Characteristics of transient receptor potential canonical calcium-permeable channels and their relevance to vascular physiology and disease

Circulation Journal

Volumn 77, Issue 3, 2013, Pages 570-579

  Beech, David J ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Calcium ion; Endothelial cells; Perivascular adipocytes; Sodium ion; Vascular smooth muscle cells

Indexed keywords

ACETYLCHOLINE; ARACHIDONIC ACID; ASCORBIC ACID; BRADYKININ; CALCIUM CHANNEL; CALCIUM ION; CHOLECYSTOKININ; CYCLIC AMP; DIACYLGLYCEROL; ENDOTHELIN 1; EPIDERMAL GROWTH FACTOR; GANGLIOSIDE; GLUTAMIC ACID; GUANOSINE TRIPHOSPHATE; HISTAMINE; LYSOPHOSPHATIDYLCHOLINE; NITRIC OXIDE; OMEGA 3 FATTY ACID; POLYCYSTIN 2; PREGNENOLONE; PROSTAGLANDIN E2; PSYCHOSINE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 1; TRANSIENT RECEPTOR POTENTIAL CHANNEL 3; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; TRANSIENT RECEPTOR POTENTIAL CHANNEL 5; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; UNINDEXED DRUG; VASCULOTROPIN;

BLOOD VESSEL FUNCTION; DISEASE ASSOCIATION; GENE EXPRESSION; HUMAN; HYPERGLYCEMIA; HYPERTENSION; MEMBRANE PERMEABILITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; REVIEW; VASCULAR DISEASE; VASCULARIZATION;

CALCIUM CHANNELS; CALCIUM SIGNALING; CARDIOVASCULAR DISEASES; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; ENDOTHELIUM, VASCULAR; HUMANS; MUSCLE, SMOOTH, VASCULAR; SIGNAL TRANSDUCTION; TRPC CATION CHANNELS;

EID: 84874400174     PISSN: 13469843     EISSN: 13474820     Source Type: Journal    
DOI: 10.1253/circj.CJ-13-0154     Document Type: Review

References (70)

1. Berridge MJ, Bootman MD, Roderick HL. Calcium signalling: Dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 2003; 4: 517-529.
2. Clapham DE. Calcium signaling. Cell 2007; 131: 1047-1058.
3. Triggle DJ. Calcium channel antagonists: Clinical uses - past, present and future. Biochem Pharmacol 2007; 74: 1-9.
4. Beech DJ. Ion channel switching and activation in smooth-muscle cells of occlusive vascular diseases. Biochem Soc Trans 2007; 35: 890-894.
5. Moran MM, McAlexander MA, Biro T, Szallasi A. Transient receptor potential channels as therapeutic targets. Nat Rev Drug Discov 2011; 10: 601-620.
6. Damann N, Voets T, Nilius B. TRPs in our senses. Curr Biol 2008; 18: R880-R889.
7. 2+ exchanger. J Biol Chem 2004; 279: 13696-13704.
8. Abramowitz J, Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 2009; 23: 297-328.
9. Hofmann T, Schaefer M, Schultz G, Gudermann T. Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci USA 2002; 99: 7461-7466.
10. 2+ stores stimulates the translocation of vanilloid transient receptor potential 4-C1 heteromeric channels to the plasma membrane. Arterioscler Thromb Vasc Biol 2010; 30: 2249-2255.
11. Tsiokas L. Function and regulation of TRPP2 at the plasma membrane. Am J Physiol Renal Physiol 2009; 297: F1-F9.
12. Beech DJ. Orai1 calcium channels in the vasculature. Pflugers Arch 2012; 463: 635-647.
13. Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE. Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 2004; 6: 709-720.
14. Odell AF, Scott JL, Van Helden DF. Epidermal growth factor induces tyrosine phosphorylation, membrane insertion, and activation of transient receptor potential channel 4. J Biol Chem 2005; 280: 37974-37987.
15. Monet M, Francoeur N, Boulay G. Involvement of phosphoinositide 3-kinase and pten protein in mechanism of activation of TRPC6 protein in vascular smooth muscle cells. J Biol Chem 2012; 287: 17672-17681.
16. Xu SZ, Muraki K, Zeng F, Li J, Sukumar P, Shah S, et al. A sphingosine-1-phosphate-activated calcium channel controlling vascular smooth muscle cell motility. Circ Res 2006; 98: 1381-1389.
17. Xu SZ, Sukumar P, Zeng F, Li J, Jairaman A, English A, et al. TRPC channel activation by extracellular thioredoxin. Nature 2008; 451: 69-72.
18. Storch U, Forst AL, Philipp M, Gudermann T, Mederos y Schnitzler M. Transient receptor potential channel 1 (TRPC1) reduces calcium permeability in heteromeric channel complexes. J Biol Chem 2012; 287: 3530-3540.
19. Beech DJ. TRPC1: Store-operated channel and more. Pflugers Arch 2005; 451: 53-60.
20. Winn MP, Conlon PJ, Lynn KL, Farrington MK, Creazzo T, Hawkins AF, et al. A mutation in the TRPC6 cation channel causes familial focal segmental glomerulosclerosis. Science 2005; 308: 1801-1804.
21. Yu Y, Keller SH, Remillard CV, Safrina O, Nicholson A, Zhang SL, et al. A functional single-nucleotide polymorphism in the TRPC6 gene promoter associated with idiopathic pulmonary arterial hypertension. Circulation 2009; 119: 2313-2322.
22. Jung C, Gene GG, Tomas M, Plata C, Selent J, Pastor M, et al. A gain-of-function SNP in TRPC4 cation channel protects against myocardial infarction. Cardiovasc Res 2011; 91: 465-471.
23. Sukumar P, Sedo A, Li J, Wilson LA, O'Regan D, Lippiat JD, et al. Constitutively active TRPC channels of adipocytes confer a mechanism for sensing dietary fatty acids and regulating adiponectin. Circ Res 2012; 111: 191-200.
24. Liu Y, Xu Y, Thilo F, Friis UG, Jensen BL, Scholze A, et al. Erythropoietin increases expression and function of transient receptor potential canonical 5 channels. Hypertension 2011; 58: 317-324.
25. Weissmann N, Dietrich A, Fuchs B, Kalwa H, Ay M, Dumitrascu R, et al. Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc Natl Acad Sci USA 2006; 103: 19093-19098.
26. Kumar B, Dreja K, Shah SS, Cheong A, Xu SZ, Sukumar P, et al. Upregulated TRPC1 channel in vascular injury in vivo and its role in human neointimal hyperplasia. Circ Res 2006; 98: 557-563.
27. 2+ current impairs agonist-dependent vasorelaxation in TRP4-/mice. Nat Cell Biol 2001; 3: 121-127.
28. 2+ entry in endothelial cells. J Biol Chem 2004; 279: 20941-20949.
29. Smedlund K, Tano JY, Vazquez G. The constitutive function of native TRPC3 channels modulates vascular cell adhesion molecule-1 expression in coronary endothelial cells through nuclear factor κB signaling. Circ Res 2010; 106: 1479-1488.
30. Yu PC, Gu SY, Bu JW, Du JL. TRPC1 is essential for in vivo angiogenesis in zebrafish. Circ Res 2010; 106: 1221-1232.
31. Paez Espinosa EV, Murad JP, Ting HJ, Khasawneh FT. Mouse transient receptor potential channel 6: Role in hemostasis and thrombogenesis. Biochem Biophys Res Commun 2012; 417: 853-856.
32. 2+ influx. Circ Res 2005; 96: 1282-1290.
33. Tauseef M, Knezevic N, Chava KR, Smith M, Sukriti S, Gianaris N, et al. TLR4 activation of TRPC6-dependent calcium signaling mediates endotoxin-induced lung vascular permeability and inflammation. J Exp Med 2012; 209: 1953-1968.
34. Koenig S, Schernthaner M, Maechler H, Kappe CO, Glasnov TN, Hoefler G, et al. A TRPC3 blocker, ethyl-1-(4-(2,3,3-trichloroacrylamide)phenyl)-5-(trifluoromethyl)-1 h-pyrazole-4-carboxylate (pyr3), prevents stent-induced arterial remodeling. J Pharmacol Exp Ther 2013; 344: 33-40.
35. Weissmann N, Sydykov A, Kalwa H, Storch U, Fuchs B, Mederos y Schnitzler M, et al. Activation of TRPC6 channels is essential for lung ischaemia-reperfusion induced oedema in mice. Nat Commun 2012; 3: 649.
36. Suresh Babu S, Wojtowicz A, Freichel M, Birnbaumer L, Hecker M, Cattaruzza M. Mechanism of stretch-induced activation of the mechanotransducer zyxin in vascular cells. Sci Signal 2012; 5: ra91.
37. Noorani MM, Noel RC, Marrelli SP. Upregulated TRPC3 and downregulated TRPC1 channel expression during hypertension is associated with increased vascular contractility in rat. Front Physiol 2011; 2: 42.
38. Zeng F, Xu SZ, Jackson PK, McHugh D, Kumar B, Fountain SJ, et al. Human TRPC5 channel activated by a multiplicity of signals in a single cell. J Physiol 2004; 559: 739-750.
39. Graham S, Ding M, Ding Y, Sours-Brothers S, Luchowski R, Gryczynski Z, et al. Canonical transient receptor potential 6 (TRPC6), a redox-regulated cation channel. J Biol Chem 2010; 285: 23466-23476.
40. Naylor J, Al-Shawaf E, McKeown L, Manna PT, Porter KE, O'Regan D, et al. TRPC5 channel sensitivities to antioxidants and hydroxylated stilbenes. J Biol Chem 2011; 286: 5078-5086.
41. Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, et al. Nitric oxide activates TRP channels by cysteine s-nitrosylation. Nat Chem Biol 2006; 2: 596-607.
42. Shen B, Kwan HY, Ma X, Wong CO, Du J, Huang Y, et al. Camp activates TRPC6 channels via the phosphatidylinositol 3-kinase (PI3K)-protein kinase B (PKB)-mitogen-activated protein kinase kinase (MEK)-ERK1/2 signaling pathway. J Biol Chem 2011; 286: 19439-19445.
43. Beech DJ. Integration of transient receptor potential canonical channels with lipids. Acta Physiol (Oxf) 2012; 204: 227-237.
44. Sung TS, Jeon JP, Kim BJ, Hong C, Kim SY, Kim J, et al. Molecular determinants of PKA-dependent inhibition of TRPC5 channel. Am J Physiol Cell Physiol 2011; 301: C823-C832.
45. Kwan HY, Huang Y, Yao X. Regulation of canonical transient receptor potential isoform 3 (TRPC3) channel by protein kinase G. Proc Natl Acad Sci USA 2004; 101: 2625-2630.
46. Hisatsune C, Kuroda Y, Nakamura K, Inoue T, Nakamura T, Michikawa T, et al. Regulation of TRPC6 channel activity by tyrosine phosphorylation. J Biol Chem 2004; 279: 18887-18894.
47. Park HW, Kim JY, Choi SK, Lee YH, Zeng W, Kim KH, et al. Serine-threonine kinase with-no-lysine 4 (WNK4) controls blood pressure via transient receptor potential canonical 3 (TRPC3) in the vasculature. Proc Natl Acad Sci USA 2011; 108: 10750-10755.
48. Shi J, Mori E, Mori Y, Mori M, Li J, Ito Y, et al. Multiple regulation by calcium of murine homologues of transient receptor potential proteins TRPC6 and TRPC7 expressed in HEK293 cells. J Physiol 2004; 561: 415-432.
49. Trebak M, Hempel N, Wedel BJ, Smyth JT, Bird GS, Putney JW Jr. Negative regulation of TRPC3 channels by protein kinase C-mediated phosphorylation of serine 712. Mol Pharmacol 2005; 67: 558-563.
50. Venkatachalam K, Zheng F, Gill DL. Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J Biol Chem 2003; 278: 29031-29040.
51. Balbuena P, Li W, Rzigalinski BA, Ehrich M. Malathion/oxon and lead acetate increase gene expression and protein levels of transient receptor potential canonical channel subunits TRPC1 and TRPC4 in rat endothelial cells of the blood-brain barrier. Int J Toxicol 2012; 31: 238-249.
52. Jeon JP, Hong C, Park EJ, Jeon JH, Cho NH, Kim IG, et al. Selective Gαi subunits as novel direct activators of transient receptor potential canonical (TRPC)4 and TRPC5 channels. J Biol Chem 2012; 287: 17029-17039.
53. Schaefer M, Plant TD, Obukhov AG, Hofmann T, Gudermann T, Schultz G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J Biol Chem 2000; 275: 17517-17526.
54. Obukhov AG, Nowycky MC. TRPC5 activation kinetics are modulated by the scaffolding protein ezrin/radixin/moesin-binding phosphoprotein-50 (EBP50). J Cell Physiol 2004; 201: 227-235.
55. Al-Shawaf E, Tumova S, Naylor J, Majeed Y, Li J, Beech DJ. GVI phospholipase A2 role in the stimulatory effect of sphingosine-1-phosphate on TRPC5 cationic channels. Cell Calcium 2011; 50: 343-350.
56. Majeed Y, Amer MS, Agarwal AK, McKeown L, Porter KE, O'Regan DJ, et al. Stereo-selective inhibition of transient receptor potential TRPC5 cation channels by neuroactive steroids. Br J Pharmacol 2011; 162: 1509-1520.
57. Miehe S, Crause P, Schmidt T, Lohn M, Kleemann HW, Licher T, et al. Inhibition of diacylglycerol-sensitive TRPC channels by synthetic and natural steroids. PLoS One 2012; 7: e35393.
58. Jung S, Muhle A, Schaefer M, Strotmann R, Schultz G, Plant TD. Lanthanides potentiate TRPC5 currents by an action at extracellular sites close to the pore mouth. J Biol Chem 2003; 278: 3562-3571.
59. El Hadri K, Mahmood DF, Couchie D, Jguirim-Souissi I, Genze F, Diderot V, et al. Thioredoxin-1 promotes anti-inflammatory macrophages of the M2 phenotype and antagonizes atherosclerosis. Arterioscler Thromb Vasc Biol 2012; 32: 1445-1452.
60. 2+ channel to maintain endothelial integrity. Proc Natl Acad Sci USA 2010; 107: 19308-19313.
61. Wong CO, Sukumar P, Beech DJ, Yao X. Nitric oxide lacks direct effect on TRPC5 channels but suppresses endogenous TRPC5-containing channels in endothelial cells. Pflugers Arch 2010; 460: 121-130.
62. 2+entry associated with metabolic syndrome and coronary atherosclerosis. Cardiovasc Res 2010; 85: 631-640.
63. Niethammer P, Grabher C, Look AT, Mitchison TJ. A tissue-scale gradient of hydrogen peroxide mediates rapid wound detection in zebrafish. Nature 2009; 459: 996-999.
64. 2+ channel in intestinal epithelial cells and regulates early mucosal restitution after wounding. Am J Physiol Gastrointest Liver Physiol 2006; 290: G782-G792.
65. Davis J, Burr AR, Davis GF, Birnbaumer L, Molkentin JD. A TRPC6- dependent pathway for myofibroblast transdifferentiation and wound healing in vivo. Dev Cell 2012; 23: 705-715.
66. 2+ entry via TRPC channels is necessary for thrombininduced NF-κB activation in endothelial cells through AMP-activated protein kinase and protein kinase Cδ. J Biol Chem 2009; 284: 563-574.
67. Eder P, Molkentin JD. TRPC channels as effectors of cardiac hypertrophy. Circ Res 2011; 108: 265-272.
68. Tai Y, Feng S, Ge R, Du W, Zhang X, He Z, et al. TRPC6 channels promote dendritic growth via the CaMKIV-CREB pathway. J Cell Sci 2008; 121: 2301-2307.
69. Tian D, Jacobo SM, Billing D, Rozkalne A, Gage SD, Anagnostou T, et al. Antagonistic regulation of actin dynamics and cell motility by TRPC5 and TRPC6 channels. Sci Signal 2010; 3: ra77.
70. Zhang W, Halligan KE, Zhang X, Bisaillon JM, Gonzalez-Cobos JC, Motiani RK, et al. Orai1-mediated I (CRAC) is essential for neointima formation after vascular injury. Circ Res 2011; 109: 534-542.