NADPH oxidase contributes to vascular inflammation, insulin resistance, and remodeling in the transgenic (mRen2) rat

Hypertension

Volumn 50, Issue 2, 2007, Pages 384-391

  Wei, Yongzhong ^a,b   Whaley Connell, Adam T ^a,b   Chen, Kemin ^a   Habibi, Javad ^a,b   Uptergrove, Grace M E ^a   Clark, Suzanne E ^a,b   Stump, Craig S ^b   Ferrario, Carlos M ^c   Sowers, James R ^a,b,d,e,f  

^a UNIVERSITY OF MISSOURI   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

^d MU Diabetes and Cardiovascular Center   (United States)

^e Division of Endocrinology   (United States)

^f University of Missouri   (United States)

Author keywords

Apoptosis; Insulin resistance; NADPH oxidase; Ren2 rat; ROS; Vascular inflammation

Indexed keywords

ACETYLCYSTEINE; ANGIOTENSIN II; C REACTIVE PROTEIN; CATALASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INSULIN; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RENIN; SUPEROXIDE DISMUTASE; TEMPOL; TUMOR NECROSIS FACTOR ALPHA; VALSARTAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; APOPTOSIS; ARTICLE; BLOOD PRESSURE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IN VIVO STUDY; INSULIN RESISTANCE; MALE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SPRAGUE DAWLEY RAT; STATISTICAL SIGNIFICANCE; TRANSGENE; TRANSGENIC RAT; VASCULITIS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BLOOD PRESSURE; BLOTTING, WESTERN; C-REACTIVE PROTEIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; INSULIN RESISTANCE; MALE; MUSCLE, SMOOTH, VASCULAR; NADPH OXIDASE; PROBABILITY; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SENSITIVITY AND SPECIFICITY; SUPEROXIDE DISMUTASE; TETRAZOLES; VALINE; VASCULITIS;

EID: 34547637839     PISSN: 0194911X     EISSN: None     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.107.089284     Document Type: Article

References (46)

1. Willerson JT, Ridker PM. Inflammation as a cardiovascular risk factor. Circulation. 2004;109(21 Suppl 1):II2-II10.
2. Roberts WL. CDC/AHA Workshop on Markers of Inflammation and Cardiovascular Disease: Application to Clinical and Public Health Practice: laboratory tests available to assess inflammation-performance and standardization: a background paper. Circulation. 2004;110:e572-e576.
3. Wei Y, Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, Morris EM, Szary N, Manrique C, Stump CS. Angiotensin II induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem. 2006;281:35137-35146.
4. 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. 1996;97:1916-1923.
5. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res. 2000;86:494-501.
6. Touyz RM. Reactive oxygen species, vascular oxidative stress, and redox signaling in hypertension: what is the clinical significance? Hypertension. 2004;44:248-252.
7. Tain YL, Baylis C. Dissecting the causes of oxidative stress in an in vivo model of hypertension. Hypertension. 2006;48:828-829.
8. O'Donnell VB, Freeman BA. Interactions between nitric oxide and lipid oxidation pathways: implications for vascular disease. Circ Res. 2001;88:12-21.
9. Hotamisligil GS, Arner P, Caro JF, Atkinson RL, Spiegelman BM. Increased adipose tissue expression of tumor necrosis factor-alpha in human obesity and insulin resistance. J Clin Invest. 1995;95:2409-2415.
10. Fard A, Tuck CH, Donis JA, Sciacca R, Di Tullio MR, Wu HD, Bryant TA, Chen NT, Torres-Tamayo M, Ramasamy R, Berglund L, Ginsberg HN, Homma S, Cannon PJ. Acute elevations of plasma asymmetric dimethylarginine and impaired endothelial function in response to a high-fat meal in patients with type 2 diabetes. Arterioscler Thromb Vasc Biol. 2000;20:2039-2044.
11. Niemann-Jonsson A, Ares MP, Yan ZQ, Bu DX, Fredrikson GN, Branen L, Porn-Ares I, Nilsson AH, Nilsson J. Increased rate of apoptosis in intimal arterial smooth muscle cells through endogenous activation of TNF receptors. Arterioscler Thromb Vasc Biol. 2001;21:1909-1914.
12. Tang V, Dhirapong A, Yabes AP, Weiss RH. TNF-alpha-mediated apoptosis in vascular smooth muscle cells requires p73. Am J Physiol Cell Physiol. 2005;289:C199-C206.
13. Touyz RM, Deschepper C, Park JB, He G, Chen X, Neves MF, Virdis A, Schiffrin EL. Inhibition of mitogen-activated protein/extracellular signal-regulated kinase improves endothelial function and attenuates Ang II-induced contractility of mesenteric resistance arteries from spontaneously hypertensive rats. J Hypertens. 2002;20:1127-1134.
14. Kuboki K, Jiang ZY, Takahara N, Ha SW, Igarashi M, Yamauchi T, Feener EP, Herbert TP, Rhodes CJ, King GL. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo : a specific vascular action of insulin. Circulation. 2000;101:676-681.
15. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest. 1996;97:2601-2610.
16. Cersosimo E, Defronzo RA. Insulin resistance and endothelial dysfunction: the road map to cardiovascular diseases. Diabetes Metab Res Rev. 2006;22:423-436.
17. Lu X, Kambe F, Cao X, Yoshida T, Ohmori S, Murakami K, Kaji T, Ishii T, Zadworny D, Seo H. DHCR24-knockout embryonic fibroblasts are susceptible to serum withdrawal-induced apoptosis because of dysfunction of caveolae and insulin-Akt-Bad signaling. Endocrinology. 2006;147:3123-3132.
18. Dandona P, Aljada A, Mohanty P. The anti-inflammatory and potential anti-atherogenic effect of insulin: a new paradigm. Diabetologia. 2002;45:924-930.
19. Sowers JR. Insulin resistance and hypertension. Am J Physiol Heart Circ Physiol. 2004;286:H1597-H1602.
20. Blendea MC, Jacobs D, Stump CS, McFarlane SI, Ogrin C, Bahtyiar G, Stas S, Kumar P, Sha Q, Ferrario CM, Sowers JR. Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am J Physiol Endocrinol Metab. 2005;288:E353-E359.
21. Kinnick TR, Youngblood EB, O'Keefe MP, Saengsirisuwan V, Teachey MK, Henriksen EJ. Modulation of insulin resistance and hypertension by voluntary exercise training in the TG(mREN2)27 rat. J Appl Physiol. 2002;93:805- 812.
22. Moriguchi A, Brosnihan KB, Kumagai H, Ganten D, Ferrario CM. Mechanisms of hypertension in transgenic rats expressing the mouse Ren-2 gene. Am J Physiol. 1994;266(4 Pt 2):R1273-R1279.
23. Whaley-Connell A, Chowdhury N, Hayden MR, Stump CS, Habibi J, Wiedmeyer CE, Gallagher PE, Tallant EA, Cooper SA, Link CD, Ferrario CM, Sowers JR. Oxidative stress and glomerular filtration barrier injury: role of the renin-angiotensin system in the Ren2 transgenic rat. Am J Physiol Renal Physiol. 2006;291:F1308-F1314.
24. Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev N, Alexander RW. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation. 2005;111:2347-2355.
25. Nathan C. Specificity of a third kind: reactive oxygen and nitrogen intermediates in cell signaling. J Clin Invest. 2003;111:769-778.
26. Clempus RE, Griendling KK. Reactive oxygen species signaling in vascular smooth muscle cells. Cardiovasc Res. 2006;71:216-225.
27. Stump CS, Henriksen EJ, Wei Y, Sowers JR. The metabolic syndrome: role of skeletal muscle metabolism. Ann Med. 2006;38:389-402.
28. Abo A, Pick E, Hall A, Totty N, Teahan CG, Segal AW. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature. 1991;353:668-670.
29. Rotrosen D, Yeung CL, Leto TL, Malech HL, Kwong CH. Cytochrome b558: the flavin-binding component of the phagocyte NADPH oxidase. Science. 1992;256:1459-1462.
30. Giacchetti G, Sechi LA, Rilli S, Carey RM. The renin-angiotensin- aldosterone system, glucose metabolism and diabetes. Trends Endocrinol Metab. 2005;16:120-126.
31. Collins T, Cybulsky MI. NF-kappaB: pivotal mediator or innocent bystander in atherogenesis? J Clin Invest. 2001;107:255-264.
32. Ashton AW, Ware GM, Kaul DK, Ware JA. Inhibition of tumor necrosis factor alpha-mediated NFkappaB activation and leukocyte adhesion, with enhanced endothelial apoptosis, by G protein-linked receptor (TP) ligands. J Biol Chem. 2003;278:11858-11866.
33. Barath P, Fishbein MC, Cao J, Berenson J, Helfant RH, Forrester JS. Detection and localization of tumor necrosis factor in human atheroma. Am J Cardiol. 1990;65:297-302.
34. Wolf G, Wenzel UO. Angiotensin II and cell cycle regulation. Hypertension. 2004;43:693-698.
35. Taniyama Y, Hitomi H, Shah A, Alexander RW, Griendling KK. Mechanisms of reactive oxygen species-dependent downregulation of insulin receptor substrate-1 by angiotensin II. Arterioscler Thromb Vasc Biol. 2005;25:1142-1147.
36. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension. 2003;42:1075-1081.
37. Brasier AR, Recinos A, III, Eledrisi MS. Vascular inflammation and the renin-angiotensin system. Arterioscler Thromb Vasc Biol. 2002;22:1257-1266.
38. Han Y, Runge MS, Brasier AR. Angiotensin II induces interleukin-6 transcription in vascular smooth muscle cells through pleiotropic activation of nuclear factor-kappa B transcription factors. Circ Res. 1999;84:695-703.
39. Muller DN, Dechend R, Mervaala EM, Park JK, Schmidt F, Fiebeler A, Theuer J, Breu V, Ganten D, Haller H, Luft FC. NF-kappaB inhibition ameliorates angiotensin II-induced inflammatory damage in rats. Hypertension. 2000;35:193-201.
40. Sun Y, Ahokas RA, Bhattacharya SK, Gerling IC, Carbone LD, Weber KT. Oxidative stress in aldosteronism. Cardiovasc Res. 2006;71:300-309.
41. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, Nakayama O, Makishima M, Matsuda M, Shimomura I. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest. 2004;114:1752-1761.
42. Moncada S, Higgs EA. The discovery of nitric oxide and its role in vascular biology. Br J Pharmacol. 2006;147 Suppl 1:S193-S201.
43. 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.
44. Sampaio WO, Souza dos Santos RA, Faria-Silva R, da Mata Machado LT, Schiffrin EL, Touyz RM. Angiotensin-(1-7) through receptor Mas mediates endothelial nitric oxide synthase activation via Akt-dependent pathways. Hypertension. 2007;49:185-192.
45. Uysal KT, Wiesbrock SM, Marino MW, Hotamisligil GS. Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature. 1997;389:610-614.
46. Picchi A, Gao X, Belmadani S, Potter BJ, Focardi M, Chilian WM, Zhang C. Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res. 2006;99:69-77.