Induction of HO-1 and redox signaling in endothelial cells by advanced glycation end products: A role for Nrf2 in vascular protection in diabetes

Nutrition, Metabolism and Cardiovascular Diseases

Volumn 21, Issue 4, 2011, Pages 277-285

  He, M ^a   Siow, R C M ^a   Sugden, D ^b   Gao, L ^a   Cheng, X ^a   Mann, G E ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Advanced glycation end products; C Jun terminal kinase; Endothelial cells; Heme oxygenase 1; NQO1; Nrf2 Keap1; Oxidative stress; Redox signaling

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ADVANCED GLYCATION END PRODUCTS BOVINE SERUM ALBUMIN; ADVANCED GLYCATION END PRODUCTS-BOVINE SERUM ALBUMIN; BOVINE SERUM ALBUMIN; HEME OXYGENASE 1; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SCAVENGER; TRANSCRIPTION FACTOR NRF2;

ANIMAL; ARTICLE; BIOSYNTHESIS; CATTLE; CELL CULTURE; CELL NUCLEUS; CYTOLOGY; DIABETES MELLITUS; DRUG EFFECT; DRUG POTENTIATION; ENZYME INDUCTION; GENETICS; HYPERGLYCEMIA; METABOLISM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TIME; VASCULAR ENDOTHELIUM;

ANIMALS; CATTLE; CELL NUCLEUS; CELLS, CULTURED; DIABETES MELLITUS; ENDOTHELIUM, VASCULAR; ENZYME INDUCTION; FREE RADICAL SCAVENGERS; GLYCOSYLATION END PRODUCTS, ADVANCED; HEME OXYGENASE-1; HYPERGLYCEMIA; NAD(P)H DEHYDROGENASE (QUINONE); NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SERUM ALBUMIN, BOVINE; SIGNAL TRANSDUCTION; TIME FACTORS;

BOVINAE;

EID: 79952700675     PISSN: 09394753     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.numecd.2009.12.008     Document Type: Article

References (35)

1. Mazzone T., Chait A., Plutzky J. Cardiovascular disease risk in type 2 diabetes mellitus: insights from mechanistic studies. Lancet 2008, 371:1800-1809.
2. Pugliese G. Do advanced glycation end products contribute to the development of long-term diabetic complications?. Nutr Metab Cardiovasc Dis 2008, 18:457-460.
3. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820.
4. 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 1994, 269:9889-9897.
5. Lee M.Y., Griendling K.K. Redox signaling, vascular function, and hypertension. Antioxid Redox Signal 2008, 10:1045-1059.
6. Gao L., Mann G.E. Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling. Cardiovasc Res 2009, 82:9-20.
7. Ishii T., Itoh K., Takahashi S., Sato H., Yanagawa T., Katoh Y., et al. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 2000, 275:16023-16029.
8. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev 1999, 13:76-86.
9. Tong K.I., Katoh Y., Kusunoki H., Itoh K., Tanaka T., Yamamoto M. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: characterization of the two-site molecular recognition model. Mol Cell Biol 2006, 26:2887-2900.
10. Bierhaus A., Schiekofer S., Schwaninger M., Andrassy M., Humpert P.M., Chen J., et al. Diabetes-associated sustained activation of the transcription factor nuclear factor-kappaB. Diabetes 2001, 50:2792-2808.
11. Sumi D., 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 2004, 53:1841-1850.
12. Baydoun A.R., Emery P.W., Pearson J.D., Mann G.E. Substrate-dependent regulation of intracellular amino acid concentrations in cultured bovine aortic endothelial cells. Biochem Biophys Res Commun 1990, 173:940-948.
13. Oldfield M.D., Bach L.A., Forbes J.M., Nikolic-Paterson D., McRobert A., Thallas V., et al. Advanced glycation end products cause epithelial-myofibroblast transdifferentiation via the receptor for advanced glycation end products (RAGE). J Clin Invest 2001, 108:1853-1863.
14. Schmidt A.M., Hori O., Chen J.X., Li J.F., Crandall J., Zhang J., et al. Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice. A potential mechanism for the accelerated vasculopathy of diabetes. J Clin Invest 1995, 96:1395-1403.
15. Warboys C.M., Toh H.B., Fraser P.A. Role of NADPH oxidase in retinal microvascular permeability increase by RAGE activation. Invest Ophthalmol Vis Sci 2009, 50:1319-1328.
16. Daiber A., Oelze M., August M., Wendt M., Sydow K., Wieboldt H., et al. Detection of superoxide and peroxynitrite in model systems and mitochondria by the luminol analogue L-012. Free Radic Res 2004, 38:259-269.
17. Churchman A.T., Anwar A.A., Li F.Y., Sato H., Ishii T., Mann G.E., et al. Transforming Growth Factorbeta-1 elicits Nrf2-mediated antioxidant responses in aortic smooth muscle cells. J Cell Mol Med 2009, 13:2282-2292.
18. Bayraktutan U., Draper N., Lang D., Shah A.M. Expression of functional neutrophil-type NADPH oxidase in cultured rat coronary microvascular endothelial cells. Cardiovasc Res 1998, 38:256-262.
19. Cai H., Griendling K.K., Harrison D.G. The vascular NAD(P)H oxidases as therapeutic targets in cardiovascular diseases. Trends Pharmacol Sci 2003, 24:471-478.
20. Watanabe N., Zmijewski J.W., Takabe W., Umezu-Goto M., Le G.C., Sekine A., et al. Activation of mitogen-activated protein kinases by lysophosphatidylcholine-induced mitochondrial reactive oxygen species generation in endothelial cells. Am J Pathol 2006, 168:1737-1748.
21. Anwar A.A., Li F.Y., Leake D.S., Ishii T., Mann G.E., Siow R.C. Induction of heme oxygenase 1 by moderately oxidized low-density lipoproteins in human vascular smooth muscle cells: role of mitogen-activated protein kinases and Nrf2. Free Radic Biol Med 2005, 39:227-236.
22. Ishii T., Itoh K., Ruiz E., Leake D.S., Unoki H., Yamamoto M., et al. Role of Nrf2 in the regulation of CD36 and stress protein expression in murine macrophages: activation by oxidatively modified LDL and 4-hydroxynonenal. Circ Res 2004, 94:609-616.
23. Vandesompele J., De P.K., Pattyn F., Poppe B., Van R.N., De P.A., et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 2002, 3. RESEARCH0034.
24. Zhu H., Itoh K., Yamamoto M., Zweier J.L., Li Y. Role of Nrf2 signaling in regulation of antioxidants and phase 2 enzymes in cardiac fibroblasts: protection against reactive oxygen and nitrogen species-induced cell injury. FEBS Lett 2005, 579:3029-3036.
25. Wautier M.P., Chappey O., Corda S., Stern D.M., Schmidt A.M., Wautier J.L. Activation of NADPH oxidase by AGE links oxidant stress to altered gene expression via RAGE. Am J Physiol Endocrinol Metab 2001, 280:E685-E694.
26. Liu J., Zhao S., Tang J., Li Z., Zhong T., Liu Y., et al. Advanced glycation end products and lipopolysaccharide synergistically stimulate proinflammatory cytokine/chemokine production in endothelial cells via activation of both mitogen-activated protein kinases and nuclear factor-kappaB. FEBS J 2009, 276:4598-4606.
27. El-Osta A., Brasacchio D., Yao D., Pocai A., Jones P.L., Roeder R.G., et al. Transient high glucose causes persistent epigenetic changes and altered gene expression during subsequent normoglycemia. J Exp Med 2008, 205:2409-2417.
28. Li L., Renier G. Activation of nicotinamide adenine dinucleotide phosphate (reduced form) oxidase by advanced glycation end products links oxidative stress to altered retinal vascular endothelial growth factor expression. Metabolism 2006, 55:1516-1523.
29. Siow R.C., Sato H., Mann G.E. Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide?. Cardiovasc Res 1999, 41:385-394.
30. Ryter S.W., Alam J., Choi A.M. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev 2006, 86:583-650.
31. Ross D., Kepa J.K., Winski S.L., Beall H.D., Anwar A., Siegel D. NAD(P)H:quinone oxidoreductase 1 (NQO1): chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem Biol Interact 2000, 129:77-97.
32. Anilkumar N., Weber R., Zhang M., Brewer A., Shah A.M. Nox4 and nox2 NADPH oxidases mediate distinct cellular redox signaling responses to agonist stimulation. Arterioscler Thromb Vasc Biol 2008, 28:1347-1354.
33. Cave A.C., Brewer A.C., Narayanapanicker A., Ray R., Grieve D.J., Walker S., et al. NADPH oxidases in cardiovascular health and disease. Antioxid Redox Signal 2006, 8:691-728.
34. Wu C.C., Hsieh C.W., Lai P.H., Lin J.B., Liu Y.C., Wung B.S. Upregulation of endothelial heme oxygenase-1 expression through the activation of the JNK pathway by sublethal concentrations of acrolein. Toxicol Appl Pharmacol 2006, 214:244-252.
35. Levy S., Jaiswal A.K., Forman H.J. The role of c-Jun phosphorylation in EpRE activation of phase II genes. Free Radic Biol Med 2009, 47:1172-1179.