Mechanosensitive channels in striated muscle and the cardiovascular system: Not quite a stretch anymore

Journal of Cardiovascular Pharmacology

Volumn 54, Issue 2, 2009, Pages 116-122

  Stiber, Jonathan A ^a   Seth, Malini ^a   Rosenberg, Paul B ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Heart Failure; Mechanically sensitive channels; TRP channels

Indexed keywords

SCAFFOLD PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL;

CARDIOVASCULAR SYSTEM; CYTOSKELETON; HEART FAILURE; HEART VENTRICLE REMODELING; PATHOGENESIS; PRIORITY JOURNAL; RECEPTOR POTENTIAL; REVIEW; SKELETAL MUSCLE;

ANIMALS; CARDIOVASCULAR DISEASES; CARDIOVASCULAR SYSTEM; CYTOSKELETON; DRUG DELIVERY SYSTEMS; HEART FAILURE; HUMANS; ION CHANNELS; MUSCLE, SKELETAL; SIGNAL TRANSDUCTION; TRANSIENT RECEPTOR POTENTIAL CHANNELS;

EID: 74249114775     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181aa233f     Document Type: Review

References (87)

1. Gottlieb PA, Suchyna TM, Ostrow LW, et al. Mechanosensitive ion channels as drug targets. Curr Drug Targets Cns Neurol Disorders. 2004; 3:287-295.
2. Bush EW, Hood DB, Papst PJ, et al. Canonical transient receptor potential channels promote cardiomyocyte hypertrophy through activation of calcineurin signaling. J Biol Chem. 2006;281:33487-33496.
3. Guinamard R, Bois P. Involvement of transient receptor potential proteins in cardiac hypertrophy. Biochimica et Biophysica Acta. 2007;1772: 885-894.
4. Kuwahara K, Wang Y, McAnally J, et al. TRPC6 fulfills a calcineurin signaling circuit during pathologic cardiac remodeling. J Clin Invest. 2006;116:3114-3126.
5. Watanabe H, Murakami M, Ohba T, et al. TRP channel and cardiovascular disease. Pharmacol Therapeutics. 2008;118:337-351.
6. Christensen AP, Corey DP. TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci. 2007;8:510-521.
7. Gottlieb P, Folgering J, Maroto R, et al. Revisiting TRPC1 and TRPC6 mechanosensitivity. Pflugers Archiv Eur J Physiol. 2008;455:1097-1103.
8. Markin VS, Sachs F. Thermodynamics of mechanosensitivity. Phys Biol. 2004;1:110-124.
9. Ervasti JM. Costameres: the Achilles' heel of Herculean muscle. J Biol Chem. 2003;278:13591-13594.
10. Pyle WG, Solaro RJ. At the crossroads of myocardial signaling: the role of Z-discs in intracellular signaling and cardiac function. Circulation Res. 2004;94:296-305.
11. Maroto R, Raso A, Wood TG, et al. TRPC1 forms the stretch-activated cation channel in vertebrate cells. Nature Cell Biol. 2005;7:179-185.
12. Sullivan MJ, Sharma RV, Wachtel RE, et al. Non-voltage-gated Ca2+ influx through mechanosensitive ion channels in aortic baroreceptor neurons. Circulation Res. 1997;80:861-867.
13. Li Y, Tran TP, Muelleman R, et al. Blunted excitability of aortic baroreceptor neurons in diabetic rats: involvement of hyperpolarizationactivated channel. Cardiovascular Res. 2008;79:715-721.
14. Wladyka CL, Feng B, Glazebrook PA, et al. The KCNQ/M-current modulates arterial baroreceptor function at the sensory terminal in rats. J Physiol. 2008;586:795-802.
15. Cooper PJ, Kohl P. Species- and preparation-dependence of stretch effects on sino-atrial node pacemaking. Ann NY Acad Sci. 2005;1047:324-335.
16. Kuijpers NH, ten Eikelder HM, Bovendeerd PH, et al. Mechanoelectric feedback leads to conduction slowing and block in acutely dilated atria: a modeling study of cardiac electromechanics. Am J Physiol. 2007;292: H2832-H2853.
17. Demion M, Bois P, Launay P, et al. TRPM4, a Ca2+-activated nonselective cation channel in mouse sino-atrial node cells. Cardiovascular Res. 2007; 73:531-538.
18. Zhang H, Shepherd N, Creazzo TL. Temperature-sensitive TREK currents contribute to setting the resting membrane potential in embryonic atrial myocytes. J Physiol. 2008;586:3645-3656.
19. Clemo HF, Stambler BS, Baumgarten CM. Persistent activation of a swelling-activated cation current in ventricular myocytes from dogs with tachycardia-induced congestive heart failure. Circulation Res. 1998;83: 147-157.
20. Liao XD, Tang AH, Chen Q, et al. Role of Ca2+ signaling in initiation of stretch-induced apoptosis in neonatal heart cells. Biochem Biophys Res Comm. 2003;310:405-411.
21. Ruknudin A, Sachs F, Bustamante JO. Stretch-activated ion channels in tissue-cultured chick heart. Am J Physiol. 1993;264:H960-H972.
22. Tung L, Zou S. Influence of stretch on excitation threshold of single frog ventricular cells. Exp Physiol. 1995;80:221-235.
23. Zeng T, Bett GC, Sachs F. Stretch-activated whole cell currents in adult rat cardiac myocytes. Am J Physiol. 2000;278:H548-H557.
24. Xian Tao L, Dyachenko V, Zuzarte M, et al. The stretch-activated potassium channel TREK-1 in rat cardiac ventricular muscle. Cardiovascul Res. 2006;69:86-97.
25. Clemo HF, Baumgarten CM. Swelling-activated Gd3+-sensitive cation current and cell volume regulation in rabbit ventricular myocytes. J Gen Physiol. 1997;110:297-312.
26. Sorota S. Swelling-induced chloride-sensitive current in canine atrial cells revealed by whole-cell patch-clamp method. Circulation Res. 1992;70: 679-687.
27. Niu W, Sachs F. Dynamic properties of stretch-activated K+ channels in adult rat atrial myocytes. Prog Biophys Mol Biol. 2003;82:121-135.
28. Spassova MA, Hewavitharana T, Xu W, et al. A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci USA. 2006;103:16586-16591.
29. Dietrich A, Kalwa H, Storch U, et al. Pressure-induced and store-operated cation influx in vascular smooth muscle cells is independent of TRPC1. Pflugers Archiv Eur J Physiol. 2007;455:465-477.
30. Dietrich A, Mederos YSM, Gollasch M, et al. Increased vascular smooth muscle contractility in TRPC6-/- mice.Mol Cell Biol. 2005;25:6980-6989.
31. Facemire CS, Mohler PJ, Arendshorst WJ. Expression and relative abundance of short transient receptor potential channels in the rat renal microcirculation. Am J Physiol. 2004;286:F546-F551.
32. Soboloff J, Spassova M, XuW, et al. Role of endogenous TRPC6 channels in Ca2+ signal generation in A7r5 smooth muscle cells. J Biol Chem. 2005;280:39786-39794.
33. Weissmann N, Dietrich A, Fuchs B, et al. Classical transient receptor potential channel ± (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc Natl Acad Sci USA. 2006;103:19093-19098.
34. Bergdahl A, Gomez MF, Wihlborg AK, et al. Plasticity of TRPC expression in arterial smooth muscle: correlation with store-operated Ca2+ entry. Am J Physiol Cell Physiol. 2005;288:C872-C880.
35. Kumar B, Dreja K, Shah SS, et al. Upregulated TRPC1 channel in vascular injury in vivo and its role in human neointimal hyperplasia. Circulation Res. 2006;98:557-563.
36. Xie A, Aihara Y, Bouryi VA, et al. Novel mechanism of endothelin-1- induced vasospasm after subarachnoid hemorrhage. J Cerebral Blood Flow Metabol. 2007;27:1692-1701.
37. Dietrich A, Chubanov V, Kalwa H, et al. Cation channels of the transient receptor potential superfamily: their role in physiological and pathophysiological processes of smooth muscle cells. Pharmacol Therap. 2006;112: 744-760.
38. Nishimura Y, Inoue T, Morooka T, et al. Mechanical stretch and angiotensin II increase interleukin-13 production and interleukin-13 receptor alpha2 expression in rat neonatal cardiomyocytes. Circulation. 2008;72:647-653.
39. Wang TL, Yang YH, Chang H, et al. Angiotensin II signals mechanical stretch-induced cardiac matrix metalloproteinase expression via JAKSTAT pathway. J Mol Cell Cardiol. 2004;37:785-794.
40. Yamazaki T, Yazaki Y. Role of tissue angiotensin II in myocardial remodelling induced by mechanical stress. J Human Hypertens. 1999;13 (Suppl 1):S43-S47.
41. Collinsworth AM, Zhang S, Kraus WE, et al. Apparent elastic modulus and hysteresis of skeletal muscle cells throughout differentiation. Am J Physiol. 2002;283:C1219-C1227.
42. Hopf FW, Turner PR, Steinhardt RA. Calcium misregulation and the pathogenesis of muscular dystrophy. Subcell Biochem. 2007;45:429-464.
43. Vandebrouck A, Sabourin J, Rivet J, et al. Regulation of capacitative calcium entries by alpha1-syntrophin: association of TRPC1 with dystrophin complex and the PDZ domain of alpha1-syntrophin. FASEB J. 2007;21:608-617.
44. Williams IA, Allen DG. Intracellular calcium handling in ventricular myocytes from mdx mice. Am J Physiol. 2007;292:H846-H855.
45. Vandebrouck C, Martin D, Colson-Van Schoor M, et al. Involvement of TRPC in the abnormal calcium influx observed in dystrophic (mdx) mouse skeletal muscle fibers. J Cell Biol. 2002;158:1089-1096.
46. Nigro G, Comi LI, Politano L, et al. The incidence and evolution of cardiomyopathy in Duchenne muscular dystrophy. Int J Cardiol. 1990;26: 271-277.
47. Cox GF, Kunkel LM. Dystrophies and heart disease. Curr Opin Cardiol. 1997;12:329-343.
48. Nilius B, Owsianik G, Voets T, et al. Transient receptor potential cation channels in disease. Physiol Rev. 2007;87:165-217.
49. Quinlan JG, Hahn HS, Wong BL, et al. Evolution of the mdx mouse cardiomyopathy: physiological and morphological findings. Neuromuscular Dis. 2004;14:491-496.
50. Suchyna TM, Sachs F. Mechanosensitive channel properties and membrane mechanics in mouse dystrophic myotubes. J Physiol. 2007; 581:369-387.
51. Hayakawa K, Tatsumi H, Sokabe M. Actin stress fibers transmit and focus force to activate mechanosensitive channels. J Cell Sci. 2008;121: 496-503.
52. Stiber JA, Zhang ZS, Burch J, et al. Mice lacking Homer 1 exhibit a skeletal myopathy characterized by abnormal transient receptor potential channel activity. Mol Cell Biol. 2008;28:2637-2647.
53. Bodding M. TRP proteins and cancer. Cell Signal. 2007;19:617-624.
54. Li Y, Jia YC, Cui K, et al. Essential role of TRPC channels in the guidance of nerve growth cones by brain-derived neurotrophic factor. Nature. 2005; 434:894-898.
55. Wang GX, Poo MM. Requirement of TRPC channels in netrin-1-induced chemotropic turning of nerve growth cones. Nature. 2005;434:898-904.
56. Wen Z, Han L, Bamburg JR, et al. BMP gradients steer nerve growth cones by a balancing act of LIM kinase and Slingshot phosphatase on ADF/cofilin. J Cell Biol. 2007;178:107-119.
57. Geiger B, Bershadsky A. Exploring the neighborhood: adhesion-coupled cell mechanosensors. Cell. 2002;110:139-142.
58. Zhang SJ, Truskey GA, Kraus WE. Effect of cyclic stretch on beta1Dintegrin expression and activation of FAK and RhoA. Am J Physiol. 2007; 292:C2057-C2069.
59. Dyachenko V, Christ A, Gubanov R, et al. Bending of z-lines by mechanical stimuli: an input signal for integrin dependent modulation of ion channels? Prog Biophys Mol Biol. 2008;97:196-216.
60. Rosenblatt N, Hu S, Suki B, et al. Contributions of the active and passive components of the cytoskeletal prestress to stiffening of airway smooth muscle cells. Ann Biomed Eng. 2007;35:224-234.
61. Shai SY, Harpf AE, Babbitt CJ, et al. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ Res. 2002;90:458-464.
62. Whitehead NP, Streamer M, Lusambili LI, et al. Streptomycin reduces stretch-induced membrane permeability in muscles from mdx mice. Neuromuscul Dis. 2006;16:845-854.
63. Wang Y, Shibasaki F, Mizuno K. Calcium signal-induced cofilin dephosphorylation is mediated by Slingshot via calcineurin. J Biol Chem. 2005;280:12683-12689.
64. Guinamard R, Chatelier A, Demion M, et al. Functional characterization of a Ca(2+)-activated non-selective cation channel in human atrial cardiomyocytes. J Physiol. 2004;558:75-83.
65. Guinamard R, Demion M, Magaud C, et al. Functional expression of the TRPM4 cationic current in ventricular cardiomyocytes from spontaneously hypertensive rats. Hypertension. 2006;48:587-594.
66. Delmas P. Polycystins: polymodal receptor/ion-channel cellular sensors. Pflugers Archiv Eur J Physiol. 2005;451:264-276.
67. Inoue R, Jensen LJ, Shi J, et al. Transient receptor potential channels in cardiovascular function and disease. Circulation Res. 2006;99:119-131.
68. Anyatonwu GI, Estrada M, Tian X, et al. Regulation of ryanodine receptor-dependent calcium signaling by polycystin-2. Proc Nat Acad Sci USA. 2007;104:6454-6459.
69. Wu G, Markowitz GS, Li L, et al. Cardiac defects and renal failure in mice with targeted mutations in Pkd2. Nat Genetics. 2000;24:75-78.
70. Boulter C, Mulroy S, Webb S, et al. Cardiovascular, skeletal, and renal defects in mice with a targeted disruption of the Pkd1 gene. Proc Nat Acad Sci USA. 2001;98:12174-12179.
71. Lee H, Caterina MJ. TRPV channels as thermosensory receptors in epithelial cells. Pflugers Archiv Eur J Physiol. 2005;451:160-167.
72. Iwata Y, Katanosaka Y, Arai Y, et al. A novel mechanism of myocyte degeneration involving the Ca2+-permeable growth factor-regulated channel. J Cell Biol. 2003;161:957-967.
73. Nakayama H, Wilkin BJ, Bodi I, et al. Calcineurin-dependent cardiomyopathy is activated by TRPC in the adult mouse heart. FASEB J. 2006;20:1660-1670.
74. Onohara N, Nishida M, Inoue R, et al. TRPC3 and TRPC6 are essential for angiotensin II-induced cardiac hypertrophy. EMBO J. 2006;25: 5305-5316.
75. He LP, Hewavitharana T, Soboloff J, et al. A functional link between storeoperated and TRPC channels revealed by the 3,5-bis(trifluoromethyl) pyrazole derivative, BTP2. J Biol Chem. 2005;280:10997-11006
76. Trevillyan JM, Chiou XG, Chen YW, et al. Potent inhibition of NFAT activation and T cell cytokine production by novel low molecular weight pyrazole compounds. J Biol Chem. 2001;276:48118-48126.
77. Bode F, Sachs F, Franz MR. Tarantula peptide inhibits atrial fibrillation. Nature. 2001;409:35-36.
78. Gottlieb PA, Suchyna TM, Ostrow LW, et al. Mechanosensitive ion channels as drug targets. Curr Drug Targ. 2004;3:287-295.
79. Whitehead NP, Streamer M, Lusambili LI, et al. Streptomycin reduces stretch-induced membrane permeability in muscles from mdx mice. Neuromuscular Dis. 2006;16:845-854.
80. Yeung EW, Whitehead NP, Suchyna TM, et al. Effects of stretch-activated channel blockers on [Ca2+]i and muscle damage in the mdx mouse. J Physiol. 2005;562:367-380.
81. Bowman CL, Gottlieb PA, Suchyna TM, et al. Mechanosensitive ion channels and the peptide inhibitor GsMTx-4: history, properties, mechanisms and pharmacology. Toxicon. 2007;49:249-270.
82. Suchyna TM, Tape SE, Koeppe RE, et al. Bilayer-dependent inhibition of mechanosensitive channels by neuroactive peptide enantiomers. Nature. 2004;430:235-240.
83. Suchyna TM, Johnson JH, Hamer K, et al. Identification of a peptide toxin from Grammostola spatulata spider venom that blocks cation-selective stretch-activated channels. J Gen Physiol. 2000;115:583-598.
84. Garcia ML. Ion channels: gate expectations. Nature. 2004;430:153-155.
85. Ohba T, Watanabe H, Murakami M, et al. Upregulation of TRPC1 in the development of cardiac hypertrophy. J Mol Cell Cardiol. 2007;42: 498-507.
86. Shan D, Marchase RB, Chatham JC. Overexpression of TRPC3 increases apoptosis but not necrosis in response to ischemia-reperfusion in adult mouse cardiomyocytes. Am J Physiol. 2008;294:C833-C841.
87. Touyz RM. Transient receptor potential melastatin ± and 7 channels, magnesium transport, and vascular biology: implications in hypertension. Am J Physiol. 2008;294:H1103-H1118.