TRPV4 calcium entry channel: A paradigm for gating diversity

American Journal of Physiology - Cell Physiology

Volumn 286, Issue 2 55-2, 2004, Pages

  Nilius, Bernd ^a   Vriens, Joris ^a   Prenen, Jean ^a   Droogmans, Guy ^a   Voets, Thomas ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Calcium channels; Transient receptor potential; Vanilloid receptor

Indexed keywords

4ALPHA PHORBOL; ANANDAMIDE; ARACHIDONIC ACID; CALCIUM CHANNEL; CANNABINOID; CYTOCHROME P450; PROTEIN; PROTEIN TRPV4; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1;

CALCIUM TRANSPORT; CELL SWELLING; CHANNEL GATING; HUMAN; MAMMAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RECEPTOR POTENTIAL; REVIEW; SEQUENCE HOMOLOGY; STIMULATION;

MAMMALIA;

EID: 0742288219     PISSN: 03636143     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajpcell.00365.2003     Document Type: Review

References (106)

1. Abe J, Okazawa M, Adachi R, Matsumura K, and Kobayashi S. Primary cold-sensitive neurons in acutely dissociated cells of rat hypothalamus. Neurosci Lett 342: 29-32, 2003.
2. Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB, and Levine JD. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 39: 497-511, 2003.
3. Basavappa S, Pedersen SF, Jorgensen NK, Ellory JC, and Hoffmann EK. Swelling-induced arachidonic acid release via the 85-kDa cPLA2 in human neuroblastoma cells. J Neurophysiol 79: 1441-1449, 1998.
4. Benham CD, Davis JB, and Randall AD. Vanilloid and TRP channels: a family of lipid-gated cation channels. Neuropharmacology 42: 873-888, 2002.
5. Boulant JA. Role of the preoptic-anterior hypothalamus in thermoregulation and fever. Clin Infect Dis 31, Suppl 5: S157-S161, 2000.
6. Bourque CW and Oliet SH. Osmoreceptors in the central nervous system. Annu Rev Physiol 59: 601-619, 1997.
7. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288: 306-313, 2000.
8. Caterina MJ, Rosen TA, Tominaga M, Brake AJ, and Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398: 436-441, 1999.
9. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
10. Chung MK, Lee H, and Caterina MJ. Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278: 32037-32046, 2003.
11. Clapham DE, Runnels LW, and Strubing C. The trp ion channel family. Nat Rev Neurosci 2: 387-396, 2001.
12. Colbert HA, Smith TL, and Bargmann CI. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17: 8259-8269, 1997.
13. Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, and Gilula NB. Molecular characterization of an enzyme that degrades neuromodulatory fatty-acid amides. Nature 384: 83-87, 1996.
14. Delany NS, Hurle M, Facer P, Alnadaf T, Plumpton C, Kinghorn I, See CG, Costigan M, Anand P, Woolf CJ, Crowther D, Sanseau P, and Tate SN. Identification and characterization of a novel human vanilloid receptor-like protein, VRL-2. Physiol Genomics 4: 165-174, 2001.
15. Di Marzo V, Fontana A, Cadas H, Schinelli S, Cimino G, Schwartz JC, and Piomelli D. Formation and inactivation of endogenous cannabinoid anandamide in central neurons. Nature 372: 686-691, 1994.
16. Di Marzo V, Melck D, Bisogno T, and De Petrocellis L. Endocannabinoids: endogenous cannabinoid receptor ligands with neuromodulatory action. Trends Neurosci 21: 521-528, 1998.
17. + conduction and selectivity. Science 280: 69-77, 1998.
18. + channel mediates regulatory volume decrease response in a human bronchial epithelial cell line. Am J Physiol Cell Physiol 283: C1705-C1714, 2002.
19. Fleming I. Cytochrome P450 enzymes in vascular homeostasis. Circ Res 89: 753-762, 2001.
20. Freund TF, Katona I, and Piomelli D. Role of endogenous cannabinoids in synaptic signaling. Physiol Rev 83: 1017-1066, 2003.
21. Gao X, Wu L, and O'Neil RG. Temperature-modulated diversity of TRPV4 channel gating: activation by physical stresses and phorbol ester derivatives through protein kinase C-dependent and -independent pathways. J Biol Chem 278: 27129-22737, 2003.
22. Garcia-Anoveros J and Corey DP. The molecules of mechanosensation. Annu Rev Neurosci 20: 567-594, 1997.
23. Garcia-Martinez C, Morenilla-Palao C, Planells-Cases R, Merino JM, and Ferrer-Montiel A. Identification of an aspartic residue in the P-loop of the vanilloid receptor that modulates pore properties. J Biol Chem 275: 32552-32558, 2000.
24. Grainger J and Boachie Ansah G. Anandamide-induced relaxation of sheep coronary arteries: the role of the vascular endothelium, arachidonic acid metabolites and potassium channels. Br J Pharmacol 134: 1003-1012, 2001.
25. Greene CC, McMillan PM, Barker SE, Kurnool P, Lomax MI, Burmeister M, and Lesperance MM. DFNA25, a novel locus for dominant nonsyndromic hereditary hearing impairment, maps to 12q21-24. Am J Hum Genet 68: 254-260, 2001.
26. Güler A, Lee H, Shimizu I, and Caterina MJ. Heat-evoked activation of TRPV4 (VR-OAC). J Neurosci 22: 6408-6414, 2002.
27. Gunthorpe MJ, Benham CD, Randall A, and Davis JB. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol Sci 23: 183-191, 2002.
28. 2+-permeable channel activated by changes in redox status confers susceptibility to cell death. Mol Cell 9: 163-173, 2002.
29. Harris D, McCulloch AI, Kendall DA, and Randall MD. Characterization of vasorelaxant response to anandamide in the rat mesenteric arterial bed. J Physiol 539: 893-902, 2002.
30. Hayes P, Meadows HJ, Gunthorpe MJ, Harries MH, Duckworth DM, Cairns W, Harrison DC, Clarke CE, Ellington K, Prinjha RK, Barton AJ, Medhurst AD, Smith GD, Topp S, Murdock P, Sanger GJ, Terrett J, Jenkins O, Benham CD, Randall AD, Gloger IS, and Davis JB. Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain 88: 205-215, 2000.
31. 3-responsive epithelia. J Biol Chem 274: 8375-8378, 1999.
32. 2+ channels TRPV5 and TRPV6. EMBO J 22: 776-785, 2003.
33. Hori A, Minato K, and Kobayashi S. Warming-activated channels of warm-sensitive neurons in rat hypothalamic slices. Neurosci Lett 275: 93-96, 1999.
34. Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D, and Oh U. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci USA 97: 6155-6160, 2000.
35. Jarai Z, Wagner JA, Goparaju SK, Wang L, Razdan RK, Sugiura T, Zimmer AM, Bonner TI, Zimmer A, and Kunos G. Cardiovascular effects of 2-arachidonoyl glycerol in anesthetized mice. Hypertension 35: 679-684, 2000.
36. Jarai Z, Wagner JA, Varga K, Lake KD, Compton DR, Martin BR, Zimmer AM, Bonner TI, Buckley NE, Mezey E, Razdan RK, Zimmer A, and Kunos G. Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proc Natl Acad Sci USA 96: 14136-14141, 1999.
37. Jia Y, McLeod RL, Wang X, Parra LE, Egan RW, and Hey JA. Anandamide induces cough in conscious guinea-pigs through VRI receptors. Br J Pharmacol 137: 831-836, 2002.
38. Jordt SE and Julius D. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108: 421-430, 2002.
39. Jung J, Lee SY, Hwang SW, Cho H, Shin J, Kang YS, Kim S, and Oh U. Agonist recognition sites in the cytosolic tails of vanilloid receptor 1. J Biol Chem 277: 44448-44454, 2002.
40. Kazanietz MG. Novel "nonkinase" phorbol ester receptors: the C1 domain connection. Mol Pharmacol 61: 759-767, 2002.
41. Kim J, Chung DY, Park D, Choix S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, and Kim C. A TRPV family ion channel required for hearing in Drosophila. Nature 424: 81-84, 2003.
42. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, and Heller S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525-535, 2000.
43. Littleton JT and Ganetzky B. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26: 35-43, 2000.
44. Maccarrone M, Bari M, Lorenzon T, Bisogno T, Di Marzo V, and Finazzi-Argo A. Anandamide uptake by human endothelial cells and its regulation by nitric oxide. J Biol Chem 275: 13484-13492, 2000.
45. Mechoulam R, Fride E, and DiMarzo V. Endocannabinoids. Eur J Pharmacol 359: 1-18, 1998.
46. Minson CT, Berry LT, and Joyner MJ. Nitric oxide and neurally mediated regulation of skin blood flow during local heating. J Appl Physiol 91: 1619-1626, 2001.
47. Mizuno A, Matsumoto N, Imai M, and Suzuki M. Impaired osmotic sensation in mice lacking TRPV4. Am J Physiol Cell Physiol 285: C96-C101, 2003.
48. Montell C. Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Science's STKE July 10, 2001; 10.1126/stke.2001.90.rel.
49. Montell C, Birnbaumer L, and Flockerzi V. The TRP channels, a remarkable functional family. Cell 108: 595-598, 2002.
50. Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham D, Harteneck C, Heller S, Julius D, Kojima I, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu S, and Zhu MX. A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9: 229-231, 2002.
51. Mutai H and Heller S. Vertebrate and invertebrate TRPV-Iike mechanoreceptor. Cell Calcium 33: 471-478, 2003.
52. 2+ entry by protein kinase C and calmodulin. Proc Natl Acad Sci USA 98: 3600-3605, 2001.
53. Nilius B, Droogmans G, and Wondergem R. TRP channels in endothelium: solving the calcium entry puzzle? Endothelium 10: 5-15, 2003.
54. 2+ channels ECaC1 and ECaC2 (TRPV5 and TRPV6). Role of the intracellular loop located between transmembrane segments 2 and 3. J Biol Chem 277: 30852-30858, 2002.
55. Nilius B, Prenen J, Wissenbach U, Bodding M, and Droogmans G. Differential activation of the volume-sensitive cation channel TRP12 (OTRPC4) and volume-regulated anion currents in HEK-293 cells. Pflügers Arch 443: 227-233, 2001.
56. 2+ channel. J Biol Chem 276: 1020-1025, 2001.
57. Olah Z, Karai L, and Iadarola MJ. Protein kinase Cα is required for vanilloid receptor 1 activation. Evidence for multiple signaling pathways. J Biol Chem 277: 35752-35759, 2002.
58. + channel. EMBO J 17: 4283-4290, 1998.
59. 2 but not the γ isoform in Ehrlich ascites tumor cells. Eur J Biochem 267: 5531-5539, 2000.
60. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, and Patapoutian A. A heat-sensitive TRP channel expressed in keratinocytes. Science 296: 2046-2049, 2002.
61. Peng JB, Brown EM, and Hediger MA. Structural conservation of the genes encoding CaT1, CaT2, and related cation channels. Genomics 76: 99-109, 2001.
62. Peng JB, Chen XZ, Berger UV, Vassilev PM, Brown EM, and Hediger MA. A rat kidney-specific calcium transporter in the distal nephron. J Biol Chem 275: 28186-28194, 2000.
63. Peng JB, Chen XZ, Berger UV, Vassilev PM, Tsukaguchi H, Brown EM, and Hediger MA. Molecular cloning and characterization of a channel-like transporter mediating intestinal calcium absorption. J Biol Chem 274: 22739-22746, 1999.
64. Peng JB, Chen XZ, Berger UV, Weremowicz S, Morton CC, Vassilev PM, Brown EM, and Hediger MA. Human calcium transport protein CaT1. Biochem Biophys Res Commun 278: 326-332, 2000.
65. Peng JB and Hediger MA. A family of calcium-permeable channels in the kidney: distinct roles in renal calcium handling. Curr Opin Nephrol Hypertens 11: 555-561, 2002.
66. Piomelli D. The ligand that came from within. Trends Pharmacol Sci 22: 17-19, 2001.
67. Premkumar LS and Ahern GP. Induction of vanilloid receptor channel activity by protein kinase C. Nature 408: 985-990, 2000.
68. 2 binding site as a determinant of capsaicin receptor sensitivity. Science 300: 1284-1288, 2003.
69. Randall MD and Kendall DA. Anandamide and endothelium-derived hyperpolarizing factor act via a common vasorelaxant mechanism in rat mesentery. Eur J Pharmacol 346: 51-53, 1998.
70. Randall MD and Kendall DA. Endocannabinoids: a new class of vasoactive substances. Trends Pharmacol Sci 19: 55-58, 1998.
71. Roman RJ. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 82: 131-185, 2002.
72. Smart D, Gunthorpe MJ, Jerman JC, Nasir S, Gray J, Muir AI, Chambers JK, Randall AD, and Davis JB. The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). Br J Pharmacol 129: 227-230, 2000.
73. Smith GD, Gunthorpe J, Kelsell RE, Hayes PD, Reilly P, Facer P, Wright JE, Jerman JC, Walhin JP, Ooi L, Egerton J, Charles KJ, Smart D, Randall AD, Anand P, and Davis JB. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418: 186-190, 2002.
74. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, and Plant TD. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2: 695-702, 2000.
75. 2+-dependent potentiation of the nonselective cation channel TRPV4 is mediated by a carboxy terminal calmodulin binding site. J Biol Chem 278: 26541-26549, 2003.
76. Suzuki M, Mizuno A, Kodaira K, and Imai M. Impaired pressure sensation with mice lacking TRPV4. J Biol Chem 270: 22664-22668, 2003.
77. Szallasi A and Blumberg PM. Vanilloid (capsaicin) receptors and mechanisms. Pharmacol Rev 51: 159-212, 1999.
78. Szallasi A, Szabo T, Biro T, Modarres S, Blumberg PM, Krause JE, Cortright DN, and Appendino G. Resiniferatoxin-type phorboid vanilloids display capsaicin-like selectivity at native vanilloid receptors on rat DRG neurons and at the cloned vanilloid receptor VR1. Br J Pharmacol 128: 428-434, 1999.
79. -/- mice interferes with increase in lung microvascular permeability. Circ Res 91: 70-76, 2002.
80. Tobin DM, Madsen DM, Kahn Kirby A, Peckol EL, Moulder G, Barstead R, Maricq AV, and Bargmann CI. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35: 307-318, 2002.
81. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, and Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531-543, 1998.
82. Toth A, Kedei N, Wang Y, and Blumberg PM. Arachidonyl dopamine as a ligand for the vanilloid receptor VR1 of the rat. Life Sci 73: 487-498, 2003.
83. Travis KA, Bockholt HJ, Zardetto Smith AM, and Johnson AK. In vitro thermosensitivity of the midline thalamus. Brain Res 686: 17-22, 1995.
84. Ueda N. Endocannabinoid hydrolases. Prostaglandins Other Lipid Mediat 68-69: 521-534, 2002.
85. Vellani V, Mapplebeck S, Moriondo A, Davis JB, and McNaughton PA. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J Physiol 534: 813-825, 2001.
86. 2+ channel. J Biol Chem 275: 3963-3969, 2000.
87. 2+ channel ECaC by extracellular pH. Pflügers Arch 442: 237-242, 2001.
88. Vennekens R, Prenen J, Hoenderop JG, Bindels RJ, Droogmans G, and Nilius B. Pore properties and ionic block of the rabbit epithelial calcium channel expressed in HEK 293 cells. J Physiol 530: 183-191, 2001.
89. 2+-dependent gating and strong inward rectification of the cation channel TRPV6. J Gen Physiol 121: 245-260, 2003.
90. Voets T, Prenen J, Fleig A, Vennekens R, Watanabe H, Hoenderop JGJ, Bindels RJM, Droogmans G, Penner R, and Nilius B. CaT1 and the calcium release-activated calcium channel manifest distinct pore properties. J Biol Chem 276: 47767-47770, 2001.
91. Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, Bödding M, Droogmans G, and Nilius B. Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277: 33704-33710, 2002.
92. a. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, and Nilius B. Cell swelling, heat and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Nad Acad Sci USA. In press.
93. Wagner JA, Varga K, Jarai Z, and Kunos G. Mesenteric vasodilation mediated by endothelial anandamide receptors. Hypertension 33, Suppl S: 429-434, 1999.
94. Wagner JA, Varga K, and Kunos G. Cardiovascular actions of cannabinoids and their generation during shock. J Mol Med 76: 824-836, 1998.
95. Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, Vriens J, Cairns W, Wissenbach U, Prenen J, Flockerzi V, Droogmans G, Benham CD, and Nilius B. Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277: 13569-13577, 2002.
96. 2+. Cell Calcium 33: 489-495, 2003.
97. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, and Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424: 434-438, 2003.
98. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, and Nilius B. Heat-evoked activation of TRPV4 channels in an HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277: 47044-47051, 2002.
99. Wilson RI and Nicoll RA. Endocannabinoid signaling in the brain. Science 296: 678-682, 2002.
100. Wissenbach U, Bodding M, Freichel M, and Flockerzi V. Trp12, a novel Trp related protein from kidney. FEBS Lett 485: 127-134, 2000.
101. Xu H, Zhao H, Tian W, Yoshida K, Roullet JB, and Cohen DM. Regulation of a TRP channel by tyrosine phosphorylafion: Src family kinase-dependent phosphorylation of TRPV4 on Y253 mediates its response to hypotonic stress. J Biol Chem 278: 11520-11527, 2003.
102. Xu HX, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y, DiStefano PS, Curtis R, and Clapham DE. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418: 181-186, 2002.
103. Yuspa SH, Kilkenny AE, Steinert PM, and Roop DR. Expression of murine epidermal differentiation markers is tightly regulated by restricted extracellular calcium concentrations in vitro. J Cell Biol 109: 1207-1217, 1989.
104. + channel-Fab complex at 2.0 Å resolution. Nature 414: 43-48, 2001.
105. Zygmunt PM, Julius I, Di Marzo I, and Hogestatt ED. Anandamide - the other side of the coin. Trends Pharmacol Sci 21: 43-44, 2000.
106. Zygmunt PM, Petersson J, Andersson DA, Chuang H, Sorgard M, Di Marzo V, Julius D, and Hogestatt ED. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400: 452-457, 1999.