Inhibition of Orai1-mediated Ca2+ entry is a key mechanism of the antiproliferative action of sirolimus in human arterial smooth muscle

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 305, Issue 11, 2013, Pages

  König, Sarah ^a   Browne, Sara ^a   Doleschal, Bernhard ^a   Schernthaner, Michaela ^a   Poteser, Michael ^a   Mächler, Heinrich ^a   Wittchow, Eric ^b   Braune, Marlen ^b   Muik, Martin ^c   Romanin, Christoph ^c   Groschner, Klaus ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b Biotronik Societas Europaea and Compagnie Kommanditgesellschaft   (Germany)

^c JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

Author keywords

Calcium signaling; Coronary restenosis; CREB; NFAT; Sirolimus

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; PIMECROLIMUS; RAPAMYCIN; THAPSIGARGIN;

ANTIPROLIFERATIVE ACTIVITY; ARTERY MUSCLE; ARTICLE; ASCENDING AORTA; BARE METAL STENT; CALCIUM CURRENT; CALCIUM SIGNALING; CELL PROLIFERATION; CONTROLLED STUDY; CORONARY ARTERY; CORONARY STENT; DRUG ELUTING STENT; DRUG MECHANISM; ELECTROPHYSIOLOGY; EX VIVO STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTRACELLULAR SIGNALING; NEOINTIMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIROLIMUS ELUTING STENT; SMOOTH MUSCLE FIBER;

CALCIUM SIGNALING; CORONARY RESTENOSIS; CREB; NFAT; SIROLIMUS;

AORTA; CALCIUM CHANNELS; CALCIUM SIGNALING; CARDIOVASCULAR AGENTS; CELL PROLIFERATION; CORONARY VESSELS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE KNOCKOUT TECHNIQUES; HEK293 CELLS; HUMANS; HYPERPLASIA; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NFATC TRANSCRIPTION FACTORS; PHOSPHORYLATION; SIROLIMUS; STENTS; TACROLIMUS; TIME FACTORS; TISSUE CULTURE TECHNIQUES; TRANSCRIPTION, GENETIC; TRANSFECTION;

EID: 84888875760     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00365.2013     Document Type: Article

References (54)

1. 2+ pump in proliferating human arterial myocytes. Am J Physiol Cell Physiol 297: C1103-C1112, 2009.
2. Berg R, Aragon J, Royter V, Shanley JF, Cogert G, Vermani R, Kar S, Eigler N, Litvack F. Pimecrolimus and dual pimecrolimus-paclitaxel eluting stents decrease neointimal proliferation in a porcine model. Catheter Cardiovasc Interv 70: 871-879, 2007.
3. Burt HM, Hunter WL. Drug-eluting stents: a multidisciplinary success story. Adv Drug Deliv Rev 58: 350-357, 2006.
4. Chen WJ, Chen YH, Lin KH, Ting CH, Yeh YH. Cilostazol promotes vascular smooth muscles cell differentiation through the cAMP response element-binding protein-dependent pathway. Arterioscler Thromb Vasc Biol 31: 2106-2113, 2011.
5. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J. Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 105: 17414-17419, 2008.
6. 2+ entry via TRPCencoded receptor-operated channels in human aortic smooth muscle cells. Am J Physiol Cell Physiol 301: C461-C468, 2011.
7. Cioffi DL, Hubler TR, Scammell JG. Organization and function of the FKBP52 and FKBP51 genes. Curr Opin Pharmacol 11: 308-313, 2011.
8. Clever YP, Cremers B, Krauss B, Bohm M, Speck U, Laufs U, Scheller B. Paclitaxel and sirolimus differentially affect growth and motility of endothelial progenitor cells and coronary artery smooth muscle cells. EuroIntervention 7, Suppl K: K32-K42, 2011.
9. Costa MA, Simon DI. Molecular basis of restenosis and drug-eluting stents. Circulation 111: 2257-2273, 2005.
10. Derler I, Hofbauer M, Kahr H, Fritsch R, Muik M, Kepplinger K, Hack ME, Moritz S, Schindl R, Groschner K, Romanin C. Dynamic but not constitutive association of calmodulin with rat TRPV6 channels enables fine tuning of Ca2+-dependent inactivation. J Physiol 577: 31-44, 2006.
11. Duan C, Liimatta MB, Bottum OL. Insulin-like growth factor (IGF)-I regulates IGF-binding protein-5 gene expression through the phosphatidylinositol 3-kinase, protein kinase B/Akt, and p70 S6 kinase signaling pathway. J Biol Chem 274: 37147-37153, 1999.
12. Giordano A, Romano A. Inhibition of human in-stent restenosis: a molecular view. Curr Opin Pharmacol 11: 372-377, 2011.
13. Gonzalez-Cobos JC, Zhang X, Zhang W, Ruhle B, Motiani RK, Schindl R, Muik M, Spinelli AM, Bisaillon JM, Shinde AV, Fahrner M, Singer HA, Matrougui K, Barroso M, Romanin C, Trebak M. Store-independent Orai1/3 channels activated by intracrine leukotriene C4: role in neointimal hyperplasia. Circ Res 112: 1013-1025, 2013.
14. Gui Y, He G, Walsh MP, Zheng XL. Signaling mechanisms mediating Up4A-induced proliferation of human vascular smooth muscle cells. J Cardiovasc Pharmacol 58: 654-662, 2011.
15. Harding MW, Galat A, Uehling DE, Schreiber SL. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 341: 758-760, 1989.
16. Ke H, Huai Q. Structures of calcineurin and its complexes with immunophilins-immunosuppressants. Biochem Biophys Res Commun 311: 1095-1102, 2003.
17. Kehlenbach RH, Dickmanns A, Gerace L. Nucleocytoplasmic shuttling factors including Ran and CRM1 mediate nuclear export of NFAT in vitro. J Cell Biol 141: 863-874, 1998.
18. 2+ signaling and phosphatidylinositol 4,5-bisphosphate hydrolysis induced by Gq protein-coupled receptor agonists through an mTOR-dependent pathway. Endocrinology 148: 3246-3257, 2007.
19. Koenig S, Schernthaner M, Maechler H, Hoefler G, Kappe CO, Glasnov TN, Braune M, Wittchow E, Groschner K. A TRPC3 blocker, ethyl-1-(4-(2, 3, 3-trichloroacrylamide)phenyl)-5-(trifluoromethyl)-1Hpyrazole-4-c arboxylate (Pyr3), prevents stent-induced arterial remodeling. J Pharmacol Exp Ther 344: 33-40, 2013.
20. Koppara T, Joner M, Bayer G, Steigerwald K, Diener T, Wittchow E. Histopathological comparison of biodegradable polymer and permanent polymer based sirolimus eluting stents in a porcine model of coronary stent implantation. Thromb Haemost 107: 1161-1171, 2012.
21. Lehnart SE, Huang F, Marx SO, Marks AR. Immunophilins and coupled gating of ryanodine receptors. Curr Top Med Chem 3: 1383-1391, 2003.
22. 2+ entry. Proc Natl Acad Sci USA 106: 3202-3206, 2009.
23. Markova B, Albers C, Breitenbuecher F, Melo JV, Brummendorf TH, Heidel F, Lipka D, Duyster J, Huber C, Fischer T. Novel pathway in Bcr-Abl signal transduction involves Akt-independent, PLC-gamma1-driven activation of mTOR/p70S6-kinase pathway. Oncogene 29: 739-751, 2009.
24. Martin KA, Merenick BL, Ding M, Fetalvero KM, Rzucidlo EM, Kozul CD, Brown DJ, Chiu HY, Shyu M, Drapeau BL, Wagner RJ, Powell RJ. Rapamycin promotes vascular smooth muscle cell differentiation through insulin receptor substrate-1/phosphatidylinositol 3-kinase/Akt2 feedback signaling. J Biol Chem 282: 36112-36120, 2007.
25. Moses JW, Leon MB, Popma JJ, Fitzgerald PJ, Holmes DR, O'Shaughnessy C, Caputo RP, Kereiakes DJ, Williams DO, Teirstein PS, Jaeger JL, Kuntz RE. Sirolimus-eluting stents versus standard stents in patients with stenosis in a native coronary artery. N Engl J Med 349: 1315-1323, 2003.
26. Moses S, Dreja K, Lindqvist A, Lovdahl C, Hellstrand P, Hultgardh-Nilsson A. Smooth muscle cell response to mechanical injury involves intracellular calcium release and ERK1/ERK2 phosphorylation. Exp Cell Res 269: 88-96, 2001.
27. Muik M, Frischauf I, Derler I, Fahrner M, Bergsmann J, Eder P, Schindl R, Hesch C, Polzinger B, Fritsch R, Kahr H, Madl J, Gruber H, Groschner K, Romanin C. Dynamic coupling of the putative coiledcoil domain of ORAI1 with STIM1 mediates ORAI1 channel activation. J Biol Chem 283: 8014-8022, 2008.
28. Nagai R, Suzuki T, Aizawa K, Miyamoto S, Amaki T, Kawai-Kowase K, Sekiguchi KI, Kurabayashi M. Phenotypic modulation of vascular smooth muscle cells: dissection of transcriptional regulatory mechanisms. Ann NY Acad Sci 947: 56-66; discussion 66-57, 2001.
29. Nakamura M, Abizaid A, Hirohata A, Honda Y, Sousa JE, Fitzgerald PJ. Efficacy of reduced-dose sirolimus-eluting stents in the human coronary artery: serial IVUS analysis of neointimal hyperplasia and luminal dimension. Catheter Cardiovasc Interv 70: 946-951, 2007.
30. 2+ entry in cells from endarterectomized tissues of patients with chronic thromboembolic pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 297: L666-L676, 2009.
31. Park SJ, Shim WH, Ho DS, Raizner AE, Park SW, Hong MK, Lee CW, Choi D, Jang Y, Lam R, Weissman NJ, Mintz GS. A paclitaxeleluting stent for the prevention of coronary restenosis. N Engl J Med 348: 1537-1545, 2003.
32. Peattie DA, Harding MW, Fleming MA, DeCenzo MT, Lippke JA, Livingston DJ, Benasutti M. Expression and characterization of human FKBP52, an immunophilin that associates with the 90-kDa heat shock protein and is a component of steroid receptor complexes. Proc Natl Acad Sci USA 89: 10974-10978, 1992.
33. Peel SE, Liu B, Hall IP. ORAI and store-operated calcium influx in human airway smooth muscle cells. Am J Respir Cell Mol Biol 38: 744-749, 2008.
34. Poteser M, Schleifer H, Lichtenegger M, Schernthaner M, Stockner T, Kappe CO, Glasnov TN, Romanin C, Groschner K. PKC-dependent coupling of calcium permeation through transient receptor potential canonical 3 (TRPC3) to calcineurin signaling in HL-1 myocytes. Proc Natl Acad Sci USA 108: 10556-10561, 2011.
35. 2+ release in myocytes from small renal arteries. Br J Pharmacol 162: 1618-1638, 2010.
36. Romano S, Di Pace A, Sorrentino A, Bisogni R, Sivero L, Romano MF. FK506 binding proteins as targets in anticancer therapy. Anticancer Agents Med Chem 10: 651-656, 2010.
37. Schernthaner M, Reisinger B, Wolinski H, Kohlwein SD, Trantina-Yates A, Fahrner M, Romanin C, Itani H, Stifter D, Leitinger G, Groschner K, Heitz J. Nanopatterned polymer substrates promote endothelial proliferation by initiation of beta-catenin transcriptional signaling. Acta Biomater 8: 2953-2962, 2012.
38. Sharma VK, Li B, Khanna A, Sehajpal PK, Suthanthiran M. Which way for drug-mediated immunosuppression? Curr Opin Immunol 6: 784-790, 1994.
39. Shim S, Yuan JP, Kim JY, Zeng W, Huang G, Milshteyn A, Kern D, Muallem S, Ming GL, Worley PF. Peptidyl-prolyl isomerase FKBP52 controls chemotropic guidance of neuronal growth cones via regulation of TRPC1 channel opening. Neuron 64: 471-483, 2009.
40. 2+ release channel in skeletal muscle. Biophys J 83: 2539-2549, 2002.
41. Siekierka JJ, Hung SH, Poe M, Lin CS, Sigal NH. A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature 341: 755-757, 1989.
42. Singh A, Severance S, Kaur N, Wiltsie W, Kosman DJ. Assembly, activation, and trafficking of the Fet3p. Ftr1p high affinity iron permease complex in Saccharomyces cerevisiae. J Biol Chem 281: 13355-13364, 2006.
43. Sinkins WG, Goel M, Estacion M, Schilling WP. Association of immunophilins with mammalian TRPC channels. J Biol Chem 279: 34521-34529, 2004.
44. Sternberg K, Grabow N, Petersen S, Weitschies W, Harder C, Ince H, Kroemer HK, Schmitz KP. Advances in coronary stent technology-active drug-loaded stent surfaces for prevention of restenosis and improvement of biocompatibility. Curr Pharm Biotechnol 14: 76-90, 2013.
45. Tamburino C, Capodanno D. Evolution of stents: past, present and future. Expert Rev Cardiovasc Ther 7: 443-446, 2009.
46. Townsend JC, Rideout P, Steinberg DH. Everolimus-eluting stents in interventional cardiology. Vasc Health Risk Manag 8: 393-404, 2012.
47. Trebak M. STIM/Orai signaling complexes in vascular smooth muscle. J Physiol 590: 4201-4208, 2012.
48. van der Hoeven BL, Pires NM, Warda HM, Oemrawsingh PV, van Vlijmen BJ, Quax PH, Schalij MJ, van der Wall EE, Jukema JW. Drug-eluting stents: results, promises and problems. Int J Cardiol 99: 9-17, 2005.
49. Verheye S, Sarno G, Muller R, Birkemeyer R, Vrints C, Jung W, Agostoni P, van Langenhove G, Haine S, Willems T, Haude M, Grube E, Wijns W. The ProLimus trial: a prospective, non-randomised, multicentre trial to evaluate the safety and clinical performance of the pimecrolimus eluting stent system (ProGenic). EuroIntervention 5: 233-238, 2009.
50. Waksman R, Pakala R, Baffour R, Hellinga D, Seabron R, Tio FO, Wittchow E, Tittelbach M, Diener T, Harder C, Virmani R, Jones R. Efficacy and safety of pimecrolimus-eluting stents in porcine coronary arteries. Cardiovasc Revasc Med 8: 259-274, 2007.
51. Wang Y, Deng X, Hewavitharana T, Soboloff J, Gill DL. Stim, ORAI and TRPC channels in the control of calcium entry signals in smooth muscle. Clin Exp Pharmacol Physiol 35: 1127-1133, 2008.
52. Yang CM, Chien CS, Hsiao LD, Pan SL, Wang CC, Chiu CT, Lin CC. Mitogenic effect of oxidized low-density lipoprotein on vascular smooth muscle cells mediated by activation of Ras/Raf/MEK/MAPK pathway. Br J Pharmacol 132: 1531-1541, 2001.
53. Yang J, Jiang H, Chen SS, Chen J, Li WQ, Xu SK, Wang JC. Lentivirus-mediated RNAi targeting CREB binding protein attenuates neointimal formation and promotes re-endothelialization in balloon injured rat carotid artery. Cell Physiol Biochem 26: 441-448, 2010.
54. Yang TT, Yu RY, Agadir A, Gao GJ, Campos-Gonzalez R, Tournier C, Chow CW. Integration of protein kinases mTOR and extracellular signal-regulated kinase 5 in regulating nucleocytoplasmic localization of NFATc4. Mol Cell Biol 28: 3489-3501, 2008.