Possible involvement of TRP channels in cardiac hypertrophy and arrhythmia

Current Topics in Medicinal Chemistry

Volumn 13, Issue 3, 2013, Pages 283-294

  Watanabe, Hiroyuki ^a   Iino, Kenji ^a   Ohba, Takayoshi ^a   Ito, Hiroshi ^a  

^a AKITA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Cardiac arrhythmia; Cardiac hypertrophy; Orai1; Stim1; TRPC1; TRPC3; TRPC6; TRPM4

Indexed keywords

CALCINEURIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM ION; CALCIUM RELEASE ACTIVATED CALCIUM CHANNEL 1; CYCLIC GMP DEPENDENT PROTEIN KINASE; STROMAL INTERACTION MOLECULE 1; TRANSCRIPTION FACTOR NFAT; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRANSIENT RECEPTOR POTENTIAL CHANNEL M4;

ANAPHYLAXIS; CARDIOVASCULAR RISK; FIBROBLAST; GENE MUTATION; GENE SILENCING; HEART ARRHYTHMIA; HEART BLOCK; HEART VENTRICLE HYPERTROPHY; HUMAN; NERVE BLOCK; NONHUMAN; PACEMAKER; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SINUS ARRHYTHMIA; STIMULATION; UPREGULATION;

ARRHYTHMIAS, CARDIAC; HEART VENTRICLES; HUMANS; MOLECULAR TARGETED THERAPY; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 84876732228     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026611313030006     Document Type: Review

References (100)

1. Niedergerke, R. Movements of Ca in Frog Heart Ventricles at Rest and during Contractures. J Physiol, 1963, 167, 515-550.
2. Ehara, T.; Noma, A.; Ono, K. Calcium-activated non-selective cation channel in ventricular cells isolated from adult guinea-pig hearts. J Physiol, 1988, 403, 117-133.
3. Sigurdson, W.; Ruknudin, A.; Sachs, F. Calcium imaging of mechanically induced fluxes in tissue-cultured chick heart: role of stretch-activated ion channels. Am J Physiol, 1992, 262, H1110-1115.
4. Tominaga, M.; Matsumori, A.; Horie, M.; Yoshida, H.; Okada, Y. Activation of Ca-permeable cation channels by myocarditisassociated antibody in guinea pig ventricular myocytes. J Clin Invest, 1993, 91, 1231-1234.
5. Magishi, K.; Kimura, J.; Kubo, Y.; Abiko, Y. Exogenous lysophosphatidylcholine increases non-selective cation current in guinea-pig ventricular myocytes. Pflugers Arch, 1996, 432, 345-350.
6. Watanabe, H.; Murakami, M.; Ohba, T.; Ono, K.; Ito, H. The pathological role of transient receptor potential channels in heart disease. Circ J, 2009, 73, 419-427.
7. Watanabe, H.; Murakami, M.; Ohba, T.; Takahashi, Y.; Ito, H. TRP channel and cardiovascular disease. Pharmacol Ther, 2008, 118, 337-351.
8. Montell, C.; Birnbaumer, L.; Flockerzi, V. The TRP channels, a remarkably functional family. Cell, 2002, 108, 595-598.
9. Pedersen, S. F.; Owsianik, G.; Nilius, B. TRP channels: an overview. Cell Calcium, 2005, 38, 233-252.
10. Venkatachalam, K.; Montell, C. TRP channels. Annu Rev Biochem, 2007, 76, 387-417.
11. Abramowitz, J.; Birnbaumer, L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J, 2009, 23, 297-328.
12. Nilius, B.; Owsianik, G.; Voets, T.; Peters, J. A. Transient receptor potential cation channels in disease. Physiol Rev, 2007, 87, 165-217.
13. Chubanov, V.; Mederos y Schnitzler, M.; Waring, J.; Plank, A.; Gudermann, T. Emerging roles of TRPM6/TRPM7 channel kinase signal transduction complexes. Naunyn Schmiedebergs Arch Pharmacol, 2005, 371, 334-341.
14. Chubanov, V.; Waldegger, S.; Mederos y Schnitzler, M.; Vitzthum, H.; Sassen, M. C.; Seyberth, H. W.; Konrad, M.; Gudermann, T. Disruption of TRPM6/TRPM7 complex formation by a mutation in the TRPM6 gene causes hypomagnesemia with secondary hypocalcemia. Proc Natl Acad Sci U S A, 2004, 101, 2894-2899.
15. Gwanyanya, A.; Amuzescu, B.; Zakharov, S. I.; Macianskiene, R.; Sipido, K. R.; Bolotina, V. M.; Vereecke, J.; Mubagwa, K. Magnesium-inhibited, TRPM6/7-like channel in cardiac myocytes: permeation of divalent cations and pH-mediated regulation. J Physiol, 2004, 559, 761-776.
16. Jiang, J.; Li, M. H.; Inoue, K.; Chu, X. P.; Seeds, J.; Xiong, Z. G. Transient receptor potential melastatin 7-like current in human head and neck carcinoma cells: role in cell proliferation. Cancer Res, 2007, 67, 10929-10938.
17. Li, M.; Jiang, J.; Yue, L. Functional characterization of homoand heteromeric channel kinases TRPM6 and TRPM7. J Gen Physiol, 2006, 127, 525-537.
18. Hill, J. A.; Olson, E. N. Cardiac plasticity. N Engl J Med, 2008, 358, 1370-1380.
19. Kehat, I.; Molkentin, J. D. Molecular pathways underlying cardiac remodeling during pathophysiological stimulation. Circulation, 2010, 122, 2727-2735.
20. Grossman, W.; Jones, D.; McLaurin, L. P. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest, 1975, 56, 56-64.
21. Molkentin, J. D.; Lu, J. R.; Antos, C. L.; Markham, B.; Richardson, J.; Robbins, J.; Grant, S. R.; Olson, E. N. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell, 1998, 93, 215-228.
22. Heineke, J.; Molkentin, J. D. Regulation of cardiac hypertrophy by intracellular signalling pathways. Nat Rev Mol Cell Biol, 2006, 7, 589-600.
23. Maillet, M.; Davis, J.; Auger-Messier, M.; York, A.; Osinska, H.; Piquereau, J.; Lorenz, J. N.; Robbins, J.; Ventura-Clapier, R.; Molkentin, J. D. Heart-specific deletion of CnB1 reveals multiple mechanisms whereby calcineurin regulates cardiac growth and function. J Biol Chem, 2010, 285, 6716-6724.
24. Heineke, J.; Ritter, O. Cardiomyocyte calcineurin signaling in subcellular domains: from the sarcolemma to the nucleus and beyond. J Mol Cell Cardiol, 2012, 52, 62-73.
25. Eble, D. M.; Qi, M.; Waldschmidt, S.; Lucchesi, P. A.; Byron, K. L.; Samarel, A. M. Contractile activity is required for sarcomeric assembly in phenylephrine-induced cardiac myocyte hypertrophy. Am J Physiol, 1998, 274, C1226-1237.
26. Marban, E.; Kitakaze, M.; Kusuoka, H.; Porterfield, J. K.; Yue, D. T.; Chacko, V. P. Intracellular free calcium concentration measured with 19F NMR spectroscopy in intact ferret hearts. Proc Natl Acad Sci U S A, 1987, 84, 6005-6009.
27. Perreault, C. L.; Shannon, R. P.; Shen, Y. T.; Vatner, S. F.; Morgan, J. P. Excitation-contraction coupling in isolated myocardium from dogs with compensated left ventricular hypertrophy. Am J Physiol, 1994, 266, H2436-2442.
28. Ruknudin, A.; Sachs, F.; Bustamante, J. O. Stretch-activated ion channels in tissue-cultured chick heart. Am J Physiol, 1993, 264, H960-972.
29. Clipstone, N. A.; Crabtree, G. R. Identification of calcineurin as a key signalling enzyme in T-lymphocyte activation. Nature, 1992, 357, 695-697.
30. Crabtree, G. R. Generic signals and specific outcomes: signaling through Ca2+, calcineurin, and NF-AT. Cell, 1999, 96, 611-614.
31. Dolmetsch, R. E.; Lewis, R. S.; Goodnow, C. C.; Healy, J. I. Differential activation of transcription factors induced by Ca2+ response amplitude and duration. Nature, 1997, 386, 855-858.
32. Klee, C. B.; Ren, H.; Wang, X. Regulation of the calmodulinstimulated protein phosphatase, calcineurin. J Biol Chem, 1998, 273, 13367-13370.
33. Timmerman, L. A.; Clipstone, N. A.; Ho, S. N.; Northrop, J. P.; Crabtree, G. R. Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature, 1996, 383, 837-840.
34. Parekh, A. B.; Putney, J. W., Jr. Store-operated calcium channels. Physiol Rev, 2005, 85, 757-810.
35. Hunton, D. L.; Lucchesi, P. A.; Pang, Y.; Cheng, X.; Dell'Italia, L. J.; Marchase, R. B. Capacitative calcium entry contributes to nuclear factor of activated T-cells nuclear translocation and hypertrophy in cardiomyocytes. J Biol Chem, 2002, 277, 14266-14273.
36. Mori, Y.; Wakamori, M.; Miyakawa, T.; Hermosura, M.; Hara, Y.; Nishida, M.; Hirose, K.; Mizushima, A.; Kurosaki, M.; Mori, E.; Gotoh, K.; Okada, T.; Fleig, A.; Penner, R.; Iino, M.; Kurosaki, T. Transient receptor potential 1 regulates capacitative Ca(2+) entry and Ca(2+) release from endoplasmic reticulum in B lymphocytes. J Exp Med, 2002, 195, 673-681.
37. Poteser, M.; Schleifer, H.; Lichtenegger, M.; Schernthaner, M.; Stockner, T.; Kappe, C. O.; Glasnov, T. N.; Romanin, C.; Groschner, K. PKC-dependent coupling of calcium permeation through transient receptor potential canonical 3 (TRPC3) to calcineurin signaling in HL-1 myocytes. Proc Natl Acad Sci U S A, 108, 10556-10561.
38. Ohba, T.; Watanabe, H.; Murakami, M.; Takahashi, Y.; Iino, K.; Kuromitsu, S.; Mori, Y.; Ono, K.; Iijima, T.; Ito, H. Upregulation of TRPC1 in the development of cardiac hypertrophy. J Mol Cell Cardiol, 2007, 42, 498-507.
39. Ohba, T.; Watanabe, H.; Takahashi, Y.; Suzuki, T.; Miyoshi, I.; Nakayama, S.; Satoh, E.; Iino, K.; Sasano, H.; Mori, Y.; Kuromitsu, S.; Imagawa, K.; Saito, Y.; Iijima, T.; Ito, H.; Murakami, M. Regulatory role of neuron-restrictive silencing factor in expression of TRPC1. Biochem Biophys Res Commun, 2006, 351, 764-770.
40. Vindis, C.; D'Angelo, R.; Mucher, E.; Negre-Salvayre, A.; Parini, A.; Mialet-Perez, J. Essential role of TRPC1 channels in cardiomyoblasts hypertrophy mediated by 5-HT2A serotonin receptors. Biochem Biophys Res Commun, 2010, 391, 979-983.
41. Ohba T W. H., Murakami M, Takahashi Y, Ito H. Increased expression of transient receptor potential C1 in rats with hypertensive hypertrophy. Akita J Med, 2005, 32, 201-207.
42. Seth, M.; Zhang, Z. S.; Mao, L.; Graham, V.; Burch, J.; Stiber, J.; Tsiokas, L.; Winn, M.; Abramowitz, J.; Rockman, H. A.; Birnbaumer, L.; Rosenberg, P. TRPC1 channels are critical for hypertrophic signaling in the heart. Circ Res, 2009, 105, 1023-1030.
43. 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, 179-185.
44. Paria, B. C.; Malik, A. B.; Kwiatek, A. M.; Rahman, A.; May, M. J.; Ghosh, S.; Tiruppathi, C. Tumor necrosis factor-alpha induces nuclear factor-kappaB-dependent TRPC1 expression in endothelial cells. J Biol Chem, 2003, 278, 37195-37203.
45. Schoenherr, C. J.; Anderson, D. J. The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science, 1995, 267, 1360-1363.
46. Kuwahara, K.; Saito, Y.; Takano, M.; Arai, Y.; Yasuno, S.; Nakagawa, Y.; Takahashi, N.; Adachi, Y.; Takemura, G.; Horie, M.; Miyamoto, Y.; Morisaki, T.; Kuratomi, S.; Noma, A.; Fujiwara, H.; Yoshimasa, Y.; Kinoshita, H.; Kawakami, R.; Kishimoto, I.; Nakanishi, M.; Usami, S.; Harada, M.; Nakao, K. NRSF regulates the fetal cardiac gene program and maintains normal cardiac structure and function. EMBO J, 2003, 22, 6310-6321.
47. Uehara, A.; Yasukochi, M.; Imanaga, I.; Nishi, M.; Takeshima, H. Store-operated Ca2+ entry uncoupled with ryanodine receptor and junctional membrane complex in heart muscle cells. Cell Calcium, 2002, 31, 89-96.
48. Hulot, J. S.; Fauconnier, J.; Ramanujam, D.; Chaanine, A.; Aubart, F.; Sassi, Y.; Merkle, S.; Cazorla, O.; Ouille, A.; Dupuis, M.; Hadri, L.; Jeong, D.; Muhlstedt, S.; Schmitt, J.; Braun, A.; Benard, L.; Saliba, Y.; Laggerbauer, B.; Nieswandt, B.; Lacampagne, A.; Hajjar, R. J.; Lompre, A. M.; Engelhardt, S. Critical role for stromal interaction molecule 1 in cardiac hypertrophy. Circulation, 2011, 124, 796-805.
49. 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, 1660-1670.
50. Bush, E. W.; Hood, D. B.; Papst, P. J.; Chapo, J. A.; Minobe, W.; Bristow, M. R.; Olson, E. N.; McKinsey, T. A. Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J Biol Chem, 2006, 281, 33487-33496.
51. Kuwahara, K.; Wang, Y.; McAnally, J.; Richardson, J. A.; BasselDuby, R.; Hill, J. A.; Olson, E. N. TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest, 2006, 116, 3114-3126.
52. 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, 5305-5316.
53. Wu, X.; Eder, P.; Chang, B.; Molkentin, J. D. TRPC channels are necessary mediators of pathologic cardiac hypertrophy. Proc Natl Acad Sci U S A, 2010, 107, 7000-7005.
54. 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.; Nakao, K. Inhibition of TRPC6 channel activity contributes to the antihypertrophic effects of natriuretic peptidesguanylyl cyclase-A signaling in the heart. Circ Res, 2010, 106, 1849-1860.
55. 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.; Mori, Y. Selective and direct inhibition of TRPC3 channels underlies biological activities of a pyrazole compound. Proc Natl Acad Sci U S A, 2009, 106, 5400-5405.
56. Zhang, S. L.; Yu, Y.; Roos, J.; Kozak, J. A.; Deerinck, T. J.; Ellisman, M. H.; Stauderman, K. A.; Cahalan, M. D. STIM1 is a Ca2+ sensor that activates CRAC channels and migrates from the Ca2+ store to the plasma membrane. Nature, 2005, 437, 902-905.
57. Huang, G. N.; Zeng, W.; Kim, J. Y.; Yuan, J. P.; Han, L.; Muallem, S.; Worley, P. F. STIM1 carboxyl-terminus activates native SOC, I(crac) and TRPC1 channels. Nat Cell Biol, 2006, 8, 1003-1010.
58. Liou, J.; Kim, M. L.; Heo, W. D.; Jones, J. T.; Myers, J. W.; Ferrell, J. E., Jr.; Meyer, T. STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr Biol, 2005, 15, 1235-1241.
59. Roos, J.; DiGregorio, P. J.; Yeromin, A. V.; Ohlsen, K.; Lioudyno, M.; Zhang, S.; Safrina, O.; Kozak, J. A.; Wagner, S. L.; Cahalan, M. D.; Velicelebi, G.; Stauderman, K. A. STIM1, an essential and conserved component of store-operated Ca2+ channel function. J Cell Biol, 2005, 169, 435-445.
60. Williams, R. T.; Manji, S. S.; Parker, N. J.; Hancock, M. S.; Van Stekelenburg, L.; Eid, J. P.; Senior, P. V.; Kazenwadel, J. S.; Shandala, T.; Saint, R.; Smith, P. J.; Dziadek, M. A. Identification and characterization of the STIM (stromal interaction molecule) gene family: coding for a novel class of transmembrane proteins. Biochem J, 2001, 357, 673-685.
61. Watanabe H O. T., Ito H. Store-operated Ca entry (SOCE) pathways Emerging signaling concepts in human pathophysiology, Springer 2012.
62. Luo, X.; Hojayev, B.; Jiang, N.; Wang, Z. V.; Tandan, S.; Rakalin, A.; Rothermel, B. A.; Gillette, T. G.; Hill, J. A. STIM1-dependent store-operated Ca(2)(+) entry is required for pathological cardiac hypertrophy. J Mol Cell Cardiol, 2012, 52, 136-147.
63. Voelkers, M.; Salz, M.; Herzog, N.; Frank, D.; Dolatabadi, N.; Frey, N.; Gude, N.; Friedrich, O.; Koch, W. J.; Katus, H. A.; Sussman, M. A.; Most, P. Orai1 and Stim1 regulate normal and hypertrophic growth in cardiomyocytes. J Mol Cell Cardiol, 2010, 48, 1329-1334.
64. Ohba, T.; Watanabe, H.; Murakami, M.; Sato, T.; Ono, K.; Ito, H. Essential role of STIM1 in the development of cardiomyocyte hypertrophy. Biochem Biophys Res Commun, 2009, 389, 172-176.
65. Feske, S. ORAI1 and STIM1 deficiency in human and mice: roles of store-operated Ca2+ entry in the immune system and beyond. Immunol Rev, 2009, 231, 189-209.
66. Darbellay, B.; Arnaudeau, S.; Konig, S.; Jousset, H.; Bader, C.; Demaurex, N.; Bernheim, L. STIM1-and Orai1-dependent storeoperated calcium entry regulates human myoblast differentiation. J Biol Chem, 2009, 284, 5370-5380.
67. Stiber, J.; Hawkins, A.; Zhang, Z. S.; Wang, S.; Burch, J.; Graham, V.; Ward, C. C.; Seth, M.; Finch, E.; Malouf, N.; Williams, R. S.; Eu, J. P.; Rosenberg, P. STIM1 signalling controls store-operated calcium entry required for development and contractile function in skeletal muscle. Nat Cell Biol, 2008, 10, 688-697.
68. Kimura, J.; Noma, A.; Irisawa, H. Na-Ca exchange current in mammalian heart cells. Nature, 1986, 319, 596-597.
69. Colquhoun, D.; Neher, E.; Reuter, H.; Stevens, C. F. Inward current channels activated by intracellular Ca in cultured cardiac cells. Nature, 1981, 294, 752-754.
70. Kass, R. S.; Tsien, R. W.; Weingart, R. Ionic basis of transient inward current induced by strophanthidin in cardiac Purkinje fibres. J Physiol, 1978, 281, 209-226.
71. Sipido, K. R.; Callewaert, G.; Carmeliet, E. [Ca2+]i transients and [Ca2+]i-dependent chloride current in single Purkinje cells from rabbit heart. J Physiol, 1993, 468, 641-667.
72. Zygmunt, A. C.; Gibbons, W. R. Calcium-activated chloride current in rabbit ventricular myocytes. Circ Res, 1991, 68, 424-437.
73. Guinamard, R.; Demion, M.; Chatelier, A.; Bois, P. Calciumactivated nonselective cation channels in mammalian cardiomyocytes. Trends Cardiovasc Med, 2006, 16, 245-250.
74. Guinamard, R.; Demion, M.; Magaud, C.; Potreau, D.; Bois, P. Functional expression of the TRPM4 cationic current in ventricular cardiomyocytes from spontaneously hypertensive rats. Hypertension, 2006, 48, 587-594.
75. Janse, M. J. Electrophysiological changes in heart failure and their relationship to arrhythmogenesis. Cardiovasc Res, 2004, 61, 208-217.
76. Nilius, B.; Vennekens, R. From cardiac cation channels to the molecular dissection of the transient receptor potential channel TRPM4. Pflugers Arch, 2006, 453, 313-321.
77. Guinamard, R.; Chatelier, A.; Demion, M.; Potreau, D.; Patri, S.; Rahmati, M.; Bois, P. Functional characterization of a Ca(2+)-activated non-selective cation channel in human atrial cardiomyocytes. J Physiol, 2004, 558, 75-83.
78. Launay, P.; Fleig, A.; Perraud, A. L.; Scharenberg, A. M.; Penner, R.; Kinet, J. P. TRPM4 is a Ca2+-activated nonselective cation channel mediating cell membrane depolarization. Cell, 2002, 109, 397-407.
79. Nilius, B.; Prenen, J.; Droogmans, G.; Voets, T.; Vennekens, R.; Freichel, M.; Wissenbach, U.; Flockerzi, V. Voltage dependence of the Ca2+-activated cation channel TRPM4. J Biol Chem, 2003, 278, 30813-30820.
80. Simard, C.; Salle, L.; Rouet, R.; Guinamard, R. Transient receptor potential melastatin 4 inhibitor 9-phenanthrol abolishes arrhythmias induced by hypoxia and re-oxygenation in mouse ventricle. Br J Pharmacol, 2012, 165, 2354-2364.
81. Kruse, M.; Schulze-Bahr, E.; Corfield, V.; Beckmann, A.; Stallmeyer, B.; Kurtbay, G.; Ohmert, I.; Brink, P.; Pongs, O. Impaired endocytosis of the ion channel TRPM4 is associated with human progressive familial heart block type I. J Clin Invest, 2009, 119, 2737-2744.
82. Liu, H.; El Zein, L.; Kruse, M.; Guinamard, R.; Beckmann, A.; Bozio, A.; Kurtbay, G.; Megarbane, A.; Ohmert, I.; Blaysat, G.; Villain, E.; Pongs, O.; Bouvagnet, P. Gain-of-function mutations in TRPM4 cause autosomal dominant isolated cardiac conduction disease. Circ Cardiovasc Genet, 2010, 3, 374-385.
83. Stallmeyer, B.; Zumhagen, S.; Denjoy, I.; Duthoit, G.; Hebert, J. L.; Ferrer, X.; Maugenre, S.; Schmitz, W.; Kirchhefer, U.; Schulze-Bahr, E.; Guicheney, P. Mutational spectrum in the Ca(2+)--activated cation channel gene TRPM4 in patients with cardiac conductance disturbances. Hum Mutat, 2012, 33, 109-117.
84. Schott, J. J.; Alshinawi, C.; Kyndt, F.; Probst, V.; Hoorntje, T. M.; Hulsbeek, M.; Wilde, A. A.; Escande, D.; Mannens, M. M.; Le Marec, H. Cardiac conduction defects associate with mutations in SCN5A. Nat Genet, 1999, 23, 20-21.
85. Tan, H. L.; Bink-Boelkens, M. T.; Bezzina, C. R.; Viswanathan, P. C.; Beaufort-Krol, G. C.; van Tintelen, P. J.; van den Berg, M. P.; Wilde, A. A.; Balser, J. R. A sodium-channel mutation causes isolated cardiac conduction disease. Nature, 2001, 409, 1043-1047.
86. Watanabe, H.; Koopmann, T. T.; Le Scouarnec, S.; Yang, T.; Ingram, C. R.; Schott, J. J.; Demolombe, S.; Probst, V.; Anselme, F.; Escande, D.; Wiesfeld, A. C.; Pfeufer, A.; Kaab, S.; Wichmann, H. E.; Hasdemir, C.; Aizawa, Y.; Wilde, A. A.; Roden, D. M.; Bezzina, C. R. Sodium channel beta1 subunit mutations associated with Brugada syndrome and cardiac conduction disease in humans. J Clin Invest, 2008, 118, 2260-2268.
87. Mathar, I.; Vennekens, R.; Meissner, M.; Kees, F.; Van der Mieren, G.; Camacho Londono, J. E.; Uhl, S.; Voets, T.; Hummel, B.; van den Bergh, A.; Herijgers, P.; Nilius, B.; Flockerzi, V.; Schweda, F.; Freichel, M. Increased catecholamine secretion contributes to hypertension in TRPM4-deficient mice. J Clin Invest, 2010, 120, 3267-3279.
88. Vennekens, R.; Olausson, J.; Meissner, M.; Bloch, W.; Mathar, I.; Philipp, S. E.; Schmitz, F.; Weissgerber, P.; Nilius, B.; Flockerzi, V.; Freichel, M. Increased IgE-dependent mast cell activation and anaphylactic responses in mice lacking the calcium-activated nonselective cation channel TRPM4. Nat Immunol, 2007, 8, 312-320.
89. Demion, M.; Bois, P.; Launay, P.; Guinamard, R. TRPM4, a Ca2+-activated nonselective cation channel in mouse sino-atrial node cells. Cardiovasc Res, 2007, 73, 531-538.
90. Du, J.; Xie, J.; Zhang, Z.; Tsujikawa, H.; Fusco, D.; Silverman, D.; Liang, B.; Yue, L. TRPM7-mediated Ca2+ signals confer fibrogenesis in human atrial fibrillation. Circ Res, 2010, 106, 992-1003.
91. 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.; Nattel, S. Transient receptor potential canonical-3 channel-dependent fibroblast regulation in atrial fibrillation. Circulation, 2012, 126, 2051-2064.
92. Zhang, Y. H.; Sun, H. Y.; Chen, K. H.; Du, X. L.; Liu, B.; Cheng, L. C.; Li, X.; Jin, M. W.; Li, G. R. Evidence for functional expression of TRPM7 channels in human atrial myocytes. Basic Res Cardiol, 2012, 107, 282.
93. Nakashima, H.; Kumagai, K. Reverse-remodeling effects of angiotensin II type 1 receptor blocker in a canine atrial fibrillation model. Circ J, 2007, 71, 1977-1982.
94. Hagiwara, N.; Masuda, H.; Shoda, M.; Irisawa, H. Stretch-activated anion currents of rabbit cardiac myocytes. J Physiol, 1992, 456, 285-302.
95. Sorota, S. Swelling-induced chloride-sensitive current in canine atrial cells revealed by whole-cell patch-clamp method. Circ Res, 1992, 70, 679-687.
96. Kim, D. Novel cation-selective mechanosensitive ion channel in the atrial cell membrane. Circ Res, 1993, 72, 225-231.
97. Bode, F.; Sachs, F.; Franz, M. R. Tarantula peptide inhibits atrial fibrillation. Nature, 2001, 409, 35-36.
98. Inoue, R.; Jian, Z.; Kawarabayashi, Y. Mechanosensitive TRP channels in cardiovascular pathophysiology. Pharmacol Ther, 2009, 123, 371-385.
99. Dyachenko, V.; Husse, B.; Rueckschloss, U.; Isenberg, G. Mechanical deformation of ventricular myocytes modulates both TRPC6 and Kir2.3 channels. Cell Calcium, 2009, 45, 38-54.
100. 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, 16586-16591.