CORONARY VESSELS; CYCLIN D1; HUMANS; IMMUNOPRECIPITATION; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NFATC TRANSCRIPTION FACTORS; POLYMERASE CHAIN REACTION; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SIGNAL TRANSDUCTION;

EID: 79952071451     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2010.12.016     Document Type: Article

References (50)

1. Wamhoff B.R., Bowles D.K., Owens G.K. Excitation-transcription coupling in arterial smooth muscle. Circ Res 2006 Apr 14, 98(7):868-878.
2. House S.J., Potier M., Bisaillon J., Singer H.A., Trebak M. The non-excitable smooth muscle: calcium signaling and phenotypic switching during vascular disease. Pflugers Arch Aug 2008, 456(5):769-785.
3. Owens G.K., Kumar M.S., Wamhoff B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev Jul 2004, 84(3):767-801.
4. Gollasch M., Haase H., Ried C., Lindschau C., Morano I., Luft F.C., et al. L-type calcium channel expression depends on the differentiated state of vascular smooth muscle cells. FASEB J May 1998, 12(7):593-601.
5. 2+) channel and dystrophin expression after balloon injury in rat aortic cells. Cardiovasc Res Jan 2001, 49(1):177-188.
6. 2+-ATPase gene transfer reduces vascular smooth muscle cell proliferation and neointima formation in the rat. Circ Res Sep 2 2005, 97(5):488-495.
7. Lipskaia L., Pourci M.L., Delomenie C., Combettes L., Goudouneche D., Paul J.L., et al. Phosphatidylinositol 3-kinase and calcium-activated transcription pathways are required for VLDL-induced smooth muscle cell proliferation. Circ Res May 30 2003, 92(10):1115-1122.
8. Massaeli H., Austria J.A., Pierce G.N. Lesions in ryanodine channels in smooth muscle cells exposed to oxidized low density lipoprotein. Arterioscler Thromb Vasc Biol Feb 2000, 20(2):328-334.
9. 2+)-dependent vascular remodeling in the Syrian hamster. Am J Pathol Jul 2007, 171(1):162-171.
10. Berridge M.J. Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta Jun 2009, 1793(6):933-940.
11. Lewis R.S. The molecular choreography of a store-operated calcium channel. Nature Mar 15 2007, 446(7133):284-287.
12. 2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture. Am J Physiol Sep 2008, 295(3):C779-C790.
13. Potier M., Gonzalez J.C., Motiani R.K., Abdullaev I.F., Bisaillon J.M., Singer H.A., et al. Evidence for STIM1- and Orai1-dependent store-operated calcium influx through ICRAC in vascular smooth muscle cells: role in proliferation and migration. FASEB J Aug 2009, 23(8):2425-2437.
14. Albert A.P., Saleh S.N., Peppiatt-Wildman C.M., Large W.A. Multiple activation mechanisms of store-operated TRPC channels in smooth muscle cells. J Physiol Aug 15 2007, 583(Pt 1):25-36.
15. 2+ response amplitude and duration. Nature Apr 24 1997, 386(6627):855-858.
16. Liu Z., Zhang C., Dronadula N., Li Q., Rao G.N. 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 Apr 15 2005, 280(15):14700-14708.
17. Peel S.E., Liu B., Hall I.P. ORAI and store-operated calcium influx in human airway smooth muscle cells. Am J Respir Cell Mol Biol Jun 2008, 38(6):744-749.
18. Takahashi Y., Watanabe H., Murakami M., Ono K., Munehisa Y., Koyama T., et al. Functional role of stromal interaction molecule 1 (STIM1) in vascular smooth muscle cells. Biochem Biophys Res Commun Oct 5 2007, 361(4):934-940.
19. Sweeney M., Yu Y., Platoshyn O., Zhang S., McDaniel S.S., Yuan J.X. Inhibition of endogenous TRP1 decreases capacitative Ca2+ entry and attenuates pulmonary artery smooth muscle cell proliferation. Am J Physiol Lung Cell Mol Physiol Jul 2002, 283(1):L144-L155.
20. Yu H., Sliedregt-Bol K., Overkleeft H., van der Marel G.A., van Berkel T.J., Biessen E.A. Therapeutic potential of a synthetic peptide inhibitor of nuclear factor of activated T cells as antirestenotic agent. Arterioscler Thromb Vasc Biol Jul 2006, 26(7):1531-1537.
21. Aubart F.C., Sassi Y., Coulombe A., Mougenot N., Vrignaud C., Leprince P., et al. RNA interference targeting STIM1 suppresses vascular smooth muscle cell proliferation and neointima formation in the rat. Mol Ther Mar 2009, 17(3):455-462.
22. Eggermont J.A., Wuytack F., Verbist J., Casteels R. Expression of endoplasmic-reticulum Ca2(+)-pump isoforms and of phospholamban in pig smooth-muscle tissues. Biochem J Nov 1 1990, 271(3):649-653.
23. Marty I., Robert M., Villaz M., De Jongh K., Lai Y., Catterall W.A., et al. Biochemical evidence for a complex involving dihydropyridine receptor and ryanodine receptor in triad junctions of skeletal muscle. Proc Natl Acad Sci USA Mar 15 1994, 91(6):2270-2274.
24. del Monte F., Harding S.E., Schmidt U., Matsui T., Kang Z.B., Dec G.W., et al. Restoration of contractile function in isolated cardiomyocytes from failing human hearts by gene transfer of SERCA2a. Circulation Dec 7 1999, 100(23):2308-2311.
25. Aramburu J., Garcia-Cozar F., Raghavan A., Okamura H., Rao A., Hogan P.G. Selective inhibition of NFAT activation by a peptide spanning the calcineurin targeting site of NFAT. Mol Cell Apr 1998, 1(5):627-637.
26. Aramburu J., Yaffe M.B., Lopez-Rodriguez C., Cantley L.C., Hogan P.G., Rao A. Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A. Science Sep 24 1999, 285(5436):2129-2133. New York, NY.
27. Rinne A., Banach K., Blatter L.A. Regulation of nuclear factor of activated T cells (NFAT) in vascular endothelial cells. J Mol Cell Cardiol Sep 2009, 47(3):400-410.
28. Hao H., Gabbiani G., Bochaton-Piallat M.L. Arterial smooth muscle cell heterogeneity: implications for atherosclerosis and restenosis development. Arterioscler Thromb Vasc Biol Sep 1 2003, 23(9):1510-1520.
29. Schwartz S.M., deBlois D., O'Brien E.R. The intima. Soil for atherosclerosis and restenosis. Circ Res Sep 1995, 77(3):445-465.
30. Stary H.C., Blankenhorn D.H., Chandler A.B., Glagov S., Insull W., Richardson M., et al. A definition of the intima of human arteries and of its atherosclerosis-prone regions. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Arterioscler Thromb Jan 1992, 12(1):120-134.
31. Rekhter M.D., Simari R.D., Work C.W., Nabel G.J., Nabel E.G., Gordon D. Gene transfer into normal and atherosclerotic human blood vessels. Circ Res Jun 29 1998, 82(12):1243-1252.
32. Gueguen M, Keuylian Z, Mateo V, Mougenot N, Lompre AM, Michel JB, et al. Implication of adenylyl cyclase 8 in pathological smooth muscle cell migration occurring in rat and human vascular remodelling. The Journal of pathology. Jul 2010;221(3): 331-42.
33. 2+ release. FASEB J Aug 2002, 16(10):1145-1150.
34. Faehling M., Kroll J., Fohr K.J., Fellbrich G., Mayr U., Trischler G., et al. Essential role of calcium in vascular endothelial growth factor A-induced signaling: mechanism of the antiangiogenic effect of carboxyamidotriazole. FASEB J Nov 2002, 16(13):1805-1807.
35. Yellaturu C.R., Ghosh S.K., Rao R.K., Jennings L.K., Hassid A., Rao G.N. 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 Nov 15 2002, 368(Pt 1):183-190.
36. Berridge M.J. Smooth muscle cell calcium activation mechanisms. J Physiol Nov 1 2008, 586(Pt 21):5047-5061.
37. Hadri L, Bobe R, Kawase Y, Ladage D, Ishikawa K, Atassi F, et al. SERCA2a gene transfer enhances eNOS expression and activity in endothelial cells. Mol Ther. Jul 2010;18(7): 1284-92.
38. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature Jan 28 1993, 361(6410):315-325.
39. Berridge M.J. Inositol trisphosphate and calcium oscillations. Biochem Soc Symp 2007, (74):1-7.
40. Berridge M.J., Dupont G. Spatial and temporal signalling by calcium. Curr Opin Cell Biol Apr 1994, 6(2):267-274.
41. 2+)-ATPases are on opposite sides of the membrane. J Biol Chem May 5 1992, 267(13):9321-9325.
42. 2+-ATPase (SERCA) 1 and 2 isoforms and characterization of Darier disease (SERCA2) mutants by steady-state and transient kinetic analyses. J Biol Chem Nov 28 2003, 278(48):47877-47889.
43. 2+-ATPase 2 isoform (SERCA2c). Biochem J Apr 15 2006, 395(2):249-258.
44. Bobe R., Bredoux R., Corvazier E., Lacabaratz-Porret C., Martin V., Kovacs T., et al. How many Ca(2)+ATPase isoforms are expressed in a cell type? A growing family of membrane proteins illustrated by studies in platelets. Platelets May-Jun 2005, 16(3-4):133-150.
45. 2+ entry and NFAT activation in lymphocytes. Cell Calcium Aug 2007, 42(2):145-156.
46. 2+ sparklet activity in arterial smooth muscle. J Gen Physiol Jun 2006, 127(6):611-622.
47. 2+ influx and NFATc3 signaling in arterial smooth muscle during hypertension. Proc Natl Acad Sci USA Oct 7 2008, 105(40):15623-15628.
48. Amberg G.C., Bonev A.D., Rossow C.F., Nelson M.T., Santana L.F. Modulation of the molecular composition of large conductance, Ca(2+) activated K(+) channels in vascular smooth muscle during hypertension. J Clin Investig Sep 2003, 112(5):717-724.
49. Wellman G.C., Santana L.F., Bonev A.D., Nelson M.T. Role of phospholamban in the modulation of arterial Ca(2+) sparks and Ca(2+)-activated K(+) channels by cAMP. Am J Physiol Sep 2001, 281(3):C1029-C1037.
50. Mercer J.C., Dehaven W.I., Smyth J.T., Wedel B., Boyles R.R., Bird G.S., et al. Large store-operated calcium selective currents due to co-expression of Orai1 or Orai2 with the intracellular calcium sensor, Stim1. J Biol Chem Aug 25 2006, 281(34):24979-24990.