Cytochrome P450-derived epoxyeicosatrienoic acids and pulmonary hypertension: Central role of transient receptor potential C6 channels

Journal of Cardiovascular Pharmacology

Volumn 57, Issue 2, 2011, Pages 140-147

  Loot, Annemarieke E ^a   Fleming, Ingrid ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

calcium signaling; endothelium derived hyperpolarizing factor; epoxyeicosatrienoic acids; transient receptor potential channel

Indexed keywords

11,12 EPOXY 5,8,14 ICOSATRIENOIC ACID; ARACHIDONIC ACID; CALCIUM CHANNEL; CYTOCHROME P450 2C; CYTOCHROME P450 4A; EPOXIDE HYDROLASE; EPOXYICOSATRIENOIC ACID; NITRIC OXIDE; PROSTAGLANDIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 6; UNCLASSIFIED DRUG; VANILLOID RECEPTOR;

BLOOD VESSEL TONE; CALCIUM TRANSPORT; CELL ACTIVATION; CELL HYPOXIA; CELL LEVEL; CELL METABOLISM; CONFERENCE PAPER; ENZYME ACTIVITY; GENE DELETION; HUMAN; LUNG VASOCONSTRICTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; SYSTEMIC CIRCULATION;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; CYTOCHROME P-450 ENZYME SYSTEM; ENZYME ACTIVATION; HUMANS; HYPERTENSION, PULMONARY; MICE; TRPC CATION CHANNELS;

EID: 79951551112     PISSN: 01602446     EISSN: None     Source Type: Journal    
DOI: 10.1097/FJC.0b013e3181ed088d     Document Type: Conference Paper

References (66)

1. von Euler US, Liljestrand G. Observations on the pulmonary arterial blood pressure in the cat. Acta Physiol Scand. 1946;12:301-320.
2. Sommer N, Dietrich A, Schermuly RT, et al. Regulation of hypoxic pulmonary vasoconstriction: basic mechanisms. Eur Respir J. 2008;32: 1639-1651.
3. Weir EK, Archer SL. Counterpoint: hypoxic pulmonary vasoconstriction is not mediated by increased production of reactive oxygen species. J Appl Physiol. 2006;101:995-998.
4. Ward JPT. Point: hypoxic pulmonary vasoconstriction is mediated by increased production of reactive oxygen species. J Appl Physiol. 2006; 101:993-995.
5. Archer SL, Reeve HL, Michelakis E, et al. O2 sensing is preserved in mice lacking the gp91 phox subunit of NADPH oxidase. Proc Natl Acad Sci U S A. 1999;96:7944-7949. (Pubitemid 29328387)
6. Li S, Tabar SS, Malec V, et al. NOX4 regulates ROS levels under normoxic and hypoxic conditions, triggers proliferation, and inhibits apoptosis in pulmonary artery adventitial fibroblasts. Antioxid Redox Signal. 2008;10:1687-1698.
7. Ahmad M, Kelly MR, Zhao X, et al. Roles for Nox4 in the contractile response of bovine pulmonary arteries to hypoxia. Am J Physiol Heart Circ Physiol. 2010;298:H1879-H1888.
8. Weissmann N, Sommer N, Schermuly RT, et al. Oxygen sensors in hypoxic pulmonary vasoconstriction. Cardiovasc Res. 2006;71: 620-629. (Pubitemid 44848000)
9. Fleming I, Michaelis UR, Bredenkotter D, et al. Endothelium-derived hyperpolarizing factor synthase (Cytochrome P450 2C9) is a functionally significant source of reactive oxygen species in coronary arteries. Circ Res. 2001;88:44-51. (Pubitemid 32064081)
10. Keseru B, Barbosa-Sicard E, Popp R, et al. Epoxyeicosatrienoic acids and the soluble epoxide hydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J. 2008;22:4306-4315.
11. Pokreisz P, Fleming I, Kiss L, et al. Cytochrome P450 epoxygenase gene function in hypoxic pulmonary vasoconstriction and pulmonary vascular remodeling. Hypertension. 2006;47:762-770. (Pubitemid 43740249)
12. Fleming I. DiscrEET regulators of homeostasis: epoxyeicosatrienoic acids, cytochrome P450 epoxygenases and vascular inflammation. Trends Pharmacol Sci. 2007;28:448-452. (Pubitemid 47376754)
13. Randriamboavonjy V, Busse R, Fleming I. 20-HETE-induced contraction of small coronary arteries depends on the activation of Rho-kinase. Hypertension. 2003;41:801-806. (Pubitemid 36314594)
14. Loot AE, Popp R, Fisslthaler B, et al. Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc Res. 2008;80:445-452.
15. Fisslthaler B, Popp R, Michaelis UR, et al. Cyclic stretch enhances the expression and activity of coronary endothelium-derived hyperpolarizing factor synthase. Hypertension. 2001;38:1427-1432. (Pubitemid 34033428)
16. Lambert IH, Pedersen SF, Poulsen KA. Activation of PLA2 isoforms by cell swelling and ischaemia/hypoxia. Acta Physiol. 2006;187:75-85. (Pubitemid 43828765)
17. Michaelis UR, Xia N, Barbosa-Sicard E, et al. Role of cytochrome P450 2C epoxygenases in hypoxia-induced cell migration and angiogenesis in retinal endothelial cells. Invest Ophthalmol Vis Sci. 2008;49:1242-1247.
18. Yang B, Graham L, Dikalov S, et al. Overexpression of cytochrome P450 CYP2J2 protects against hypoxia-reoxygenation injury in cultured bovine aortic endothelial cells. Mol Pharmacol. 2001;60:310-320. (Pubitemid 32678296)
19. Jacobs ER, Zeldin DC. The lung HETEs (and EETs) up. Am J Physiol Heart Circ Physiol. 2001;280:H1-H10.
20. Kiss L, Schutte H, Mayer K, et al. Synthesis of arachidonic acid-derived lipoxygenase and cytochrome P450 products in the intact human lung vasculature. Am J Respir Crit Care Med. 2000;161:1917-1923. (Pubitemid 30418130)
21. Townsley MI, Morisseau C, Hammock B, et al. Impact of epoxyeicosa-trienoic acids in lung ischemia-reperfusion injury. Microcirculation. 2010;17:137-146.
22. Jian MY, King JA, Al-Mehdi AB, et al. High vascular pressure-induced lung injury requires P450 epoxygenase-dependent activation of TRPV4. Am J Respir Cell Mol Biol. 2008;38:386-392. (Pubitemid 351758684)
23. Bonnet S, Archer SL. Potassium channel diversity in the pulmonary arteries and pulmonary veins: implications for regulation of the pulmonary vasculature in health and during pulmonary hypertension. Pharmacol Ther. 2007;115:56-69. (Pubitemid 46992809)
24. Zhu D, Zhang C, Medhora M, et al. CYP4A mRNA, protein, and product in rat lungs: novel localization in vascular endothelium. J Appl Physiol. 2002;93:330-337. (Pubitemid 34686229)
25. Bodiga S, Gruenloh SK, Gao Y, et al. 20-HETE-induced nitric oxide production in pulmonary artery endothelial cells is mediated by NADPH oxidase, H2O2, and PI3-kinase/Akt. Am J Physiol Lung Cell Mol Physiol. 2010;298:L564-L574.
26. Zhu D, Birks EK, Dawson CA, et al. Hypoxic pulmonary vasoconstriction is modified by P-450 metabolites. Am J Physiol Heart Circ Physiol. 2000; 279:H1526-H1533.
27. Zeldin DC, Foley J, Ma J, et al. CYP2J subfamily P450s in the lung: expression, localization, and potential functional significance. Mol Pharmacol. 1996;50:1111-1117. (Pubitemid 26384849)
28. Stephenson AH, Sprague RS, Lonigro AJ. 5,6-Epoxyeicosatrienoic acid reduces increases in pulmonary vascular resistance in the dog. Am J Physiol. 1998;275:H100-H109.
29. Stephenson AH, Sprague RS, Losapio JL, et al. Differential effects of 5,6-EETon segmental pulmonary vasoactivity in the rabbit. Am J Physiol Heart Circ Physiol. 2003;284:H2153-H2161. (Pubitemid 36622427)
30. Zhu D, Bousamra M, Zeldin DC, et al. Epoxyeicosatrienoic acids constrict isolated pressurized rabbit pulmonary arteries. Am J Physiol Lung Cell Mol Physiol. 2000;278:L335-L343. (Pubitemid 30131219)
31. Miller MA, Hales CA. Role of cytochrome P-450 in alveolar hypoxic pulmonary vasoconstriction in dogs. J Clin Invest. 1979;64:666-673. (Pubitemid 9235014)
32. Kiss L, Roder Y, Bier J, et al. Direct eicosanoid profiling of the hypoxic lung by comprehensive analysis via capillary liquid chromatography with dual online photodiode-array and tandem mass-spectrometric detection. Anal Bioanal Chem. 2008;390:697-714.
33. Alonso MT, Alvarez J, Montero M, et al. Agonist-induced Ca2+ influx into human platelets is secondary to the emptying of intracellular Ca2+ stores. Biochem J. 1991;280:783-789.
34. Sargeant P, Clarkson WD, Sage SO, et al. Calcium influx evoked by Ca2+ store depletion in human platelets is more susceptible to cytochrome P-450 inhibitors than receptor-mediated calcium entry. Cell Calcium. 1992;13:553-564.
35. Graier WF, Simecek S, Sturek M. Cytochrome P450 mono-oxygenase-regulated signalling of Ca2+ entry in human and bovine endothelial cells. J Physiol (Lond). 1995;482:259-274.
36. Michaelis UR, Fleming I. From endothelium-derived hyperpolarizing factor (EDHF) to angiogenesis: epoxyeicosatrienoic acids (EETs) and cell signaling. Pharmacol Ther. 2006;111:584-595. (Pubitemid 44160519)
37. Watanabe H, Vriens J, Prenen J, et al. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature. 2003; 424:434-438. (Pubitemid 36917492)
38. Vriens J, Owsianik G, Fisslthaler B, et al. Modulation of the Ca2+ permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res. 2005;97:908-915. (Pubitemid 41552676)
39. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Annu Rev Physiol. 2006;68:619-647.
40. Song MY, Yuan JX. Introduction to TRP channels: structure, function, and regulation. Adv Exp Med Biol. 2010;661:99-108.
41. Clapham DE. TRP channels as cellular sensors. Nature. 2003;426:517-524. (Pubitemid 37522633)
42. Large WA, Saleh SN, Albert AP. Role of phosphoinositol 4,5-bisphosphate and diacylglycerol in regulating native TRPC channel proteins in vascular smooth muscle. Cell Calcium. 2009;45:574-582.
43. Fuchs B, Dietrich A, Gudermann T, et al. The role of classical transient receptor potential channels in the regulation of hypoxic pulmonary vasoconstriction. Adv Exp Med Biol. 2010;661:187-200.
44. Soboloff J, Spassova M, Hewavitharana T, et al. TRPC channels: integrators of multiple cellular signals. Handb Exp Pharmacol. 2007;179:575-591.
45. Spassova MA, Hewavitharana T, Xu W, et al. A common mechanism underlies stretch activation and receptor activation of TRPC6 channels. Proc Natl Acad Sci U S A. 2006;103:16586-16591 (Pubitemid 44715239)
46. Mederos y Schnitzler M, Storch U, Meibers S, et al. Gq-coupled receptors as mechanosensors mediating myogenic vasoconstriction. EMBO J. 2008; 27:3092-3103.
47. Bezzerides VJ, Ramsey IS, Kotecha S, et al. Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol. 2004;6:709-720. (Pubitemid 39144476)
48. Cayouette S, Boulay G. Intracellular trafficking of TRP channels. Cell Calcium. 2007;42:225-232. (Pubitemid 47029596)
49. Jeske NA, Patwardhan AM, Ruparel NB, et al. A-kinase anchoring protein 150 controls protein kinase C-mediated phosphorylation and sensitization of TRPV1. Pain. 2009;146:301-307.
50. Fleming I, Rueben A, Popp R, et al. Epoxyeicosatrienoic acids regulate Trp channel dependent Ca2+ signaling and hyperpolarization in endothelial cells. Arterioscler Thromb Vasc Biol. 2007;27: 2612-2618. (Pubitemid 350158913)
51. Hoebel BG, Graier WF. 11,12-Epoxyeicosatrienoic acid stimulates tyrosine kinase activity in porcine aortic endothelial cells. Eur J Pharmacol. 1998;346:115-117. (Pubitemid 28197097)
52. Hisatsune C, Kuroda Y, Nakamura K, et al. Regulation of TRPC6 channel activity by tyrosine phosphorylation. J Biol Chem. 2004;279: 18887-18894. (Pubitemid 38623316)
53. Wegierski T, Lewandrowski U, Muller B, et al. Tyrosine phosphorylation modulates the activity of TRPV4 in response to defined stimuli. J Biol Chem. 2009;284:2923-2933.
54. Ling S, Woronuk G, Sy L, et al. Enhanced activity of a large conductance, calcium-sensitive K+ channel in the presence of Src tyrosine kinase. J Biol Chem. 2000;275:30683-30689.
55. Tian L, McClafferty H, Chen L, et al. Reversible tyrosine protein phosphorylation regulates large conductance voltage- and calcium-activated potassium channels via cortactin. J Biol Chem. 2008;283: 3067-3076.
56. Weissmann N, Dietrich A, Fuchs B, et al. Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc Natl Acad Sci U S A. 2006;103:19093-19098. (Pubitemid 350002833)
57. Inoue R, Jensen LJ, Jian Z, et al. Synergistic activation of vascular TRPC6 channel by receptor and mechanical stimulation via phospholipase C/ diacylglycerol and phospholipase A2/v-hydroxylase/20-HETE pathways. Circ Res. 2009;104:1399-1409.
58. Pokreisz P, Fleming I, Kiss L, et al. Cytochrome P450 epoxygenase gene function in hypoxic pulmonary vasoconstriction and pulmonary vascular remodeling. Hypertension. 2006;47:762-770. (Pubitemid 43740249)
59. Keserü B, Barbosa-Sicard E, Schermuly RT, et al. Hypoxia-induced pulmonary hypertension: comparison of soluble epoxide hydrolase deletion versus inhibition. Cardiovasc Res. 2010;85:232-240.
60. Fagan KA, Oka M, Bauer NR, et al. Attenuation of acute hypoxic pulmonary vasoconstriction and hypoxic pulmonary hypertension in mice by inhibition of Rho-kinase. Am J Physiol Lung Cell Mol Physiol. 2004; 287:L656-L664. (Pubitemid 39249378)
61. Singh I, Knezevic N, Ahmmed GU, et al. Gaq-TRPC6-mediated Ca2+ entry induces RhoA activation and resultant endothelial cell shape change in response to thrombin. J Biol Chem. 2007;282:7833-7843. (Pubitemid 47093600)
62. Vafeas C, Mieyal PA, Urbano F, et al. Hypoxia stimulates the synthesis of cytochrome P450-derived inflammatory eicosanoids in rabbit corneal epithelium. J Pharmacol Exp Ther. 1998;287:903-910. (Pubitemid 29131599)
63. Michaelis UR, Fisslthaler B, Barbosa-Sicard E, et al. Cytochrome P450 epoxygenases 2C8 and 2C9 are implicated in hypoxia-induced endothelial cell migration and angiogenesis. J Cell Sci. 2005;118:5489-5498. (Pubitemid 43079290)
64. Yamaura K, Gebremedhin D, Zhang C, et al. Contribution of epoxy-eicosatrienoic acids to the hypoxia-induced activation of Ca2+-activated K+ channel current in cultured rat hippocampal astrocytes. Neuroscience. 2006;143:703-716. (Pubitemid 44751362)
65. Dhanasekaran A, Gruenloh SK, Buonaccorsi JN, et al. Multiple antiapoptotic targets of the PI3K/Akt survival pathway are activated by epoxyeicosatrienoic acids to protect cardiomyocytes from hypoxia/anoxia. Am J Physiol Heart Circ Physiol. 2008;294:H724-H735. (Pubitemid 351253284)
66. Muldowney JA III, Painter CA, Sanders-Bush E, et al. Acute tissue-type plasminogen activator release in human microvascular endothelial cells: the roles of Gaq, PLCb, inositol 1,4,5-trisphophate and 5,6-epoxyeico-satrienoic acid. Thromb Haemost. 2007;97:263-271. (Pubitemid 46592147)