Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Canonical Transient Receptor Potential Channels and Their Link with Cardio/Cerebro-Vascular Diseases

  • Xiao, Xiong (Department of Pharmacology, School of Pharmacy, Fourth Military Medical University) ;
  • Liu, Hui-Xia (Department of Pharmacology, School of Pharmacy, Fourth Military Medical University) ;
  • Shen, Kuo (Cadet Brigade, School of Pharmacy, Fourth Military Medical University) ;
  • Cao, Wei (Department of Natural Medicine & Institute of Materia Medica, School of Pharmacy, Fourth Military Medical University) ;
  • Li, Xiao-Qiang (Department of Pharmacology, School of Pharmacy, Fourth Military Medical University)
  • Received : 2016.05.09
  • Accepted : 2016.12.27
  • Published : 2017.09.01
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Abstract

The canonical transient receptor potential channels (TRPCs) constitute a series of nonselective cation channels with variable degrees of $Ca^{2+}$ selectivity. TRPCs consist of seven mammalian members, TRPC1, TRPC2, TRPC3, TRPC4, TRPC5, TRPC6, and TRPC7, which are further divided into four subtypes, TRPC1, TRPC2, TRPC4/5, and TRPC3/6/7. These channels take charge of various essential cell functions such as contraction, relaxation, proliferation, and dysfunction. This review, organized into seven main sections, will provide an overview of current knowledge about the underlying pathogenesis of TRPCs in cardio/cerebro-vascular diseases, including hypertension, pulmonary arterial hypertension, cardiac hypertrophy, atherosclerosis, arrhythmia, and cerebrovascular ischemia reperfusion injury. Collectively, TRPCs could become a group of drug targets with important physiological functions for the therapy of human cardio/cerebro-vascular diseases.

Keywords

References

  1. Anderson, M., Kim, E. Y., Hagmann, H., Benzing, T. and Dryer, S. E. (2013) Opposing effects of podocin on the gating of podocyte TRPC6 channels evoked by membrane stretch or diacylglycerol. Am. J. Physiol., Cell Physiol. 305, C276-C289. https://doi.org/10.1152/ajpcell.00095.2013
  2. Bae, Y. M., Kim, A., Lee, Y. J., Lim, W., Noh, Y. H., Kim, E. J., Kim, J., Kim, T. K., Park, S. W., Kim, B., Cho, S. I., Kim, D. K. and Ho, W. K. (2007) Enhancement of receptor-operated cation current and TRPC6 expression in arterial smooth muscle cells of deoxycorticosterone acetate-salt hypertensive rats. J. Hypertens. 25, 809-817. https://doi.org/10.1097/HJH.0b013e3280148312
  3. Beamish, J. A., He, P., Kottke-Marchant, K. and Marchant, R. E. (2010) Molecular regulation of contractile smooth muscle cell phenotype:implications for vascular tissue engineering. Tissue Eng. Part B Rev. 16, 467-491. https://doi.org/10.1089/ten.teb.2009.0630
  4. Bergdahl, A., Gomez, M. F., Dreja, K., Xu, S. Z., Adner, M., Beech, D. J., Broman, J., Hellstrand, P. and Sward, K. (2003) Cholesterol depletion impairs vascular reactivity to endothelin-1 by reducing store-operated $Ca^{2+}$ entry dependent on TRPC1. Circ. Res. 93, 839-847. https://doi.org/10.1161/01.RES.0000100367.45446.A3
  5. Berridge, M. J., Bootman, M. D. and Roderick, H. L. (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat. Rev. Mol. Cell Biol. 4, 517-529.
  6. Birnbaumer, L., Zhu, X., Jiang, M., Boulay, G., Peyton, M., Vannier, B., Brown, D., Platano, D., Sadeghi, H., Stefani, E. and Birnbaumer, M. (1996) On the molecular basis and regulation of cellular capacitative calcium entry: roles for Trp proteins. Proc. Natl. Acad. Sci. U.S.A. 93, 15195-15202. https://doi.org/10.1073/pnas.93.26.15195
  7. Bowman, C. L., Gottlieb, P. A., Suchyna, T. M., Murphy, Y. K. and Sachs, F. (2007) Mechanosensitive ion channels and the peptide inhibitor GsMTx-4: history, properties, mechanisms and pharmacology. Toxicon 49, 249-270. https://doi.org/10.1016/j.toxicon.2006.09.030
  8. Brookes, P. S., Yoon, Y., Robotham, J. L., Anders, M. W. and Sheu, S. S. (2004) Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am. J. Physiol., Cell Physiol. 287, C817-C833. https://doi.org/10.1152/ajpcell.00139.2004
  9. Bush, E. W., Hood, D. B., Papst, P. J., Chapo, J. A., Minobe, W., Bristow, M. R., Olson, E. N. and McKinsey, T. A. (2006) Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J. Biol. Chem. 281, 33487-33496. https://doi.org/10.1074/jbc.M605536200
  10. Carafoli, E. (2002) Calcium signaling: a tale for all seasons. Proc. Natl. Acad. Sci. U.S.A. 99, 1115-1122. https://doi.org/10.1073/pnas.032427999
  11. Chaudhuri, P., Rosenbaum, M. A., Sinharoy, P., Damron, D. S., Birnbaumer, L. and Graham, L. M. (2016) Membrane translocation of TRPC6 channels and endothelial migration are regulated by calmodulin and PI3 kinase activation. Proc. Natl. Acad. Sci. U.S.A. 113, 2110-2115. https://doi.org/10.1073/pnas.1600371113
  12. Chen, J., Crossland, R. F., Noorani, M. M. and Marrelli, S. P. (2009) Inhibition of TRPC1/TRPC3 by PKG contributes to NO-mediated vasorelaxation. Am. J. Physiol. Heart Circ. Physiol. 297, H417-H424. https://doi.org/10.1152/ajpheart.01130.2008
  13. Chen, X., Yang, D., Ma, S., He, H., Luo, Z., Feng, X., Cao, T., Ma, L., Yan, Z., Liu, D., Tepel, M. and Zhu, Z. (2010) Increased rhythmicity in hypertensive arterial smooth muscle is linked to transient receptor potential canonical channels. J. Cell. Mol. Med. 14, 2483-2494. https://doi.org/10.1111/j.1582-4934.2009.00890.x
  14. Cheng, K. T., Liu, X., Ong, H. L. and Ambudkar, I. S. (2008) Functional requirement for Orai1 in store-operated TRPC1-STIM1 channels. J. Biol. Chem. 283, 12935-12940. https://doi.org/10.1074/jbc.C800008200
  15. Christian, H. and Maik, G. (2011) Pharmacological Modulation of Diacylglycerol-Sensitive TRPC3/6/7 Channels. Curr. Pharm. Biotechnol. 12, 35-41. https://doi.org/10.2174/138920111793937943
  16. Cosens, D. J. and Manning, A. (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224, 285-287. https://doi.org/10.1038/224285a0
  17. Dietrich, A., Chubanov, V., Kalwa, H., Rost, B. R. and Gudermann, T. (2006) Cation channels of the transient receptor potential superfamily:their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacol. Ther. 112, 744-760. https://doi.org/10.1016/j.pharmthera.2006.05.013
  18. Dietrich, A., Kalwa, H. and Gudermann, T. (2010) TRPC channels in vascular cell function. Thromb. Haemost. 103, 262-270. https://doi.org/10.1160/TH09-08-0517
  19. Dietrich, A., Mederos, Y. S. M., Gollasch, M., Gross, V., Storch, U., Dubrovska, G., Obst, M., Yildirim, E., Salanova, B., Kalwa, H., Essin, K., Pinkenburg, O., Luft, F. C., Gudermann, T. and Birnbaumer, L. (2005) Increased vascular smooth muscle contractility in $Trpc6^{-/-}mice$. Mol. Cell. Biol. 25, 6980-6989. https://doi.org/10.1128/MCB.25.16.6980-6989.2005
  20. Du, W., Huang, J., Yao, H., Zhou, K., Duan, B. and Wang, Y. (2010) Inhibition of TRPC6 degradation suppresses ischemic brain damage in rats. J. Clin. Invest. 120, 3480-3492. https://doi.org/10.1172/JCI43165
  21. Dyachenko, V., Husse, B., Rueckschloss, U. and Isenberg, G. (2009) Mechanical deformation of ventricular myocytes modulates both TRPC6 and Kir2.3 channels. Cell Calcium 45, 38-54. https://doi.org/10.1016/j.ceca.2008.06.003
  22. Eder, P. and Molkentin, J. D. (2011) TRPC channels as effectors of cardiac hypertrophy. Circ. Res. 108, 265-272. https://doi.org/10.1161/CIRCRESAHA.110.225888
  23. Edwards, J. M., Neeb, Z. P., Alloosh, M. A., Long, X., Bratz, I. N., Peller, C. R., Byrd, J. P., Kumar, S., Obukhov, A. G. and Sturek, M. (2010) Exercise training decreases store-operated $Ca^{2+}$ entry associated with metabolic syndrome and coronary atherosclerosis. Cardiovasc. Res. 85, 631-640. https://doi.org/10.1093/cvr/cvp308
  24. Farooqi, A. A., Riaz, A. M. and Bhatti, S. (2013) TRPC signaling mechanisms and therapeutic opportunities: trapdoors are monitored by gatekeepers. Pak. J. Pharm. Sci. 26, 847-852.
  25. Franz, M. R. and Bode, F. (2003) Mechano-electrical feedback underlying arrhythmias: the atrial fibrillation case. Prog. Biophys. Mol. Biol. 82, 163-174. https://doi.org/10.1016/S0079-6107(03)00013-0
  26. Fuchs, B., Dietrich, A., Gudermann, T., Kalwa, H., Grimminger, F. and Weissmann, N. (2010) The role of classical transient receptor potential channels in the regulation of hypoxic pulmonary vasoconstriction. Adv. Exp. Med. Biol. 661, 187-200.
  27. Golovina, V. A., Platoshyn, O., Bailey, C. L., Wang, J., Limsuwan, A., Sweeney, M., Rubin, L. J. and Yuan, J. X. (2001) Upregulated TRP and enhanced capacitative $Ca^{2+}$ entry in human pulmonary artery myocytes during proliferation. Am. J. Physiol. Heart Circ. Physiol. 280, H746-H755. https://doi.org/10.1152/ajpheart.2001.280.2.H746
  28. Gopal, S., Sogaard, P., Multhaupt, H. A., Pataki, C., Okina, E., Xian, X., Pedersen, M. E., Stevens, T., Griesbeck, O., Park, P. W., Pocock, R. and Couchman, J. R. (2015) Transmembrane proteoglycans control stretch-activated channels to set cytosolic calcium levels. J. Cell Biol. 210, 1199-1211. https://doi.org/10.1083/jcb.201501060
  29. Harada, M., Luo, X., Qi, X. Y., Tadevosyan, A., Maguy, A., Ordog, B., Ledoux, J., Kato, T., Naud, P., Voigt, N., Shi, Y., Kamiya, K., Murohara, T., Kodama, I., Tardif, J. C., Schotten, U., Van Wagoner, D. R., Dobrev, D. and Nattel, S. (2012) Transient receptor potential canonical-3 channel-dependent fibroblast regulation in atrial fibrillation. Circulation 126, 2051-2064. https://doi.org/10.1161/CIRCULATIONAHA.112.121830
  30. Hofmann, T., Obukhov, A. G., Schaefer, M., Harteneck, C., Gudermann, T. and Schultz, G. (1999) Direct activation of human TRPC6 and TRPC3 channels by diacylglycerol. Nature 397, 259-263. https://doi.org/10.1038/16711
  31. Inoue, R., Jensen, L. J., Jian, Z., Shi, J., Hai, L., Lurie, A. I., Henriksen, F. H., Salomonsson, M., Morita, H., Kawarabayashi, Y., Mori, M., Mori, Y. and Ito, Y. (2009) Synergistic activation of vascular TRPC6 channel by receptor and mechanical stimulation via phospholipase C/diacylglycerol and phospholipase A2/omega-hydroxylase/20-HETE pathways. Circ. Res. 104, 1399-1409. https://doi.org/10.1161/CIRCRESAHA.108.193227
  32. Inoue, R., Jensen, L. J., Shi, J., Morita, H., Nishida, M., Honda, A. and Ito, Y. (2006) Transient receptor potential channels in cardiovascu lar function and disease. Circ. Res. 99, 119-131. https://doi.org/10.1161/01.RES.0000233356.10630.8a
  33. Iwasaki, Y. K., Nishida, K., Kato, T. and Nattel, S. (2011) Atrial fibrillation pathophysiology: implications for management. Circulation 124, 2264-2274. https://doi.org/10.1161/CIRCULATIONAHA.111.019893
  34. Kinoshita, H., Kuwahara, K., Nishida, M., Jian, Z., Rong, X., Kiyonaka, S., Kuwabara, Y., Kurose, H., Inoue, R., Mori, Y., Li, Y., Nakagawa, Y., Usami, S., Fujiwara, M., Yamada, Y., Minami, T., Ueshima, K. and Nakao, K. (2010) Inhibition of TRPC6 channel activity contributes to the antihypertrophic effects of natriuretic peptides-guanylyl cyclase-A signaling in the heart. Circ. Res. 106, 1849-1860. https://doi.org/10.1161/CIRCRESAHA.109.208314
  35. Kiyonaka, S., Kato, K., Nishida, M., Mio, K., Numaga, T., Sawaguchi, Y., Yoshida, T., Wakamori, M., Mori, E., Numata, T., Ishii, M., Takemoto, H., Ojida, A., Watanabe, K., Uemura, A., Kurose, H., Morii, T., Kobayashi, T., Sato, Y., Sato, C., Hamachi, I. and Mori, Y. (2009) Selective and direct inhibition of TRPC3 channels underlies biological activities of a pyrazole compound. Proc. Natl. Acad. Sci. U.S.A. 106, 5400-5405. https://doi.org/10.1073/pnas.0808793106
  36. Koenig, S., Schernthaner, M., Maechler, H., Kappe, C. O., Glasnov, T. N., Hoefler, G., Braune, M., Wittchow, E. and Groschner, K. (2013) A TRPC3 blocker, ethyl-1-(4-(2,3,3-trichloroacrylamide)phenyl)-5-(trifluoromethyl)-1H-pyrazole-4-c arboxylate (Pyr3), prevents stentinduced arterial remodeling. J. Pharmacol. Exp. Ther. 344, 33-40. https://doi.org/10.1124/jpet.112.196832
  37. Kuhr, F. K., Smith, K. A., Song, M. Y., Levitan, I. and Yuan, J. X. (2012) New mechanisms of pulmonary arterial hypertension: role of $Ca^{2+}$ signaling. Am. J. Physiol. Heart Circ. Physiol. 302, H1546-H1562. https://doi.org/10.1152/ajpheart.00944.2011
  38. Kukkonen, J. P. (2011) A menage a trois made in heaven: G-proteincoupled receptors, lipids and TRP channels. Cell Calcium 50, 9-26. https://doi.org/10.1016/j.ceca.2011.04.005
  39. 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. https://doi.org/10.1161/01.RES.0000204724.29685.db
  40. Kuwahara, K., Wang, Y., McAnally, J., Richardson, J. A., Bassel-Duby, R., Hill, J. A. and Olson, E. N. (2006) TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J. Clin. Invest. 116, 3114-3126. https://doi.org/10.1172/JCI27702
  41. Kwan, H. Y., Huang, Y. and Yao, X. (2004) Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G. Proc. Natl. Acad. Sci. U.S.A. 101, 2625-2630. https://doi.org/10.1073/pnas.0304471101
  42. Leypold, B. G., Yu, C. R., Leinders-Zufall, T., Kim, M. M., Zufall, F. and Axel, R. (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc. Natl. Acad. Sci. U.S.A. 99, 6376-6381. https://doi.org/10.1073/pnas.082127599
  43. Lin, M. J., Leung, G. P., Zhang, W. M., Yang, X. R., Yip, K. P., Tse, C. M. and Sham, J. S. (2004) Chronic hypoxia-induced upregulation of store-operated and receptor-operated $Ca^{2+}$ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ. Res. 95, 496-505. https://doi.org/10.1161/01.RES.0000138952.16382.ad
  44. Lin, Y., Chen, F., Zhang, J., Wang, T., Wei, X., Wu, J., Feng, Y., Dai, Z. and Wu, Q. (2013) Neuroprotective effect of resveratrol on ischemia/reperfusion injury in rats through TRPC6/CREB pathways. J. Mol. Neurosci. 50, 504-513. https://doi.org/10.1007/s12031-013-9977-8
  45. Liu, D., Maier, A., Scholze, A., Rauch, U., Boltzen, U., Zhao, Z., Zhu, Z. and Tepel, M. (2008) High glucose enhances transient receptor potential channel canonical type 6-dependent calcium influx in human platelets via phosphatidylinositol 3-kinase-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 28, 746-751. https://doi.org/10.1161/ATVBAHA.108.162222
  46. Liu, D., Scholze, A., Zhu, Z., Krueger, K., Thilo, F., Burkert, A., Streffer, K., Holz, S., Harteneck, C., Zidek, W. and Tepel, M. (2006) Transient receptor potential channels in essential hypertension. J. Hypertens. 24, 1105-1114. https://doi.org/10.1097/01.hjh.0000226201.73065.14
  47. Liu, D., Yang, D., He, H., Chen, X., Cao, T., Feng, X., Ma, L., Luo, Z., Wang, L., Yan, Z., Zhu, Z. and Tepel, M. (2009) Increased transient receptor potential canonical type 3 channels in vasculature from hypertensive rats. Hypertension 53, 70-76. https://doi.org/10.1161/HYPERTENSIONAHA.108.116947
  48. Liu, D. Y., Scholze, A., Kreutz, R., Wehland-von-Trebra, M., Zidek, W., Zhu, Z. M. and Tepel, M. (2007a) Monocytes from spontaneously hypertensive rats show increased store-operated and second messenger-operated calcium influx mediated by transient receptor potential canonical Type 3 channels. Am. J. Hypertens. 20, 1111-1118. https://doi.org/10.1016/j.amjhyper.2007.04.004
  49. Liu, D. Y., Thilo, F., Scholze, A., Wittstock, A., Zhao, Z. G., Harteneck, C., Zidek, W., Zhu, Z. M. and Tepel, M. (2007b) Increased storeoperated and 1-oleoyl-2-acetyl-sn-glycerol-induced calcium influx in monocytes is mediated by transient receptor potential canonical channels in human essential hypertension. J. Hypertens. 25, 799-808. https://doi.org/10.1097/HJH.0b013e32803cae2b
  50. Liu, H., Yang, L., Chen, K. H., Sun, H. Y., Jin, M. W., Xiao, G. S., Wang, Y. and Li, G. R. (2016) SKF-96365 blocks human ether-ago-go-related gene potassium channels stably expressed in HEK 293 cells. Pharmacol. Res. 104, 61-69. https://doi.org/10.1016/j.phrs.2015.12.012
  51. Liu, X. R., Zhang, M. F., Yang, N., Liu, Q., Wang, R. X., Cao, Y. N., Yang, X. R., Sham, J. S. and Lin, M. J. (2012) Enhanced storeoperated $Ca^{2+}$ entry and TRPC channel expression in pulmonary arteries of monocrotaline-induced pulmonary hypertensive rats. Am. J. Physiol., Cell Physiol. 302, C77-C87. https://doi.org/10.1152/ajpcell.00247.2011
  52. Loga, F., Domes, K., Freichel, M., Flockerzi, V., Dietrich, A., Birnbaumer, L., Hofmann, F. and Wegener, J. W. (2013) The role of cGMP/cGKI signalling and Trpc channels in regulation of vascular tone. Cardiovasc. Res. 100, 280-287. https://doi.org/10.1093/cvr/cvt176
  53. Lu, W., Ran, P., Zhang, D., Peng, G., Li, B., Zhong, N. and Wang, J. (2010) Sildenafil inhibits chronically hypoxic upregulation of canonical transient receptor potential expression in rat pulmonary arterial smooth muscle. Am. J. Physiol., Cell Physiol. 298, C114-C123. https://doi.org/10.1152/ajpcell.00629.2008
  54. Lu, W., Wang, J., Shimoda, L. A. and Sylvester, J. T. (2008) Differences in STIM1 and TRPC expression in proximal and distal pulmonary arterial smooth muscle are associated with differences in $Ca^{2+}$ responses to hypoxia. Am. J. Physiol. Lung Cell Mol. Physiol. 295, L104-L113. https://doi.org/10.1152/ajplung.00058.2008
  55. Maier, T., Follmann, M., Hessler, G., Kleemann, H. W., Hachtel, S., Fuchs, B., Weissmann, N., Linz, W., Schmidt, T., Lohn, M., Schroeter, K., Wang, L., Rutten, H. and Strubing, C. (2015) Discovery and pharmacological characterization of a novel potent inhibitor of diacylglycerol-sensitive TRPC cation channels. Br. J. Pharmacol. 172, 3650-3660. https://doi.org/10.1111/bph.13151
  56. Malczyk, M., Veith, C., Fuchs, B., Hofmann, K., Storch, U., Schermuly, R. T., Witzenrath, M., Ahlbrecht, K., Fecher-Trost, C., Flockerzi, V., Ghofrani, H. A., Grimminger, F., Seeger, W., Gudermann, T., Dietrich, A. and Weissmann, N. (2013) Classical transient receptor potential channel 1 in hypoxia-induced pulmonary hypertension. Am. J. Respir. Crit. Care Med. 188, 1451-1459. https://doi.org/10.1164/rccm.201307-1252OC
  57. Merritt, J. E., Armstrong, W. P., Benham, C. D., Hallam, T. J., Jacob, R., Jaxa-Chamiec, A., Leigh, B. K., McCarthy, S. A., Moores, K. E. and Rink, T. J. (1990) SK&F 96365, a novel inhibitor of receptormediated calcium entry. Biochem. J. 271, 515-522. https://doi.org/10.1042/bj2710515
  58. Minke, B. (2006) TRP channels and $Ca^{2+}$ signaling. Cell Calcium 40, 261-275. https://doi.org/10.1016/j.ceca.2006.05.002
  59. Montell, C. (2005) Drosophila TRP channels. Pflugers Arch. 451, 19-28. https://doi.org/10.1007/s00424-005-1426-2
  60. Montell, C., Birnbaumer, L., Flockerzi, V., Bindels, R. J., Bruford, E. A., Caterina, M. J., Clapham, D. E., Harteneck, C., Heller, S., Julius, D., Kojima, I., Mori, Y., Penner, R., Prawitt, D., Scharenberg, A. M., Schultz, G., Shimizu, N. and Zhu, M. X. (2002) A unified nomenclature for the superfamily of TRP cation channels. Mol. Cell 9, 229-231. https://doi.org/10.1016/S1097-2765(02)00448-3
  61. Nakashima, H. and Kumagai, K. (2007) Reverse-remodeling effects of angiotensin II type 1 receptor blocker in a canine atrial fibrillation model. Circ. J. 71, 1977-1982. https://doi.org/10.1253/circj.71.1977
  62. Nakayama, H., Wilkin, B. J., Bodi, I. and Molkentin, J. D. (2006) Calcineurin-dependent cardiomyopathy is activated by TRPC in the adult mouse heart. FASEB J. 20, 1660-1670. https://doi.org/10.1096/fj.05-5560com
  63. Nattel, S. (2011) From guidelines to bench: implications of unresolved clinical issues for basic investigations of atrial fibrillation mechanisms. Can. J. Cardiol. 27, 19-26. https://doi.org/10.1016/j.cjca.2010.11.004
  64. Ng, L. C. and Gurney, A. M. (2001) Store-operated channels mediate $Ca^{2+}$ influx and contraction in rat pulmonary artery. Circ. Res. 89, 923-929. https://doi.org/10.1161/hh2201.100315
  65. Nilius, B., Owsianik, G., Voets, T. and Peters, J. A. (2007) Transient receptor potential cation channels in disease. Physiol. Rev. 87, 165-217. https://doi.org/10.1152/physrev.00021.2006
  66. Nilius, B. and Voets, T. (2005) TRP channels: a TR(I)P through a world of multifunctional cation channels. Pflugers Arch. 451, 1-10. https://doi.org/10.1007/s00424-005-1462-y
  67. Ohba, T., Watanabe, H., Murakami, M., Takahashi, Y., Iino, K., Kuromitsu, S., Mori, Y., Ono, K., Iijima, T. and Ito, H. (2007) Upregula tion of TRPC1 in the development of cardiac hypertrophy. J. Mol. Cell. Cardiol. 42, 498-507. https://doi.org/10.1016/j.yjmcc.2006.10.020
  68. Ohga, K., Takezawa, R., Arakida, Y., Shimizu, Y. and Ishikawa, J. (2008) Characterization of YM-58483/BTP2, a novel store-operated $Ca^{2+}$ entry blocker, on T cell-mediated immune responses in vivo. Int. Immunopharmacol. 8, 1787-1792. https://doi.org/10.1016/j.intimp.2008.08.016
  69. Okada, T., Inoue, R., Yamazaki, K., Maeda, A., Kurosaki, T., Yamakuni, T., Tanaka, I., Shimizu, S., Ikenaka, K., Imoto, K. and Mori, Y. (1999) Molecular and functional characterization of a novel mouse transient receptor potential protein homologue TRP7. $Ca^{2+}$-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J. Biol. Chem. 274, 27359-27370. https://doi.org/10.1074/jbc.274.39.27359
  70. Onohara, N., Nishida, M., Inoue, R., Kobayashi, H., Sumimoto, H., Sato, Y., Mori, Y., Nagao, T. and Kurose, H. (2006) TRPC3 and TRPC6 are essential for angiotensin II-induced cardiac hypertrophy. EMBO J. 25, 5305-5316. https://doi.org/10.1038/sj.emboj.7601417
  71. Philipp, S., Wissenbach, U. and Flockerzi, V. (2000) Molecular biology of calcium channels. In Calcium Signaling (J. W. J. Putney, Ed.), pp. 321-342. CRC Press, Boca Raton.
  72. Piper, H. M., Abdallah, Y. and Schafer, C. (2004) The first minutes of reperfusion: a window of opportunity for cardioprotection. Cardiovasc. Res. 61, 365-371. https://doi.org/10.1016/j.cardiores.2003.12.012
  73. Plant, T. D. and Schaefer, M. (2003) TRPC4 and TRPC5: receptoroperated $Ca^{2+}$-permeable nonselective cation channels. Cell Calcium 33, 441-450. https://doi.org/10.1016/S0143-4160(03)00055-1
  74. Poteser, M., Graziani, A., Rosker, C., Eder, P., Derler, I., Kahr, H., Zhu, M. X., Romanin, C. and Groschner, K. (2006) TRPC3 and TRPC4 associate to form a redox-sensitive cation channel. Evidence for expression of native TRPC3-TRPC4 heteromeric channels in endothelial cells. J. Biol. Chem. 281, 13588-13595. https://doi.org/10.1074/jbc.M512205200
  75. Putney, J. W., Jr. (1986) A model for receptor-regulated calcium entry. Cell Calcium 7, 1-12. https://doi.org/10.1016/0143-4160(86)90026-6
  76. Riccio, A., Medhurst, A. D., Mattei, C., Kelsell, R. E., Calver, A. R., Randall, A. D., Benham, C. D. and Pangalos, M. N. (2002) mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res. Mol. Brain Res. 109, 95-104. https://doi.org/10.1016/S0169-328X(02)00527-2
  77. Rosenbaum, M. A., Chaudhuri, P. and Graham, L. M. (2015) Hypercholesterolemia inhibits re-endothelialization of arterial injuries by TRPC channel activation. J. Vasc. Surg. 62, 1040-1047.e2. https://doi.org/10.1016/j.jvs.2014.04.033
  78. Rowell, J., Koitabashi, N. and Kass, D. A. (2010) TRP-ing up heart and vessels: canonical transient receptor potential channels and cardiovascular disease. J. Cardiovasc. Transl. Res. 3, 516-524. https://doi.org/10.1007/s12265-010-9208-4
  79. Sabourin, J., Robin, E. and Raddatz, E. (2011) A key role of TRPC channels in the regulation of electromechanical activity of the developing heart. Cardiovasc. Res. 92, 226-236. https://doi.org/10.1093/cvr/cvr167
  80. Satoh, S., Tanaka, H., Ueda, Y., Oyama, J., Sugano, M., Sumimoto, H., Mori, Y. and Makino, N. (2007) Transient receptor potential (TRP) protein 7 acts as a G protein-activated $Ca^{2+}$ channel mediating angiotensin II-induced myocardial apoptosis. Mol. Cell. Biochem. 294, 205-215. https://doi.org/10.1007/s11010-006-9261-0
  81. Schaefer, M., Plant, T. D., Obukhov, A. G., Hofmann, T., Gudermann, T. and Schultz, G. (2000) Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 275, 17517-17526. https://doi.org/10.1074/jbc.275.23.17517
  82. Schleifer, H., Doleschal, B., Lichtenegger, M., Oppenrieder, R., Derler, I., Frischauf, I., Glasnov, T. N., Kappe, C. O., Romanin, C. and Groschner, K. (2012) Novel pyrazole compounds for pharmacological discrimination between receptor-operated and store-operated $Ca^{2+}$ entry pathways. Br. J. Pharmacol. 167, 1712-1722. https://doi.org/10.1111/j.1476-5381.2012.02126.x
  83. Seo, K., Rainer, P. P., Shalkey Hahn, V., Lee, D. I., Jo, S. H., Andersen, A., Liu, T., Xu, X., Willette, R. N., Lepore, J. J., Marino, J. P., Jr., Birnbaumer, L., Schnackenberg, C. G. and Kass, D. A. (2014) Combined TRPC3 and TRPC6 blockade by selective small-molecule or genetic deletion inhibits pathological cardiac hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 111, 1551-1556. https://doi.org/10.1073/pnas.1308963111
  84. Seth, M., Zhang, Z. S., Mao, L., Graham, V., Burch, J., Stiber, J., Tsiokas, L., Winn, M., Abramowitz, J., Rockman, H. A., Birnbaumer, L. and Rosenberg, P. (2009) TRPC1 channels are critical for hypertrophic signaling in the heart. Circ. Res. 105, 1023-1030. https://doi.org/10.1161/CIRCRESAHA.109.206581
  85. Shan, D., Marchase, R. B. and Chatham, J. C. (2008) Overexpression of TRPC3 increases apoptosis but not necrosis in response to ischemia-reperfusion in adult mouse cardiomyocytes. Am. J. Physiol., Cell Physiol. 294, C833-C841. https://doi.org/10.1152/ajpcell.00313.2007
  86. Shaywitz, A. J. and Greenberg, M. E. (1999) CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68, 821-861. https://doi.org/10.1146/annurev.biochem.68.1.821
  87. Shi, J., Ju, M., Abramowitz, J., Large, W. A., Birnbaumer, L. and Albert, A. P. (2012) TRPC1 proteins confer PKC and phosphoinositol activation on native heteromeric TRPC1/C5 channels in vascular smooth muscle: comparative study of wild-type and $Trpc1^{-/-}$ mice. FASEB J. 26, 409-419. https://doi.org/10.1096/fj.11-185611
  88. Shi, J., Miralles, F., Birnbaumer, L., Large, W. A. and Albert, A. P. (2016) Store depletion induces Galphaq-mediated PLCbeta1 activity to stimulate TRPC1 channels in vascular smooth muscle cells. FASEB J. 30, 702-715. https://doi.org/10.1096/fj.15-280271
  89. Short, A. D., Bian, J., Ghosh, T. K., Waldron, R. T., Rybak, S. L. and Gill, D. L. (1993) Intracellular $Ca^{2+}$ pool content is linked to control of cell growth. Proceedings of the National Academy of Sciences of the United States of America 90, 4986-4990. https://doi.org/10.1073/pnas.90.11.4986
  90. Smedlund, K., Tano, J. Y. and Vazquez, G. (2010) The constitutive function of native TRPC3 channels modulates vascular cell adhesion molecule-1 expression in coronary endothelial cells through nuclear factor ${\kappa}B$ signaling. Circ. Res. 106, 1479-1488. https://doi.org/10.1161/CIRCRESAHA.109.213314
  91. Smedlund, K. and Vazquez, G. (2008) Involvement of native TRPC3 proteins in ATP-dependent expression of VCAM-1 and monocyte adherence in coronary artery endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28, 2049-2055. https://doi.org/10.1161/ATVBAHA.108.175356
  92. Smedlund, K. B., Birnbaumer, L. and Vazquez, G. (2015) Increased size and cellularity of advanced atherosclerotic lesions in mice with endothelial overexpression of the human TRPC3 channel. Proc. Natl. Acad. Sci. U.S.A. 112, E2201-E2206. https://doi.org/10.1073/pnas.1505410112
  93. Soboloff, J., Spassova, M., Xu, W., He, L. P., Cuesta, N. and Gill, D. L. (2005) Role of endogenous TRPC6 channels in $Ca^{2+}$ signal generation in A7r5 smooth muscle cells. J. Biol. Chem. 280, 39786-39794. https://doi.org/10.1074/jbc.M506064200
  94. Stowers, L., Holy, T. E., Meister, M., Dulac, C. and Koentges, G. (2002) Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295, 1493-1500. https://doi.org/10.1126/science.1069259
  95. Tabas, I., Tall, A. and Accili, D. (2010) The impact of macrophage insulin resistance on advanced atherosclerotic plaque progression. Circ. Res. 106, 58-67. https://doi.org/10.1161/CIRCRESAHA.109.208488
  96. Tai, Y., Feng, S., Ge, R., Du, W., Zhang, X., He, Z. and Wang, Y. (2008) TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J. Cell Sci. 121, 2301-2307. https://doi.org/10.1242/jcs.026906
  97. Takahashi, S., Lin, H., Geshi, N., Mori, Y., Kawarabayashi, Y., Takami, N., Mori, M. X., Honda, A. and Inoue, R. (2008) Nitric oxide-cGMPprotein kinase G pathway negatively regulates vascular transient receptor potential channel TRPC6. J. Physiol. 586, 4209-4223. https://doi.org/10.1113/jphysiol.2008.156083
  98. Takahashi, Y., Watanabe, H., Murakami, M., Ohba, T., Radovanovic, M., Ono, K., Iijima, T. and Ito, H. (2007) Involvement of transient receptor potential canonical 1 (TRPC1) in angiotensin II-induced vascular smooth muscle cell hypertrophy. Atherosclerosis 195, 287-296. https://doi.org/10.1016/j.atherosclerosis.2006.12.033
  99. Tano, J. Y., Lee, R. H. and Vazquez, G. (2012) Macrophage function in atherosclerosis: potential roles of TRP channels. Channels (Austin) 6, 141-148. https://doi.org/10.4161/chan.20292
  100. Tauseef, M., Farazuddin, M., Sukriti, S., Rajput, C., Meyer, J. O., Ramasamy, S. K. and Mehta, D. (2016) Transient receptor potential channel 1 maintains adherens junction plasticity by suppressing sphingosine kinase 1 expression to induce endothelial hyperpermeability. FASEB J. 30, 102-110. https://doi.org/10.1096/fj.15-275891
  101. Thilo, F., Loddenkemper, C., Berg, E., Zidek, W. and Tepel, M. (2009) Increased TRPC3 expression in vascular endothelium of patients with malignant hypertension. Mod. Pathol. 22, 426-430. https://doi.org/10.1038/modpathol.2008.200
  102. Toth, P., Csiszar, A., Tucsek, Z., Sosnowska, D., Gautam, T., Koller, A., Schwartzman, M. L., Sonntag, W. E. and Ungvari, Z. (2013) Role of 20-HETE, TRPC channels, and BKCa in dysregulation of pressureinduced $Ca^{2+}$ signaling and myogenic constriction of cerebral arteries in aged hypertensive mice. Am. J. Physiol. Heart Circ. Physiol. 305, H1698-H1708. https://doi.org/10.1152/ajpheart.00377.2013
  103. Venkatachalam, K., Zheng, F. and Gill, D. L. (2003) Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J. Biol. Chem. 278, 29031-29040. https://doi.org/10.1074/jbc.M302751200
  104. Wakili, R., Voigt, N., Kaab, S., Dobrev, D. and Nattel, S. (2011) Recent advances in the molecular pathophysiology of atrial fibrillation. J. Clin. Invest. 121, 2955-2968. https://doi.org/10.1172/JCI46315
  105. Wang, J., Fu, X., Yang, K., Jiang, Q., Chen, Y., Jia, J., Duan, X., Wang, E. W., He, J., Ran, P., Zhong, N., Semenza, G. L. and Lu, W. (2015) Hypoxia inducible factor-1-dependent up-regulation of BMP4 mediates hypoxia-induced increase of TRPC expression in PASMCs. Cardiovasc. Res. 107, 108-118. https://doi.org/10.1093/cvr/cvv122
  106. Wang, J., Jiang, Q., Wan, L., Yang, K., Zhang, Y., Chen, Y., Wang, E., Lai, N., Zhao, L., Jiang, H., Sun, Y., Zhong, N., Ran, P. and Lu, W. (2013a) Sodium tanshinone IIA sulfonate inhibits canonical transient receptor potential expression in pulmonary arterial smooth muscle from pulmonary hypertensive rats. Am. J. Respir. Cell Mol. Biol. 48, 125-134. https://doi.org/10.1165/rcmb.2012-0071OC
  107. Wang, J., Weigand, L., Lu, W., Sylvester, J. T., Semenza, G. L. and Shimoda, L. A. (2006) Hypoxia inducible factor 1 mediates hypoxia-induced TRPC expression and elevated intracellular $Ca^{2+}$ in pulmonary arterial smooth muscle cells. Circ. Res. 98, 1528-1537. https://doi.org/10.1161/01.RES.0000227551.68124.98
  108. Wang, Z. T., Wang, Z. and Hu, Y. W. (2016) Possible roles of plateletderived microparticles in atherosclerosis. Atherosclerosis 248, 10-16. https://doi.org/10.1016/j.atherosclerosis.2016.03.004
  109. Weber, E. W., Han, F., Tauseef, M., Birnbaumer, L., Mehta, D. and Muller, W. A. (2015) TRPC6 is the endothelial calcium channel that regulates leukocyte transendothelial migration during the inflammatory response. J. Exp. Med. 212, 1883-1899. https://doi.org/10.1084/jem.20150353
  110. Welsh, D. G., Morielli, A. D., Nelson, M. T. and Brayden, J. E. (2002) Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ. Res. 90, 248-250. https://doi.org/10.1161/hh0302.105662
  111. Winn, M. P., Conlon, P. J., Lynn, K. L., Farrington, M. K., Creazzo, T., Hawkins, A. F., Daskalakis, N., Kwan, S. Y., Ebersviller, S., Burchette, J. L., Pericak-Vance, M. A., Howell, D. N., Vance, J. M. and Rosenberg, P. B. (2005) A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 308, 1801-1804. https://doi.org/10.1126/science.1106215
  112. Wu, X., Eder, P., Chang, B. and Molkentin, J. D. (2010) TRPC channels are necessary mediators of pathologic cardiac hypertrophy. Proc. Natl. Acad. Sci. U.S.A. 107, 7000-7005. https://doi.org/10.1073/pnas.1001825107
  113. Wuensch, T., Thilo, F., Krueger, K., Scholze, A., Ristow, M. and Tepel, M. (2010) High glucose-induced oxidative stress increases transient receptor potential channel expression in human monocytes. Diabetes 59, 844-849. https://doi.org/10.2337/db09-1100
  114. Xia, Y., Yang, X. R., Fu, Z., Paudel, O., Abramowitz, J., Birnbaumer, L. and Sham, J. S. (2014) Classical transient receptor potential 1 and 6 contribute to hypoxic pulmonary hypertension through differential regulation of pulmonary vascular functions. Hypertension 63, 173-180. https://doi.org/10.1161/HYPERTENSIONAHA.113.01902
  115. Xu, S. Z. and Beech, D. J. (2001) TrpC1 is a membrane-spanning subunit of store-operated $Ca^{2+}$ channels in native vascular smooth muscle cells. Circ. Res. 88, 84-87. https://doi.org/10.1161/01.RES.88.1.84
  116. Yu, Y., Fantozzi, I., Remillard, C. V., Landsberg, J. W., Kunichika, N., Platoshyn, O., Tigno, D. D., Thistlethwaite, P. A., Rubin, L. J. and Yuan, J. X. (2004) Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proc. Natl. Acad. Sci. U.S.A. 101, 13861-13866. https://doi.org/10.1073/pnas.0405908101
  117. Yue, Z., Xie, J., Yu, A. S., Stock, J., Du, J. and Yue, L. (2015) Role of TRP channels in the cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 308, H157-H182. https://doi.org/10.1152/ajpheart.00457.2014
  118. Zhang, S., Remillard, C. V., Fantozzi, I. and Yuan, J. X. (2004) ATPinduced mitogenesis is mediated by cyclic AMP response elementbinding protein-enhanced TRPC4 expression and activity in human pulmonary artery smooth muscle cells. Am. J. Physiol., Cell Physiol. 287, C1192-C1201. https://doi.org/10.1152/ajpcell.00158.2004
  119. Zhang, Y., Lu, W., Yang, K., Xu, L., Lai, N., Tian, L., Jiang, Q., Duan, X., Chen, M. and Wang, J. (2013) Bone morphogenetic protein 2 decreases TRPC expression, store-operated $Ca^{2+}$ entry, and basal [$Ca^{2+}$]i in rat distal pulmonary arterial smooth muscle cells. Am. J. Physiol., Cell Physiol. 304, C833-C843. https://doi.org/10.1152/ajpcell.00036.2012
  120. Zhang, Y., Wang, Y., Yang, K., Tian, L., Fu, X., Wang, Y., Sun, Y., Jiang, Q., Lu, W. and Wang, J. (2014) BMP4 increases the expression of TRPC and basal [$Ca^{2+}$]i via the p38MAPK and ERK1/2 pathways independent of BMPRII in PASMCs. PLoS ONE 9, e112695. https://doi.org/10.1371/journal.pone.0112695
  121. Zhu, D. Y., Lau, L., Liu, S. H., Wei, J. S. and Lu, Y. M. (2004) Activation of cAMP-response-element-binding protein (CREB) after focal cerebral ischemia stimulates neurogenesis in the adult dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 101, 9453-9457. https://doi.org/10.1073/pnas.0401063101
  122. Zhu, X., Chu, P. B., Peyton, M. and Birnbaumer, L. (1995) Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Lett. 373, 193-198. https://doi.org/10.1016/0014-5793(95)01038-G

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