Nitric oxide up-regulates endothelial expression of angiotensin II type 2 receptors

Biochemical Pharmacology

Volumn 112, Issue , 2016, Pages 24-36

  Dao, Vu Thao Vi ^a,d   Medini, Sawsan ^a   Bisha, Marion ^a   Balz, Vera ^b   Suvorava, Tatsiana ^a   Bas, Murat ^c   Kojda, Georg ^a  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Angiotensin converting enzyme 1; Angiotensin II type 2 receptor; Endothelial nitric oxide synthase; Exercise; Nitric oxide

Indexed keywords

ANGIOTENSIN 2 RECEPTOR; ANGIOTENSIN 2 RECEPTOR ANTAGONIST; DACTINOMYCIN; DIPEPTIDYL CARBOXYPEPTIDASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; N(G) NITROARGININE; NITRIC OXIDE; ENZYME INHIBITOR; NITRIC OXIDE DONOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; FEMALE; GENE OVEREXPRESSION; GENETIC STABILITY; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PIG; PRIORITY JOURNAL; RANDOMIZATION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECTS; GENETICS; METABOLISM; MOTOR ACTIVITY; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; TRANSGENIC MOUSE; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALS; ENDOTHELIAL CELLS; ENZYME INHIBITORS; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; RECEPTOR, ANGIOTENSIN, TYPE 2; RENIN-ANGIOTENSIN SYSTEM; SWINE; UP-REGULATION;

EID: 84973522279     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2016.05.011     Document Type: Article

References (59)

1. G. Kojda, and R. Hambrecht Molecular mechanisms of vascular adaptations to exercise. Physical activity as an effective antioxidant therapy? Cardiovasc. Res. 67 2005 187 197
2. S.J. Keteyian, E.S. Leifer, N. Houston-Miller, W.E. Kraus, C.A. Brawner, C.M. O'Connor, and et al. Relation between volume of exercise and clinical outcomes in patients with heart failure J. Am. Coll. Cardiol. 60 2012 1899 1905
3. R. Belardinelli, D. Georgiou, G. Cianci, and A. Purcaro 10-Year exercise training in chronic heart failure: a randomized controlled trial J. Am. Coll. Cardiol. 60 2012 1521 1528
4. H. Noda, H. Iso, H. Toyoshima, C. Date, A. Yamamoto, S. Kikuchi, and et al. Walking and sports participation and mortality from coronary heart disease and stroke J. Am. Coll. Cardiol. 46 2005 1761 1767
5. S. Gielen, G. Schuler, and V. Adams Cardiovascular effects of exercise training: molecular mechanisms Circulation 122 2010 1221 1238
6. R. Hambrecht, A. Wolf, S. Gielen, A. Linke, J. Hofer, S. Erbs, and et al. Effect of exercise on coronary endothelial function in patients with coronary artery disease N. Engl. J. Med. 342 2000 454 460
7. T. Fukai, M.R. Siegfried, M. Ushio-Fukai, Y. Cheng, G. Kojda, and D.G. Harrison Regulation of the vascular extracellular superoxide dismutase by nitric oxide and exercise training J. Clin. Invest. 105 2000 1631 1639
8. V. Adams, A. Linke, N. Krankel, S. Erbs, S. Gielen, S. Möbius-Winkler, and et al. Impact of Regular Physical Activity on the NAD(P)H Oxidase and Angiotensin Receptor System in Patients With Coronary Artery Disease Circulation 111 2005 555 562
9. C.A. Lemarie, and E.L. Schiffrin The angiotensin II type 2 receptor in cardiovascular disease J. Renin Angiotensin Aldosterone Syst. 11 2010 19 31
10. U.M. Steckelings, M. Larhed, A. Hallberg, R.E. Widdop, E.S. Jones, C. Wallinder, and et al. Non-peptide AT2-receptor agonists Curr. Opin. Pharmacol. 11 2011 187 192
11. L. Zhu, O.A. Carretero, T.D. Liao, P. Harding, H. Li, C. Sumners, and et al. Role of prolylcarboxypeptidase in angiotensin II type 2 receptor-mediated bradykinin release in mouse coronary artery endothelial cells Hypertension 56 2010 384 390
12. Z. Shariat-Madar, F. Mahdi, and A.H. Schmaier Identification and characterization of prolylcarboxypeptidase as an endothelial cell prekallikrein activator J. Biol. Chem. 277 2002 17962 17969
13. T.E. Hunley, M. Tamura, B.J. Stoneking, H. Nishimura, T. Ichiki, T. Inagami, and et al. The angiotensin type II receptor tonically inhibits angiotensin- converting enzyme in AT2 null mutant mice Kidney Int. 57 2000 570 577
14. D.J. Campbell, H. Krum, and M.D. Esler Losartan increases bradykinin levels in hypertensive humans Circulation 111 2005 315 320
15. S. Yusuf, P. Sleight, J. Pogue, J. Bosch, R. Davies, and G. Dagenais Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The heart outcomes prevention evaluation study investigators N. Engl. J. Med. 342 2000 145 153
16. J.J. McMurray, R.R. Holman, S.M. Haffner, M.A. Bethel, B. Holzhauer, T.A. Hua, and et al. Effect of valsartan on the incidence of diabetes and cardiovascular events N. Engl. J. Med. 362 2010 1477 1490
17. M. Oppermann, V. Balz, V. Adams, V.T. Dao, M. Bas, T. Suvorava, and et al. Pharmacologic induction of vascular extracellular superoxide dismutase expression in-vivo J. Cell Mol. Med. 13 2009 1271 1278
18. M. Oppermann, T. Suvorava, T. Freudenberger, V.T. Dao, J.W. Fischer, M. Weber, and et al. Regulation of vascular guanylyl cyclase by endothelial nitric oxide-dependent posttranslational modification Basic Res. Cardiol. 106 2011 539 549
19. G. Kojda, Y. Cheng, J. Burchfield, and D.G. Harrison Dysfunctional regulation of eNOS expression in response to exercise in mice lacking one eNOS gene Circulation 103 2001 2839 2844
20. V.T. Dao, M. Floeren, S. Kumpf, C. Both, B. Peter, V. Balz, and et al. Catalase activity prevents exercise-induced up-regulation of vasoprotective proteins in venous tissue J. Cell Mol. Med. 15 2011 2326 2334
21. T. Suvorava, N. Lauer, and G. Kojda Physical inactivity causes endothelial dysfunction in healthy young mice J. Am. Coll. Cardiol. 44 2004 1320 1327
22. J.A. Gordon Use of vanadate as protein-phosphotyrosine phosphatase inhibitor Methods Enzymol. 201 1991 477 482
23. B.A. Murray, D.J. Walsh, and R.J. Fitzgerald Modification of the furanacryloyl-l-phenylalanylglycylglycine assay for determination of angiotensin-I-converting enzyme inhibitory activity J. Biochem. Biophys. Methods 59 2004 127 137
24. G. Kojda, J.B. Laursen, S. Ramasamy, J.D. Kent, S. Kurz, J. Burchfield, and et al. Protein expression, vascular reactivity and soluble guanylate cyclase activity in mice lacking the endothelial nitric oxide synthase: contributions of NOS isoforms to blood pressure and heart rate control Cardiovasc. Res. 42 1999 206 213
25. D.L. Mattson, and C.J. Meister Renal cortical and medullary blood flow responses to L-NAME and ANG II in wild-type, nNOS null mutant, and eNOS null mutant mice Am. J. Physiol. Regul. Integr. Comp. Physiol. 289 2005 R991 R997
26. T.J. Calvert, L.G. Chicoine, Y. Liu, and L.D. Nelin Deficiency of mitogen-activated protein kinase phosphatase-1 results in iNOS-mediated hypotension in response to low-dose endotoxin Am. J. Physiol. Heart Circ. Physiol. 294 2008 H1621 H1629
27. T. Suvorava, S. Kumpf, B.H. Rauch, V.T. Dao, V. Adams, and G. Kojda Hydrogen peroxide inhibits exercise-induced increase of circulating stem cells with endothelial progenitor capacity Free Radic. Res. 44 2010 199 207
28. T. Suvorava, N. Lauer, S. Kumpf, R. Jacob, W. Meyer, and G. Kojda Endogenous vascular hydrogen peroxide regulates arteriolar tension in vivo Circulation 112 2005 2487 2495
29. M. Tanaka, S. Tsuchida, T. Imai, N. Fujii, H. Miyazaki, T. Ichiki, and et al. Vascular response to angiotensin II is exaggerated through an upregulation of AT1 receptor in AT2 knockout mice Biochem. Biophys. Res. Commun. 258 1999 194 198
30. A. Ackermann, M.S. Fernandez-Alfonso, D.R. Sanchez, T. Ortega, M. Paul, and C. Gonzalez Modulation of angiotensin-converting enzyme by nitric oxide Br. J. Pharmacol. 124 1998 291 298
31. G. Kojda, M. Patzner, A. Hacker, and E. Noack Nitric oxide inhibits vascular bioactivation of glyceryl trinitrate. A novel mechanism to explain preferential venodilation of organic nitrates Mol. Pharmacol. 53 1998 547 554
32. E.G. Shesely, N. Maeda, H.S. Kim, K.M. Desai, J.H. Krege, V.E. Laubach, and et al. Elevated blood pressures in mice lacking endothelial nitric oxide synthase Proc. Natl. Acad. Sci. U.S.A. 93 1996 13176 13181
33. T. Wang, F.M. Inglis, and R.G. Kalb Defective fluid and HCO(3)(-) absorption in proximal tubule of neuronal nitric oxide synthase-knockout mice Am. J. Physiol. Renal Physiol. 279 2000 F518 F524
34. G. Kojda, Y.C. Cheng, J. Burchfield, and D.G. Harrison Dysfunctional regulation of endothelial nitric oxide synthase (eNOS) expression in response to exercise in mice lacking one eNOS gene Circulation 103 2001 2839 2844
35. N. Lauer, T. Suvorava, U. Rüther, R. Jacob, A. Meyer, D.G. Harrison, and et al. Critical involvement of hydrogen peroxide in exercise-induced upregulation of endothelial NO-synthase Cardiovasc. Res. 65 2005 254 262
36. J. Raingeaud, S. Gupta, J.S. Rogers, M. Dickens, J. Han, R.J. Ulevitch, and et al. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine J. Biol. Chem. 270 1995 7420 7426
37. F. Hofmann, D. Bernhard, R. Lukowski, and P. Weinmeister CGMP regulated protein kinases (cGK) Handb. Exp. Pharmacol. 137 2009
38. A. Cuadrado, and A.R. Nebreda Mechanisms and functions of p38 MAPK signalling Biochem. J. 429 2010 403 417
39. Y. Li, S. Batra, A. Sassano, B. Majchrzak, D.E. Levy, M. Gaestel, and et al. Activation of mitogen-activated protein kinase kinase (MKK) 3 and MKK6 by type I interferons J. Biol. Chem. 280 2005 10001 10010
40. G.E. Mann, B. Bonacasa, T. Ishii, and R.C. Siow Targeting the redox sensitive Nrf2-Keap1 defense pathway in cardiovascular disease: protection afforded by dietary isoflavones Curr. Opin. Pharmacol. 9 2009 139 145
41. C. Lee, and C.H. Huang LASAGNA-search: an integrated web tool for transcription factor binding site search and visualization Biotechniques 54 2013 141 153
42. M. De Gasparo, K.J. Catt, T. Inagami, J.W. Wright, and T. Unger International union of pharmacology. XXIII. The angiotensin II receptors Pharmacol. Rev. 52 2000 415 472
43. M. Saito, Y. Shinohara, H. Sasaki, Y. Netsu, M. Yoshida, and N. Nakahata Type 1 angiotensin receptor (AT1-R)-mediated decrease in type 2 angiotensin receptor mRNA level is dependent on Gq and extracellular signal-regulated kinase 1//2 in AT1-R-transfected PC12 cells J. Neuroendocrinol. 20 2008 299 308
44. M. Usui, T. Ichiki, M. Katoh, K. Egashira, and A. Takeshita Regulation of angiotensin II receptor expression by nitric oxide in rat adrenal gland Hypertension 32 1998 527 533
45. A. Gödecke, U. Decking, Z. Ding, J. Hirchenhain, H.J. Bidmon, S. Godecke, and et al. Coronary hemodynamics in endothelial NO synthase knockout mice Circ. Res. 82 1998 186 194
46. K.G. Lamping, D.W. Nuno, E.G. Shesely, N. Maeda, and F.M. Faraci Vasodilator mechanisms in the coronary circulation of endothelial nitric oxide synthase-deficient mice Am. J. Physiol. Heart Circ. Physiol. 279 2000 H1906 H1912
47. G.J. Waldron, H. Ding, F. Lovren, P. Kubes, and C.R. Triggle Acetylcholine-induced relaxation of peripheral arteries isolated from mice lacking endothelial nitric oxide synthase Br. J. Pharmacol. 128 1999 653 658
48. W. Meng, C. Ayata, C. Waeber, P.L. Huang, and M.A. Moskowitz Neuronal NOS-cGMP-dependent ACh-induced relaxation in pial arterioles of endothelial NOS knockout mice Am. J. Physiol. Heart Circ. Physiol. 274 1998 H411 H415
49. D. Sun, A. Huang, C.J. Smith, C.J. Stackpole, J.A. Connetta, E.G. Shesely, and et al. Enhanced release of prostaglandins contributes to flow-induced arteriolar dilation in eNOS knockout mice Circ. Res. 85 1999 288 293
50. 2 production in mouse cerebral arteries Cardiovasc. Res. 73 2007 73 81
51. J.V. Gainer, J.D. Morrow, A. Loveland, D.J. King, and N.J. Brown Effect of bradykinin-receptor blockade on the response to angiotensin-converting-enzyme inhibitor in normotensive and hypertensive subjects N. Engl. J. Med. 339 1998 1285 1292
52. A.J. Fox, U.G. Lalloo, M.G. Belvisi, M. Bernareggi, K.F. Chung, and P.J. Barnes Bradykinin-evoked sensitization of airway sensory nerves: a mechanism for ACE-inhibitor cough Nat. Med. 2 1996 814 817
53. M. Bas, J. Greve, K. Stelter, M. Havel, U. Strassen, N. Rotter, and et al. A randomized trial of icatibant in ACE-inhibitor-induced angioedema N. Engl. J. Med. 372 2015 418 425
54. M. Bas, J. Greve, K. Stelter, H. Bier, T. Stark, T.K. Hoffmann, and et al. Therapeutic efficacy of icatibant in angioedema induced by angiotensin-converting enzyme inhibitors: a case series Ann. Emerg. Med. 56 2010 278 282
55. M. Bas, J. Greve, U. Strassen, F. Khosravani, T.K. Hoffmann, and G. Kojda Angioedema induced by cardiovascular drugs: new players join old friends Allergy 70 2015 1196 1200
56. Z. Shariat-Madar, F. Mahdi, and A.H. Schmaier Recombinant prolylcarboxypeptidase activates plasma prekallikrein Blood 103 2004 4554 4561
57. Y. Tsutsumi, H. Matsubara, H. Masaki, H. Kurihara, S. Murasawa, S. Takai, and et al. Angiotensin II type 2 receptor overexpression activates the vascular kinin system and causes vasodilation J. Clin. Invest. 104 1999 925 935
58. L.M. Leeb-Lundberg, F. Marceau, W. Muller-Esterl, D.J. Pettibone, and B.L. Zuraw International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences Pharmacol. Rev. 57 2005 27 77
59. E.L. Schiffrin, J.B. Park, H.D. Intengan, and R.M. Touyz Correction of arterial structure and endothelial dysfunction in human essential hypertension by the angiotensin receptor antagonist losartan Circulation 101 2000 1653 1659