Activation of endothelial TRPV4 channels mediates flow-induced dilation in human coronary arterioles: Role of Ca 2+ entry and mitochondrial ROS signaling

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 3, 2012, Pages

  Bubolz, Aaron H ^a,b   Mendoza, Suelhem A ^a,b   Zheng, Xiaodong ^a,b   Zinkevich, Natalya S ^a,b   Li, Rongshan ^a   Gutterman, David D ^a,b,c   Zhang, David X ^a,b  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b Cardiovascular Center   (United States)

^c CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Coronary; Free radicals; Mitochondria; Reactive oxygen species; Shear stress; Transient receptor potential; Transient receptor potential vanilloid type 4 channel

Indexed keywords

4ALPHA PHORBOL DIDECANOATE; CALCIUM ION; CATALASE; DRUG METABOLIZING ENZYME; HYDROGEN PEROXIDE; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; SUPEROXIDE; VANILLOID RECEPTOR 4;

ADULT; ARTERIOLE; ARTERY ENDOTHELIUM; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DILATATION; CORONARY ARTERY DISEASE; CORONARY BLOOD VESSEL; ENDOTHELIUM CELL; FEMALE; FLUORESCENCE ANALYSIS; HEART MITOCHONDRION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

AGED; ARTERIOLES; ATRIAL APPENDAGE; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CORONARY CIRCULATION; ENDOTHELIAL CELLS; FEMALE; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; OXIDATIVE STRESS; PHENANTHRIDINES; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; TRPV CATION CHANNELS; VASODILATION;

EID: 84863016934     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00717.2011     Document Type: Article

References (42)

1. Arniges M, Fernández-Fernández JM, Albrecht N, Schaefer M, Valverde MA. Human TRPV4 channel splice variants revealed a key role of ankyrin domains in multimerization and trafficking. J Biol Chem 281: 1580-1586, 2006.
2. Buga GM, Gold ME, Fukuto JM, Ignarro LJ. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension 17: 187-193, 1991.
3. Busse R, Fleming I. Regulation of endothelium-derived vasoactive auta-coid production by hemodynamic forces. Trends Pharmacol Sci 24: 24-29, 2003.
4. Cooke JP, Rossitch E Jr, Andon NA, Loscalzo J, Dzau VJ. Flow activates an endothelial potassium channel to release an endogenous nitrovasodilator. J Clin Invest 88: 1663-1671, 1991.
5. Dhanasekaran A, Kotamraju S, Kalivendi SV, Matsunaga T, Shang T, Keszler A, Joseph J, Kalyanaraman B. Supplementation of endothelial cells with mitochondria-targeted antioxidants inhibit peroxide-induced mitochondrial iron uptake, oxidative damage, and apoptosis. J Biol Chem 279: 37575-37587, 2004.
6. Duffy SJ, Castle SF, Harper RW, Meredith IT. Contribution of vasodilator prostanoids and nitric oxide to resting flow, metabolic vasodilation, and flow-mediated dilation in human coronary circulation. Circulation 100: 1951-1957, 1999.
7. Falcone JC, Kuo L, Meininger GA. Endothelial cell calcium increases during flow-induced dilation in isolated arterioles. Am J Physiol Heart Circ Physiol 264: H653-H659, 1993.
8. 2+ and ROS. Front Biosci 14: 1197-1218, 2009.
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 278: 27129-27137, 2003.
10. 2+ signaling: old guests, new functions. Pflügers Arch 455: 375-396, 2007.
11. Güler AD, Lee H, Iida T, Shimizu I, Tominaga M, Caterina M. Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22: 6408-6414, 2002.
12. Hartmannsgruber V, Heyken WT, Kacik M, Kaistha A, Grgic I, Harteneck C, Liedtke W, Hoyer J, Köhler R. Arterial response to shear stress critically depends on endothelial TRPV4 expression. PLos One 2: e827, 2007.
13. Helmlinger G, Berk B, Nerem RM. Pulsatile and steady flow-induced calcium oscillations in single cultured endothelial cell. J Vasc Res 33: 360-369, 1996.
14. 2+ oscillations and STOC activation in endothelial cells. FASEB J 12: 359-366, 1998.
15. Joannides R, Haefeli WE, Linder L, Richard V, Bakkali EH, Thuillez C, Luscher TF. Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation 91: 1314-1319, 1995.
16. Köhler R, Heyken WT, Heinau P, Schubert R, Si H, Kacik M, Busch C, Grgic I, Maier T, Hoyer J. Evidence for a functional role of endothelial transient receptor potential V4 in shear stress-induced vasodilatation. Arterioscler Thromb Vasc Biol 26: 1495-1502, 2006.
17. Koller A, Sun D, Kaley G. Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circ Res 72: 1276-1284, 1993.
18. Kuo L, Davis MJ, Chilian WM. Endothelium-dependent, flow-induced dilation of isolated coronary arterioles. Am J Physiol Heart Circ Physiol 259: H1063-H1070, 1990.
19. Liedtke W, Choe Y, Martí-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S. Vanilloid receptor-related os-motically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103: 525-535, 2000.
20. Liu Y, Bubolz AH, Mendoza S, Zhang DX, Gutterman DD. H2O2 is the transferrable factor mediating flow-induced dilation in human coronary arterioles. Circ Res 108: 566-573, 2011.
21. Liu Y, Li H, Bubolz AH, Zhang DX, Gutterman DD. Endothelial cytoskeletal elements are critical for flow-mediated dilation in human coronary arterioles. Med Biol Eng Comput 46: 469-478, 2008.
22. Liu Y, Zhao H, Li H, Kalyanaraman B, Nicolosi AC, Gutterman DD. Mitochondrial sources of H2O2 generation play a key role in flow-mediated dilation in human coronary resistance arteries. Circ Res 93: 573-580, 2003.
23. Loot AE, Popp R, Fisslthaler B, Vriens J, Nilius B, Fleming I. Role of cytochrome P450-dependent transient receptor potential V4 activation in flow-induced vasodilatation. Cardiovasc Res 80: 445-452, 2008.
24. 2+ influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol 298: H466-H476, 2010.
25. Miller FJ Jr, Dellsperger KC, Gutterman DD. Pharmacologic activation of the human coronary microcirculation in vitro: endothelium-dependent dilation and differential responses to acetylcholine. Cardiovasc Res 38: 744-750, 1998.
26. Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD. Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 92: e31-e40, 2003.
27. + channels. Circ Res 83: 501-507, 1998.
28. + channels. Circulation 103: 1992-1998, 2001.
29. Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD. OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2: 695-702, 2000.
30. + secretion from the cortical collecting duct. Am J Physiol Renal Physiol 292: F667-F673, 2007.
31. Thodeti CK, Matthews B, Ravi A, Mammoto A, Ghosh K, Bracha AL, Ingber DE. TRPV4 channels mediate cyclic strain-induced endothelial cell reorientation through integrin-to-integrin signaling. Circ Res 104: 1123-1130, 2009.
32. Vincent F, Acevedo A, Nguyen MT, Dourado M, DeFalco J, Gustafson A, Spiro P, Emerling DE, Kelly MG, Duncton MA. Identification and characterization of novel TRPV4 modulators. Biochem Biophys Res Com-mun 389: 490-494, 2009.
33. Vriens J, Appendino G, Nilius B. Pharmacology of vanilloid transient receptor potential cation channels. Mol Pharmacol 75: 1262-1279, 2009.
34. 2+ permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res 97: 908-915, 2005.
35. 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 277: 13569-13577, 2002.
36. Watanabe H, Vriens J, Prenen J, Droogmans G, Voets T, Nilius B. Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels. Nature 424: 434-438, 2003.
37. 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 277: 47044-47051, 2002.
38. Wu L, Gao X, Brown RC, Heller S, O'Neil RG. Dual role of the TRPV4 channel as a sensor of flow and osmolality in renal epithelial cells. Am J Physiol Renal Physiol 293: F1699-F1713, 2007.
39. 2+ mobilization through cADP-ribose signaling in coronary arterial smooth muscle cells. Am J Physiol Heart Circ Physiol 279: H873-H881, 2000.
40. Zhang DX, Gutterman DD. Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am J Physiol Heart Circ Physiol 292: H2023-H2031, 2007.
41. Zhang DX, Gutterman DD. TRP channel activation and endothelium-dependent dilation in the systemic circulation. J Cardiovasc Pharmacol 57: 133-139, 2011.
42. Zinkevich NS, Gutterman DD. ROS-induced ROS release in vascular biology: redox-redox signaling. Am J Physiol Heart Circ Physiol 301: H647-H653, 2011.