Interleukin-10 counteracts impaired endothelium-dependent relaxation induced by ANG II in murine aortic rings

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 292, Issue 6, 2007, Pages

  Zemse, Saiprasad M ^a   Hilgers, Rob H P ^a   Webb, R Clinton ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

NADPH oxidase

Indexed keywords

ACETYLCHOLINE; ANGIOTENSIN II; APOCYNIN; INTERLEUKIN 10; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; WATER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CORONARY ARTERY DILATATION; DRUG EFFECT; ENDOTHELIUM CELL; HEART MUSCLE RELAXATION; IMMUNOHISTOCHEMISTRY; INCUBATION TIME; LONG TERM CARE; MALE; MOUSE; MYOGRAPHY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATISTICAL SIGNIFICANCE; TEMPERATURE; VASCULAR RING; WESTERN BLOTTING;

ACETOPHENONES; ACETYLCHOLINE; ANGIOTENSIN II; ANIMALS; AORTA; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; INTERLEUKIN-10; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MYOGRAPHY; NADPH OXIDASE; ORGAN CULTURE TECHNIQUES; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; VASODILATION; VASODILATOR AGENTS;

EID: 34447507847     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00456.2006     Document Type: Article

References (46)

1. Alexander RW, Brock TA, Gimbrone MA Jr, Rittenhouse SE. Angiotensin increases inositol trisphosphate and calcium in vascular smooth muscle. Hypertension 7: I105-I109, 1985.
2. Berk BC, Vekshtein V, Gordon HM, Tsuda T. Angiotensin II-stimulated protein synthesis in cultured vascular smooth muscle cells. Hypertension 13: 305-314, 1989.
3. Berry C, Hamilton CA, Brosnan MJ, Magill FG, Berg GA, McMurray JJV, Dominiczak AF. Investigation into the sources of superoxide in human blood vessels: angiotensin II increases superoxide production in human internal mammary arteries. Circulation 101: 2206-2212, 2000.
4. Bossowska AKRB, Bossowski A, Galar B, Sowinski P. Cytokines in patients with ischaemic heart disease or myocardial infarction. Kardiologia Polska 59: 105-114, 2003.
5. Cai H, Griendling KK, Harrison DG. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci 24: 471-478, 2003.
6. Cattaruzza M, Slodowski W, Stojakovic M, Krzesz R, Hecker M. Interleukin-10 induction of nitric-oxide synthase expression attenuates CD40-mediated interleukin-12 synthesis in human endothelial cells. J Biol Chem 278: 37874-37880, 2003.
7. phox contributes to NADPH oxidase activity in aortic fibroblasts but not smooth muscle cells. Am J Physiol Heart Circ Physiol 285: H2284-H2289, 2003.
8. Cherry PD, Omar HA, Farrell KA, Stuart JS, Wolin MS. Superoxide anion inhibits cGMP-associated bovine pulmonary arterial relaxation. Am J Physiol Heart Circ Physiol 259: H1056-H1062, 1990.
9. Di Wang H, Pagano PJ, Du Y, Cayatte AJ, Quinn MT, Brecher P, Cohen RA. Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circ Res 82: 810-818, 1998.
10. Fortuno A, Jose GS, Moreno MU, Diez J, Zalba G. Oxidative stress and vascular remodelling. Exp Physiol 90: 457-462, 2005.
11. Fukui T, Ishizaka N, Rajagopalan S, Laursen JB, Capers Q, Taylor WR, Harrison DG, de Leon H, Wilcox JN, Griendling KK. p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ Res 80: 45-51, 1997.
12. Gorlach A, Brandes RP, Nguyen K, Amidi M, Dehghani F, Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res 87: 26-32, 2000.
13. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 74: 1141-1148, 1994.
14. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501, 2000.
15. Gryglewski RJ, Palmer RMJ, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 320: 454-456, 1986.
16. Gunnett CA, Heistad DD, Berg DJ, Faraci FM. IL-10 deficiency increases superoxide and endothelial dysfunction during inflammation. Am J Physiol Heart Circ Physiol 279: H1555-H1562, 2000.
17. Gunnett CA, Heistad DD, Faraci FM. Interleukin-10 protects nitric oxide-dependent relaxation during diabetes: role of superoxide. Diabetes 51: 1931-1937, 2002.
18. Heistad DD. A radical review of the superfamily of cardiovascular risk factors. Circulation 67: 805-809, 2003.
19. Ishibashi M, Egashira K, Zhao Q, Hiasa K, Ohtani K, Ihara Y, Charo IF, Kura S, Tsuzuki T, Takeshita A, Sunagawa K. Bone marrowderived monocyte chemoattractant protein-1 receptor CCR2 is critical in angiotensin II-induced acceleration of atherosclerosis and aneurysm formation in hypercholesterolemic mice. Arterioscler Thromb Vasc Biol 24: e174-e178, 2004.
20. Kofler SNT, Weis M. Role of cytokines in cardiovascular diseases: a focus on endothelial responses to inflammation. Clin Sci (Colch) 108: 205-213, 2005.
21. Kuga SOT, Niiro H, Nunoi H, Nemoto Y, Nakano T, Ogo T, Umei T, Niho Y. Suppression of superoxide anion production by interleukin-10 is accompanied by a downregulation of the genes for subunit proteins of NADPH oxidase. Exp Haematol 24: 151-157, 1996.
22. Lassegue B, Sorescu D, Szocs K, Yin Q, Akers M, Zhang Y, Grant SL, Lambeth JD, Griendling KK. Novel gp91phox homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ Res 88: 888-894, 2001.
23. Laursen JB, Rajagopalan S, Galis Z, Tarpey M, Freeman BA, Harrison DG. Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation 95: 588-593, 1997.
24. Le Moine O, Louis H, Stordeur P, Collet JM, Goldman M, Deviere J. Role of reactive oxygen intermediates in interleukin 10 release after cold liver ischemia and reperfusion in mice. Gastroenterology 113: 1701-1706, 1997.
25. Mallat Z, Besnard S, Duriez M, Deleuze V, Emmanuel F, Bureau MF, Soubrier F, Esposito B, Duez H, Fievet C, Staels B, Duverger N, Scherman D, Tedgui A. Protective role of interleukin-10 in atherosclerosis. Circ Res 85: 17e-24e, 1999.
26. Mollnau H, Wendt M, Szocs K, Lassegue B, Schulz E, Oelze M, Li H, Bodenschatz M, August M, Kleschyov AL, Tsilimingas N, Walter U, Forstermann U, Meinertz T, Griendling K, Munzel T. Effects of angiotensin II infusion on the expression and function of NAD(P)H oxidase and components of nitric oxide/cGMP signaling. Circ Res 90: 58e-65e, 2002.
27. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19: 683-765, 2001.
28. Omar HACP, Mortelliti MP, Burke-Wolin T, Wolin MS. Inhibition of coronary artery superoxide dismutase attenuates endothelium-dependent and -independent nitrovasodilator relaxation. Circ Res 69: 601-608, 1991.
29. Orange S, Rasko JE, Thompson JF, Vaughan J, Olive E, Pedler M, Horvath JS, Hennessy A. Interleukin-10 regulates arterial pressure in early primate pregnancy. Cytokine 29: 176-185, 2005.
30. Passerini AG, Polacek DC, Shi C, Francesco NM, Manduchi E, Grant GR, Pritchard WF, Powell S, Chang GY, Stoeckert CJ Jr, Davies PF. Coexisting proinflammatory and antioxidative endothelial transcription profiles in a disturbed flow region of the adult porcine aorta. Proc Natl Acad Sci USA 101: 2482-2487, 2004.
31. Pinderski LJ, Fischbein MP, Subbanagounder G, Fishbein MC, Kubo N, Cheroutre H, Curtiss LK, Berliner JA, Boisvert WA. Overexpression of interleukin-10 by activated T lymphocytes inhibits atherosclerosis in LDL receptor-deficient mice by altering lymphocyte and macrophage phenotypes. Circ Res 90: 1064-1071, 2002.
32. Pollman MJ, Yamada T, Horiuchi M, Gibbons GH. Vasoactive substances regulate vascular smooth muscle cell apoptosis: countervailing influences of nitric oxide and angiotensin II. Circ Res 79: 748-756, 1996.
33. Pueyo ME, Arnal JF, Rami J, Michel JB. Angiotensin II stimulates the production of NO and peroxynitrite in endothelial cells. Am J Physiol Cell Physiol 274: C214-C220, 1998.
34. Raines EW, Garton KJ, Ferri N. Beyond the endothelium: NF-κB regulation of smooth muscle function. Circ Res 94: 706-708, 2004.
35. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, Harrison DG. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation. Contribution to alterations of vasomotor tone. J Clin Invest 97: 1916-1923, 1996.
36. Rey FE, Li XC, Carretero OA, Garvin JL, Pagano PJ. Perivascular superoxide anion contributes to impairment of endothelium-dependent relaxation: role of gp91phox. Circulation 106: 2497-2502, 2002.
37. Ryan MJ, Didion SP, Mathur S, Faraci FM, Sigmund CD. Angiotensin II-induced vascular dysfunction is mediated by the AT1A receptor in mice. Hypertension 43: 1074-1079, 2004.
38. Schiffrin EL, Touyz RM. Inflammation and vascular hypertrophy induced by angiotensin II: role of NADPH oxidase-derived reactive oxygen species independently of blood pressure elevation? Arterioscler Thromb Vasc Biol 23: 707-709, 2003.
39. Sowers JR. Hypertension, angiotensin II, and oxidative stress. N Engl J Med 346: 1999-2001, 2002.
40. Tham DM, Martin-McNulty B, Wang Y, Wilson DW, Vergona R, Sullivan ME, Dole W, Rutledge JC. Angiotensin II is associated with activation of NF-κB-mediated genes and downregulation of PPARs. Physiol Genomics 11: 21-30, 2002.
41. Torres MB, Vega VL, Bedri M, Saad D, Trentzsch H, Reeves RH, De Maio A. IL-10 plasma levels are elevated after LPS injection in splenectomized A/J mice 1. J Surg Res 129: 101-106, 2005.
42. Touyz RM, Chen X, Tabet F, Yao G, He G, Quinn MT, Pagano PJ, Schiffrin EL. Expression of a functionally active gp91phox-containing neutrophil-type NAD(P)H oxidase in smooth muscle cells from human resistance arteries: regulation by angiotensin II. Circ Res 90: 1205-1213, 2002.
43. Touyz RM, Schiffrin EL. ANG II-stimulated superoxide production is mediated via phospholipase D in human vascular smooth muscle cells. Hypertension 34: 976-982, 1999.
44. Uyemura K, Demer LL, Castle SC, Jullien D, Berliner JA, Gately MK, Warrier RR, Pham N, Fogelman AM, Modlin RL. Cross-regulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. J Clin Invest 97: 2130-2138, 1996.
45. Virdis AS, Ernesto L. Vascular inflammation: a role in vascular disease in hypertension? Pathophysiology of hypertension. Curr Opin Nephrol Hypertens 12: 181-187, 2003.
46. Wassmann S, Stumpf M, Strehlow K, Schmid A, Schieffer B, Bohm M, Nickenig G. Interleukin-6 induces oxidative stress and endothelial dysfunction by overexpression of the angiotensin II type 1 receptor. Circ Res 94: 534-541, 2004.