Roles for redox signaling by NADPH oxidase in hyperglycemia-induced heme oxygenase-1 expression in the diabetic retina

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 6, 2013, Pages 4092-4101

  He, Meihua ^a,b,c   Pan, Hong ^a,b,c   Xiao, Chunxia ^a   Pu, Mingliang ^a,b,c  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b Peking University   (China)

^c PEKING UNIVERSITY   (China)

Author keywords

Antioxidant response element; Db db mouse; Diabetic retina; Heme oxygenase 1; Nadph oxidase

Indexed keywords

APOCYNIN; GLUCOSE; HEME OXYGENASE 1; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENSITOMETRY; DIABETES MELLITUS; HYPERGLYCEMIA; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; WESTERN BLOTTING;

ANTIOXIDANT RESPONSE ELEMENT; DB/DB MOUSE; DIABETIC RETINA; HEME OXYGENASE-1; NADPH OXIDASE;

ACETOPHENONES; ANIMALS; ANTIOXIDANT RESPONSE ELEMENTS; BLOTTING, WESTERN; DIABETIC RETINOPATHY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GLUCOSE; HEME OXYGENASE-1; HYPERGLYCEMIA; IMIDAZOLES; MALE; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; NADPH OXIDASE; ORGAN CULTURE TECHNIQUES; OXIDATION-REDUCTION; OXIDATIVE STRESS; PYRROLES; REACTIVE OXYGEN SPECIES; RETINA; SIGNAL TRANSDUCTION;

EID: 84878989596     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12004     Document Type: Article

References (51)

1. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature. 2001;414:813-820.
2. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376:124-136.
3. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283-290.
4. Gaddini L, Villa M, Matteucci A, et al. Early effects of high glucose in retinal tissue cultures renin-angiotensin systemdependent and -independent signaling. Neurobiol Dis. 2009; 35:278-285.
5. Antonetti DA, Barber AJ, Bronson SK, et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes. 2006;55:2401-2411.
6. Sugimoto M, Sasoh M, Ido M, Wakitani Y, Takahashi C, Uji Y. Detection of early diabetic change with optical coherence tomography in type 2 diabetes mellitus patients without retinopathy. Ophthalmologica. 2005;219:379-385.
7. Fletcher EL, Phipps JA, Ward MM, Puthussery T, Wilkinson-Berka JL. Neuronal and glial cell abnormality as predictors of progression of diabetic retinopathy. Curr Pharm Des. 2007; 13:2699-2712.
8. Xiao C, He M, Nan Y, et al. Physiological effects of superoxide dismutase on altered visual function of retinal ganglion cells in db/db mice. PLoS One. 2012;7:e30343.
9. Baynes JW. Role of oxidative stress in development of complications in diabetes. Diabetes. 1991;40:405-412.
10. Du Y, Miller CM, Kern TS. Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic Biol Med. 2003;35:1491-1499.
11. Gao X, Talalay P. Induction of phase 2 genes by sulforaphane protects retinal pigment epithelial cells against photooxidative damage. Proc Natl Acad Sci U S A. 2004;101:10446-10451.
12. Wolin MS. Reactive oxygen species and the control of vascular function. Am J Physiol Heart Circ Physiol. 2009;296:H539-H549.
13. Cheung AK, Fung MK, Lo AC, et al. Aldose reductase deficiency prevents diabetes-induced blood-retinal barrier breakdown, apoptosis, and glial reactivation in the retina of db/db mice. Diabetes. 2005;54:3119-3125.
14. Li J, Wang JJ, Yu Q, Chen K, Mahadev K, Zhang SX. Inhibition of reactive oxygen species by Lovastatin downregulates vascular endothelial growth factor expression and ameliorates blood-retinal barrier breakdown in db/db mice: role of NADPH oxidase 4. Diabetes. 2010;59:1528-1538.
15. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev. 2007;87:245-313.
16. Cave A, Grieve D, Johar S, Zhang M, Shah AM. NADPH oxidasederived reactive oxygen species in cardiac pathophysiology. Philos Trans R Soc Lond B Biol Sci. 2005;360:2327-2334.
17. Gao L, Mann GE. Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling. Cardiovasc Res. 2009;82:9-20.
18. Wu M, Yang S, Elliott MH, et al. Oxidative and endoplasmic reticulum stresses mediate apoptosis induced by modified LDL in human retinal M̈uller cells. Invest Ophthalmol Vis Sci. 2012; 53:4595-4604.
19. Yamagishi S, Nakamura K, Ueda S, Kato S, Imaizumi T. Pigment epithelium-derived factor (PEDF) blocks angiotensin II signaling in endothelial cells via suppression of NADPH oxidase: a novel anti-oxidative mechanism of PEDF. Cell Tissue Res. 2005; 320:437-445.
20. Al-Shabrawey M, Bartoli M, El-Remessy AB, et al. Role of NADPH oxidase and Stat3 in statin-mediated protection against diabetic retinopathy. Invest Ophthalmol Vis Sci. 2008;49: 3231-3238.
21. Yoshida Y, Yamagishi S, Matsui T, et al. Protective role of pigment epithelium-derived factor (PEDF) in early phase of experimental diabetic retinopathy. Diabetes Metab Res Rev. 2009;25:678-686.
22. da Silva JL, Stoltz RA, Dunn MW, Abraham NG, Shibahara S. Diminished heme oxygenase-1 mRNA expression in RPE cells from diabetic donors as quantitated by competitive RT/PCR. Curr Eye Res. 1997;16:380-386.
23. Di FC, Marfella R, Cuzzocrea S, et al. Hyperglycemia in streptozotocin-induced diabetic rat increases infarct size associated with low levels of myocardial HO-1 during ischemia/reperfusion. Diabetes. 2005;54:803-810.
24. Liu X, Wei J, Peng DH, Layne MD, Yet SF. Absence of heme oxygenase-1 exacerbates myocardial ischemia/reperfusion injury in diabetic mice. Diabetes. 2005;54:778-784.
25. Motohashi H, O'Connor T, Katsuoka F, Engel JD, Yamamoto M. Integration and diversity of the regulatory network composed of Maf and CNC families of transcription factors. Gene. 2002; 294:1-12.
26. Shyong MP, Lee FL, Hen WH, et al. Viral delivery of heme oxygenase-1 attenuates photoreceptor apoptosis in an experimental model of retinal detachment. Vision Res. 2008;48: 2394-2402.
27. Geraldes P, Yagi K, Ohshiro Y, et al. Selective regulation of heme oxygenase-1 expression and function by insulin through IRS1/phosphoinositide 3-kinase/Akt-2 pathway. J Biol Chem. 2008;283:34327-34336.
28. Siow RC, Sato H, Mann GE. Heme oxygenase-carbon monoxide signalling pathway in atherosclerosis: anti-atherogenic actions of bilirubin and carbon monoxide? Cardiovasc Res. 1999;41:385-394.
29. Kodama H, Fujita M, Yamaguchi I. Development of hyperglycaemia and insulin resistance in conscious genetically diabetic (C57BL/KsJ-db/db) mice. Diabetologia. 1994;37:739-744.
30. Barile GR, Pachydaki SI, Tari SR, et al. The RAGE axis in early diabetic retinopathy. Invest Ophthalmol Vis Sci. 2005;46: 2916-2924.
31. He M, Siow RC, Sugden D, Gao L, Cheng X, Mann GE. Induction of HO-1 and redox signaling in endothelial cells by advanced glycation end products: a role for Nrf2 in vascular protection in diabetes. Nutr Metab Cardiovasc Dis. 2011;21: 277-285.
32. Brewer AC, Murray TV, Arno M, et al. Nox4 regulates Nrf2 and glutathione redox in cardiomyocytes in vivo. Free Radic Biol Med. 2011;51:205-215.
33. Ungvari Z, Bailey-Downs L, Sosnowska D, et al. Vascular oxidative stress in aging: a homeostatic failure due to dysregulation of NRF2-mediated antioxidant response. Am J Physiol Heart Circ Physiol. 2011;301:H363-H372.
34. Fan J, Xu G, Jiang T, Qin Y. Pharmacologic induction of heme oxygenase-1 plays a protective role in diabetic retinopathy in rats. Invest Ophthalmol Vis Sci. 2012;53:6541-6556.
35. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem. 1991;266:11632-11639.
36. Papaiahgari S, Kleeberger SR, Cho HY, Kalvakolanu DV, Reddy SP. NADPH oxidase and ERK signaling regulates hyperoxiainduced Nrf2-ARE transcriptional response in pulmonary epithelial cells. J Biol Chem. 2004;279:42302-42312.
37. Siow RC, Ishii T, Mann GE. Modulation of antioxidant gene expression by 4-hydroxynonenal: atheroprotective role of the Nrf2/ARE transcription pathway. Redox Rep. 2007;12:11-15.
38. Alam J, Igarashi K, Immenschuh S, Shibahara S, Tyrrell RM. Regulation of heme oxygenase-1 gene transcription: recent advances and highlights from the International Conference (Uppsala, 2003) on Heme Oxygenase. Antioxid Redox Signal. 2004;6:924-933.
39. Ryter SW, Alam J, Choi AM. Heme oxygenase-1/carbon monoxide: from basic science to therapeutic applications. Physiol Rev. 2006;86:583-650.
40. Martin D, Rojo AI, Salinas M, et al. Regulation of heme oxygenase-1 expression through the phosphatidylinositol 3- kinase/Akt pathway and the Nrf2 transcription factor in response to the antioxidant phytochemical carnosol. J Biol Chem. 2004;279:8919-8929.
41. Wei Y, Gong J, Yoshida T, et al. Nrf2 has a protective role against neuronal and capillary degeneration in retinal ischemia- reperfusion injury. Free Radic Biol Med. 2011;51:216-224.
42. Cheng X, Siow RC, Mann GE. Impaired redox signaling and antioxidant gene expression in endothelial cells in diabetes: a role for mitochondria and the nuclear factor-E2-related factor 2-Kelch-like ECH-associated protein 1 defense pathway. Antioxid Redox Signal. 2011;14:469-487.
43. Jeong WS, Jun M, Kong AN. Nrf2: a potential molecular target for cancer chemoprevention by natural compounds. Antioxid Redox Signal. 2006;8:99-106.
44. Hsieh HL, Wang HH, Wu CY, Yang CM. Reactive oxygen species-dependent c-fos/activator protein 1 induction upregulates heme oxygenase-1 expression by bradykinin in brain astrocytes. Antioxid Redox Signal. 2010;13:1829-1844.
45. Dikalov SI, Dikalova AE, Bikineyeva AT, Schmidt HH, Harrison DG, Griendling KK. Distinct roles of Nox1 and Nox4 in basal and angiotensin II-stimulated superoxide and hydrogen peroxide production. Free Radic Biol Med. 2008;45:1340-1351.
46. Serrander L, Cartier L, Bedard K, et al. NOX4 activity is determined by mRNA levels and reveals a unique pattern of ROS generation. Biochem J. 2007;406:105-114.
47. Groeger G, Mackey AM, Pettigrew CA, Bhatt L, Cotter TG. Stress-induced activation of Nox contributes to cell survival signalling via production of hydrogen peroxide. J Neurochem. 2009;109:1544-1554.
48. Schroder K, Zhang M, Benkhoff S, et al. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circ Res. 2012;110:1217-1225.
49. Yokota H, Narayanan SP, Zhang W, et al. Neuroprotection from retinal ischemia/reperfusion injury by NOX2 NADPH oxidase deletion. Invest Ophthalmol Vis Sci. 2011;52:8123-8131.
50. Nagai N, Thimmulappa RK, Cano M, et al. Nrf2 is a critical modulator of the innate immune response in a model of uveitis. Free Radic Biol Med. 2009;47:300-306.
51. Zou X, Feng Z, Li Y, et al. Stimulation of GSH synthesis to prevent oxidative stress-induced apoptosis by hydroxytyrosol in human retinal pigment epithelial cells: activation of Nrf2 and JNK-p62/SQSTM1 pathways. J Nutr Biochem. 2012;23: 994-1006.