Pharmacologic induction of heme oxygenase-1 plays a protective role in diabetic retinopathy in rats

Investigative Ophthalmology and Visual Science

Volumn 53, Issue 10, 2012, Pages 6541-6556

  Fan, Jiawen ^a   Xu, Gezhi ^a   Jiang, Tingting ^a   Qin, Yaowu ^a  

^a FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUCOSE; GLYCOSYLATED HEMOGLOBIN; HEME OXYGENASE 1; HEMIN; HEMOGLOBIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN BCL 2; PROTEIN P53; TRANSCRIPTION FACTOR NRF2; VASCULOTROPIN A; HEME OXYGENASE; HIF1A PROTEIN, RAT; HMOX1 PROTEIN, RAT; MESSENGER RNA; SUPEROXIDE DISMUTASE; VASCULAR ENDOTHELIAL GROWTH FACTOR A, RAT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BLOOD SAMPLING; BODY WEIGHT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DIABETIC RETINOPATHY; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RETINA GANGLION CELL; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; BLOOD; DRUG EFFECT; ENZYME INDUCTION; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION; GENETICS; INTRAPERITONEAL DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; BLOTTING, WESTERN; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; ENZYME INDUCTION; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; HEME OXYGENASE (DECYCLIZING); HEMIN; HEMOGLOBIN A, GLYCOSYLATED; HEMOGLOBINS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IN SITU NICK-END LABELING; INJECTIONS, INTRAPERITONEAL; MALE; MAP KINASE SIGNALING SYSTEM; MICROSCOPY, CONFOCAL; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RETINAL GANGLION CELLS; RNA, MESSENGER; SUPEROXIDE DISMUTASE; TUMOR SUPPRESSOR PROTEIN P53; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84871883194     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.11-9241     Document Type: Article

References (60)

1. Rungger-Br̈andle E, Dosso AA, Leuenberger PM. Glial reactivity, an early feature of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2000;41:1971-1980.
2. Antonetti DA, Barber AJ, Bronson SK, et al. Diabetic Retinopathy Center Group. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes. 2006;55:2401-2411.
3. Otterbein LE, Soares MP, Yamashita K, Bach FH. Heme oxygenase-1: unleashing the protective properties of heme. Trends Immunol. 2003;24:449-455.
4. Soares MP, Bach FH. Heme oxygenase-1: from biology to therapeutic potential. Trends Mol Med. 2009;15:50-58.
5. Zhang M, Zhang BH, Chen L, An W. Overexpression of heme oxygenase-1 protects smooth muscle cells against oxidative injury and inhibits cell proliferation. Cell Res. 2002;12:123-132.
6. Tamion F, Richard V, Renet S, Thuillez C. Intestinal preconditioning prevents inflammatory response by modulatinghemeoxygenase-1 expression in endotoxic shock model. Am J Physiol Gastrointest Liver Physiol. 2007;293:G1308-G1314.
7. Choi BM, Kim BR. Upregulation of heme oxygenase-1 by brazilin via the phosphatidylinositol 3-kinase/Akt and ERK pathways and its protective effect against oxidative injury. Eur J Pharmacol. 2008;580:12-18.
8. Ndisang JF. Role of heme oxygenase in inflammation, insulinsignalling, diabetes and obesity. Mediators Inflamm. 2010; 2010:359732.
9. Kruger AL, Peterson SJ, Schwartzman ML, et al. Up-regulation of heme oxygenase provides vascular protection in an animal model of diabetes through its antioxidant and antiapoptotic effects. J Pharmacol Exp Ther. 2006;319:1144-1152.
10. Arai-Gaun S, Katai N, Kikuchi T, Kurokawa T, Ohta K, Yoshimura N. Heme oxygenase-1 induced in muller cells plays a protective role in retinal ischemia-reperfusion injury in rats. Invest Ophthalmol Vis Sci. 2004;45:4226-4232.
11. Sun MH, Pang JH, Chen SL, et al. Retinal protection from acute glaucoma-induced ischemia-reperfusion injury through pharmacologic induction of heme oxygenase-1. Invest Ophthalmol Vis Sci. 2010;51:4798-4808.
12. Sun MH, Pang JH, Chen SL, et al. Photoreceptor protection against light damage by AAV-mediated overexpression of heme oxygenase-1. Invest Ophthalmol Vis Sci. 2007;48:5699-5707.
13. Lin JH, Villalon P, Martasek P, Abraham NG. Regulation of heme oxygenase gene expression by cobalt in rat liver and kidney. Eur J Biochem. 1990;192:577-582.
14. Shibahara S, M̈uller RM, Taguchi H. Transcriptional control of rat heme oxygenase by heat shock. J Biol Chem. 1987;262: 12889-12892.
15. Desbuards N, Rochefort GY, Schlecht D, et al. Heme oxygenase-1 inducer hemin prevents vascular thrombosis. Thromb Haemost. 2007;98:614-620.
16. Morita K, Lee MS, Her S. Possible relation of hemin-induced HO-1 expression to the upregulation of VEGF and BDNF mRNA levels in rat C6 glioma cells. J Mol Neurosci. 2009;38: 31-40.
17. Zijlstra GS, Brandsma CA, Harpe MF, et al. Dry powder inhalation of hemin to induce heme oxygenase expression in the lung. Eur J Pharm Biopharm. 2007;67:667-675.
18. Nussler AK, Hao L, Knobeloch D, et al. Protective role of HO-1 for alcohol-dependent liver damage. Dig Dis. 2010;28:792-798.
19. Naughton P, Hoque M, Green CJ, Foresti R, Motterlini R. Interaction of heme with nitroxyl or nitric oxide amplifies heme oxygenase-1 induction: involvement of the transcription factor Nrf2. Cell Mol Biol (Noisy-le-grand). 2002;48:885-894.
20. Kim J, Cha YN, Surh YJ. A protective role of nuclear factorerythroid 2-related factor-2 (Nrf2) in inflammatory disorders. Mutat Res. 2010;690:12-23.
21. Calkins MJ, Johnson DA, Townsend JA, et al. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal. 2009;11:497-508.
22. Gong P, Hu B, Cederbaum AI. Diallyl sulfide induces heme oxygenase-1 through MAPK pathway. Arch Biochem Biophys. 2004;432:252-260.
23. Balogun E, Hoque M, Gong P, et al. Curcumin activates the haem oxygenase-1 gene via regulation of Nrf2 and the antioxidant-responsive element. Biochem J. 2003;371:887-895.
24. Steinle JJ, Chin VC, Williams KP, Panjala SR. Beta-adrenergic receptor stimulation modulates iNOS protein levels through p38 and ERK1/2 signaling in human retinal endothelial cells. Exp Eye Res. 2008;87:30-34.
25. Ye X, Xu G, Chang Q, et al. ERK1/2 signaling pathways involved in VEGF release in diabetic rat retina. Invest Ophthalmol Vis Sci. 2010;51:5226-5233.
26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2_DDC T method. Methods. 2001;25:402-408.
27. Vidal-Sanz M, Villegas-Perez MP, Bray GM, Aguayo AJ. Persistent retrograde labeling of adult rat retinal ganglion cells with the carbocyanine dye DiI. Exp Neurol. 1988;102:92-101.
28. Ndisang JF, Jadhav A. Upregulating the heme oxygenase system suppresses left ventricular hypertrophy in adult spontaneously hypertensive rats for 3 months. J Card Fail. 2009;15:616-628.
29. Wang RQ, Nan YM, Wu WJ, et al. Induction of heme oxygenase-1 protects against nutritional fibrosing steatohepatitis in mice. Lipids Health Dis. 2011;10:31.
30. Natarajan R, Fisher BJ, Fowler AA III. Hypoxia inducible factor-1 modulates hemin-induced IL-8 secretion in microvascular endothelium. Microvasc Res. 2007;73:163-172.
31. Choi KM, Gibbons SJ, Nguyen TV, et al. Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology. 2008;135: 2055-2064.
32. Fouad AA, Qureshi HA, Al-Sultan AI, Yacoubi MT, Ali AA. Protective effect of hemin against cadmium-induced testicular damage in rats. Toxicology. 2009;257:153-160.
33. Wang X, Ye XL, Liu R, et al. Antioxidant activities of oleanolic acid in vitro: possible role of Nrf2 and MAP kinases. Chem Biol Interact. 2010;184:328-337.
34. Bringmann A, Pannicke T, Grosche J, et al. M̈uller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424.
35. de Melo Reis RA, Ventura AL, Schitine CS, de Mello MC, de Mello FG. M̈uller glia as an active compartment modulating nervous activity in the vertebrate retina: neurotransmitters and trophic factors. Neurochem Res. 2008;33:1466-1474.
36. Liu W, Xu GZ, Jiang CH, Da CD. Expression of macrophage colony-stimulating factor (M-CSF) and its receptor in streptozotocin-induced diabetic rats. Curr Eye Res. 2009;34:123-133.
37. Kowluru RA, Chan PS. Oxidative stress and diabetic retinopathy. Exp Diabetes Res. 2007;2007:43603.
38. Valdivia A, Ṕerez-Alvarez S, Aroca-Aguilar JD, Ikuta I, Jord́an J. Superoxide dismutases: a physiopharmacological update. J Physiol Biochem. 2009;65:195-208.
39. Turan B. Role of antioxidants in redox regulation of diabetic cardiovascular complications. Curr Pharm Biotechnol. 2010; 11:819-836.
40. Du Y, Miller CM, Kern TS. Hyperglycemia increases mitochondrial superoxide in retina and retinal cells. Free Radic Biol Med. 2003;35:1491-1499.
41. Craven PA, Melhem MF, Phillips SL, DeRubertis FR. Overexpression of Cu2+/Zn2+superoxide dismutase protects against early diabetic glomerular injury in transgenic mice. Diabetes. 2001;50:2114-2125.
42. DeRubertis FR, Craven PA, Melhem MF, Salah EM. Attenuation of renal injury in db/db mice overexpressing superoxide dismutase: evidence for reduced superoxide-nitric oxide interaction. Diabetes. 2004;53:762-768.
43. Nyengaard JR, Ido Y, Kilo C, Williamson JR. Interactions between hyperglycemia and hypoxia: implications for diabetic retinopathy. Diabetes. 2004;53:2931-2938.
44. Arden GB, Sivaprasad S. Hypoxia and oxidative stress in the causation of diabetic retinopathy. Curr Diabetes Rev. 2011;7: 291-304.
45. Goda N, Ryan HE, Khadivi B, McNulty W, Rickert RC, Johnson RS. Hypoxia-inducible factor 1alpha is essential for cell cycle arrest during hypoxia. Mol Cell Biol. 2003;23:359-369.
46. Ozaki H, Yu AY, Della N, et al. Hypoxia inducible factor-1alpha is increased in ischemic retina: temporal and spatial correlation with VEGF expression. Invest Ophthalmol Vis Sci. 1999; 40:182-189.
47. Schmid T, Zhou J, Br̈une B. HIF-1 and p53: communication of transcription factors under hypoxia. J Cell Mol Med. 2004;8: 423-431.
48. Lin M, Chen Y, Jin J, et al. Ischaemia-induced retinal neovascularisation and diabetic retinopathy in mice with conditional knockout of hypoxia-inducible factor-1 in retinal M̈uller cells. Diabetologia. 2011;54:1554-1566.
49. Nakamura M, Kanamori A, Negi A. Diabetes mellitus as a risk factor for glaucomatous optic neuropathy. Ophthalmologica. 2005;219:1-10.
50. van Dijk HW, Verbraak FD, Kok PH, et al. Decreased retinal ganglion cell layer thickness in patients with type 1 diabetes. Invest Ophthalmol Vis Sci. 2010;51:3660-3665.
51. Panahian N, Yoshiura M, Maines MD. Overexpression of heme oxygenase-1 is neuroprotective in a model of permanent middle cerebral artery occlusion in transgenic mice. J Neurochem. 1999;72:1187-1203.
52. Adamis AP, Miller JW, Bernal MT, et al. Increased vascular endothelial growth factor levels in the vitreous of eyes with proliferative diabetic retinopathy. Am J Ophthalmol. 1994; 118:445-450.
53. Aiello LP, Pierce EA, Foley ED, et al. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci U S A. 1995;92:10457-10461.
54. Ferrara N. Vascular endothelial growth factor. Arterioscler Thromb Vasc Biol. 2009;29:789-791.
55. Joussen AM, Poulaki V, Qin W, et al. Retinal vascular endothelial growth factor induces intercellular adhesion molecule-1 and endothelial nitric oxide synthase expression and initiates early diabetic retinal leukocyte adhesion in vivo. Am J Pathol. 2002;160:501-509.
56. Rangasamy S, McGuire PG, Das A. Diabetic retinopathy and inflammation: novel therapeutic targets. Middle East Afr J Ophthalmol. 2012;19:52-59.
57. Nguyen QD, Brown DM, Marcus DM, et al. RISE and RIDE Research Group. Ranibizumab for diabetic macular edema: results from 2 phase iii randomized trials: RISE and RIDE. Ophthalmology. 2012;119:789-801.
58. Yu DY, Cringle SJ, Su EN, Yu PK, Jerums G, Cooper ME. Pathogenesis and intervention strategies in diabetic retinopathy. Clin Experiment Ophthalmol. 2001;29:164-166.
59. International Expert Committee. International Expert Committee report on the role of the A1C assay in the diagnosis of diabetes. Diabetes Care. 2009;32:1327-1334.
60. American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care Suppl 1. 2010;33:S62-S69.