Catalase therapy corrects oxidative stress-induced pathophysiology in incipient diabetic retinopathy

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 5, 2015, Pages 3095-3102

  Giordano, Courtney R ^a   Roberts, Robin ^a   Krentz, Kendra A ^a   Bissig, David ^a   Talrej, Deepa ^b   Kumar, Ashok ^a,b   Terlecky, Stanley R ^a   Berkowitz, Bruce A ^a,b  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WAYNE STATE UNIVERSITY   (United States)

Author keywords

Catalase; Diabetes; MEMRI; Oxidative stress; Retina

Indexed keywords

CAT SKL DERIVATIVE; CATALASE; CELL PENETRATING PEPTIDE; EFLORNITHINE; HYDROGEN PEROXIDE; LIPID HYDROPEROXIDE; MANGANESE; UNCLASSIFIED DRUG; ANTIOXIDANT; GLUCOSE; ORNITHINE DECARBOXYLASE INHIBITOR;

ARTICLE; BIOTINYLATION; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENZYME ACTIVITY; FLUORESCENCE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RETINA CELL; STREPTOZOTOCIN-INDUCED DIABETES MELLITUS; ANIMAL; C57BL MOUSE; CULTURE TECHNIQUE; DIABETES MELLITUS, EXPERIMENTAL; DRUG EFFECTS; MACROGLIA; METABOLISM; PIGMENT EPITHELIUM;

ANIMALS; ANTIOXIDANTS; CATALASE; CELL CULTURE TECHNIQUES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; EFLORNITHINE; EPENDYMOGLIAL CELLS; GLUCOSE; HUMANS; HYDROGEN PEROXIDE; MAGNETIC RESONANCE IMAGING; MANGANESE; MICE; MICE, INBRED C57BL; ORNITHINE DECARBOXYLASE INHIBITORS; OXIDATIVE STRESS; RETINAL PIGMENT EPITHELIUM;

EID: 84939599869     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.14-16194     Document Type: Article

References (48)

1. Du Y, Veenstra A, Palczewski K, Kern TS. Photoreceptor cells are major contributors to diabetes-induced oxidative stress and local inflammation in the retina. Proc Natl Acad Sci U S A. 2013;110:16586–16591.
2. Kowluru RA, Atasi L, Ho YS. Role of mitochondrial superoxide dismutase in the development of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2006;47:1594–1599.
3. Kowluru RA, Kowluru V, Xiong Y, Ho YS. Overexpression of mitochondrial superoxide dismutase in mice protects the retina from diabetes-induced oxidative stress. Free Rad Biol Med. 2006;41:1191–1196.
4. Kanwar M, Chan PS, Kern TS, Kowluru RA. Oxidative damage in the retinal mitochondria of diabetic mice: possible protection by superoxide dismutase. Invest Ophthalmol Vis Sci. 2007;48:3805–3811.
5. Lee J, Giordano S, Zhang J. Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem J. 2012;441:523–540.
6. Ivashchenko O, Van Veldhoven PP, Brees C, Ho YS, Terlecky SR, Fransen M. Intraperoxisomal redox balance in mammalian cells: oxidative stress and interorganellar cross-talk. Mol Biol Cell. 2011;22:1440–1451.
7. Terlecky SR, Terlecky LJ, Giordano CR. Peroxisomes, oxidative stress, and inflammation. World J Biol Chem. 2012;3:93–97.
8. Giordano CR, Terlecky SR. Peroxisomes, cell senescence, and rates of aging. Biochim Biophys Acta. 2012;1822:1358–1362.
9. Terlecky SR, Koepke JI, Walton PA. Peroxisomes and aging. Biochim Biophys Acta. 2006;1763:1749–1754.
10. Zhang H, Agardh CD, Agardh E. Retinal nitro blue tetrazolium staining and catalase activity in rat models of diabetes. Graefes Arch Klin Exp Ophthalmol. 1996;234:324–330.
11. Kowluru RA, Kern TS, Engerman RL. Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system. Free Rad Biol Med. 1997;22:587–592.
12. Kocak G, Aktan F, Canbolat O, et al. Alpha-lipoic acid treatment ameliorates metabolic parameters, blood pressure, vascular reactivity and morphology of vessels already damaged by streptozotocin-diabetes. Diab Nutr Metab. 2000;13:308–318.
13. Obrosova IG, Drel VR, Kumagai AK, Szabo C, Pacher P, Stevens MJ. Early diabetes-induced biochemical changes in the retina: comparison of rat and mouse models. Diabetologia. 2006;49: 2525–2533.
14. Sadi G, Yilmaz O, Guray T. Effect of vitamin C and lipoic acid on streptozotocin-induced diabetes gene expression: mRNA and protein expressions of Cu-Zn SOD and catalase. Mol Cell Biochem. 2008;309:109–116.
15. Biedermann B, Skatchkov SN, Brunk I, et al. Spermine/spermidine is expressed by retinal glial (Muller) cells and controls distinct Kþ channels of their membrane. Glia. 1998; 23:209–220.
16. Ishizaki E, Fukumoto M, Puro DG. Functional K(ATP) channels in the rat retinal microvasculature: topographical distribution, redox regulation, spermine modulation and diabetic alteration. J Physiol. 2009;587:2233–2253.
17. Nicoletti R, Venza I, Ceci G, Visalli M, Teti D, Reibaldi A. Vitreous polyamines spermidine, putrescine, and spermine in human proliferative disorders of the retina. Br J Ophthalmol. 2003;87:1038–1042.
18. Berkowitz BA, Roberts R, Goebel DJ, Luan H. Noninvasive and simultaneous imaging of layer-specific retinal functional adaptation by manganese-enhanced MRI. Invest Ophthalmol Vis Sci. 2006;47:2668–2674.
19. Berkowitz BA, Gradianu M, Schafer S, et al. Ionic dysregulatory phenotyping of pathologic retinal thinning with manganese-enhanced MRI. Invest Ophthalmol Vis Sci. 2008;49:3178–3184.
20. Berkowitz BA, Roberts R, Oleske DA, et al. Quantitative mapping of ion channel regulation by visual cycle activity inrodent photoreceptors in vivo. Invest Ophthalmol Vis Sci. 2009;50:1880–1885.
21. Ramos de Carvalho JE, Verbraak FD, Aalders MC, van Noorden CJ, Schlingemann RO. Recent advances in ophthalmic molecular imaging. Surv Ophthalmol. 2014;59:393–413.
22. Berkowitz BA, Roberts R, Stemmler A, Luan H, Gradianu M. Impaired apparent ion demand in experimental diabetic retinopathy: correction by lipoic Acid. Invest Ophthalmol Vis Sci. 2007;48:4753–4758.
23. Berkowitz BA, Gradianu M, Bissig D, Kern TS, Roberts R. Retinal ion regulation in a mouse model of diabetic retinopathy: natural history and the effect of Cu/Zn superoxide dismutase overexpression. Invest Ophthalmol Vis Sci. 2009;50:2351–2358.
24. Shamsuddin N, Kumar A. TLR2 mediates the innate response of retinal Muller glia to Staphylococcus aureus. J Immunol. 2011;186:7089–7097.
25. Koepke JI, Nakrieko KA, Wood CS, et al. Restoration of peroxisomal catalase import in a model of human cellular aging. Traffic. 2007;8:1590–1600.
26. Young CN, Koepke JI, Terlecky LJ, Borkin MS, Boyd Savoy L, Terlecky SR. Reactive oxygen species in tumor necrosis factoralpha- activated primary human keratinocytes: implications for psoriasis and inflammatory skin disease. J Invest Dermatol. 2008;128:2606–2614.
27. Storrie B, Madden EA. Isolation of subcellular organelles. Methods Enzymol. 1990;182:203–225.
28. Berkowitz BA, Bissig D, Patel P, Bhatia A, Roberts R. Acute systemic 11-cis-retinal intervention improves abnormal outer retinal ion channel closure in diabetic mice. Mol Vis. 2012;18: 372–376.
29. Bissig D, Berkowitz BA. Same-session functional assessment of rat retina and brain with manganese-enhanced MRI. Neuro- Image. 2011;58:749–760.
30. Berkowitz BA, Grady EM, Khetarpal N, Patel A, Roberts R. Oxidative stress and light-evoked responses of the posterior segment in a mouse model of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2015;56:606–615.
31. Berkowitz BA, Grady EM, Roberts R. Confirming a prediction of the calcium hypothesis of photoreceptor aging in mice. Neurobiol Aging. 2014;35:1883–1891.
32. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42:121–130.
33. von Deutsch AW, Mitchell CD, Williams CE, et al. Polyamines protect against radiation-induced oxidative stress. Grav Space Biol Bull. 2005;18:109–110.
34. Minois N, Carmona-Gutierrez D, Madeo F. Polyamines in aging and disease. Aging. 2011;3:716–732.
35. Kowluru RA, Kern TS, Engerman RL, Armstrong D. Abnormalities of retinal metabolism in diabetes or experimental galactosemia. III. Effects of antioxidants. Diabetes. 1996;45: 1233–1237.
36. Kowluru RA, Tang J, Kern TS. Abnormalities of retinal metabolism in diabetes and experimental galactosemia. VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes. 2001;50:1938–1942.
37. Marmorstein LY, Wu J, McLaughlin P, et al. The light peak of the electroretinogram is dependent on voltage-gated calcium channels and antagonized by bestrophin (best-1). J Gen Physiol. 2006;127:577–589.
38. Lu H, Xi ZX, Gitajn L, Rea W, Yang Y, Stein EA. Cocaineinduced brain activation detected by dynamic manganeseenhanced magnetic resonance imaging (MEMRI). Proc Natl Acad Sci U S A. 2007;104:2489–2494.
39. Drapeau P, Nachshen DA. Manganese fluxes and manganesedependent neurotransmitter release in presynaptic nerve endings isolated from rat brain. J Physiol. 1984;348:493–510.
40. Carlson RO, Masco D, Brooker G, Spiegel S. Endogenous ganglioside GM1 modulates L-type calcium channel activity in N18 neuroblastoma cells. J Neurosci. 1994;14:2272–2281.
41. Berkowitz BA, Roberts R, Penn JS, Gradianu M. Highresolution manganese-enhanced MRI of experimental retinopathy of prematurity. Invest Ophthalmol Vis Sci. 2007;48: 4733–4740.
42. Cross DJ, Flexman JA, Anzai Y, et al. In vivo manganese MR imaging of calcium influx in spontaneous rat pituitary adenoma. Am J Neuroradiol. 2007;28:1865–1871.
43. Berkowitz BA, Bissig D, Bergman D, Bercea E, Kasturi VK, Roberts R. Intraretinal calcium channels and retinal morbidity in experimental retinopathy of prematurity. Mol Vis. 2011;17: 2516–2526.
44. Rex TS, Tsui I, Hahn P, et al. Adenovirus-mediated delivery of catalase to retinal pigment epithelial cells protects neighboring photoreceptors from photo-oxidative stress. Hum Gene Ther. 2004;15:960–967.
45. Atalla L, Fernandez MA, Rao NA. Immunohistochemical localization of catalase in ocular tissue. Curr Eye Res. 1987; 6:1181–1187.
46. Wangsa-Wirawan ND, Linsenmeier RA. Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol. 2003;121:547–557.
47. Zhi Z, Chao JR, Wietecha T, Hudkins KL, Alpers CE, Wang RK. Noninvasive imaging of retinal morphology and microvasculature in obese mice using optical coherence tomography and optical microangiography. Invest Ophthalmol Vis Sci. 2014; 55:1024–1030.
48. Paques M, Tadayoni R, Sercombe R, et al. Structural and hemodynamic analysis of the mouse retinal microcirculation. Invest Ophthalmol Vis Sci. 2003;44:4960–4967.