Nox1-based NADPH oxidase-derived superoxide is required for VSMC activation by advanced glycation end-products

Free Radical Biology and Medicine

Volumn 42, Issue 11, 2007, Pages 1671-1679

  San Martin, Alejandra ^a   Foncea, Rocio ^b   Laurindo, Francisco R ^c   Ebensperger, Roberto ^b   Griendling, Kathy K ^a   Leighton, Federico ^b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Advanced glycated end products; Diabetes; Free radicals; Inflammation; iNOS; NADPH oxidase; Nox1; ROS; Superoxide

Indexed keywords

3 NITROTYROSINE; ADVANCED GLYCATION END PRODUCT; CATALASE; DIPHENYLIODONIUM SALT; GLYCOPROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LUCIGENIN; MANGANESE (III) TETRAKIS (4 BENZOIC ACID)PORPHYRIN; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; PORPHYRIN DERIVATIVE; PROTEIN NOX1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SMALL INTERFERING RNA; SUPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL STIMULATION; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG EFFECT; ELECTRON SPIN RESONANCE; ENZYME SUBUNIT; GLYCATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VASCULAR SMOOTH MUSCLE;

ANIMALS; CELLS, CULTURED; GLYCOSYLATION END PRODUCTS, ADVANCED; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NADH, NADPH OXIDOREDUCTASES; NF-KAPPA B; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SUPEROXIDES; TRANSCRIPTION, GENETIC; TYROSINE; VASCULAR DISEASES;

EID: 34247209253     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2007.02.002     Document Type: Article

References (51)

1. Schwartz S.M., Campbell G.R., and Campbell J.H. Replication of smooth muscle cells in vascular disease. Circ. Res. 58 (1986) 427-444
2. Thyberg J., Hedin U., Sjolund M., Palmberg L., and Bottger B.A. Regulation of differentiated properties and proliferation of arterial smooth muscle cells. Arteriosclerosis 10 (1990) 966-990
3. Ruderman N.B., Williamson J.R., and Brownlee M. Glucose and diabetic vascular disease. FASEB J. 6 (1992) 2905-2914
4. Yan S.F., Ramasamy R., Naka Y., and Schmidt A.M. Glycation, inflammation, and RAGE: a scaffold for the macrovascular complications of diabetes and beyond. Circ. Res. 93 (2003) 1159-1169
5. Namiki M. Chemistry of Maillard reactions: recent studies on the browning reaction mechanism and the development of antioxidants and mutagens. Adv. Food Res. 32 (1988) 115-184
6. Vlassara H., Bucala R., and Striker L. Pathogenic effects of advanced glycosylation: biochemical, biologic, and clinical implications for diabetes and aging. Lab. Invest. 70 (1994) 138-151
7. Schmidt A.M., Vianna M., Gerlach M., Brett J., Ryan J., Kao J., et al. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J. Biol. Chem. 267 (1992) 14987-14997
8. Bierhaus A., Chevion S., Chevion M., Hofmann M., Quehenberger P., Illmer T., et al. Advanced glycation end product-induced activation of NF-kappaB is suppressed by alpha-lipoic acid in cultured endothelial cells. Diabetes 46 (1997) 1481-1490
9. Wautier J.L., Wautier M.P., Schmidt A.M., Anderson G.M., Hori O., Zoukourian C., et al. Advanced glycation end products (AGEs) on the surface of diabetic erythrocytes bind to the vessel wall via a specific receptor inducing oxidant stress in the vasculature: a link between surface-associated AGEs and diabetic complications. Proc. Natl. Acad. Sci. USA 91 (1994) 7742-7746
10. Yan S.D., Schmidt A.M., Anderson G.M., Zhang J., Brett J., Zou Y.S., et al. Enhanced cellular oxidant stress by the interaction of advanced glycation end products with their receptors/binding proteins. J. Biol. Chem. 269 (1994) 9889-9897
11. Zhang M., Kho A.L., Anilkumar N., Chibber R., Pagano P.J., Shah A.M., et al. Glycated proteins stimulate reactive oxygen species production in cardiac myocytes: involvement of Nox2 (gp91phox)-containing NADPH oxidase. Circulation 113 (2006) 1235-1243
12. Basta G., Lazzerini G., Del Turco S., Ratto G.M., Schmidt A.M., and De Caterina R. At least 2 distinct pathways generating reactive oxygen species mediate vascular cell adhesion molecule-1 induction by advanced glycation end products. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1401-1407
13. Mohazzab K.M., and Wolin M.S. Sites of superoxide anion production detected by lucigenin in calf pulmonary artery smooth muscle. Am. J. Physiol. 267 6 Pt. 1 (1994) L815-L822
14. Rajagopalan S., Kurz S., Munzel T., Tarpey M., Freeman B.A., Griendling K.K., et al. 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 (1996) 1916-1923
15. 2 in angiotensin II-induced vascular hypertrophy. Hypertension 32 (1998) 488-495
16. Tummala P.E., Chen X.L., Sundell C.L., Laursen J.B., Hammes C.P., Alexander R.W., et al. Angiotensin II induces vascular cell adhesion molecule-1 expression in rat vasculature: a potential link between the renin-angiotensin system and atherosclerosis. Circulation 100 (1999) 1223-1229
17. Wang H.D., Pagano P.J., Du Y., Cayatte A.J., Quinn M.T., Brecher P., et al. Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circ. Res. 82 (1998) 810-818
18. Wang H.D., Xu S., Johns D.G., Du Y., Quinn M.T., Cayatte A.J., et al. Role of NADPH oxidase in the vascular hypertrophic and oxidative stress response to angiotensin II in mice [see comment]. Circ. Res. 88 (2001) 947-953
19. Babior B.M. The respiratory burst oxidase. Curr. Opin. Hematol. 2 (1995) 55-60
20. Griendling K.K., and Ushio-Fukai M. Redox control of vascular smooth muscle proliferation. J. Lab. Clin. Med. 132 (1998) 9-15
21. Lassegue B., Sorescu D., Szocs K., Yin Q., Akers M., Zhang Y., et al. Novel gp91(phox) homologues in vascular smooth muscle cells: Nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways [see comment]. Circ. Res. 88 (2001) 888-894
22. Hilenski L.L., Clempus R.E., Quinn M.T., Lambeth J.D., and Griendling K.K. Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells [see comment]. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 677-683
23. Wautier M.P., Chappey O., Corda S., Stern D.M., Schmidt A.M., and Wautier J.L. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am. J. Physiol. Endocrinol. Metab. 280 (2001) E685-E694
24. Pertynska-Marczewska M., Kiriakidis S., Wait R., Beech J., Feldmann M., and Paleolog E.M. Advanced glycation end products upregulate angiogenic and pro-inflammatory cytokine production in human monocyte/macrophages. Cytokine 28 (2004) 35-47
25. Poteser M., and Wakabayashi I. Serum albumin induces iNOS expression and NO production in RAW 267.4 macrophages. Br. J. Pharmacol. 143 (2004) 143-151
26. Sumi D., and Ignarro L.J. Regulation of inducible nitric oxide synthase expression in advanced glycation end product-stimulated RAW 264.7 cells: the role of heme oxygenase-1 and endogenous nitric oxide. Diabetes 53 (2004) 1841-1850
27. Hecker M., Cattaruzza M., and Wagner A.H. Regulation of inducible nitric oxide synthase gene expression in vascular smooth muscle cells. Gen. Pharmacol. 32 (1999) 9-16
28. Morris Jr. S.M., and Billiar T.R. New insights into the regulation of inducible nitric oxide synthesis. Am. J. Physiol. 266 6 Pt. 1 (1994) E829-E839
29. Velarde V., Ullian M.E., Morinelli T.A., Mayfield R.K., and Jaffa A.A. Mechanisms of MAPK activation by bradykinin in vascular smooth muscle cells. Am. J. Physiol. 277 2 Pt. 1 (1999) C253-C261
30. Doi T., Vlassara H., Kirstein M., Yamada Y., Striker G.E., and Striker L.J. Receptor-specific increase in extracellular matrix production in mouse mesangial cells by advanced glycosylation end products is mediated via platelet-derived growth factor. Proc. Natl. Acad. Sci. USA 89 (1992) 2873-2877
31. Pongor S., Ulrich P.C., Bencsath F.A., and Cerami A. Aging of proteins: isolation and identification of a fluorescent chromophore from the reaction of polypeptides with glucose. Proc. Natl. Acad. Sci. USA 81 (1984) 2684-2688
32. Dignam J.D., Martin P.L., Shastry B.S., and Roeder R.G. Eukaryotic gene transcription with purified components. Methods Enzymol. 101 (1983) 582-598
33. Lin C.L., Huang C.C., Yu C.C., Yang H.Y., Chuang F.R., and Yang C.W. Reduction of advanced glycation end product levels by on-line hemodiafiltration in long-term hemodialysis patients. Am. J. Kidney Dis. 42 (2003) 524-531
34. Satoh H., Togo M., Hara M., Miyata T., Han K., Maekawa H., et al. Advanced glycation endproducts stimulate mitogen-activated protein kinase and proliferation in rabbit vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 239 (1997) 111-115
35. Touyz R.M., Tabet F., and Schiffrin E.L. Redox-dependent signalling by angiotensin II and vascular remodelling in hypertension. Clin. Exp. Pharmacol. Physiol. 30 (2003) 860-866
36. Soulis T., Thallas V., Youssef S., Gilbert R.E., McWilliam B.G., Murray-McIntosh R.P., et al. Advanced glycation end products and their receptors co-localise in rat organs susceptible to diabetic microvascular injury. Diabetologia 40 (1997) 619-628
37. Hecker M., Preiss C., Schini-Kerth V.B., and Busse R. Antioxidants differentially affect nuclear factor kappa B-mediated nitric oxide synthase expression in vascular smooth muscle cells. FEBS Lett. 380 (1996) 224-228
38. Spink J., Cohen J., and Evans T.J. The cytokine responsive vascular smooth muscle cell enhancer of inducible nitric oxide synthase: activation by nuclear factor-kappa B. J. Biol. Chem. 270 (1995) 29541-29547
39. Teng X., Zhang H., Snead C., and Catravas J.D. Molecular mechanisms of iNOS induction by IL-1 beta and IFN-gamma in rat aortic smooth muscle cells. Am. J. Physiol. Cell Physiol. 282 (2002) C144-C152
40. Li N., and Karin M. Is NF-kappaB the sensor of oxidative stress?. FASEB J. 13 (1999) 1137-1143
41. Li P.F., Dietz R., and von Harsdorf R. Differential effect of hydrogen peroxide and superoxide anion on apoptosis and proliferation of vascular smooth muscle cells. Circulation 96 (1997) 3602-3609
42. Su B., Mitra S., Gregg H., Flavahan S., Chotani M.A., Clark K.R., et al. Redox regulation of vascular smooth muscle cell differentiation. Circ. Res. 89 (2001) 39-46
43. 2 for platelet-derived growth factor signal transduction. Science 270 (1995) 296-299
44. Fries D.M., Paxinou E., Themistocleous M., Swanberg E., Griendling K.K., Salvemini D., et al. Expression of inducible nitric-oxide synthase and intracellular protein tyrosine nitration in vascular smooth muscle cells: role of reactive oxygen species. J. Biol. Chem. 278 (2003) 22901-22907
45. Schmidt A.M., Yan S.D., Yan S.F., and Stern D.M. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J. Clin. Invest. 108 (2001) 949-955
46. Kleinert H., Schwarz P.M., and Forstermann U. Regulation of the expression of inducible nitric oxide synthase. Biol. Chem. 384 (2003) 1343-1364
47. Seshiah P.N., Weber D.S., Rocic P., Valppu L., Taniyama Y., and Griendling K.K. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ. Res. 91 (2002) 406-413
48. Spink J., Cohen J., and Evans T.J. The cytokine responsive vascular smooth muscle cell enhancer of inducible nitric oxide synthase: activation by nuclear factor-kappa B. J. Biol. Chem. 270 (1995) 29541-29547
49. Griendling K.K., Sorescu D., and Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ. Res. 86 (2000) 494-501
50. Chabrashvili T., Tojo A., Onozato M.L., Kitiyakara C., Quinn M.T., Fujita T., et al. Expression and cellular localization of classic NADPH oxidase subunits in the spontaneously hypertensive rat kidney. Hypertension 39 (2002) 269-274
51. Szocs K., Lassegue B., Sorescu D., Hilenski L.L., Valppu L., Couse T.L., et al. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 21-27