Modulation of the Ca2+ permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium

Circulation Research

Volumn 97, Issue 9, 2005, Pages 908-915

  Vriens, J ^a   Owsianik, G ^a   Fisslthaler, B ^b   Suzuki, M ^d   Janssens, A ^a   Voets, T ^a   Morisseau, C ^c   Hammock, B D ^c   Fleming, I ^b   Busse, R ^b   Nilius, B ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b GOETHE UNIVERSITY   (Germany)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

Endothelium; Epoxide hydrolases; Epoxygenases; TRP channels

Indexed keywords

1 ADAMANTYL 3 CYCLO HEXYUREA; 4ALPHA PHORBOL DIDECANOATE; 5,6 EPOXY 8,11,14 ICOSATRIENOIC ACID; 8,9 EPOXYICOSATRIENOIC ACID; ARACHIDONIC ACID; CALCIUM ION; CATION CHANNEL; CYTOCHROME P450; CYTOCHROME P450 2C; CYTOCHROME P450 EPOXYGENASE; EPOXIDE HYDROLASE; EPOXYICOSATRIENOIC ACID; HYPOTONIC SOLUTION; INDOMETACIN; PHORBOL ESTER; SULFAPHENAZOLE; TRANSIENT RECEPTOR POTENTIAL CHANNEL; UNCLASSIFIED DRUG; UREA DERIVATIVE; 5,6-EPOXY-8,11,14-EICOSATRIENOIC ACID; 8,9-EPOXYEICOSATRIENOIC ACID; CALCIUM; CYTOCHROME P 450 CYP2C SUBFAMILY; CYTOCHROME P-450 CYP2C SUBFAMILY; DIHOMO GAMMA LINOLENIC ACID; DRUG DERIVATIVE; NIFEDIPINE; TRPV4 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL CELL; AORTA; ARACHIDONIC ACID METABOLISM; ARTICLE; CALCIUM TRANSPORT; CATION CHANNEL TRPV4; CELL SWELLING; CHANNEL GATING; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; HEAT TREATMENT; HYDROLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TEMPERATURE DEPENDENCE; TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; VASCULAR ENDOTHELIUM; WILD TYPE; ANIMAL; CELL CULTURE; DRUG ANTAGONISM; METABOLISM; PHYSIOLOGY;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; CALCIUM; CELLS, CULTURED; CYTOCHROME P-450 ENZYME SYSTEM; ENDOTHELIAL CELLS; EPOXIDE HYDROLASES; MICE; NIFEDIPINE; TRPV CATION CHANNELS;

EID: 27644497526     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000187474.47805.30     Document Type: Article

References (42)

1. Nilius B, Droogmans G, Wondergem R. Transient receptor potential channels in endothelium: solving the calcium entry puzzle? Endothelium. 2003;10:5-15.
2. Nilius B, Vriens J, Prenen J, Droogmans G, Voets T. TRPV4 calcium entry channel: a paradigm for gating diversity. Am J Physiol Cell Physiol. 2004;286:C195-C205.
3. Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell. 2000;103:525-535.
4. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol. 2000;2:695-702.
5. Wissenbach U, Bodding M, Freichel M, Flockerzi V. Trp12, a novel Trp related protein from kidney. FEBS Lett. 2000;485:127-134.
6. Nilius B, Prenen J, Wissenbach U, Bodding M, Droogmans G. Differential activation of the volume-sensitive cation channel TRP12 (OTRPC4) and volume-regulated anion currents in HEK-293 cells. Pflügers Arch Eur J Physiol. 2001;443:227-233.
7. Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB, Levine JD. Hypotonicity induces TRPV4-mediated nociception in rat. Neuron. 2003;39:497-511.
8. Vriens J, Watanabe H, Janssens A, Droogmans G, Voets T, Nilius B. Cell swelling, heat, and chemical agonists use distinct pathways for the activation of the cation channel TRPV4. Proc Natl Acad Sci U S A. 2004; 101:396-401.
9. Gao X, Wu L, 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. 2003;278:27129-22737.
10. -/- mice. Proc Natl Acad Sci U S A. 2003;100:13698-13703.
11. Suzuki M, Mizuno A, Kodaira K, Imai M. Impaired pressure sensation in mice lacking TRPV4. J Biol Chem. 2003;278:22664-22668.
12. Alessandri-Haber N, Dina OA, Yeh JJ, Parada CA, Reichling DB, Levine JD. Transient receptor potential vanilloid 4 is essential in chemotherapy-induced neuropathic pain in the rat. J Neurosci. 2004;24:4444-4452.
13. Guler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M. Heat-evoked activation of the ion channel, TRPV4. J Neurosci. 2002;22: 6408-6414.
14. Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B. Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem. 2002; 277:47044-47051.
15. Lee H, Iida T, Mizuno A, Suzuki M, Caterina MJ. Altered thermal selection behavior in mice lacking transient receptor potential vanilloid 4. J Neurosci. 2005;25:1304-1310.
16. 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, Nilius B. Activation of TRPV4 channels (hVRL-2/ mTRP12) by phorbol derivatives. J Biol Chem. 2002;277:13569-13577.
17. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature. 2003;424:434-438.
18. Zhao X, Yamamoto T, Newman JW, Kim IH, Watanabe T, Hammock BD, Stewart J, Pollock JS, Pollock DM, Imig JD. Soluble epoxide hydrolase inhibition protects the kidney from hypertension-induced damage. J Am Soc Nephrol. 2004;15:1244-1253.
19. Fisslthaler B, Popp R, Kiss L, Potente M, Harder DR, Fleming I, Busse R. Cytochrome P450 2C is an EDHF synthase in coronary arteries. Nature. 1999;401:493-497.
20. Campbell WB, Gebremedhin D, Pratt PF, Harder DR. Identification of epoxyeicosatrienoic acids as endothelium-derived hyperpolarizing factors. Circ Res. 1996;78:415-423.
21. Lu T, Katakam PV, VanRollins M, Weintraub NL, Spector AA, Lee HC. Dihydroxyeicosatrienoic acids are potent activators of Ca(2+)-activated K(+) channels in isolated rat coronary arterial myocytes. J Physiol. 2001;534:651-667.
22. Campbell WB, Deeter C, Gauthier KM, Ingraham RH, Falck JR, Li PL. 14,15-Dihydroxyeicosatrienoic acid relaxes bovine coronary arteries by activation of K(Ca) channels. Am J Physiol Heart Circ Physiol. 2002; 282:H1656-H1664.
23. Suh SH, Vennekens R, Manolopoulos VG, Freichel M, Schweig U, Prenen J, Flockerzi V, Droogmans G, Nilius B. Characterisation of explanted endothelial cells from mouse aorta: electrophysiology and Ca2+ signaling. Pflugers Arch. 1999;438:612-620.
24. Edgell CJ, McDonald CC, Graham JB. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci U S A. 1983;80:3734-3737.
25. Vriens J, Janssens A, Prenen J, Nilius B, Wondergem R. TRPV channels and modulation by hepatocyte growth factor/scatter factor in human hepatoblastoma (HepG2) cells. Cell Calcium. 2004;36:19-28.
26. Van Baelen K, Vanoevelen J, Callewaert G, Parys JB, De Smedt H, Raeymaekers L, Rizzuto R, Missiaen L, Wuytack F. The contribution of the SPCA1 Ca2+ pump to the Ca2+ accumulation in the Golgi apparatus of HeLa cells assessed via RNA-mediated interference. Biochem Biophys Res Commun. 2003;306:430-436.
27. Morisseau C, Goodrow MH, Newman JW, Wheelock CE, Dowdy DL, Hammock BD. Structural refinement of inhibitors of urea-based soluble epoxide hydrolases. Biochem Pharmacol. 2002;63:1599-1608.
28. Fisslthaler B, Hinsch N, Chataigneau T, Popp R, Kiss L, Busse R, Fleming I. Nifedipine increases cytochrome P4502C expression and endothelium-derived hyperpolarizing factor-mediated responses in coronary arteries. Hypertension. 2000;36:270-275.
29. Brian WR, Srivastava PK, Umbenhauer DR, Lloyd RS, Guengerich FP. Expression of a human liver cytochrome P-450 protein with tolbutamide hydroxylase activity in Saccharomyces cerevisiae. Biochemistry. 1989; 28:4993-4999.
30. Sai Y, Dai R, Yang TJ, Krausz KW, Gonzalez FJ, Gelboin HV, Shou M. Assessment of specificity of eight chemical inhibitors using cDNA-expressed cytochromes P450. Xenobiotica. 2000;30:327-343.
31. Mancy A, Dijols S, Poli S, Guengerich P, Mansuy D. Interaction of sulfaphenazole derivatives with human liver cytochromes P450 2C: molecular origin of the specific inhibitory effects of sulfaphenazole on CYP 2C9 and consequences for the substrate binding site topology of CYP 2C9. Biochemistry. 1996;35:16205-16212.
32. Yu Z, Xu F, Huse LM, Morisseau C, Draper AJ, Newman JW, Parker C, Graham L, Engler MM, Hammock BD, Zeldin DC, Kroetz DL. Soluble epoxide hydrolase regulates hydrolysis of vasoactive epoxyeicosatrienoic acids. Circ Res. 2000;87:992-998.
33. Morisseau C, Goodrow MH, Dowdy D, Zheng J, Greene JF, Sanborn JR, Hammock BD. Potent urea and carbamate inhibitors of soluble epoxide hydrolases. Proc Natl Acad Sci U S A. 1999;96:8849-8854.
34. Carroll MA, Garcia MP, Falck JR, McGiff JC. Cyclooxygenase dependency of the renovascular actions of cytochrome P450-derived arachidonate metabolites. J Pharmacol Exp Ther. 1992;260:104-109.
35. Smith GD, Gunthorpe MJ, 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, Davis JB. TRPV3 is a temperature-sensitive vanilloid receptor-lute protein. Nature. 2002;418:186-190.
36. Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, Imaizumi Y. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res. 2003;93:829-838.
37. Grimm C, Kraft R, Sauerbruch S, Schultz G, Harteneck C. Molecular and functional characterization of the melastatin-related cation channel TRPM3. J Biol Chem. 2003;278:21493-21501.
38. Fleming I. Cytochrome p450 and vascular homeostasis. Circ Res. 2001; 89:753-762.
39. Popp R, Brandes RP, Ott G, Busse R, Fleming I. Dynamic modulation of interendothelial gap junctional communication by 11,12-epoxyeicosatrienoic acid. Circ Res. 2002;90:800-806.
40. Michaelis UR, Falck JR, Schmidt R, Busse R, Fleming I. Cytochrome P4502C9-derived epoxyeicosatrienoic acids induce the expression of cyclooxygenase-2 in endothelial cells. Arterioscler Thromb Vasc Biol. 2005;25:321-326.
41. Jung O, Brandes RP, Kim IH, Schweda F, Schmidt R, Hammock BD, Busse R, Fleming I. Soluble epoxide hydrolase is a main effector of angiotensin II-induced hypertension. Hypertension. 2005;45:759-765.
42. Fang X, Weintraub NL, McCaw RB, Hu S, Harmon SD, Rice JB, Hammock BD, Spector AA. Effect of soluble epoxide hydrolase inhibition on epoxyeicosatrienoic acid metabolism in human blood vessels. Am J Physiol Heart Circ Physiol. 2004;287:H2412-H2420.