Vascular hypoxic preconditioning relies on TRPV4-dependent calcium influx and proper intercellular gap junctions communication

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 9, 2012, Pages 2241-2249

  Rath, Géraldine ^a   Saliez, Julie ^a   Behets, Gaëtane ^a   Romero Perez, Miguel ^a   Leon Gomez, Elvira ^a   Bouzin, Caroline ^a   Vriens, Joris ^b   Nilius, Bernd ^c   Feron, Olivier ^a   Dessy, Chantal ^a  

^a UNIVERSITY OF LOUVAIN MEDICAL SCHOOL   (Belgium)

^b UNIVERSITY HOSPITALS LEUVEN   (Belgium)

^c Katholieke Universiteit Leuven Campus Gasthuisberg O N1   (Belgium)

Author keywords

endothelium derived hyperpolarization; gap junctions; hypoxic preconditioning; NO; TRPV4

Indexed keywords

CARBENOXOLONE; CAVEOLIN 1; CONNEXIN 40; CONNEXIN 43; ENDOTHELIUM DERIVED HYPERPOLARIZING FACTOR; NITRIC OXIDE; VANILLOID RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; GAP JUNCTION; HYPOXIA; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; STIMULUS RESPONSE; VASODILATATION;

ANIMALS; ANOXIA; BIOLOGICAL FACTORS; CALCIUM SIGNALING; CAVEOLAE; CAVEOLIN 1; CELL COMMUNICATION; CELLS, CULTURED; CONNEXINS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; GAP JUNCTIONS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; TIME FACTORS; TRPV CATION CHANNELS; VASODILATION; VASODILATOR AGENTS;

EID: 84865470618     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.252783     Document Type: Article

References (47)

1. Tsao PS, Aoki N, Lefer DJ, Johnson G 3rd, Lefer AM. Time course of endothelial dysfunction and myocardial injury during myocardial ischemia and reperfusion in the cat. Circulation. 1990;82:1402-1412.
2. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986;74:1124-1136.
3. Rezkalla SH, Kloner RA. Preconditioning in humans. Heart Fail Rev. 2007;12:201-206.
4. Laude K, Beauchamp P, Thuillez C, Richard V. Endothelial protective effects of preconditioning. Cardiovasc Res. 2002;55:466-473.
5. Rubino A, Yellon DM. Ischaemic preconditioning of the vasculature: an overlooked phenomenon for protecting the heart? Trends Pharmacol Sci. 2000;21:225-230.
6. Bolli R, Bhatti ZA, Tang XL, Qiu Y, Zhang Q, Guo Y, Jadoon AK. Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the generation of nitric oxide. Circ Res. 1997;81:42-52.
7. Sun JZ, Tang XL, Park SW, Qiu Y, Turrens JF, Bolli R. Evidence for an essential role of reactive oxygen species in the genesis of late preconditioning against myocardial stunning in conscious pigs. J Clin Invest. 1996;97:562-576.
8. Laude K, Richard V, Thuillez C. Coronary endothelial cells: a target of ischemia reperfusion and its treatment? Arch Mal Coeur Vaiss. 2004;97:250-254.
9. Gori T, Dragoni S, Di Stolfo G, Sicuro S, Liuni A, Luca MC, Thomas G, Oelze M, Daiber A, Parker JD. Tolerance to nitroglycerin-induced preconditioning of the endothelium: a human in vivo study. Am J Physiol Heart Circ Physiol. 2010;298:H340-H345.
10. Parker JD, Parker JO. Nitrate therapy for stable angina pectoris. N Engl J Med. 1998;338:520-531.
11. Merla R, Daher IN, Ye Y, Uretsky BF, Birnbaum Y. Pretreatment with statins may reduce cardiovascular morbidity and mortality after elective surgery and percutaneous coronary intervention: clinical evidence and possible underlying mechanisms. Am Heart J. 2007;154:391-402.
12. McLean PG, Aston D, Sarkar D, Ahluwalia A. Protease-activated receptor-2 activation causes EDHF-like coronary vasodilation: selective preservation in ischemia/reperfusion injury: involvement of lipoxygenase products, VR1 receptors, and C-fibers. Circ Res. 2002;90:465-472.
13. Ren Z, Yang Q, Floten HS, Furnary AP, Yim AP, He GW. ATP-sensitive potassium channel openers may mimic the effects of hypoxic preconditioning on the coronary artery. Ann Thorac Surg. 2001;71:642-647.
14. Ren Z, Yang Q, Floten HS, He GW. Hypoxic preconditioning in coronary microarteries: role of EDHF and K+ channel openers. Ann Thorac Surg. 2002;74:143-148.
15. Marrelli SP. Mechanisms of endothelial P2Y(1)-and P2Y(2)-mediated vasodilatation involve differential [Ca2+]i responses. Am J Physiol Heart Circ Physiol. 2001;281:H1759-H1766.
16. Busse R, Edwards G, Félétou M, Fleming I, Vanhoutte PM, Weston AH. EDHF: bringing the concepts together. Trends Pharmacol Sci. 2002;23:374-380.
17. Saliez J, Bouzin C, Rath G, Ghisdal P, Desjardins F, Rezzani R, Rodella LF, Vriens J, Nilius B, Feron O, Balligand JL, Dessy C. Role of caveolar compartmentation in endothelium-derived hyperpolarizing factor-mediated relaxation: Ca2+ signals and gap junction function are regulated by caveolin in endothelial cells. Circulation. 2008;117:1065-1074.
18. Griffith TM. Endothelium-dependent smooth muscle hyperpolarization: do gap junctions provide a unifying hypothesis? Br J Pharmacol. 2004;141:881-903.
19. Boettcher M, de Wit C. Distinct endothelium-derived hyperpolarizing factors emerge in vitro and in vivo and are mediated in part via connexin 40-dependent myoendothelial coupling. Hypertension. 2011;57:802-808.
20. Navarro-Antolín J, Levitsky KL, Calderón E, Ordóñez A, López-Barneo J. Decreased expression of maxi-K+ channel beta1-subunit and altered vasoregulation in hypoxia. Circulation. 2005;112:1309-1315.
21. Brouet A, Sonveaux P, Dessy C, Balligand JL, Feron O. Hsp90 ensures the transition from the early Ca2+-dependent to the late phosphorylation-dependent activation of the endothelial nitric-oxide synthase in vascular endothelial growth factor-exposed endothelial cells. J Biol Chem. 2001;276:32663-32669.
22. Hoffmann A, Gloe T, Pohl U, Zahler S. Nitric oxide enhances de novo formation of endothelial gap junctions. Cardiovasc Res. 2003;60:421-430.
23. Czyz J, Irmer U, Schulz G, Mindermann A, Hülser DF. Gap-junctional coupling measured by flow cytometry. Exp Cell Res. 2000;255:40-46.
24. Kameritsch P, Hoffmann A, Pohl U. Opposing effects of nitric oxide on different connexins expressed in the vascular system. Cell Commun Adhes. 2003;10:305-309.
25. Figueroa XF, Duling BR. Gap junctions in the control of vascular function. Antioxid Redox Signal. 2009;11:251-266.
26. Feron O, Dessy C, Opel DJ, Arstall MA, Kelly RA, Michel T. Modulation of the endothelial nitric-oxide synthase-caveolin interaction in cardiac myocytes. Implications for the autonomic regulation of heart rate. J Biol Chem. 1998;273:30249-30254.
27. Balligand JL, Feron O, Dessy C. eNOS activation by physical forces: from short-term regulation of contraction to chronic remodeling of cardiovascular tissues. Physiol Rev. 2009;89:481-534.
28. Schulz R, Boengler K, Totzeck A, Luo Y, Garcia-Dorado D, Heusch G. Connexin 43 in ischemic pre-and postconditioning. Heart Fail Rev. 2007;12:261-266.
29. Jain SK, Schuessler RB, Saffitz JE. Mechanisms of delayed electrical uncoupling induced by ischemic preconditioning. Circ Res. 2003;92:1138-1144.
30. Lin JH, Lou N, Kang N, Takano T, Hu F, Han X, Xu Q, Lovatt D, Torres A, Willecke K, Yang J, Kang J, Nedergaard M. A central role of connexin 43 in hypoxic preconditioning. J Neurosci. 2008;28:681-695.
31. 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. 2008;80:445-452.
32. Mendoza SA, Fang J, Gutterman DD, Wilcox DA, Bubolz AH, Li R, Suzuki M, Zhang DX. TRPV4-mediated endothelial Ca2+ influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol. 2010;298:H466-H476.
33. Marrelli SP. Altered endothelial Ca2+ regulation after ischemia/reperfusion produces potentiated endothelium-derived hyperpolarizing factor-mediated dilations. Stroke. 2002;33:2285-2291.
34. 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. 2006;26:1495-1502.
35. Earley S, Pastuszyn A, Walker BR. Cytochrome p-450 epoxygenase products contribute to attenuated vasoconstriction after chronic hypoxia. Am J Physiol Heart Circ Physiol. 2003;285:H127-H136.
36. Vriens J, Owsianik G, Fisslthaler B, Suzuki M, Janssens A, Voets T, Morisseau C, Hammock BD, Fleming I, Busse R, Nilius B. Modulation of the Ca2 permeable cation channel TRPV4 by cytochrome P450 epoxygenases in vascular endothelium. Circ Res. 2005;97:908-915.
37. Freichel M, Suh SH, Pfeifer A, Schweig U, Trost C, Weissgerber P, Biel M, Philipp S, Freise D, Droogmans G, Hofmann F, Flockerzi V, Nilius B. Lack of an endothelial store-operated Ca2+ current impairs agonist-dependent vasorelaxation in TRP4-/-mice. Nat Cell Biol. 2001;3:21-127.
38. Murata T, Lin MI, Stan RV, Bauer PM, Yu J, Sessa WC. Genetic evidence supporting caveolae microdomain regulation of calcium entry in endothelial cells. J Biol Chem. 2007;282:16631-16643.
39. Koval M, Billaud M, Straub AC, Johnstone SR, Zarbock A, Duling BR, Isakson BE. Spontaneous lung dysfunction and fibrosis in mice lacking connexin 40 and endothelial cell connexin 43. Am J Pathol. 2011;178:2536-2546.
40. Langlois S, Cowan KN, Shao Q, Cowan BJ, Laird DW. Caveolin-1 and-2 interact with connexin43 and regulate gap junctional intercellular communication in keratinocytes. Mol Biol Cell. 2008;19:912-928.
41. Dessy C, Feron O, Balligand JL. The regulation of endothelial nitric oxide synthase by caveolin: a paradigm validated in vivo and shared by the 'endothelium-derived hyperpolarizing factor'. Pflugers Arch. 2010;459:817-827.
42. Pfenniger A, Derouette JP, Verma V, Lin X, Foglia B, Coombs W, Roth I, Satta N, Dunoyer-Geindre S, Sorgen P, Taffet S, Kwak BR, Delmar M. Gap junction protein Cx37 interacts with endothelial nitric oxide synthase in endothelial cells. Arterioscler Thromb Vasc Biol. 2010;30:827-834.
43. Alonso F, Boittin FX, Bény JL, Haefliger JA. Loss of connexin40 is associated with decreased endothelium-dependent relaxations and eNOS levels in the mouse aorta. Am J Physiol Heart Circ Physiol. 2010;299:H1365-H1373.
44. Looft-Wilson RC, Billaud M, Johnstone SR, Straub AC, Isakson BE. Interaction between nitric oxide signaling and gap junctions: Effects on vascular function. Biochim Biophys Acta. 2012;1818:1895-1902.
45. Adapala RK, Talasila PK, Bratz IN, Zhang DX, Suzuki M, Meszaros JG, Thodeti CK. PKCa mediates acetylcholine-induced activation of TRPV4-dependent calcium influx in endothelial cells. Am J Physiol Heart Circ Physiol. 2011;301:H757-H765.
46. Yin J, Hoffmann J, Kaestle SM, Neye N, Wang L, Baeurle J, Liedtke W, Wu S, Kuppe H, Pries AR, Kuebler WM. Negative-feedback loop attenuates hydrostatic lung edema via a cGMP-dependent regulation of transient receptor potential vanilloid 4. Circ Res. 2008;102:966-974.
47. Ong HL, Ambudkar IS. The dynamic complexity of the TRPC1 channelosome. Channels (Austin). 2011;5:424-431.