Interplay between Connexin40 and nitric oxide signaling during hypertension

Hypertension

Volumn 65, Issue 4, 2015, Pages 910-915

  Le Gal, Loïc ^a   Alonso, Florian ^a   Mazzolai, Lucia ^a   Meda, Paolo ^b   Haefliger, Jacques Antoine ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

Author keywords

1 kidney, 1 clip (1K1C); connexins; endothelial cells; endothelial nitric oxide synthase; gap junctions; hypertension

Indexed keywords

CONNEXIN 37; CONNEXIN 40; ENDOTHELIAL NITRIC OXIDE SYNTHASE; RENIN; GAP JUNCTION PROTEIN; RNA;

1 KIDNEY 1 CLIP; 2 KIDNEY 1 CLIP; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HEART WEIGHT; HYPERTENSION; IMMUNOHISTOCHEMISTRY; MEDICAL PROCEDURES; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SMOOTH MUSCLE FIBER; ANIMAL; BIOSYNTHESIS; BLOOD PRESSURE; C57BL MOUSE; COMPARATIVE STUDY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; VASCULAR ENDOTHELIUM;

ANIMALS; BLOOD PRESSURE; CONNEXINS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HYPERTENSION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE III; REAL-TIME POLYMERASE CHAIN REACTION; RNA;

EID: 84929133900     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.114.04775     Document Type: Article

References (34)

1. Cavalcante JL, Lima JA, Redheuil A, Al-Mallah MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol. 2011; 57: 1511-1522. doi: 10.1016/j.jacc.2010.12.017
2. Safar ME, Balkau B, Lange C, Protogerou AD, Czernichow S, Blacher J, Levy BI, Smulyan H. Hypertension and vascular dynamics in men and women with metabolic syndrome. J Am Coll Cardiol. 2013; 61: 12-19. doi: 10.1016/j.jacc.2012.01.088
3. Safar ME, Boudier HS. Vascular development, pulse pressure, and the mechanisms of hypertension. Hypertension. 2005; 46: 205-209. doi: 10.1161/01.HYP.0000167992.80876.26
4. Krattinger N, Capponi A, Mazzolai L, Aubert JF, Caille D, Nicod P, Waeber G, Meda P, Haefliger JA. Connexin40 regulates renin production and blood pressure. Kidney Int. 2007; 72: 814-822. doi: 10.1038/sj.ki.5002423
5. 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. doi: 10.1152/ajpheart.00029.2010
6. Alonso F, Krattinger N, Mazzolai L, Simon A, Waeber G, Meda P, Haefliger JA. An angiotensin II-and NF-kappaB-dependent mechanism increases connexin 43 in murine arteries targeted by renin-dependent hypertension. Cardiovasc Res. 2010; 87: 166-176. doi: 10.1093/cvr/cvq031
7. Boittin FX, Alonso F, Le Gal L, Allagnat F, Bény JL, Haefliger JA. Connexins and M3 muscarinic receptors contribute to heterogeneous Ca(2+) signaling in mouse aortic endothelium. Cell Physiol Biochem. 2013; 31: 166-178. doi: 10.1159/000343358
8. Le Gal L, Alonso F, Wagner C, Germain S, Nardelli Haefliger D, Meda P, Haefliger JA. Restoration of connexin 40 (Cx40) in Renin-producing cells reduces the hypertension of Cx40 null mice. Hypertension. 2014; 63: 1198-1204. doi: 10.1161/HYPERTENSIONAHA.113.02976
9. Haefliger JA, Nicod P, Meda P. Contribution of connexins to the function of the vascular wall. Cardiovasc Res. 2004; 62: 345-356. doi: 10.1016/j. cardiores.2003.11.015
10. Meens MJ, Pfenniger A, Kwak BR, Delmar M. Regulation of cardiovascular connexins by mechanical forces and junctions. Cardiovasc Res. 2013; 99: 304-314. doi: 10.1093/cvr/cvt095
11. Kurtz L, Schweda F, De Wit C, Kriz W, Witzgall R, Warth R, Sauter A, Kurtz A, Wagner C. Lack of connexin 40 causes displacement of renin-producing cells from afferent arterioles to the extraglomerular mesangium. J Am Soc Nephrol. 2007; 18: 1103-1111. doi: 10.1681/ASN.2006090953
12. Wagner C. Function of connexins in the renal circulation. Kidney Int. 2008; 73: 547-555. doi: 10.1038/sj.ki.5002720
13. Wagner C, De Wit C, Kurtz L, Grünberger C, Kurtz A, Schweda F. Connexin40 is essential for the pressure control of renin synthesis and secretion. Circ Res. 2007; 100: 556-563. doi: 10.1161/01. RES.0000258856.19922.45
14. De Wit C, Roos F, Bolz SS, Kirchhoff S, Krüger O, Willecke K, Pohl U. Impaired conduction of vasodilation along arterioles in connexin40-deficient mice. Circ Res. 2000; 86: 649-655
15. 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. doi: 10.1161/ATVBAHA.109.200816
16. Schäfer SC, Pellegrin M, Wyss C, Aubert JF, Nussberger J, Hayoz D, Lehr HA, Mazzolai L. Intravital microscopy reveals endothelial dysfunction in resistance arterioles in Angiotensin II-induced hypertension. Hypertens Res. 2012; 35: 855-861. doi: 10.1038/hr.2012.58
17. Wiesel P, Mazzolai L, Nussberger J, Pedrazzini T. Two-kidney, one clip and one-kidney, one clip hypertension in mice. Hypertension. 1997; 29: 1025-1030
18. Figueroa XF, Duling BR. Gap junctions in the control of vascular function. Antioxid Redox Signal. 2009; 11: 251-266. doi: 10.1089/ars.2008.2117
19. Brisset AC, Isakson BE, Kwak BR. Connexins in vascular physiology and pathology. Antioxid Redox Signal. 2009; 11: 267-282. doi: 10.1089/ars.2008.2115
20. Haefliger JA, Meda P, Formenton A, Wiesel P, Zanchi A, Brunner HR, Nicod P, Hayoz D. Aortic connexin43 is decreased during hypertension induced by inhibition of nitric oxide synthase. Arterioscler Thromb Vasc Biol. 1999; 19: 1615-1622
21. Haefliger JA, Castillo E, Waeber G, Bergonzelli GE, Aubert JF, Sutter E, Nicod P, Waeber B, Meda P. Hypertension increases connexin43 in a tissue-specific manner. Circulation. 1997; 95: 1007-1014
22. Figueroa XF, Isakson BE, Duling BR. Vascular gap junctions in hypertension. Hypertension. 2006; 48: 804-811. doi: 10.1161/01. HYP.0000242483.03361.da
23. De Wit C, Roos F, Bolz SS, Pohl U. Lack of vascular connexin 40 is associated with hypertension and irregular arteriolar vasomotion. Physiol Genomics. 2003; 13: 169-177. doi: 10.1152/physiolgenomics.00169.2002
24. Figueroa XF, Paul DL, Simon AM, Goodenough DA, Day KH, Damon DN, Duling BR. Central role of connexin40 in the propagation of electrically activated vasodilation in mouse cremasteric arterioles in vivo. Circ Res. 2003; 92: 793-800. doi: 10.1161/01.RES.0000065918.90271.9A
25. Jobs A, Schmidt K, Schmidt VJ, Lübkemeier I, van Veen TA, Kurtz A, Willecke K, De Wit C. Defective Cx40 maintains Cx37 expression but intact Cx40 is crucial for conducted dilations irrespective of hypertension. Hypertension. 2012; 60: 1422-1429. doi: 10.1161/HYPERTENSIONAHA.112.201194
26. Wagner C, Jobs A, Schweda F, Kurtz L, Kurt B, Lopez ML, Gomez RA, van Veen TA, De Wit C, Kurtz A. Selective deletion of Connexin 40 in renin-producing cells impairs renal baroreceptor function and is associated with arterial hypertension. Kidney Int. 2010; 78: 762-768. doi: 10.1038/ki.2010.257
27. Retamal MA, Cortés CJ, Reuss L, Bennett MV, Sáez JC. S-nitrosylation and permeation through connexin 43 hemichannels in astrocytes: induction by oxidant stress and reversal by reducing agents. Proc Natl Acad Sci USA. 2006; 103: 4475-4480. doi: 10.1073/pnas.0511118103
28. Retamal MA, Yin S, Altenberg GA, Reuss L. Modulation of Cx46 hemichannels by nitric oxide. Am J Physiol Cell Physiol. 2009; 296: C1356-C1363. doi: 10.1152/ajpcell.00054.2009
29. Straub AC, Billaud M, Johnstone SR, Best AK, Yemen S, Dwyer ST, Looft-Wilson R, Lysiak JJ, Gaston B, Palmer L, Isakson BE. Compartmentalized connexin 43 s-nitrosylation/denitrosylation regulates heterocellular communication in the vessel wall. Arterioscler Thromb Vasc Biol. 2011; 31: 399-407. doi: 10.1161/ATVBAHA.110.215939
30. 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. doi: 10.1016/j.bbamem.2011.07.031
31. Saura M, Marquez S, Reventun P, Olea-Herrero N, Arenas MI, Moreno-Gómez-Toledano R, Gómez-Parrizas M, Muñóz-Moreno C, González-Santander M, Zaragoza C, Bosch RJ. Oral administration of bisphenol A induces high blood pressure through angiotensin II/CaMKII-dependent uncoupling of eNOS. FASEB J. 2014; 28: 4719-4728. doi: 10.1096/fj.14-252460
32. Kim JA, Jang HJ, Martinez-Lemus LA, Sowers JR. Activation of mTOR/p70S6 kinase by ANG II inhibits insulin-stimulated endothelial nitric oxide synthase and vasodilation. Am J Physiol Endocrinol Metab. 2012; 302: E201-E208. doi: 10.1152/ajpendo.00497.2011
33. Dimmeler S, Zeiher AM. Nitric oxide-an endothelial cell survival factor. Cell Death Differ. 1999; 6: 964-968. doi: 10.1038/sj.cdd.4400581
34. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature. 1999; 399: 597-601. doi: 10.1038/21218