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Current Molecular Pharmacology

Author(s): Kazuhiro Nishiyama, Tomohiro Tanaka, Akiyuki Nishimura and Motohiro Nishida*

DOI: 10.2174/1874467213666200407090121

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TRPC3-Based Protein Signaling Complex as a Therapeutic Target of Myocardial Atrophy

Page: [123 - 131] Pages: 9

  • * (Excluding Mailing and Handling)

Abstract

Transient receptor potential (TRP) channels, especially canonical TRP channel subfamily members 3 (TRPC3) and 6 (TRPC6), have gained attention as a putative therapeutic target of heart failure. Moreover, TRPC3 and TRPC6 channels are physiologically important for maintaining cellular homeostasis. How TRPC3/C6 channels alter intracellular signaling from adaptation to maladaptation, has been discussed for many years. We have recently shown that the formation of a protein signal complex between TRPC3 and NADPH oxidase (Nox) 2 caused by environmental stresses (e.g., hypoxia, nutritional deficiency, and anti-cancer drug treatment) promotes Nox2-dependent reactive oxygen species production and cardiac stiffness, including myocardial atrophy and interstitial fibrosis, in rodents. In fact, pharmacological prevention of the TRPC3 -Nox2 protein complex can maintain cardiac flexibility in mice after anti-cancer drug treatment.

In this mini-review, we discuss the relationship between TRPC3/C6 channels and cardiovascular disease, and propose a new therapeutic strategy by focusing on pathology-specific protein–protein interactions.

Keywords: TRPC3, TRPC6, Nox2, oncocardiology, protein–protein interaction, drug repurposing.

Graphical Abstract

[1]
Montell, C.; Rubin, G.M. Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron, 1989, 2(4), 1313-1323.
[http://dx.doi.org/10.1016/0896-6273(89)90069-X] [PMID: 2516726]
[2]
Xiao, X.; Liu, H.X.; Shen, K.; Cao, W.; Li, X.Q. Canonical transient receptor potential channels and their link with cardio/cerebro-vascular diseases. Biomol. Ther. (Seoul), 2017, 25(5), 471-481.
[http://dx.doi.org/10.4062/biomolther.2016.096] [PMID: 28274093]
[3]
Blair, H.A. Capsaicin 8% Dermal Patch: A Review in Peripheral Neuropathic Pain. Drugs, 2018, 78(14), 1489-1500.
[http://dx.doi.org/10.1007/s40265-018-0982-7] [PMID: 30251173]
[4]
Iwata, Y.; Katayama, Y.; Okuno, Y.; Wakabayashi, S. Novel inhibitor candidates of TRPV2 prevent damage of dystrophic myocytes and ameliorate against dilated cardiomyopathy in a hamster model. Oncotarget, 2018, 9(18), 14042-14057.
[http://dx.doi.org/10.18632/oncotarget.24449] [PMID: 29581825]
[5]
Matsumura, T.; Matsui, M.; Iwata, Y.; Asakura, M.; Saito, T.; Fujimura, H.; Sakoda, S. A pilot study of tranilast for cardiomyopathy of muscular dystrophy. Intern. Med., 2018, 57(3), 311-318.
[http://dx.doi.org/10.2169/internalmedicine.8651-16] [PMID: 29093384]
[6]
Eder, P.; Molkentin, J.D. TRPC channels as effectors of cardiac hypertrophy. Circ. Res., 2011, 108(2), 265-272.
[http://dx.doi.org/10.1161/CIRCRESAHA.110.225888] [PMID: 21252153]
[7]
Lucas, P.; Ukhanov, K.; Leinders-Zufall, T.; Zufall, F. A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: mechanism of pheromone transduction. Neuron, 2003, 40(3), 551-561.
[http://dx.doi.org/10.1016/S0896-6273(03)00675-5] [PMID: 14642279]
[8]
Liu, X.; Cheng, K.T.; Bandyopadhyay, B.C.; Pani, B.; Dietrich, A.; Paria, B.C.; Swaim, W.D.; Beech, D.; Yildrim, E.; Singh, B.B.; Birnbaumer, L.; Ambudkar, I.S. Attenuation of store-operated Ca2+ current impairs salivary gland fluid secretion in TRPC1(-/-) mice. Proc. Natl. Acad. Sci. USA, 2007, 104(44), 17542-17547.
[http://dx.doi.org/10.1073/pnas.0701254104] [PMID: 17956991]
[9]
Wes, P.D.; Chevesich, J.; Jeromin, A.; Rosenberg, C.; Stetten, G.; Montell, C. TRPC1, a human homolog of a Drosophila store-operated channel. Proc. Natl. Acad. Sci. USA, 1995, 92(21), 9652-9656.
[http://dx.doi.org/10.1073/pnas.92.21.9652] [PMID: 7568191]
[10]
Sabourin, J.; Bartoli, F.; Antigny, F.; Gomez, A.M.; Benitah, J.P. Transient receptor potential canonical (trpc)/orai1-dependent store-operated ca 2+ channels; new targets of aldosterone in cardiomyocytes. J. Biol. Chem., 2016, 291(25), 13394-13409.
[http://dx.doi.org/10.1074/jbc.M115.693911] [PMID: 27129253]
[11]
Vazquez, G.; Wedel, B.J.; Aziz, O.; Trebak, M.; Putney, J.W., Jr The mammalian TRPC cation channels. Biochim. Biophys. Acta, 2004, 1742(1-3), 21-36.
[http://dx.doi.org/10.1016/j.bbamcr.2004.08.015] [PMID: 15590053]
[12]
Dietrich, A.; Kalwa, H.; Rost, B.R.; Gudermann, T. The diacylgylcerol-sensitive TRPC3/6/7 subfamily of cation channels: functional characterization and physiological relevance. Pflugers Arch., 2005, 451(1), 72-80.
[http://dx.doi.org/10.1007/s00424-005-1460-0] [PMID: 15971081]
[13]
Nishida, M.; Hara, Y.; Yoshida, T.; Inoue, R.; Mori, Y. TRP channels: molecular diversity and physiological function. Microcirculation, 2006, 13(7), 535-550.
[http://dx.doi.org/10.1080/10739680600885111] [PMID: 16990213]
[14]
Poteser, M.; Graziani, A.; Rosker, C.; Eder, P.; Derler, I.; Kahr, H.; Zhu, M.X.; Romanin, C.; Groschner, K. 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., 2006, 281(19), 13588-13595.
[http://dx.doi.org/10.1074/jbc.M512205200] [PMID: 16537542]
[15]
Maroto, R.; Raso, A.; Wood, T.G.; Kurosky, A.; Martinac, B.; Hamill, O.P. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nat. Cell Biol., 2005, 7(2), 179-185.
[http://dx.doi.org/10.1038/ncb1218] [PMID: 15665854]
[16]
Spassova, M.A.; Hewavitharana, T.; Xu, W.; Soboloff, J.; Gill, D.L. A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc. Natl. Acad. Sci. USA, 2006, 103(44), 16586-16591.
[http://dx.doi.org/10.1073/pnas.0606894103] [PMID: 17056714]
[17]
Weissmann, N.; Sydykov, A.; Kalwa, H.; Storch, U.; Fuchs, B.; Mederos, Y. Schnitzler, M.; Brandes, R. P.; Grimminger, F.; Meissner, M.; Freichel, M.; Offermanns, S.; Veit, F.; Pak, O.; Krause, K. H.; Schermuly, R. T.; Brewer, A. C.; Schmidt, H. H. H. W.; Seeger, W.; Shah, A. M.; Gudermann, T.; Ghofrani, H. A.; Dietrich, A., Activation of TRPC6 channels is essential for lung ischaemia-reperfusion induced oedema in mice. Nat. Commun., 2012, 3
[18]
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.; Ito, Y. Synergistic activation of vascular TRPC6 channel by receptor and mechanical stimulation via phospholipase C/diacylglycerol and phospholipase A2/ω-hydroxylase/20-HETE pathways. Circ. Res., 2009, 104(12), 1399-1409.
[http://dx.doi.org/10.1161/CIRCRESAHA.108.193227] [PMID: 19443836]
[19]
Kiselyov, K.; Kim, J.Y.; Zeng, W.; Muallem, S. Protein-protein interaction and functionTRPC channels. Pflugers Arch., 2005, 451(1), 116-124.
[http://dx.doi.org/10.1007/s00424-005-1442-2] [PMID: 16044307]
[20]
Nishida, M.; Sugimoto, K.; Hara, Y.; Mori, E.; Morii, T.; Kurosaki, T.; Mori, Y. Amplification of receptor signalling by Ca2+ entry-mediated translocation and activation of PLCgamma2 in B lymphocytes. EMBO J., 2003, 22(18), 4677-4688.
[http://dx.doi.org/10.1093/emboj/cdg457] [PMID: 12970180]
[21]
Numaga, T.; Nishida, M.; Kiyonaka, S.; Kato, K.; Katano, M.; Mori, E.; Kurosaki, T.; Inoue, R.; Hikida, M.; Putney, J.W., Jr; Mori, Y. Ca2+ influx and protein scaffolding via TRPC3 sustain PKCbeta and ERK activation in B cells. J. Cell Sci., 2010, 123(Pt 6), 927-938.
[http://dx.doi.org/10.1242/jcs.061051] [PMID: 20179100]
[22]
Nishioka, K.; Nishida, M.; Ariyoshi, M.; Jian, Z.; Saiki, S.; Hirano, M.; Nakaya, M.; Sato, Y.; Kita, S.; Iwamoto, T.; Hirano, K.; Inoue, R.; Kurose, H. Cilostazol suppresses angiotensin II-induced vasoconstriction via protein kinase A-mediated phosphorylation of the transient receptor potential canonical 6 channel. Arterioscler. Thromb. Vasc. Biol., 2011, 31(10), 2278-2286.
[http://dx.doi.org/10.1161/ATVBAHA.110.221010] [PMID: 21799177]
[23]
Liu, D.; Yang, D.; He, H.; Chen, X.; Cao, T.; Feng, X.; Ma, L.; Luo, Z.; Wang, L.; Yan, Z.; Zhu, Z.; Tepel, M. Increased transient receptor potential canonical type 3 channels in vasculature from hypertensive rats. Hypertension, 2009, 53(1), 70-76.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.108.116947] [PMID: 19029480]
[24]
Onohara, N.; Nishida, M.; Inoue, R.; Kobayashi, H.; Sumimoto, H.; Sato, Y.; Mori, Y.; Nagao, T.; Kurose, H. TRPC3 and TRPC6 are essential for angiotensin II-induced cardiac hypertrophy. EMBO J., 2006, 25(22), 5305-5316.
[http://dx.doi.org/10.1038/sj.emboj.7601417] [PMID: 17082763]
[25]
Thilo, F.; Loddenkemper, C.; Berg, E.; Zidek, W.; Tepel, M. Increased TRPC3 expression in vascular endothelium of patients with malignant hypertension. Mod. Pathol., 2009, 22(3), 426-430.
[http://dx.doi.org/10.1038/modpathol.2008.200] [PMID: 19136933]
[26]
Wang, B.; Xiong, S.; Lin, S.; Xia, W.; Li, Q.; Zhao, Z.; Wei, X.; Lu, Z.; Wei, X.; Gao, P.; Liu, D.; Zhu, Z. Enhanced mitochondrial transient receptor potential channel, canonical type 3-mediated calcium handling in the vasculature from hypertensive rats. J. Am. Heart Assoc., 2017, 6(7), e005812.
[http://dx.doi.org/10.1161/JAHA.117.005812] [PMID: 28711865]
[27]
Wang, M.; Tang, Y.B.; Ma, M.M.; Chen, J.H.; Hu, C.P.; Zhao, S.P.; Peng, D.Q.; Zhou, J.G.; Guan, Y.Y.; Zhang, Z. TRPC3 channel confers cerebrovascular remodelling during hypertension via transactivation of EGF receptor signalling. Cardiovasc. Res., 2016, 109(1), 34-43.
[http://dx.doi.org/10.1093/cvr/cvv246] [PMID: 26598506]
[28]
Toth, P.; Csiszar, A.; Tucsek, Z.; Sosnowska, D.; Gautam, T.; Koller, A.; Schwartzman, M.L.; Sonntag, W.E.; Ungvari, Z. Role of 20-HETE, TRPC channels, and BKCa in dysregulation of pressure-induced Ca2+ signaling and myogenic constriction of cerebral arteries in aged hypertensive mice. Am. J. Physiol. Heart Circ. Physiol., 2013, 305(12), H1698-H1708.
[http://dx.doi.org/10.1152/ajpheart.00377.2013] [PMID: 24097425]
[29]
Welsh, D.G.; Morielli, A.D.; Nelson, M.T.; Brayden, J.E. Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ. Res., 2002, 90(3), 248-250.
[http://dx.doi.org/10.1161/hh0302.105662] [PMID: 11861411]
[30]
Dietrich, A.; Mederos Y Schnitzler, 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.; Birnbaumer, L. Increased vascular smooth muscle contractility in TRPC6-/- mice. Mol. Cell. Biol., 2005, 25(16), 6980-6989.
[http://dx.doi.org/10.1128/MCB.25.16.6980-6989.2005] [PMID: 16055711]
[31]
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.; Ho, W.K. Enhancement of receptor-operated cation current and TRPC6 expression in arterial smooth muscle cells of deoxycorticosterone acetate-salt hypertensive rats. J. Hypertens., 2007, 25(4), 809-817.
[http://dx.doi.org/10.1097/HJH.0b013e3280148312] [PMID: 17351373]
[32]
Yu, Y.; Fantozzi, I.; Remillard, C.V.; Landsberg, J.W.; Kunichika, N.; Platoshyn, O.; Tigno, D.D.; Thistlethwaite, P.A.; Rubin, L.J.; Yuan, J.X.J. Enhanced expression of transient receptor potential channels in idiopathic pulmonary arterial hypertension. Proc. Natl. Acad. Sci. USA, 2004, 101(38), 13861-13866.
[http://dx.doi.org/10.1073/pnas.0405908101] [PMID: 15358862]
[33]
Weissmann, N.; Dietrich, A.; Fuchs, B.; Kalwa, H.; Ay, M.; Dumitrascu, R.; Olschewski, A.; Storch, U.; Mederos y Schnitzler, M.; Ghofrani, H.A.; Schermuly, R.T.; Pinkenburg, O.; Seeger, W.; Grimminger, F.; Gudermann, T. Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc. Natl. Acad. Sci. USA, 2006, 103(50), 19093-19098.
[http://dx.doi.org/10.1073/pnas.0606728103] [PMID: 17142322]
[34]
Zhang, Y.; Lu, W.; Yang, K.; Xu, L.; Lai, N.; Tian, L.; Jiang, Q.; Duan, X.; Chen, M.; Wang, J. 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., 2013, 304(9), C833-C843.
[http://dx.doi.org/10.1152/ajpcell.00036.2012] [PMID: 23447035]
[35]
Yu, Y.; Keller, S.H.; Remillard, C.V.; Safrina, O.; Nicholson, A.; Zhang, S.L.; Jiang, W.; Vangala, N.; Landsberg, J.W.; Wang, J.Y.; Thistlethwaite, P.A.; Channick, R.N.; Robbins, I.M.; Loyd, J.E.; Ghofrani, H.A.; Grimminger, F.; Schermuly, R.T.; Cahalan, M.D.; Rubin, L.J.; Yuan, J.X.J. A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation, 2009, 119(17), 2313-2322.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.108.782458] [PMID: 19380626]
[36]
Pousada, G.; Baloira, A.; Valverde, D. Molecular and clinical analysis of TRPC6 and AGTR1 genes in patients with pulmonary arterial hypertension. Orphanet J. Rare Dis., 2015, 10(1), 1.
[http://dx.doi.org/10.1186/s13023-014-0216-3] [PMID: 25603901]
[37]
Amoasii, L.; Hildyard, J.C.W.; Li, H.; Sanchez-Ortiz, E.; Mireault, A.; Caballero, D.; Harron, R.; Stathopoulou, T.R.; Massey, C.; Shelton, J.M.; Bassel-Duby, R.; Piercy, R.J.; Olson, E.N. Gene editing restores dystrophin expression in a canine model of Duchenne muscular dystrophy. Science, 2018, 362(6410), 86-91.
[http://dx.doi.org/10.1126/science.aau1549] [PMID: 30166439]
[38]
Komor, A.C.; Kim, Y.B.; Packer, M.S.; Zuris, J.A.; Liu, D.R. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature, 2016, 533(7603), 420-424.
[http://dx.doi.org/10.1038/nature17946] [PMID: 27096365]
[39]
Gaudelli, N.M.; Komor, A.C.; Rees, H.A.; Packer, M.S.; Badran, A.H.; Bryson, D.I.; Liu, D.R. Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage. Nature, 2017, 551(7681), 464-471.
[http://dx.doi.org/10.1038/nature24644] [PMID: 29160308]
[40]
Tabas, I.; Tall, A.; Accili, D. The impact of macrophage insulin resistance on advanced atherosclerotic plaque progression. Circ. Res., 2010, 106(1), 58-67.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.208488] [PMID: 20056946]
[41]
Moroni, F.; Ammirati, E.; Norata, G. D.; Magnoni, M.; Camici, P. G. The role of monocytes and macrophages in human atherosclerosis, plaque neoangiogenesis, and atherothrombosis. Mediators of Inflammation, 2019, e2019.
[http://dx.doi.org/10.1155/2019/7434376]
[42]
Nishiyama, K.; Fujimoto, Y.; Takeuchi, T.; Azuma, Y.T. Aggressive Crosstalk Between Fatty Acids and Inflammation in Macrophages and Their Influence on Metabolic Homeostasis. Neurochem. Res., 2018, 43(1), 19-26.
[http://dx.doi.org/10.1007/s11064-017-2269-x] [PMID: 28424949]
[43]
Tano, J.Y.; Smedlund, K.; Lee, R.; Abramowitz, J.; Birnbaumer, L.; Vazquez, G. Impairment of survival signaling and efferocytosis in TRPC3-deficient macrophages. Biochem. Biophys. Res. Commun., 2011, 410(3), 643-647.
[http://dx.doi.org/10.1016/j.bbrc.2011.06.045] [PMID: 21684255]
[44]
Smedlund, K.; Tano, J.Y.; Vazquez, G. The constitutive function of native TRPC3 channels modulates vascular cell adhesion molecule-1 expression in coronary endothelial cells through nuclear factor kappaB signaling. Circ. Res., 2010, 106(9), 1479-1488.
[http://dx.doi.org/10.1161/CIRCRESAHA.109.213314] [PMID: 20360250]
[45]
Smedlund, K.; Vazquez, G. Involvement of native TRPC3 proteins in ATP-dependent expression of VCAM-1 and monocyte adherence in coronary artery endothelial cells. Arterioscler. Thromb. Vasc. Biol., 2008, 28(11), 2049-2055.
[http://dx.doi.org/10.1161/ATVBAHA.108.175356] [PMID: 18787184]
[46]
Tano, J.Y.K.; Lee, R.H.; Vazquez, G. Macrophage function in atherosclerosis: potential roles of TRP channels. Channels (Austin), 2012, 6(3), 141-148.
[http://dx.doi.org/10.4161/chan.20292] [PMID: 22909953]
[47]
Dube, P.R.; Chikkamenahalli, L.L.; Birnbaumer, L.; Vazquez, G. Reduced calcification and osteogenic features in advanced atherosclerotic plaques of mice with macrophage-specific loss of TRPC3. Atherosclerosis, 2018, 270, 199-204.
[http://dx.doi.org/10.1016/j.atherosclerosis.2017.12.025] [PMID: 29290366]
[48]
Smedlund, K.B.; Birnbaumer, L.; Vazquez, G. Increased size and cellularity of advanced atherosclerotic lesions in mice with endothelial overexpression of the human TRPC3 channel. Proc. Natl. Acad. Sci. USA, 2015, 112(17), E2201-E2206.
[http://dx.doi.org/10.1073/pnas.1505410112] [PMID: 25870279]
[49]
Frey, N.; Katus, H.A.; Olson, E.N.; Hill, J.A. Hypertrophy of the heart: a new therapeutic target? Circulation, 2004, 109(13), 1580-1589.
[http://dx.doi.org/10.1161/01.CIR.0000120390.68287.BB] [PMID: 15066961]
[50]
Hill, J.A.; Olson, E.N. Cardiac plasticity. N. Engl. J. Med., 2008, 358(13), 1370-1380.
[http://dx.doi.org/10.1056/NEJMra072139] [PMID: 18367740]
[51]
Nakayama, H.; Wilkin, B.J.; Bodi, I.; Molkentin, J.D. Calcineurin-dependent cardiomyopathy is activated by TRPC in the adult mouse heart. FASEB J., 2006, 20(10), 1660-1670.
[http://dx.doi.org/10.1096/fj.05-5560com] [PMID: 16873889]
[52]
Morine, K.J.; Paruchuri, V.; Qiao, X.; Aronovitz, M.; Huggins, G.S.; DeNofrio, D.; Kiernan, M.S.; Karas, R.H.; Kapur, N.K. Endoglin selectively modulates transient receptor potential channel expression in left and right heart failure. Cardiovasc. Pathol., 2016, 25(6), 478-482.
[http://dx.doi.org/10.1016/j.carpath.2016.08.004] [PMID: 27614169]
[53]
Houser, S.R.; Molkentin, J.D. Does contractile Ca2+ control calcineurin-NFAT signaling and pathological hypertrophy in cardiac myocytes? Sci. Signal., 2008, 1(25), pe31.
[http://dx.doi.org/10.1126/scisignal.125pe31] [PMID: 18577756]
[54]
Kitajima, N.; Numaga-Tomita, T.; Watanabe, M.; Kuroda, T.; Nishimura, A.; Miyano, K.; Yasuda, S.; Kuwahara, K.; Sato, Y.; Ide, T.; Birnbaumer, L.; Sumimoto, H.; Mori, Y.; Nishida, M. TRPC3 positively regulates reactive oxygen species driving maladaptive cardiac remodeling. Sci. Rep., 2016, 6, 37001.
[http://dx.doi.org/10.1038/srep37001] [PMID: 27833156]
[55]
Numaga-Tomita, T.; Kitajima, N.; Kuroda, T.; Nishimura, A.; Miyano, K.; Yasuda, S.; Kuwahara, K.; Sato, Y.; Ide, T.; Birnbaumer, L.; Sumimoto, H.; Mori, Y.; Nishida, M. TRPC3-GEF-H1 axis mediates pressure overload-induced cardiac fibrosis. Sci. Rep., 2016, 6, 39383.
[http://dx.doi.org/10.1038/srep39383] [PMID: 27991560]
[56]
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.; Kass, D.A. Combined TRPC3 and TRPC6 blockade by selective small-molecule or genetic deletion inhibits pathological cardiac hypertrophy. Proc. Natl. Acad. Sci. USA, 2014, 111(4), 1551-1556.
[http://dx.doi.org/10.1073/pnas.1308963111] [PMID: 24453217]
[57]
Lin, B.L.; Matera, D.; Doerner, J.F.; Zheng, N.; Del Camino, D.; Mishra, S.; Bian, H.; Zeveleva, S.; Zhen, X.; Blair, N.T.; Chong, J.A.; Hessler, D.P.; Bedja, D.; Zhu, G.; Muller, G.K.; Ranek, M.J.; Pantages, L.; McFarland, M.; Netherton, M.R.; Berry, A.; Wong, D.; Rast, G.; Qian, H.S.; Weldon, S.M.; Kuo, J.J.; Sauer, A.; Sarko, C.; Moran, M.M.; Kass, D.A.; Pullen, S.S. In vivo selective inhibition of TRPC6 by antagonist BI 749327 ameliorates fibrosis and dysfunction in cardiac and renal disease. Proc. Natl. Acad. Sci. USA, 2019, 116(20), 10156-10161.
[http://dx.doi.org/10.1073/pnas.1815354116] [PMID: 31028142]
[58]
Shimauchi, T.; Numaga-Tomita, T.; Ito, T.; Nishimura, A.; Matsukane, R.; Oda, S.; Hoka, S.; Ide, T.; Koitabashi, N.; Uchida, K.; Sumimoto, H.; Mori, Y.; Nishida, M. TRPC3-Nox2 complex mediates doxorubicin-induced myocardial atrophy. JCI Insight, 2017, 2(15), 93358.
[http://dx.doi.org/10.1172/jci.insight.93358] [PMID: 28768915]
[59]
Zhao, Y.; McLaughlin, D.; Robinson, E.; Harvey, A.P.; Hookham, M.B.; Shah, A.M.; McDermott, B.J.; Grieve, D.J. Nox2 NADPH oxidase promotes pathologic cardiac remodeling associated with Doxorubicin chemotherapy. Cancer Res., 2010, 70(22), 9287-9297.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-2664] [PMID: 20884632]
[60]
Looi, Y.H.; Grieve, D.J.; Siva, A.; Walker, S.J.; Anilkumar, N.; Cave, A.C.; Marber, M.; Monaghan, M.J.; Shah, A.M. Involvement of Nox2 NADPH oxidase in adverse cardiac remodeling after myocardial infarction. Hypertension, 2008, 51(2), 319-325.
[http://dx.doi.org/10.1161/HYPERTENSIONAHA.107.101980] [PMID: 18180403]
[61]
Li, J.M.; Gall, N.P.; Grieve, D.J.; Chen, M.; Shah, A.M. Activation of NADPH oxidase during progression of cardiac hypertrophy to failure. Hypertension, 2002, 40(4), 477-484.
[http://dx.doi.org/10.1161/01.HYP.0000032031.30374.32] [PMID: 12364350]
[62]
Lassègue, B.; San Martín, A.; Griendling, K.K. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ. Res., 2012, 110(10), 1364-1390.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.243972] [PMID: 22581922]
[63]
Noubade, R.; Wong, K.; Ota, N.; Rutz, S.; Eidenschenk, C.; Valdez, P.A.; Ding, J.; Peng, I.; Sebrell, A.; Caplazi, P.; DeVoss, J.; Soriano, R.H.; Sai, T.; Lu, R.; Modrusan, Z.; Hackney, J.; Ouyang, W. NRROS negatively regulates reactive oxygen species during host defence and autoimmunity. Nature, 2014, 509(7499), 235-239.
[http://dx.doi.org/10.1038/nature13152] [PMID: 24739962]
[64]
Oda, S.; Numaga-Tomita, T.; Kitajima, N.; Toyama, T.; Harada, E.; Shimauchi, T.; Nishimura, A.; Ishikawa, T.; Kumagai, Y.; Birnbaumer, L.; Nishida, M. TRPC6 counteracts TRPC3-Nox2 protein complex leading to attenuation of hyperglycemia-induced heart failure in mice. Sci. Rep., 2017, 7(1), 7511.
[http://dx.doi.org/10.1038/s41598-017-07903-4] [PMID: 28790356]
[65]
Li, J.Z.; Yu, S.Y.; Wu, J.H.; Shao, Q.R.; Dong, X.M. Paeoniflorin protects myocardial cell from doxorubicin-induced apoptosis through inhibition of NADPH oxidase. Can. J. Physiol. Pharmacol., 2012, 90(12), 1569-1575.
[http://dx.doi.org/10.1139/y2012-140] [PMID: 23210435]
[66]
Trautmann, A. Extracellular ATP in the immune system: more than just a “danger signal”. Sci. Signal., 2009, 2(56), pe6.
[http://dx.doi.org/10.1126/scisignal.256pe6] [PMID: 19193605]
[67]
Sudi, S.B.; Tanaka, T.; Oda, S.; Nishiyama, K.; Nishimura, A.; Sunggip, C.; Mangmool, S.; Numaga-Tomita, T.; Nishida, M. TRPC3-Nox2 axis mediates nutritional deficiency-induced cardiomyocyte atrophy. Sci. Rep., 2019, 9(1), 9785.
[http://dx.doi.org/10.1038/s41598-019-46252-2] [PMID: 31278358]
[68]
Faigle, M.; Seessle, J.; Zug, S.; El Kasmi, K.C.; Eltzschig, H.K. ATP release from vascular endothelia occurs across Cx43 hemichannels and is attenuated during hypoxia. PLoS One, 2008, 3(7), e2801.
[http://dx.doi.org/10.1371/journal.pone.0002801] [PMID: 18665255]
[69]
Paul, P.K.; Bhatnagar, S.; Mishra, V.; Srivastava, S.; Darnay, B.G.; Choi, Y.; Kumar, A. The E3 ubiquitin ligase TRAF6 intercedes in starvation-induced skeletal muscle atrophy through multiple mechanisms. Mol. Cell. Biol., 2012, 32(7), 1248-1259.
[http://dx.doi.org/10.1128/MCB.06351-11] [PMID: 22290431]
[70]
Dolmatova, E.; Spagnol, G.; Boassa, D.; Baum, J.R.; Keith, K.; Ambrosi, C.; Kontaridis, M.I.; Sorgen, P.L.; Sosinsky, G.E.; Duffy, H.S. Cardiomyocyte ATP release through pannexin 1 aids in early fibroblast activation. Am. J. Physiol. Heart Circ. Physiol., 2012, 303(10), H1208-H1218.
[http://dx.doi.org/10.1152/ajpheart.00251.2012] [PMID: 22982782]
[71]
Hai, S.; Cao, L.; Wang, H.; Zhou, J.; Liu, P.; Yang, Y.; Hao, Q.; Dong, B. Association between sarcopenia and nutritional status and physical activity among community-dwelling Chinese adults aged 60 years and older. Geriatr. Gerontol. Int., 2017, 17(11), 1959-1966.
[http://dx.doi.org/10.1111/ggi.13001] [PMID: 28188973]
[72]
Hida, T.; Imagama, S.; Ando, K.; Kobayashi, K.; Muramoto, A.; Ito, K.; Ishikawa, Y.; Tsushima, M.; Nishida, Y.; Ishiguro, N.; Hasegawa, Y. Sarcopenia and physical function are associated with inflammation and arteriosclerosis in community-dwelling people: The Yakumo study. Mod. Rheumatol., 2018, 28(2), 345-350.
[http://dx.doi.org/10.1080/14397595.2017.1349058] [PMID: 28741974]
[73]
Nishiyama, K.; Numaga-Tomita, T.; Fujimoto, Y.; Tanaka, T.; Toyama, C.; Nishimura, A.; Yamashita, T.; Matsunaga, N.; Koyanagi, S.; Azuma, Y.T.; Ibuki, Y.; Uchida, K.; Ohdo, S.; Nishida, M. Ibudilast attenuates doxorubicin-induced cytotoxicity by suppressing formation of TRPC3 channel and NADPH oxidase 2 protein complexes. Br. J. Pharmacol., 2019, 176(18), 3723-3738.
[http://dx.doi.org/10.1111/bph.14777] [PMID: 31241172]
[74]
Hassan, F.; Islam, S.; Mu, M.M.; Ito, H.; Koide, N.; Mori, I.; Yoshida, T.; Yokochi, T. Lipopolysaccharide prevents doxorubicin-induced apoptosis in RAW 264.7 macrophage cells by inhibiting p53 activation. Mol. Cancer Res., 2005, 3(7), 373-379.
[http://dx.doi.org/10.1158/1541-7786.MCR-05-0046] [PMID: 16046548]
[75]
Solanki, S.; Dube, P.R.; Tano, J.Y.; Birnbaumer, L.; Vazquez, G. Reduced endoplasmic reticulum stress-induced apoptosis and impaired unfolded protein response in TRPC3-deficient M1 macrophages. Am. J. Physiol. Cell Physiol., 2014, 307(6), C521-C531.
[http://dx.doi.org/10.1152/ajpcell.00369.2013] [PMID: 25031020]
[76]
Tano, J.Y.; Solanki, S.; Lee, R.H.; Smedlund, K.; Birnbaumer, L.; Vazquez, G. Bone marrow deficiency of TRPC3 channel reduces early lesion burden and necrotic core of advanced plaques in a mouse model of atherosclerosis. Cardiovasc. Res., 2014, 101(1), 138-144.
[http://dx.doi.org/10.1093/cvr/cvt231] [PMID: 24101197]
[77]
Fan, C.; Choi, W.; Sun, W.; Du, J.; Lü, W. Structure of the human lipid-gated cation channel TRPC3. eLife, 2018, 7, 7.
[http://dx.doi.org/10.7554/eLife.36852] [PMID: 29726814]
[78]
Magnani, F.; Nenci, S.; Millana Fananas, E.; Ceccon, M.; Romero, E.; Fraaije, M.W.; Mattevi, A. Crystal structures and atomic model of NADPH oxidase. Proc. Natl. Acad. Sci. USA, 2017, 114(26), 6764-6769.
[http://dx.doi.org/10.1073/pnas.1702293114] [PMID: 28607049]
[79]
Álvarez-Miguel, I.; Cidad, P.; Pérez-García, M.T.; López-López, J.R. Differences in TRPC3 and TRPC6 channels assembly in mesenteric vascular smooth muscle cells in essential hypertension. J. Physiol., 2017, 595(5), 1497-1513.
[http://dx.doi.org/10.1113/JP273327] [PMID: 27861908]
[80]
Numaga-Tomita, T.; Shimauchi, T.; Oda, S.; Tanaka, T.; Nishiyama, K.; Nishimura, A.; Birnbaumer, L.; Mori, Y.; Nishida, M. TRPC6 regulates phenotypic switching of vascular smooth muscle cells through plasma membrane potential-dependent coupling with PTEN. FASEB J., 2019, 33(9), 9785-9796.
[http://dx.doi.org/10.1096/fj.201802811R] [PMID: 31162976]
[81]
Gibon, J.; Tu, P.; Bohic, S.; Richaud, P.; Arnaud, J.; Zhu, M.; Boulay, G.; Bouron, A. The over-expression of TRPC6 channels in HEK-293 cells favours the intracellular accumulation of zinc. Biochim. Biophys. Acta, 2011, 1808(12), 2807-2818.
[http://dx.doi.org/10.1016/j.bbamem.2011.08.013] [PMID: 21864503]
[82]
Mwanjewe, J.; Grover, A.K. Role of transient receptor potential canonical 6 (TRPC6) in non-transferrin-bound iron uptake in neuronal phenotype PC12 cells. Biochem. J., 2004, 378(Pt 3), 975-982.
[http://dx.doi.org/10.1042/bj20031187] [PMID: 14640978]
[83]
Hasna, J.; Abi Nahed, R.; Sergent, F.; Alfaidy, N.; Bouron, A. The deletion of TRPC6 channels perturbs iron and zinc homeostasis and pregnancy outcome in mice. Cell. Physiol. Biochem., 2019, 52(3), 455-467.
[http://dx.doi.org/10.33594/000000033] [PMID: 30873821]
[84]
Numaga-Tomita, T.; Oda, S.; Nishiyama, K.; Tanaka, T.; Nishimura, A.; Nishida, M. TRPC channels in exercise-mimetic therapy. Pflugers Arch., 2019, 471(3), 507-517.
[http://dx.doi.org/10.1007/s00424-018-2211-3] [PMID: 30298191]
[85]
Joyner, M.J.; Green, D.J. Exercise protects the cardiovascular system: effects beyond traditional risk factors. J. Physiol., 2009, 587(Pt 23), 5551-5558.
[http://dx.doi.org/10.1113/jphysiol.2009.179432] [PMID: 19736305]
[86]
Balady, G.J.; Ades, P.A.; Bittner, V.A.; Franklin, B.A.; Gordon, N.F.; Thomas, R.J.; Tomaselli, G.F.; Yancy, C.W. American Heart Association Science Advisory and Coordinating Committee. Referral, enrollment, and delivery of cardiac rehabilitation/secondary prevention programs at clinical centers and beyond: a presidential advisory from the American Heart Association. Circulation, 2011, 124(25), 2951-2960.
[http://dx.doi.org/10.1161/CIR.0b013e31823b21e2] [PMID: 22082676]