Targeted STIM deletion impairs calcium homeostasis, NFAT activation, and growth of smooth muscle

FASEB Journal

Volumn 27, Issue 3, 2013, Pages 893-906

  Mancarella, Salvatore ^a   Potireddy, Santhi ^a   Wang, Youjun ^a   Gao, Hui ^a   Gandhirajan, Rajesh Kumar ^a   Autieri, Michael ^a   Scalia, Rosario ^a   Cheng, Zhongjian ^a   Wang, Hong ^a   Madesh, Muniswamy ^a   Houser, Steven R ^a   Gill, Donald L ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Gastrointestinal development; Mouse knockout; Orai channel; Transcription factor; Vascular function

Indexed keywords

CALCIUM; CRE RECOMBINASE; PLATELET DERIVED GROWTH FACTOR; STROMAL INTERACTION MOLECULE 1; STROMAL INTERACTION MOLECULE 2; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA CONSTRICTION; ARTICLE; BLOOD VESSEL REACTIVITY; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CAROTID ARTERY LIGATION; CELL COUNT; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; GENE ACTIVATION; GENE DELETION; GENE EXPRESSION; GENE TARGETING; GENE TRANSLOCATION; IN VITRO STUDY; INTESTINE MUSCLE; MALE; MEMBRANE DEPOLARIZATION; MORPHOLOGY; MORPHOMETRICS; MOUSE; MUSCLE GROWTH; NEOINTIMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE CONTRACTION; SMOOTH MUSCLE FIBER; STIMULATION; STRESS; VASCULAR SMOOTH MUSCLE; WEIGHT REDUCTION;

ANIMALS; CALCIUM; CELL PROLIFERATION; GENE DELETION; HOMEOSTASIS; INTESTINES; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MUSCLE CONTRACTION; MUSCLE, SMOOTH, VASCULAR; NEOINTIMA; NFATC TRANSCRIPTION FACTORS; PLATELET-DERIVED GROWTH FACTOR; TRANSCRIPTION, GENETIC;

EID: 84874600299     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.12-215293     Document Type: Article

References (67)

1. Roos, J., DiGregorio, P. J., Yeromin, A. V., Ohlsen, K., Lioudyno, M., Zhang, S., Safrina, O., Kozak, J. A., Wagner, S. L., Cahalan, M. D., Velicelebi, G., and Stauderman, K. A. (2005) STIM1, an essential and conserved component of store-operated Ca2+ channel function. J. Cell Biol. 169, 435-445 (Pubitemid 40686694)
2. Liou, J., Kim, M. L., Heo, W. D., Jones, J. T., Myers, J. W., Ferrell, J. E., Jr., and Meyer, T. (2005) STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15, 1235-1241 (Pubitemid 40950523)
3. Lewis, R. S. (2011) Store-operated calcium channels: new perspectives on mechanism and function. Cold Spring Harbor Perspect. Biol. 3 a003970
4. Carrasco, S., and Meyer, T. (2011) STIM proteins and the endoplasmic reticulum-plasma membrane junctions. Annu. Rev. Biochem. 80, 973-1000
5. Soboloff, J., Rothberg, B. S., Madesh, M., and Gill, D. L. (2012) STIM proteins: dynamic calcium signal transducers. Nat. Rev. Mol. Cell Biol. 13, 549-565
6. Parekh, A. B. (2011) Decoding cytosolic Ca2+ oscillations. Trends Biochem. Sci. 36, 78-87
7. Di Capite, J., Ng, S. W., and Parekh, A. B. (2009) Decoding of cytoplasmic Ca2+ oscillations through the spatial signature drives gene expression. Curr. Biol. 19, 853-858
8. Mancarella, S., Wang, Y., and Gill, D. L. (2009) Calcium signals: STIM dynamics mediate spatially unique oscillations. Curr. Biol. 19, R950-R952
9. Kar, P., Bakowski, D., Di Capite, J., Nelson, C., and Parekh, A. B. (2012) Different agonists recruit different stromal interaction molecule proteins to support cytoplasmic Ca2+ oscillations and gene expression. Proc. Natl. Acad. Sci. U. S. A. 109, 6969-6974
10. Kar, P., Nelson, C., and Parekh, A. B. (2012) CRAC channels drive digital activation and provide analog control and synergy to Ca2+-dependent gene regulation. Curr. Biol. 22, 242-247
11. Brandman, O., Liou, J., Park, W. S., and Meyer, T. (2007) STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels. Cell 131, 1327-1339 (Pubitemid 350297421)
12. Deng, X., Wang, Y., Zhou, Y., Soboloff, J., and Gill, D. L. (2009) STIM and Orai-dynamic intermembrane coupling to control cellular calcium signals. J. Biol. Chem. 284, 22501-22505
13. Stiber, J., Hawkins, A., Zhang, Z. S., Wang, S., Burch, J., Graham, V., Ward, C. C., Seth, M., Finch, E., Malouf, N., Williams, R. S., Eu, J. P., and Rosenberg, P. (2008) STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat.Cell Biol. 10, 688-697 (Pubitemid 351772934)
14. Rosenberg, P. B. (2009) Calcium entry in skeletal muscle. J. Physiol. 587, 3149-3151
15. Li, T., Finch, E. A., Graham, V., Zhang, Z. S., Ding, J. D., Burch, J., Oh-Hora, M., and Rosenberg, P. (2012) STIM1-Ca2+ signaling is required for the hypertrophic growth of skeletal muscle in mice. Mol. Cell. Biol. 32, 3009-3017
16. Hulot, J. S., Fauconnier, J., Ramanujam, D., Chaanine, A., Aubart, F., Sassi, Y., Merkle, S., Cazorla, O., Ouille, A., Dupuis, M., Hadri, L., Jeong, D., Muhlstedt, S., Schmitt, J., Braun, A., Benard, L., Saliba, Y., Laggerbauer, B., Nieswandt, B., Lacampagne, A., Hajjar, R. J., Lompre, A. M., and Engelhardt, S. (2011) Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation 124, 796-805
17. Luo, X., Hojayev, B., Jiang, N., Wang, Z. V., Tandan, S., Rakalin, A., Rothermel, B. A., Gillette, T. G., and Hill, J. A. (2012) STIM1- dependent store-operated Ca2+ entry is required for pathological cardiac hypertrophy. J. Mol. Cell. Cardiol. 52, 136-147
18. Wang, Y., Deng, X., Hewavitharana, T., Soboloff, J., and Gill, D. L. (2008) Stim, ORAI and TRPC channels in the control of calcium entry signals in smooth muscle. Clin. Exp. Pharmacol. Physiol. 35, 1127-1133
19. Trebak, M. (2012) STIM/Orai signaling complexes in vascular smooth muscle. J. Physiol. 590, 4201-4208
20. Potier, M., Gonzalez, J. C., Motiani, R. K., Abdullaev, I. F., Bisaillon, J. M., Singer, H. A., and 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
21. Guo, R. W., Wang, H., Gao, P., Li, M. Q., Zeng, C. Y., Yu, Y., Chen, J. F., Song, M. B., Shi, Y. K., and Huang, L. (2009) An essential role for stromal interaction molecule 1 in neointima formation following arterial injury. Cardiovasc. Res. 81, 660-668
22. Aubart, F. C., Sassi, Y., Coulombe, A., Mougenot, N., Vrignaud, C., Leprince, P., Lechat, P., Lompre, A. M., and Hulot, J. S. (2009) RNA interference targeting STIM1 suppresses vascular smooth muscle cell proliferation and neointima formation in the rat. Mol. Ther. 17, 455-462
23. Baryshnikov, S. G., Pulina, M. V., Zulian, A., Linde, C. I., and Golovina, V. A. (2009) Orai1, a critical component of storeoperated Ca2+ entry, is functionally associated with Na+/Ca2+ exchanger in proliferating human arterial myocytes. Am. J. Physiol. Cell Physiol 297, C1103-C1112
24. Bisaillon, J. M., Motiani, R. K., Gonzalez-Cobos, J. C., Potier, M., Halligan, K. E., Alzawahra, W. F., Barroso, M., Singer, H. A., Jourd'heuil, D., and 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
25. Zhang, W., Halligan, K. E., Zhang, X., Bisaillon, J. M., Gonzalez- Cobos, J. C., Motiani, R. K., Hu, G., Vincent, P. A., Zhou, J., Barroso, M., Singer, H. A., Matrougui, K., and Trebak, M. (2011) Orai1-mediated I (CRAC) is essential for neointima formation after vascular injury. Circ. Res. 109, 534-542
26. Pulver, R. A., Rose-Curtis, P., Roe, M. W., Wellman, G. C., and Lounsbury, K. M. (2004) Store-operated Ca2+ entry activates the CREB transcription factor in vascular smooth muscle. Circ. Res. 94, 1351-1358 (Pubitemid 38724481)
27. Owens, G. K., Kumar, M. S., and Wamhoff, B. R. (2004) Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol. Rev. 84, 767-801 (Pubitemid 38823766)
28. Wamhoff, B. R., Bowles, D. K., and Owens, G. K. (2006) Excitation-transcription coupling in arterial smooth muscle. Circ. Res. 98, 868-878
29. Beech, D. J. (2007) Ion channel switching and activation in smooth-muscle cells of occlusive vascular diseases. Biochem. Soc. Trans. 35, 890-894 (Pubitemid 350206389)
30. Hill-Eubanks, D. C., Gomez, M. F., Stevenson, A. S., and Nelson, M. T. (2003) NFAT regulation in smooth muscle. Trends Cardiovasc. Med. 13, 56-62 (Pubitemid 36173860)
31. Graef, I. A., Chen, F., Chen, L., Kuo, A., and Crabtree, G. R. (2001) Signals transduced by Ca2+/calcineurin and NFATc3/c4 pattern the developing vasculature. Cell 105, 863-875 (Pubitemid 32635088)
32. Stevenson, A. S., Gomez, M. F., Hill-Eubanks, D. C., and Nelson, M. T. (2001) NFAT4 movement in native smooth muscle. A role for differential Ca2+ signaling. J. Biol. Chem. 276, 15018-15024
33. Wu, H., Peisley, A., Graef, I. A., and Crabtree, G. R. (2007) NFAT signaling and the invention of vertebrates. Trends Cell Biol. 17, 251-260 (Pubitemid 46829850)
34. Beech, D. J. (2005) Emerging functions of 10 types of TRP cationic channel in vascular smooth muscle. Clin. Exp. Pharmacol. Physiol. 32, 597-603 (Pubitemid 41025819)
35. Kumar, B., Dreja, K., Shah, S. S., Cheong, A., Xu, S. Z., Sukumar, P., Naylor, J., Forte, A., Cipollaro, M., McHugh, D., Kingston, P. A., Heagerty, A. M., Munsch, C. M., Bergdahl, A., Hultgardh-Nilsson, A., Gomez, M. F., Porter, K. E., Hellstrand, P., and Beech, D. J. (2006) Upregulated TRPC1 channel in vascular injury in vivo and its role in human neointimal hyperplasia. Circ. Res. 98, 557-563
36. Oh-Hora, M., Yamashita, M., Hogan, P. G., Sharma, S., Lamperti, E., Chung, W., Prakriya, M., Feske, S., and Rao, A. (2008) Dual functions for the endoplasmic reticulum calcium sensors STIM1 and STIM2 in T cell activation and tolerance. Nat. Immunol. 9, 432-443 (Pubitemid 351405113)
37. Varga-Szabo, D., Braun, A., Kleinschnitz, C., Bender, M., Pleines, I., Pham, M., Renne, T., Stoll, G., and Nieswandt, B. (2008) The calcium sensor STIM1 is an essential mediator of arterial thrombosis and ischemic brain infarction. J. Exp. Med. 205, 1583-1591 (Pubitemid 351962022)
38. Zhang, J., Zhong, W., Cui, T., Yang, M., Hu, X., Xu, K., Xie, C., Xue, C., Gibbons, G. H., Liu, C., Li, L., and Chen, Y. E. (2006) Generation of an adult smooth muscle cell-targeted Cre recombinase mouse model. Arterioscler. Thromb. Vasc. Biol. 26, e23-24
39. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L., and Luo, L. (2007) A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605 (Pubitemid 350013057)
40. Mancarella, S., Wang, Y., Deng, X., Landesberg, G., Scalia, R., Panettieri, R. A., Mallilankaraman, K., Tang, X. D., Madesh, M., and Gill, D. L. (2011) Hypoxia-induced acidosis uncouples the STIM-Orai calcium signaling complex. J. Biol. Chem. 286, 44788-44798
41. Sommerville, L. J., Kelemen, S. E., and Autieri, M. V. (2008) Increased smooth muscle cell activation and neointima formation in response to injury in AIF-1 transgenic mice. Arterioscler. Thromb. Vasc. Biol. 28, 47-53
42. Harmon, K. J., Couper, L. L., and Lindner, V. (2000) Straindependent vascular remodeling phenotypes in inbred mice. Am. J. Pathol. 156, 1741-1748 (Pubitemid 30646711)
43. Autieri, M. V., Kelemen, S., Thomas, B. A., Feller, E. D., Goldman, B. I., and Eisen, H. J. (2002) Allograft inflammatory factor-1 expression correlates with cardiac rejection and development of cardiac allograft vasculopathy. Circulation 106, 2218-2223 (Pubitemid 35222216)
44. Ray, J. B., Arab, S., Deng, Y., Liu, P., Penn, L., Courtman, D. W., and Ward, M. E. (2008) Oxygen regulation of arterial smooth muscle cell proliferation and survival. Am. J. Physiol. Heart Circ. Physiol. 294, H839-H852 (Pubitemid 351253295)
45. Ray, J. L., Leach, R., Herbert, J. M., and Benson, M. (2001) Isolation of vascular smooth muscle cells from a single murine aorta. Methods Cell Sci. 23, 185-188 (Pubitemid 34863290)
46. Wang, Y., Deng, X., Mancarella, S., Hendron, E., Eguchi, S., Soboloff, J., Tang, X. D., and Gill, D. L. (2010) The calcium store-sensor, STIM1, reciprocally controls Orai and CaV1.2 channels. Science 330, 105-109
47. Wang, Y., Deng, X., Zhou, Y., Hendron, E., Mancarella, S., Ritchie, M. F., Tang, X. D., Baba, Y., Kurosaki, T., Mori, Y., Soboloff, J., and Gill, D. L. (2009) STIM protein coupling in the activation of Orai channels. Proc. Natl. Acad. Sci. U. S. A. 106, 7391-7396
48. Chen, X., Nakayama, H., Zhang, X., Ai, X., Harris, D. M., Tang, M., Zhang, H., Szeto, C., Stockbower, K., Berretta, R. M., Eckhart, A. D., Koch, W. J., Molkentin, J. D., and Houser, S. R. (2011) Calcium influx through Cav1.2 is a proximal signal for pathological cardiomyocyte hypertrophy. J. Mol. Cell. Cardiol. 50, 460-470
49. Rozenblum, G. T., and Gimona, M. (2008) Calponins: adaptable modular regulators of the actin cytoskeleton. Int. J. Biochem. Cell Biol. 40, 1990-1995 (Pubitemid 352004269)
50. Park, C. Y., Shcheglovitov, A., and Dolmetsch, R. (2010) The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels. Science 330, 101-105
51. Leung, F. P., Yung, L. M., Yao, X., Laher, I., and Huang, Y. (2008) Store-operated calcium entry in vascular smooth muscle. Br. J. Pharmacol. 153, 846-857 (Pubitemid 351328924)
52. Giachini, F. R., Chiao, C. W., Carneiro, F. S., Lima, V. V., Carneiro, Z. N., Dorrance, A. M., Tostes, R. C., and Webb, R. C. (2009) Increased activation of stromal interaction molecule-1/ Orai-1 in aorta from hypertensive rats: a novel insight into vascular dysfunction. Hypertension 53, 409-416
53. Soboloff, J., Spassova, M. A., Xu, W., He, L. P., Cuesta, N., and Gill, D. L. (2005) Role of endogenous TRPC6 channels in Ca2+ signal generation in A7r5 smooth muscle cells. J. Biol. Chem. 280, 39786-39794 (Pubitemid 41779111)
54. Mackie, A. R., and Byron, K. L. (2008) Cardiovascular KCNQ (Kv7) potassium channels: physiological regulators and new targets for therapeutic intervention. Mol. Pharmacol. 74, 1171-1179
55. Ruusalepp, A., Vaage, J., and Valen, G. (2003) A model of neointima formation in the atherosclerotic carotid artery of mice. Interact. Cardiovasc. Thorac. Surg. 2, 196-200 (Pubitemid 38352645)
56. Hewavitharana, T., Deng, X., Wang, Y., Ritchie, M. F., Girish, G. V., Soboloff, J., and Gill, D. L. (2008) Location and function of STIM1 in the activation of Ca2+ entry signals. J. Biol. Chem. 283, 26252-26262
57. Berridge, M. J. (2008) Smooth muscle cell calcium activation mechanisms. J. Physiol. 586, 5047-5061
58. Yoshida, T., Gan, Q., Franke, A. S., Ho, R., Zhang, J., Chen, Y. E., Hayashi, M., Majesky, M. W., Somlyo, A. V., and Owens, G. K. (2010) Smooth and cardiac muscle-selective knock-out of Kruppel-like factor 4 causes postnatal death and growth retardation. J. Biol. Chem. 285, 21175-21184
59. Zhang, S. L., Yeromin, A. V., Hu, J., Amcheslavsky, A., Zheng, H., and Cahalan, M. D. (2011) Mutations in Orai1 transmembrane segment 1 cause STIM1-independent activation of Orai1 channels at glycine 98 and channel closure at arginine 91. Proc. Natl. Acad. Sci. U. S. A. 108, 17838-17843
60. Brueggemann, L. I., Markun, D. R., Henderson, K. K., Cribbs, L. L., and Byron, K. L. (2006) Pharmacological and electrophysiological characterization of store-operated currents and capacitative Ca2+ entry in vascular smooth muscle cells. J. Pharmacol. Exp. Ther. 317, 488-499
61. Cheng, K. T., Alevizos, I., Liu, X., Swaim, W. D., Yin, H., Feske, S., Oh-Hora, M., and Ambudkar, I. S. (2012) STIM1 and STIM2 protein deficiency in T lymphocytes underlies development of the exocrine gland autoimmune disease, Sjogren's syndrome. Proc. Natl. Acad. Sci. U. S. A. 109, 14544-14549
62. Soboloff, J., Spassova, M. A., Hewavitharana, T., He, L. P., Xu, W., Johnstone, L. S., Dziadek, M. A., and Gill, D. L. (2006) STIM2 is an inhibitor of STIM1-mediated store-operated Ca2+ entry. Curr. Biol. 16, 1465-1470 (Pubitemid 44088459)
63. Picard, C., McCarl, C. A., Papolos, A., Khalil, S., Luthy, K., Hivroz, C., LeDeist, F., Rieux-Laucat, F., Rechavi, G., Rao, A., Fischer, A., and Feske, S. (2009) STIM1 mutation associated with a syndrome of immunodeficiency and autoimmunity. N. Engl. J. Med. 360, 1971-1980
64. Feske, S., Picard, C., and Fischer, A. (2010) Immunodeficiency due to mutations in ORAI1 and STIM1. Clin. Immunol. 135, 169-182
65. Moller, H. U., Fledelius, H. C., Milewicz, D. M., Regalado, E. S., and Ostergaard, J. R. (2012) Eye features in three Danish patients with multisystemic smooth muscle dysfunction syndrome. Brit. J. Ophthalmol. 96, 1227-1231
66. Boeck, A., Buckley, R. H., and Schiff, R. I. (1997) Gastroesophageal reflux and severe combined immunodeficiency. J. Allergy Clin. Immunol. 99, 420-424 (Pubitemid 27123924)
67. Larrieu, D., Thiebaud, P., Duplaa, C., Sibon, I., Theze, N., and Lamaziere, J. M. (2005) Activation of the Ca2+/calcineurin/ NFAT2 pathway controls smooth muscle cell differentiation. Exp. Cell Res. 310, 166-175 (Pubitemid 41393697)