Table of Contents
Journal of Signal Transduction
Volume 2012 (2012), Article ID 951497, 16 pages
http://dx.doi.org/10.1155/2012/951497
Review Article

Pathogenic Role of Store-Operated and Receptor-Operated Channels in Pulmonary Arterial Hypertension

1Section of Pulmonary, Critical Care, Sleep and Allergy Medicine, Department of Pharmacology, Institute for Personalized Respiratory Medicine, Center for Cardiovascular Research, University of Illinois at Chicago, Chicago, IL 60612, USA
2Department of Medicine, University of Illinois at Chicago, Chicago, IL 60612, USA

Received 17 May 2012; Revised 12 July 2012; Accepted 16 July 2012

Academic Editor: Jesus Garcia

Copyright © 2012 Ruby A. Fernandez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. L. Firth, J. Mandel, and J. X. J. Yuan, “Idiopathic pulmonary arterial hypertension,” DMM Disease Models and Mechanisms, vol. 3, no. 5-6, pp. 268–273, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. D. B. Badesch, H. C. Champion, M. A. Gomez Sanchez et al., “Diagnosis and assessment of pulmonary arterial hypertension,” Journal of the American College of Cardiology, vol. 54, no. 1, pp. S55–S66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Mandegar, Y. C. B. Fung, W. Huang, C. V. Remillard, L. J. Rubin, and J. X. J. Yuan, “Cellular and molecular mechanisms of pulmonary vascular remodeling: role in the development of pulmonary hypertension,” Microvascular Research, vol. 68, no. 2, pp. 75–103, 2004. View at Publisher · View at Google Scholar · View at Scopus
  4. I. M. Robbins, “Epidemiolgoy and classification of pulmonary hypertension,” Advances in Pulmonary Hypertension, vol. 8, pp. 77–78, 2009. View at Google Scholar
  5. G. Simonneau, I. M. Robbins, M. Beghetti et al., “Updated clinical classification of pulmonary hypertension,” Journal of the American College of Cardiology, vol. 54, no. 1, pp. S43–S54, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. L. J. Rubin, “Diagnosis and management of pulmonary arterial hypertension: ACCP evidence-based clinical practice guidelines,” Chest, vol. 126, no. 1, pp. 4S–6S, 2004. View at Publisher · View at Google Scholar · View at Scopus
  7. P. Escribano-Subias, I. Blanco, M. Lopez-Meseguer et al., “Survival in pulmonary hypertension in spain insights from the spanish registry,” European Respiratory Journal, vol. 40, no. 3, pp. 596–603, 2012. View at Google Scholar
  8. D. E. Bedford, W. Evans, and D. S. Short, “Solitary pulmonary hypertension,” British Heart Journal, vol. 19, no. 1, pp. 93–116, 1957. View at Google Scholar · View at Scopus
  9. W. Huang, R. T. Yen, M. McLaurine, and G. Bledsoe, “Morphometry of the human pulmonary vasculature,” Journal of Applied Physiology, vol. 81, no. 5, pp. 2123–2133, 1996. View at Google Scholar · View at Scopus
  10. J. K. Belknap, E. C. Orton, B. Ensley, A. Tucker, and K. R. Stenmark, “Hypoxia increases bromodeoxyuridine labeling indices in bovine neonatal pulmonary arteries,” American Journal of Respiratory Cell and Molecular Biology, vol. 16, no. 4, pp. 366–371, 1997. View at Google Scholar · View at Scopus
  11. N. W. Morrell, S. Adnot, S. L. Archer et al., “Cellular and molecular basis of pulmonary arterial hypertension,” Journal of the American College of Cardiology, vol. 54, no. 1, pp. S20–S31, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. J. X. J. Yuan and L. J. Rubin, “Pathogenesis of pulmonary arterial hypertension: the need for multiple hits,” Circulation, vol. 111, no. 5, pp. 534–538, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. L. Reid, “Vascular remodeling,” in The Pulmonary Circulation: Normal and Abnormal Mechansimc, Management, and the National Registry, A. Fishman, Ed., p. 264, University of Pennsylvania Press, Philadelphia, Pa, USA, 1990. View at Google Scholar
  14. S. Zhang, I. Fantozzi, D. D. Tigno et al., “Bone morphogenetic proteins induce apoptosis in human pulmonary vascular smooth muscle cells,” American Journal of Physiology, vol. 285, no. 3, pp. L740–L754, 2003. View at Google Scholar · View at Scopus
  15. B. Meyrick and L. Reid, “Hypoxia and incorporation of 3H-thymidine by cells of the rat pulmonary arteries and alveolar wall,” American Journal of Pathology, vol. 96, no. 1, pp. 51–70, 1979. View at Google Scholar · View at Scopus
  16. J. Chamley-Campbell, G. R. Campbell, and R. Ross, “The smooth muscle cell in culture,” Physiological Reviews, vol. 59, no. 1, pp. 1–61, 1979. View at Google Scholar · View at Scopus
  17. G. K. Owens, M. S. Kumar, and B. R. Wamhoff, “Molecular regulation of vascular smooth muscle cell differentiation in development and disease,” Physiological Reviews, vol. 84, no. 3, pp. 767–801, 2004. View at Publisher · View at Google Scholar · View at Scopus
  18. K. Sobue, K. Hayashi, and W. Nishida, “Expressional regulation of smooth muscle cell-specific genes in association with phenotypic modulation,” Molecular and Cellular Biochemistry, vol. 190, no. 1-2, pp. 105–118, 1999. View at Google Scholar · View at Scopus
  19. M. G. Frid, E. P. Moiseeva, and K. R. Stenmark, “Multiple phenotypically distinct smooth muscle cell populations exist in the adult and developing bovine pulmonary arterial media in vivo,” Circulation Research, vol. 75, no. 4, pp. 669–681, 1994. View at Google Scholar · View at Scopus
  20. E. D. Michelakis, V. Hampl, A. Nsair et al., “Diversity in mitochondrial function explains differences in vascular oxygen sensing,” Circulation Research, vol. 90, no. 12, pp. 1307–1315, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. L. J. Rubin, “Primary pulmonary hypertension,” New England Journal of Medicine, vol. 336, no. 2, pp. 111–117, 1997. View at Publisher · View at Google Scholar · View at Scopus
  22. K. R. Stenmark, N. Davie, M. Frid, E. Gerasimovskaya, and M. Das, “Role of the adventitia in pulmonary vascular remodeling,” Physiology, vol. 21, no. 2, pp. 134–145, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. G. E. Hardingham, S. Chawla, C. M. Johnson, and H. Bading, “Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression,” Nature, vol. 385, no. 6613, pp. 260–265, 1997. View at Publisher · View at Google Scholar · View at Scopus
  24. A. P. Somlyo and A. V. Somlyo, “Signal transduction and regulation in smooth muscle,” Nature, vol. 372, no. 6503, pp. 231–236, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. S. S. Mcdaniel, O. Platoshyn, J. Wang et al., “Capacitative Ca2+ entry in agonist-induced pulmonary vasoconstriction,” American Journal of Physiology, vol. 280, no. 5, pp. L870–L880, 2001. View at Google Scholar · View at Scopus
  26. A. R. Means, “Calcium, calmodulin and cell cycle regulation,” FEBS Letters, vol. 347, no. 1, pp. 1–4, 1994. View at Publisher · View at Google Scholar · View at Scopus
  27. D. D. Ginty, “Calcium regulation of gene expression: isn't that spatial?” Neuron, vol. 18, no. 2, pp. 183–186, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. M. J. Berridge, “Calcium signalling and cell proliferation,” BioEssays, vol. 17, no. 6, pp. 491–500, 1995. View at Google Scholar · View at Scopus
  29. I. A. Graef, F. Chen, L. Chen, A. Kuo, and G. R. Crabtree, “Signals transduced by Ca2+/calcineurin and NFATc3/c4 pattern the developing vasculature,” Cell, vol. 105, no. 7, pp. 863–875, 2001. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Sheng, G. McFadden, and M. E. Greenberg, “Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB,” Neuron, vol. 4, no. 4, pp. 571–582, 1990. View at Publisher · View at Google Scholar · View at Scopus
  31. O. Platoshyn, V. A. Golovina, C. L. Bailey et al., “Sustained membrane depolarization and pulmonary artery smooth muscle cell proliferation,” American Journal of Physiology, vol. 279, no. 5, pp. C1540–C1549, 2000. View at Google Scholar · View at Scopus
  32. A. D. Short, J. Bian, T. K. Ghosh, R. T. Waldron, S. L. Rybak, and D. L. Gill, “Intracellular Ca2+ pool content is linked to control of cell growth,” Proceedings of the National Academy of Sciences of the United States of America, vol. 90, no. 11, pp. 4986–4990, 1993. View at Google Scholar · View at Scopus
  33. N. Takuwa, W. Zhou, and Y. Takuwa, “Calcium, calmodulin and cell cycle progression,” Cellular Signalling, vol. 7, no. 2, pp. 93–104, 1995. View at Publisher · View at Google Scholar · View at Scopus
  34. C. V. Remillard and J. X. J. Yuan, “TRP channels, CCE, and the pulmonary vascular smooth muscle,” Microcirculation, vol. 13, no. 8, pp. 671–692, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Makino, A. L. Firth, and J. X. J. Yuan, “Endothelial and smooth muscle cell ion channels in pulmonary vasoconstriction and vascular remodeling,” in Comprehensive Physiology, John Wiley & Sons, 2011. View at Google Scholar
  36. M. D. Cahalan, “STIMulating store-operated Ca2+ entry,” Nature Cell Biology, vol. 11, no. 6, pp. 669–677, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. T. T. Chen, K. D. Luykenaar, E. J. Walsh, M. P. Walsh, and W. C. Cole, “Key role of Kv1 channels in vasoregulation,” Circulation Research, vol. 99, no. 1, pp. 53–60, 2006. View at Publisher · View at Google Scholar · View at Scopus
  38. F. Plane, R. Johnson, P. Kerr et al., “Heteromultimeric Kv1 channels contribute to myogenic control of arterial diameter,” Circulation Research, vol. 96, no. 2, pp. 216–224, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. M. D. Cahalan, “How to STIMulate calcium channels,” Science, vol. 330, no. 6000, pp. 43–44, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Y. Park, A. Shcheglovitov, and R. Dolmetsch, “The CRAC channel activator STIM1 binds and inhibits L-type voltage-gated calcium channels,” Science, vol. 330, no. 6000, pp. 101–105, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. Y. Wang, X. Deng, S. Mancarella et al., “The calcium store sensor, STIM1, reciprocally controls Orai and Ca V1.2 channels,” Science, vol. 330, no. 6000, pp. 105–109, 2010. View at Publisher · View at Google Scholar · View at Scopus
  42. J. W. Putney Jr., “A model for receptor-regulated calcium entry,” Cell Calcium, vol. 7, no. 1, pp. 1–12, 1986. View at Google Scholar · View at Scopus
  43. J. Roos, P. J. DiGregorio, A. V. Yeromin et al., “STIM1, an essential and conserved component of store-operated Ca 2+ channel function,” Journal of Cell Biology, vol. 169, no. 3, pp. 435–445, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Wang, J. F. Li, L. Zhao et al., “Inhibition of SOC/Ca2+/NFAT pathway is involved in the anti-proliferative effect of sildenafil on pulmonary artery smooth muscle cells,” Respiratory Research, vol. 10, article 123, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. J. Wang, L. Weigand, W. Lu, J. T. Sylvester, G. L. Semenza, and L. A. Shimoda, “Hypoxia inducible factor 1 mediates hypoxia-induced TRPC expression and elevated intracellular Ca2+ in pulmonary arterial smooth muscle cells,” Circulation Research, vol. 98, no. 12, pp. 1528–1537, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. R. T. Williams, S. S. M. Manji, N. J. Parker et al., “Identification and characterization of the STIM (stromal interaction molecule) gene family: coding for a novel class of transmembrane proteins,” Biochemical Journal, vol. 357, no. 3, pp. 673–685, 2001. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Zheng, P. B. Stathopulos, R. Schindl, G. Y. Li, C. Romanin, and M. Ikura, “Auto-inhibitory role of the EF-SAM domain of STIM proteins in store-operated calcium entry,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 4, pp. 1337–1342, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. S. L. Zhang, Y. Yu, J. Roos et al., “STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane,” Nature, vol. 437, no. 7060, pp. 902–905, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. X. Deng, Y. Wang, Y. Zhou, J. Soboloff, and D. L. Gill, “STIM and orai: dynamic intermembrane coupling to control cellular calcium signals,” Journal of Biological Chemistry, vol. 284, no. 34, pp. 22501–22505, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Liou, M. L. Kim, D. H. Won et al., “STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx,” Current Biology, vol. 15, no. 13, pp. 1235–1241, 2005. View at Publisher · View at Google Scholar · View at Scopus
  51. R. M. Luik, B. Wang, M. Prakriya, M. M. Wu, and R. S. Lewis, “Oligomerization of STIM1 couples ER calcium depletion to CRAC channel activation,” Nature, vol. 454, no. 7203, pp. 538–542, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Y. Kim and S. Muallem, “Unlocking SOAR releases STIM,” EMBO Journal, vol. 30, no. 9, pp. 1673–1675, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. O. Brandman, J. Liou, W. S. Park, and T. Meyer, “STIM2 is a feedback regulator that stabilizes basal cytosolic and endoplasmic reticulum Ca2+ levels,” Cell, vol. 131, no. 7, pp. 1327–1339, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Zheng, P. B. Stathopulos, G. Y. Li, and M. Ikura, “Biophysical characterization of the EF-hand and SAM domain containing Ca2+ sensory region of STIM1 and STIM2,” Biochemical and Biophysical Research Communications, vol. 369, no. 1, pp. 240–246, 2008. View at Publisher · View at Google Scholar · View at Scopus
  55. S. Parvez, A. Beck, C. Peinelt et al., “STIM2 protein mediates distinct store-dependent and store-independent modes of CRAC channel activation,” FASEB Journal, vol. 22, no. 3, pp. 752–761, 2008. View at Publisher · View at Google Scholar · View at Scopus
  56. M. Y. Song, A. Makino, and J. X. Yuan, “STIM2 contributes to enhanced store-operated Ca entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension,” Pulmonary Circulation, vol. 1, pp. 84–94, 2011. View at Google Scholar
  57. V. A. Golovina, O. Platoshyn, C. L. Bailey et al., “Upregulated TRP and enhanced capacitative Ca2+ entry in human pulmonary artery myocytes during proliferation,” American Journal of Physiology, vol. 280, no. 2, pp. H746–H755, 2001. View at Google Scholar · View at Scopus
  58. H. L. Sweeney, Z. Yang, G. Zhi, J. T. Stull, and K. M. Trybus, “Charge replacement near the phosphorylatable serine of the myosin regulatory light chain mimics aspects of phosphorylation,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 4, pp. 1490–1494, 1994. View at Google Scholar · View at Scopus
  59. A. Penna, A. Demuro, A. V. Yeromin et al., “The CRAC channel consists of a tetramer formed by Stim-induced dimerization of Orai dimers,” Nature, vol. 456, no. 7218, pp. 116–120, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. Y. Wang, X. Deng, T. Hewavitharana, J. Soboloff, and D. L. Gill, “STIM, ORAI and TRPC channels in the control of calcium entry signals in smooth muscle,” Clinical and Experimental Pharmacology and Physiology, vol. 35, no. 9, pp. 1127–1133, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. D. L. Cioffi, C. Barry, and T. Stevens, “Store-operated calcium entry channels in pulmonary endotheliumml: the emerging story of TRPCS and Orai1,” Advances in Experimental Medicine and Biology, vol. 661, pp. 137–154, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. M. Prakriya, S. Feske, Y. Gwack, S. Srikanth, A. Rao, and P. G. Hogan, “Orai1 is an essential pore subunit of the CRAC channel,” Nature, vol. 443, no. 7108, pp. 230–233, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. P. G. Hogan, R. S. Lewis, and A. Rao, “Molecular basis of calcium signaling in lymphocytes: STIM and ORAI,” Annual Review of Immunology, vol. 28, pp. 491–533, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Berra-Romani, A. Mazzocco-Spezzia, M. V. Pulina, and V. A. Golovina, “Ca2+ handling is altered when arterial myocytes progress from a contractile to a proliferative phenotype in culture,” American Journal of Physiology, vol. 295, no. 3, pp. C779–C790, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. S. G. Baryshnikov, M. V. Pulina, A. Zulian, C. I. Linde, and V. A. Golovina, “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,” American Journal of Physiology, vol. 297, no. 5, pp. C1103–C1112, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. J. M. Bisaillon, R. K. Motiani, J. C. Gonzalez-Cobos et al., “Essential role for STIM1/Orai1-mediated calcium influx in PDGF-induced smooth muscle migration,” American Journal of Physiology, vol. 298, no. 5, pp. C993–C1005, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. W. Zhang, K. E. Halligan, X. Zhang et al., “Orai1-mediated ICRAC Is essential for neointima formation after vascular injury,” Circulation Research, vol. 109, pp. 534–542, 2011. View at Publisher · View at Google Scholar · View at Scopus
  68. J. M. Edwards, Z. P. Neeb, M. A. Alloosh et al., “Exercise training decreases store-operated Ca2+ entry associated with metabolic syndrome and coronary atherosclerosis,” Cardiovascular Research, vol. 85, no. 3, pp. 631–640, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Ogawa, A. L. Firth, K. A. Smith, M. V. Maliakal, and J. X. Yuan, “PDGF enhances store-operated Ca2+ entry by upregulating STIM1/Orai1 via activation of Akt/mTOR in human pulmonary arterial smooth muscle cells,” American Journal of Physiology Cell Physiology, vol. 302, pp. C405–C411, 2012. View at Google Scholar
  70. T. Y. Chuang, L. C. Au, L. C. Wang, L. T. Ho, D. M. Yang, and C. C. Juan, “Potential effect of resistin on the ET-1-increased reactions of blood pressure in rats and Ca2+ signaling in vascular smooth muscle cells,” Journal of Cell Physiology, vol. 227, pp. 1610–1618, 2012. View at Google Scholar
  71. A. Lis, C. Peinelt, A. Beck et al., “CRACM1, CRACM2, and CRACM3 are store-operated Ca2+ channels with distinct functional properties,” Current Biology, vol. 17, no. 9, pp. 794–800, 2007. View at Publisher · View at Google Scholar · View at Scopus
  72. A. V. Yeromin, S. L. Zhang, W. Jiang, Y. Yu, O. Safrina, and M. D. Cahalan, “Molecular identification of the CRAC channel by altered ion selectivity in a mutant of Orai,” Nature, vol. 443, no. 7108, pp. 226–229, 2006. View at Publisher · View at Google Scholar · View at Scopus
  73. W. I. DeHaven, J. T. Smyth, R. R. Boyles, and J. W. Putney, “Calcium inhibition and calcium potentiation of Orai1, Orai2, and Orai3 calcium release-activated calcium channels,” Journal of Biological Chemistry, vol. 282, no. 24, pp. 17548–17556, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. P. C. Sundivakkam, M. Freichel, V. Singh et al., “The Ca2+ sensor stromal interaction molecule 1 (STIM1) is necessary and sufficient for the store-operated Ca2+ entry function of transient receptor potential canonical (TRPC) 1 and 4 channels in endothelial cells,” Molecular Pharmacology, vol. 81, pp. 510–526, 2012. View at Google Scholar
  75. G. M. Salido, I. Jardín, and J. A. Rosado, “The TRPC ion channels: association with Orai1 and STIM1 proteins and participation in capacitative and non-capacitative calcium entry,” Advances in Experimental Medicine and Biology, vol. 704, pp. 413–433, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. J. W. Putney Jr., M. Trebak, G. Vazquez, B. Wedel, and G. S. J. Bird, “Signalling mechanisms for TRPC3 channels,” Novartis Foundation Symposium, vol. 258, pp. 123–139, 2004. View at Google Scholar · View at Scopus
  77. G. Vazquez, B. J. Wedel, M. Trebak, G. S. J. Bird, and J. W. Putney Jr., “Expression level of the canonical transient receptor potential 3 (TRPC3) channel determines its mechanism of activation,” Journal of Biological Chemistry, vol. 278, no. 24, pp. 21649–21654, 2003. View at Publisher · View at Google Scholar · View at Scopus
  78. A. P. Albert and W. A. Large, “Store-operated Ca2+-permeable non-selective cation channels in smooth muscle cells,” Cell Calcium, vol. 33, no. 5-6, pp. 345–356, 2003. View at Publisher · View at Google Scholar · View at Scopus
  79. P. C. Sundivakkam, A. M. Kwiatek, T. T. Sharma, R. D. Minshall, A. B. Malik, and C. Tiruppathi, “Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells,” American Journal of Physiology, vol. 296, no. 3, pp. C403–C413, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. W. Lu, P. Ran, D. Zhang et al., “Sildenafil inhibits chronically hypoxic upregulation of canonical transient receptor potential expression in rat pulmonary arterial smooth muscle,” American Journal of Physiology, vol. 298, no. 1, pp. C114–C123, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. G. Peng, W. Lu, X. Li et al., “Expression of store-operated Ca2+ entry and transient receptor potential canonical and vanilloid-related proteins in rat distal pulmonary venous smooth muscle,” American Journal of Physiology, vol. 299, no. 5, pp. L621–L630, 2010. View at Publisher · View at Google Scholar · View at Scopus
  82. J. Wang, L. A. Shimoda, and J. T. Sylvester, “Capacitative calcium entry and TRPC channel proteins are expressed in rat distal pulmonary arterial smooth muscle,” American Journal of Physiology, vol. 286, no. 4, pp. L848–L858, 2004. View at Google Scholar · View at Scopus
  83. M. J. Lin, G. P. H. Leung, W. M. Zhang et al., “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,” Circulation Research, vol. 95, no. 5, pp. 496–505, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. B. Kumar, K. Dreja, S. S. Shah et al., “Upregulated TRPC1 channel in vascular injury in vivo and its role in human neointimal hyperplasia,” Circulation Research, vol. 98, no. 4, pp. 557–563, 2006. View at Publisher · View at Google Scholar · View at Scopus
  85. X. R. Liu, M. F. Zhang, N. Yang et al., “Enhanced store-operated Ca2+ entry and TRPC channel expression in pulmonary arteries of monocrotaline-induced pulmonary hypertensive rats,” American Journal of Physiology, vol. 302, pp. C77–C87, 2012. View at Google Scholar
  86. J. P. T. Ward, G. A. Knock, V. A. Snetkov, and P. I. Aaronson, “Protein kinases in vascular smooth muscle tone-role in the pulmonary vasculature and hypoxic pulmonary vasoconstriction,” Pharmacology and Therapeutics, vol. 104, no. 3, pp. 207–231, 2004. View at Publisher · View at Google Scholar · View at Scopus
  87. S. N. Saleh, A. P. Albert, and W. A. Large, “Activation of native TRPC1/C5/C6 channels by endothelin-1 is mediated by both PIP3 and PIP2 in rabbit coronary artery myocytes,” Journal of Physiology, vol. 587, no. 22, pp. 5361–5375, 2009. View at Publisher · View at Google Scholar · View at Scopus
  88. J. W. Landsberg and J. X. J. Yuan, “Calcium and TRP channels in pulmonary vascular smooth muscle cell proliferation,” News in Physiological Sciences, vol. 19, no. 2, pp. 44–50, 2004. View at Publisher · View at Google Scholar · View at Scopus
  89. A. B. Parekh and J. W. Putney, “Store-operated calcium channels,” Physiological Reviews, vol. 85, no. 2, pp. 757–810, 2005. View at Publisher · View at Google Scholar · View at Scopus
  90. J. P. Yuan, W. Zeng, G. N. Huang, P. F. Worley, and S. Muallem, “STIM1 heteromultimerizes TRPC channels to determine their function as store-operated channels,” Nature Cell Biology, vol. 9, no. 6, pp. 636–645, 2007. View at Publisher · View at Google Scholar · View at Scopus
  91. J. Li, P. Sukumar, C. J. Milligan et al., “Interactions, functions, and independence of plasma membrane STIM1 and TRPC1 in vascular smooth muscle cells,” Circulation Research, vol. 103, no. 8, pp. e97–e104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. W. Zeng, J. P. Yuan, M. S. Kim et al., “STIM1 gates TRPC channels, but not Orai1, by electrostatic interaction,” Molecular Cell, vol. 32, no. 3, pp. 439–448, 2008. View at Publisher · View at Google Scholar · View at Scopus
  93. M. S. Kim, W. Zeng, J. P. Yuan, D. M. Shin, P. F. Worley, and S. Muallem, “Native store-operated Ca2+ influx requires the channel function of Orai 1 and TRPC1,” Journal of Biological Chemistry, vol. 284, no. 15, pp. 9733–9741, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. Y. Liao, C. Erxleben, J. Abramowitz et al., “Functional interactions among Orai1, TRPCs, and STIM1 suggest a STIM-regulated heteromeric Orai/TRPC model for SOCE/Icrac channels,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 8, pp. 2895–2900, 2008. View at Publisher · View at Google Scholar · View at Scopus
  95. Y. Liao, C. Erxleben, E. Yildirim, J. Abramowitz, D. L. Armstrong, and L. Birnbaumer, “Orai proteins interact with TRPC channels and confer responsiveness to store depletion,” Proceedings of the National Academy of Sciences of the United States of America, vol. 104, no. 11, pp. 4682–4687, 2007. View at Publisher · View at Google Scholar · View at Scopus
  96. T. C. Kwong, X. Liu, L. O. Hwei, and I. S. Ambudkar, “Functional requirement for Orai1 in store-operated TRPC1-STIM1 channels,” Journal of Biological Chemistry, vol. 283, no. 19, pp. 12935–12940, 2008. View at Publisher · View at Google Scholar · View at Scopus
  97. D. L. Cioffi, S. Wu, and H. Chen, “Orai1 determines calcium selectivity of an endogenous TRPC heterotetramer channel,” Circulation Research, vol. 110, pp. 1435–1444, 2012. View at Google Scholar
  98. N. Kunichika, J. W. Landsberg, Y. Yu et al., “Bosentan inhibits transient receptor potential channel expression in pulmonary vascular myocytes,” American Journal of Respiratory and Critical Care Medicine, vol. 170, no. 10, pp. 1101–1107, 2004. View at Publisher · View at Google Scholar · View at Scopus
  99. N. Kunichika, Y. Yu, C. V. Remillard, O. Platoshyn, S. Zhang, and J. X. J. Yuan, “Overexpression of TRPC1 enhances pulmonary vasoconstriction induced by capacitative Ca2+ entry,” American Journal of Physiology, vol. 287, no. 5, pp. L962–L969, 2004. View at Publisher · View at Google Scholar · View at Scopus
  100. Y. Yu, I. Fantozzi, C. V. Remillard et al., “Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 38, pp. 13861–13866, 2004. View at Publisher · View at Google Scholar · View at Scopus
  101. A. Dietrich, Y. S. M. Mederos, M. Gollasch et al., “Increased vascular smooth muscle contractility in TRPC6 -/- mice,” Molecular and Cellular Biology, vol. 25, pp. 6980–6989, 2005. View at Google Scholar
  102. Y. Yu, S. H. Keller, C. V. Remillard et al., “A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension,” Circulation, vol. 119, no. 17, pp. 2313–2322, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. M. Trebak, G. Vazquez, G. S. J. Bird, and J. W. Putney, “The TRPC3/6/7 subfamily of cation channels,” Cell Calcium, vol. 33, no. 5-6, pp. 451–461, 2003. View at Publisher · View at Google Scholar · View at Scopus
  104. N. Weissmann, A. Dietrich, B. Fuchs et al., “Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 50, pp. 19093–19098, 2006. View at Publisher · View at Google Scholar · View at Scopus
  105. A. Dietrich, H. Kalwa, B. Fuchs, F. Grimminger, N. Weissmann, and T. Gudermann, “In vivo TRPC functions in the cardiopulmonary vasculature,” Cell Calcium, vol. 42, no. 2, pp. 233–244, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. R. Inoue, T. Okada, H. Onoue et al., “The transient receptor potential protein homologue TRP6 is the essential component of vascular alpha;1-adrenoceptor-activated Ca2+-permeable cation channel,” Circulation Research, vol. 88, no. 3, pp. 325–332, 2001. View at Google Scholar · View at Scopus
  107. S. Jung, R. Strotmann, G. Schultz, and T. D. Plant, “TRCP6 is a candidate channel involved in receptor stimulated cation currents in A7r5 smooth muscle cells,” American Journal of Physiology, vol. 282, no. 2, pp. C347–C359, 2002. View at Google Scholar · View at Scopus
  108. B. Fuchs, M. Rupp, H. A. Ghofrani et al., “Diacylglycerol regulates acute hypoxic pulmonary vasoconstriction via TRPC6,” Respiratory Research, vol. 12, article 20, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. H. Sawada, Y. Mitani, J. Maruyama et al., “A nuclear factor-κB inhibitor pyrrolidine dithiocarbamate ameliorates pulmonary hypertension in rats,” Chest, vol. 132, no. 4, pp. 1265–1274, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. Y. Jia and L. Y. Lee, “Role of TRPV receptors in respiratory diseases,” Biochimica et Biophysica Acta, vol. 1772, pp. 915–927, 2007. View at Publisher · View at Google Scholar · View at Scopus
  111. Y. X. Wang, J. Wang, C. Wang et al., “Functional expression of transient receptor potential vanilloid-related channels in chronically hypoxic human pulmonary arterial smooth muscle cells,” Journal of Membrane Biology, vol. 223, no. 3, pp. 151–159, 2008. View at Publisher · View at Google Scholar · View at Scopus
  112. B. Minke and M. Parnas, “Insights on TRP channels from in vivo studies in Drosophila,” Annual Review of Physiology, vol. 68, pp. 649–684, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. X. R. Yang, M. J. Lin, L. S. McIntosh, and J. S. K. Sham, “Functional expression of transient receptor potential melastatin- and vanilloid-related channels in pulmonary arterial and aortic smooth muscle,” American Journal of Physiology, vol. 290, no. 6, pp. L1267–L1276, 2006. View at Publisher · View at Google Scholar · View at Scopus
  114. S. Earley, T. J. Heppner, M. T. Nelson, and J. E. Brayden, “TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels,” Circulation Research, vol. 97, no. 12, pp. 1270–1279, 2005. View at Publisher · View at Google Scholar · View at Scopus
  115. M. T. Nelson, H. Cheng, M. Rubart et al., “Relaxation of arterial smooth muscle by calcium sparks,” Science, vol. 270, no. 5236, pp. 633–637, 1995. View at Google Scholar · View at Scopus
  116. T. Ducret, C. Guibert, R. Marthan, and J. P. Savineau, “Serotonin-induced activation of TRPV4-like current in rat intrapulmonary arterial smooth muscle cells,” Cell Calcium, vol. 43, no. 4, pp. 315–323, 2008. View at Publisher · View at Google Scholar · View at Scopus
  117. T. Kark, Z. Bagi, E. Lizanecz et al., “Tissue-specific regulation of microvascular diameter: opposite functional roles of neuronal and smooth muscle located vanilloid receptor-1,” Molecular Pharmacology, vol. 73, no. 5, pp. 1405–1412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  118. K. Muraki, Y. Iwata, Y. Katanosaka et al., “TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes,” Circulation Research, vol. 93, no. 9, pp. 829–838, 2003. View at Publisher · View at Google Scholar · View at Scopus
  119. H. Y. Yoo, S. J. Park, E. Y. Seo et al., “Role of thromboxane A(2)-activated nonselective cation channels in hypoxic pulmonary vasoconstriction of rat,” American Journal of Physiology, vol. 302, pp. C307–C317, 2012. View at Google Scholar
  120. R. Inoue, L. J. Jensen, J. Shi et al., “Transient receptor potential channels in cardiovascular function and disease,” Circulation Research, vol. 99, no. 2, pp. 119–131, 2006. View at Publisher · View at Google Scholar · View at Scopus
  121. B. Nilius, J. Prenen, G. Droogmans et al., “Voltage dependence of the Ca2+-activated cation channel TRPM4,” Journal of Biological Chemistry, vol. 278, no. 33, pp. 30813–30820, 2003. View at Publisher · View at Google Scholar · View at Scopus
  122. B. Nilius, J. Prenen, A. Janssens et al., “The selectivity filter of the cation channel TRPM4,” Journal of Biological Chemistry, vol. 280, no. 24, pp. 22899–22906, 2005. View at Publisher · View at Google Scholar · View at Scopus
  123. A. L. Gonzales, G. C. Amberg, and S. Earley, “Ca2+ release from the sarcoplasmic reticulum is required for sustained TRPM4 activity in cerebral artery smooth muscle cells,” American Journal of Physiology, vol. 299, no. 2, pp. C279–C288, 2010. View at Publisher · View at Google Scholar · View at Scopus
  124. S. A. Reading and J. E. Brayden, “Central role of TRPM4 channels in cerebral blood flow regulation,” Stroke, vol. 38, no. 8, pp. 2322–2328, 2007. View at Publisher · View at Google Scholar · View at Scopus
  125. Y. He, G. Yao, C. Savoia, and R. M. Touyz, “Transient receptor potential melastatin 7 ion channels regulate magnesium homeostasis in vascular smooth muscle cells: role of angiotensin II,” Circulation Research, vol. 96, no. 2, pp. 207–215, 2005. View at Publisher · View at Google Scholar · View at Scopus
  126. C. Nasuhoglu, S. Feng, Y. Mao et al., “Modulation of cardiac PIP2 by cardioactive hormones and other physiologically relevant interventions,” American Journal of Physiology, vol. 283, no. 1, pp. C223–C234, 2002. View at Google Scholar · View at Scopus
  127. C. D. Johnson, D. Melanaphy, A. Purse, S. A. Stokesberry, P. Dickson, and A. V. Zholos, “Transient receptor potential melastatin 8 channel involvement in the regulation of vascular tone,” American Journal of Physiology, vol. 296, no. 6, pp. H1868–H1877, 2009. View at Publisher · View at Google Scholar · View at Scopus
  128. F. Mahieu, G. Owsianik, L. Verbert et al., “TRPM8-independent menthol-induced Ca2+ release from endoplasmic reticulum and Golgi,” Journal of Biological Chemistry, vol. 282, no. 5, pp. 3325–3336, 2007. View at Publisher · View at Google Scholar · View at Scopus