Role of STIM1 (Stromal Interaction Molecule 1) in Hypertrophy-Related Contractile Dysfunction

Circulation Research

Volumn 121, Issue 2, 2017, Pages 125-136

  Troupes, Constantine D ^a   Wallner, Markus ^a   Borghetti, Giulia ^a   Zhang, Chen ^a   Mohsin, Sadia ^a   Von Lewinski, Dirk ^b   Berretta, Remus M ^a   Kubo, Hajime ^a   Chen, Xiongwen ^a   Soboloff, Jonathan ^a   Houser, Steven ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

calcium; myocytes, cardiac; stromal interaction molecule 1

Indexed keywords

ACTININ; BTP 2; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; MESSENGER RNA; ORAI CHANNEL; SODIUM CALCIUM EXCHANGE PROTEIN; STROMAL INTERACTION MOLECULE 1; THREONINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; UNCLASSIFIED DRUG; VERAPAMIL; STIM1 PROTEIN, HUMAN; TUMOR PROTEIN;

ACTION POTENTIAL; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL CULTURE; CELL DEATH; CONTROLLED STUDY; DIASTOLIC BLOOD PRESSURE; DISEASE ASSOCIATION; DISEASE COURSE; ENZYME ACTIVITY; EXPERIMENTAL CAT; HEART LEFT VENTRICLE OVERLOAD; HEART MUSCLE CONTRACTILITY; HEART VENTRICLE HYPERTROPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SARCOPLASMIC RETICULUM; ANIMAL; BIOSYNTHESIS; CARDIOMEGALY; CAT; HEART CONTRACTION; MALE; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CARDIOMEGALY; CATS; CELLS, CULTURED; MALE; MYOCARDIAL CONTRACTION; NEOPLASM PROTEINS; STROMAL INTERACTION MOLECULE 1;

EID: 85021983254     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.117.311094     Document Type: Article

References (57)

1. Dodge HT. Functional characteristics of the left ventricle in heart disease. Ann Intern Med. 1968;69:941-948.
2. Kennedy JW, Twiss RD, Blackmon JR, Dodge HT. Quantitative angiocardiography. 3. Relationships of left ventricular pressure, volume, and mass in aortic valve disease. Circulation. 1968;38:838-845.
3. Zaino EC, Tabor SH. Cardiac hypertrophy in acute myocardial infarction. A study based on 100 autopsied cases. Circulation. 1963;28:1081-1083.
4. Sampson KJ, Kass RS. Molecular mechanisms of adrenergic stimulation in the heart. Heart Rhythm. 2010;7:1151-1153. doi: 10.1016/j. hrthm.2010.02.013.
5. Grossman W, Jones D, McLaurin LP. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest. 1975;56:56-64. doi: 10.1172/JCI108079.
6. MacLellan WR, Schneider MD. Genetic dissection of cardiac growth control pathways. Annu Rev Physiol. 2000;62:289-319. doi: 10.1146/annurev. physiol.62.1.289.
7. Goonasekera SA, Molkentin JD. Unraveling the secrets of a double life: contractile versus signaling Ca2+ in a cardiac myocyte. J Mol Cell Cardiol. 2012;52:317-322. doi: 10.1016/j.yjmcc.2011.05.001.
8. Makarewich CA, Correll RN, Gao H, Zhang H, Yang B, Berretta RM, Rizzo V, Molkentin JD, Houser SR. A caveolae-targeted L-type Ca2+ channel antagonist inhibits hypertrophic signaling without reducing cardiac contractility. Circ Res. 2012;110:669-674. doi: 10.1161/CIRCRESAHA.111.264028.
9. Wu X, Eder P, Chang B, Molkentin JD. TRPC channels are necessary mediators of pathologic cardiac hypertrophy. Proc Natl Acad Sci U S A. 2010;107:7000-7005. doi: 10.1073/pnas.1001825107.
10. Luo M, Anderson ME. Mechanisms of altered Ca2+ handling in heart failure. Circ Res. 2013;113:690-708. doi: 10.1161/CIRCRESAHA.113.301651.
11. Houser SR, Piacentino V 3rd, Weisser J. Abnormalities of calcium cycling in the hypertrophied and failing heart. J Mol Cell Cardiol. 2000;32:1595-1607. doi: 10.1006/jmcc.2000.1206.
12. Pogwizd SM, Schlotthauer K, Li L, Yuan W, Bers DM. Arrhythmogenesis and contractile dysfunction in heart failure: Roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ Res. 2001;88:1159-1167.
13. Nattel S, Maguy A, Le Bouter S, Yeh YH. Arrhythmogenic ion-channel remodeling in the heart: heart failure, myocardial infarction, and atrial fibrillation. Physiol Rev. 2007;87:425-456. doi: 10.1152/physrev.00014.2006.
14. Levy D, Garrison RJ, Savage DD, Kannel WB, Castelli WP. Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study. N Engl J Med. 1990;322:1561-1566. doi: 10.1056/NEJM199005313222203.
15. Haider AW, Larson MG, Benjamin EJ, Levy D. Increased left ventricular mass and hypertrophy are associated with increased risk for sudden death. J Am Coll Cardiol. 1998;32:1454-1459.
16. Zhao G, Li T, Brochet DX, Rosenberg PB, Lederer WJ. STIM1 enhances SR Ca2+ content through binding phospholamban in rat ventricular myocytes. Proc Natl Acad Sci U S A. 2015;112:E4792-E4801. doi: 10.1073/pnas.1423295112.
17. Saliba Y, Keck M, Marchand A, Atassi F, Ouillé A, Cazorla O, Trebak M, Pavoine C, Lacampagne A, Hulot JS, Farès N, Fauconnier J, Lompré AM. Emergence of Orai3 activity during cardiac hypertrophy. Cardiovasc Res. 2015;105:248-259. doi: 10.1093/cvr/cvu207.
18. Luo X, Hojayev B, Jiang N, Wang ZV, Tandan S, Rakalin A, Rothermel BA, Gillette TG, Hill JA. STIM1-dependent store-operated Ca2+ entry is required for pathological cardiac hypertrophy. J Mol Cell Cardiol. 2012;52:136-147. doi: 10.1016/j.yjmcc.2011.11.003.
19. Hulot JS, Fauconnier J, Ramanujam D, et al. Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation. 2011;124:796-805. doi: 10.1161/CIRCULATIONAHA.111.031229.
20. Liou J, Kim ML, Heo WD, Jones JT, Myers JW, Ferrell JE Jr, Meyer T. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol. 2005;15:1235-1241. doi: 10.1016/j.cub.2005.05.055.
21. Roos J, DiGregorio PJ, Yeromin AV, Ohlsen K, Lioudyno M, Zhang S, Safrina O, Kozak JA, Wagner SL, Cahalan MD, Veliçelebi G, Stauderman KA. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol. 2005;169:435-445. doi: 10.1083/jcb.200502019.
22. Soboloff J, Spassova MA, Hewavitharana T, He LP, Xu W, Johnstone LS, Dziadek MA, Gill DL. STIM2 is an inhibitor of STIM1-mediated storeoperated Ca2+ Entry. Curr Biol. 2006;16:1465-1470. doi: 10.1016/j. cub.2006.05.051.
23. Prakriya M, Lewis RS. Store-operated calcium channels. Physiol Rev. 2015;95:1383-1436. doi: 10.1152/physrev.00020.2014.
24. Salido GM, Sage SO, Rosado JA. Biochemical and functional properties of the store-operated Ca2+ channels. Cell Signal. 2009;21:457-461. doi: 10.1016/j.cellsig.2008.11.005.
25. Soboloff J, Rothberg BS, Madesh M, Gill DL. STIM proteins: dynamic calcium signal transducers. Nat Rev Mol Cell Biol. 2012;13:549-565. doi: 10.1038/nrm3414.
26. Bers DM. Cardiac excitation-contraction coupling. Nature. 2002;415:198-205. doi: 10.1038/415198a.
27. Makarewich CA, Zhang H, Davis J, Correll RN, Trappanese DM, Hoffman NE, Troupes CD, Berretta RM, Kubo H, Madesh M, Chen X, Gao E, Molkentin JD, Houser SR. Transient receptor potential channels contribute to pathological structural and functional remodeling after myocardial infarction. Circ Res. 2014;115:567-580. doi: 10.1161/CIRCRESAHA.115.303831.
28. Correll RN, Goonasekera SA, van Berlo JH, Burr AR, Accornero F, Zhang H, Makarewich CA, York AJ, Sargent MA, Chen X, Houser SR, Molkentin JD. STIM1 elevation in the heart results in aberrant Ca2+ handling and cardiomyopathy. J Mol Cell Cardiol. 2015;87:38-47. doi: 10.1016/j. yjmcc.2015.07.032.
29. Bers DM. Excitation-Contraction Coupling and Cardiac Contractile Force. 2nd ed. Dordrecht, The Netherlands: Kluwer Academic Publishers; 2001.
30. Bers DM. Cardiac Na/Ca exchange function in rabbit, mouse and man: what's the difference? J Mol Cell Cardiol. 2002;34:369-373. doi: 10.1006/jmcc.2002.1530.
31. Harris DM, Mills GD, Chen X, Kubo H, Berretta RM, Votaw VS, Santana LF, Houser SR. Alterations in early action potential repolarization causes localized failure of sarcoplasmic reticulum Ca2+ release. Circ Res. 2005;96:543-550. doi: 10.1161/01.RES.0000158966.58380.37.
32. Chen X, Zhang X, Kubo H, Harris DM, Mills GD, Moyer J, Berretta R, Potts ST, Marsh JD, Houser SR. Ca2+ influx-induced sarcoplasmic reticulum Ca2+ overload causes mitochondrial-dependent apoptosis in ventricular myocytes. Circ Res. 2005;97:1009-1017. doi: 10.1161/01. RES.0000189270.72915.D1.
33. Pollack PS, Carson NL, Nuss HB, Marino TA, Houser SR. Mechanical properties of adult feline ventricular myocytes in culture. Am J Physiol. 1991;260:H234-H241.
34. Mitcheson JS, Hancox JC, Levi AJ. Action potentials, ion channel currents and transverse tubule density in adult rabbit ventricular myocytes maintained for 6 days in cell culture. Pflugers Arch. 1996;431:814-827.
35. Mills GD, Kubo H, Harris DM, Berretta RM, Piacentino V 3rd, Houser SR. Phosphorylation of phospholamban at threonine-17 reduces cardiac adrenergic contractile responsiveness in chronic pressure overload-induced hypertrophy. Am J Physiol Heart Circ Physiol. 2006;291:H61-H70. doi: 10.1152/ajpheart.01353.2005.
36. Bailey BA, Houser SR. Calcium transients in feline left ventricular myocytes with hypertrophy induced by slow progressive pressure overload. J Mol Cell Cardiol. 1992;24:365-373.
37. Bailey BA, Houser SR. Sarcoplasmic reticulum-related changes in cytosolic calcium in pressure-overload-induced feline LV hypertrophy. Am J Physiol. 1993;265:H2009-H2016.
38. Nuss HB, Houser SR. T-type Ca2+ current is expressed in hypertrophied adult feline left ventricular myocytes. Circ Res. 1993;73:777-782.
39. Kleiman RB, Houser SR. Calcium currents in normal and hypertrophied isolated feline ventricular myocytes. Am J Physiol. 1988;255:H1434-H1442.
40. Bers DM. Cardiac sarcoplasmic reticulum calcium leak: basis and roles in cardiac dysfunction. Annu Rev Physiol. 2014;76:107-127. doi: 10.1146/annurev-physiol-020911-153308.
41. Zitt C, Strauss B, Schwarz EC, Spaeth N, Rast G, Hatzelmann A, Hoth M. Potent inhibition of Ca2+ release-activated Ca2+ channels and T-lymphocyte activation by the pyrazole derivative BTP2. J Biol Chem. 2004;279:12427-12437. doi: 10.1074/jbc.M309297200.
42. Park CY, Shcheglovitov A, Dolmetsch R. The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science. 2010;330:101-105. doi: 10.1126/science.1191027.
43. Wang Y, Deng X, Mancarella S, Hendron E, Eguchi S, Soboloff J, Tang XD, Gill DL. The calcium store sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science. 2010;330:105-109. doi: 10.1126/science.1191086.
44. Asahi M, McKenna E, Kurzydlowski K, Tada M, MacLennan DH. Physical interactions between phospholamban and sarco(endo)plasmic reticulum Ca2+-ATPases are dissociated by elevated Ca2+, but not by phospholamban phosphorylation, vanadate, or thapsigargin, and are enhanced by ATP. J Biol Chem. 2000;275:15034-15038.
45. Prakriya M, Feske S, Gwack Y, Srikanth S, Rao A, Hogan PG. Orai1 is an essential pore subunit of the CRAC channel. Nature. 2006;443:230-233. doi: 10.1038/nature05122.
46. Shan D, Marchase RB, Chatham JC. Overexpression of TRPC3 increases apoptosis but not necrosis in response to ischemia-reperfusion in adult mouse cardiomyocytes. Am J Physiol Cell Physiol. 2008;294:C833-C841. doi: 10.1152/ajpcell.00313.2007.
47. Yuan JP, Zeng W, Huang GN, Worley PF, Muallem S. STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels. Nat Cell Biol. 2007;9:636-645. doi: 10.1038/ncb1590.
48. Erickson JR, He BJ, Grumbach IM, Anderson ME. CaMKII in the cardiovascular system: sensing redox states. Physiol Rev. 2011;91:889-915. doi: 10.1152/physrev.00018.2010.
49. Vila-Petroff M, Salas MA, Said M, Valverde CA, Sapia L, Portiansky E, Hajjar RJ, Kranias EG, Mundiña-Weilenmann C, Mattiazzi A. CaMKII inhibition protects against necrosis and apoptosis in irreversible ischemiareperfusion injury. Cardiovasc Res. 2007;73:689-698. doi: 10.1016/j. cardiores.2006.12.003.
50. Collins HE, He L, Zou L, Qu J, Zhou L, Litovsky SH, Yang Q, Young ME, Marchase RB, Chatham JC. Stromal interaction molecule 1 is essential for normal cardiac homeostasis through modulation of ER and mitochondrial function. Am J Physiol Heart Circ Physiol. 2014;306:H1231-H1239. doi: 10.1152/ajpheart.00075.2014.
51. Ohga K, Takezawa R, Arakida Y, Shimizu Y, Ishikawa J. Characterization of YM-58483/BTP2, a novel store-operated Ca2+ entry blocker, on T cell-mediated immune responses in vivo. Int Immunopharmacol. 2008;8:1787-1792. doi: 10.1016/j.intimp.2008.08.016.
52. Voelkers M, Salz M, Herzog N, Frank D, Dolatabadi N, Frey N, Gude N, Friedrich O, Koch WJ, Katus HA, Sussman MA, Most P. Orai1 and Stim1 regulate normal and hypertrophic growth in cardiomyocytes. J Mol Cell Cardiol. 2010;48:1329-1334. doi: 10.1016/j.yjmcc.2010.01.020.
53. Borlaug BA, Paulus WJ. Heart failure with preserved ejection fraction: pathophysiology, diagnosis, and treatment. Eur Heart J. 2011;32:670-679. doi: 10.1093/eurheartj/ehq426.
54. Braunwald E. Heart failure. JACC Heart Fail. 2013;1:1-20. doi: 10.1016/j. jchf.2012.10.002.
55. Ishikawa J, Ohga K, Yoshino T, Takezawa R, Ichikawa A, Kubota H, Yamada T. A pyrazole derivative, YM-58483, potently inhibits storeoperated sustained Ca2+ influx and IL-2 production in T lymphocytes. J Immunol. 2003;170:4441-4449.
56. Chen X, Nakayama H, Zhang X, Ai X, Harris DM, Tang M, Zhang H, Szeto C, Stockbower K, Berretta RM, Eckhart AD, Koch WJ, Molkentin JD, Houser SR. Calcium influx through Cav1.2 is a proximal signal for pathological cardiomyocyte hypertrophy. J Mol Cell Cardiol. 2011;50:460-470. doi: 10.1016/j.yjmcc.2010.11.012.
57. Nakayama H, Chen X, Baines CP, Klevitsky R, Zhang X, Zhang H, Jaleel N, Chua BH, Hewett TE, Robbins J, Houser SR, Molkentin JD. Ca2+-and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J Clin Invest. 2007;117:2431-2444. doi: 10.1172/JCI31060.