Curcumin prevents experimental diabetic retinopathy in rats through its hypoglycemic, antioxidant, and anti-inflammatory mechanisms

Journal of Ocular Pharmacology and Therapeutics

Volumn 27, Issue 2, 2011, Pages 123-130

  Gupta, Suresh Kumar ^a   Kumar, Binit ^a   Nag, Tapas Chandra ^b   Agrawal, Shyam Sunder ^a   Agrawal, Renu ^c   Agrawal, Puneet ^d   Saxena, Rohit ^e   Srivastava, Sushma ^a  

^a UNIVERSITY OF DELHI   (India)

^b ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^c UNIVERSITI TEKNOLOGI MARA   (Malaysia)

^d INTERNATIONAL MEDICAL UNIVERSITY   (Malaysia)

^e ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CURCUMIN; GLUTATHIONE; STREPTOZOCIN; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR ALPHA; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; CAPILLARY BASEMENT MEMBRANE; CELL ORGANELLE; CONTROLLED STUDY; DIABETIC RETINOPATHY; ENDOTHELIUM CELL; ENZYME ACTIVITY; EYE FUNDUS; HISTOPATHOLOGY; HYPERGLYCEMIA; HYPOGLYCEMIA; NONHUMAN; RAT; RETINA BLOOD VESSEL; STREPTOZOCIN DIABETES; THICKNESS; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; BASEMENT MEMBRANE; CURCUMIN; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC RETINOPATHY; HYPOGLYCEMIC AGENTS; MALE; MICROSCOPY, ELECTRON; RATS; RATS, WISTAR; RETINA; STREPTOZOCIN; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 79955008744     PISSN: 10807683     EISSN: None     Source Type: Journal    
DOI: 10.1089/jop.2010.0123     Document Type: Article

References (67)

1. Baynes, J.W. Role of oxidative stress in development of complications in diabetes. Diabetes 40:405-412, 1991.
2. Aiello, L.P., Pierce, E.A., Foley, E.D., Takagi, H., Chen, H., Riddle, L., Ferrara, N., King, G.L., and Smith, L.E.H. Sup-pression 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. 92:10457-10461, 1995.
3. Limb, GA., Soomro, H., Janikoun, S., Hollifield, R.D., and Shilling, J. Evidence for control of tumour necrosis factor-alpha (TNF-alpha) activity by TNF receptors in patients with proliferative diabetic retinopathy. Clin. Exp. Immunol. 115: 409-414, 1999. (Pubitemid 29130353)
4. Joussen, A.M., Doehmen, S., Le, M.L., Koizumi, K., Radetzky, S., Krohne, T.U., Poulaki, V., Semkova, I., and Kociok, N. TNF-α mediated apoptosis plays an important role in the development of early diabetic retinopathy and long-term histopathological alterations. Mol. Vis. 15:1418-1428, 2009.
5. Honjo, M., Tanihara, H., Nishijima, K., Kiryu, J., Honda, Y., Yue, B.Y.J.T., and Sawamura, T. Statin inhibits leukocyte-endothelial interaction and prevents neuronal death induced by ischemia-reperfusion injury in the rat retina. Arch. Oph-thalmol. 120:1707-1713, 2002. (Pubitemid 36401807)
6. Mandarino, L.J. Current hypotheses for the biochemical ba-sis of diabetic retinopathy. Diabetes Care 15:1892-1901, 1992.
7. Suryanarayana, P., Satyanarayana, A., Balakrishna, N., Kumar, P.U., and Reddy, GB. Effect of turmeric and cur-cumin on oxidative stress and antioxidant enzymes in streptozotocin-induced diabetic rat. Med. Sci. Monit. 13: BR286-BR292, 2007. (Pubitemid 350272876)
8. Vucetic, M., Jensen, P.K., and Jansen, E.C. Diameter varia-tions of retinal blood vessels during and after treatment with hyperbaric oxygen. Br. J. Opthalmol. 88:771-775, 2004. (Pubitemid 38725586)
9. Moron, M.S., Depierre, J.W., and Mannervik, B. Levels of glu-tathione, glutathione reductase and glutathione-S-transferase activities in lung and liver. Biochem. Biophys. Acta 82:67-78, 1979. (Pubitemid 9065588)
10. Misra, H.P., and Fridovich, I. The oxidation of phenylhy-drazine: superoxide and mechanism. Biochemistry 15:681-687, 1976.
11. Aebi, H. Catalase. In: Bergmeyer, H.U., ed. Methods in En-zymatic Analysis, vol. 2, 1st ed. New York: Academic Press; 1974; pp. 673-677
12. Lowry, O.H., Rosenbrough, N.J., Farr, A.L., and Randall, R.J. Protein measurement with the Folin-phenol reagent. J. Biol. Chem. 193:265-275, 1951.
13. DCCT Research Group. The effects of intensive treatment of diabetes on the development and progression of long-term complications in insulin dependent diabetes mellitus. N. Engl. J. Med. 329:977-986, 1993.
14. UKPDS Group. Intensive blood-glucose control with sul-phonylureas or insulin compared with conventional treat-ment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 352:837-853, 1998.
15. Patumraj, S., Wongeakin, N., Sridulyakul, P., Jar-iyapongskul, A., Futrakul, N., and Bunnag, S. Combined effects of curcumin and vitamin C to protect endothelial dysfunction in the iris tissue of STZ-induced diabetic rats. Clin. Hemorheol. Microcirc 35:481-489, 2006. (Pubitemid 44812461)
16. Wongeakin, N., Sridulyakul, P., Jariyapongskul, A., Suk-samrarn, A., and Patumraj, S. Effects of curcumin and tet-rahydrocurcumin on diabetes-induced endothelial dysfunction. Afr. J. Biochem. Res. 3:259-265, 2009.
17. Cheung, N., and Wong, T.Y. Diabetic retinopathy and sys-temic vascular complications. Prog. Retin. Eye Res. 27:161-176, 2008.
18. Cheung, N., Tikellis, G., and Wang, J.J. Diabetic retinopathy. Ophthalmology 114:2098-2099, 2007 (Pubitemid 350016382)
19. Klein, R, Klein, B.E., Moss, S.E., Wong, T.Y., Hubbard, L., Cruickshanks, K.J., and Palta, M. The relation of retinal vessel caliber to the incidence and progression of diabetic retinopathy. XIX. The Wisconsin epidemiologic study of diabetic retinopathy. Arch. Opthalmol. 122:76-83, 2004. (Pubitemid 38063609)
20. Klein, R., Klein, B.E.K., Moss, S.E., Wong, T.Y., and Sharrett, A.R. Retinal vascular caliber in persons with type 2 diabetes. The Wisconsin epidemiologic study of diabetic retinopathy. XX. Opthalmology 113:1488-1498, 2006. (Pubitemid 44292299)
21. Klein, R, Klein, B.E.K., Moss, S.E., and Wong, T.Y. Retinal vessel caliber and microvascular and macrovascular disease in type 2 diabetes. XXI. The Wisconsin epidemiologic study of diabetic retinopathy. Opthalmology 114:1884-1892, 2007. (Pubitemid 47483910)
22. Rogers, S.L., Tikellis, G., Cheung, N., Tapp, R., Shaw, J., Zimmet, P.Z., Mitchell, P., Wang, J.J., and Wong, T.Y. Ret-inal arteriolar caliber predicts incident retinopathy. The Australia Diabetes, Obesity and Lifestyle (Ausdiab) Study. Diabetes Care 31:25-38, 2008.
23. Shinohara, M., Masuyama, T., and Kakehashi, A. The spontaneously diabetic torii (SDT) rat with retinopathy le-sions resembling those of human. In: Shafrir, E., Ed. Animal Models ofDiabetes: Frontiers in Research. Boca Raton, FL: CRC Press; 2007; pp. 315-316.
24. Kowluru, R.A., Tang, J., and Kern, T.S. Abnormalities of retinal metabolism in diabetes and experimental galacto-semia. VII. Effect of long-term administration of antioxidants on the development of retinopathy. Diabetes 50:1938-1942, 2001. (Pubitemid 33641616)
25. Haskins, K., Bradley, B., Powers, K., Fadok, V., Flores, S., Ling, X., Pugazhenthi, S., Reusch, J., and Kench, J. Oxidative stress in type 1 diabetes. Ann. N. Y. Acad. Sci. 1005:43-54, 2003. (Pubitemid 38507733)
26. Meister, A. Glutathione metabolism and its selective modi-fication. J. Biol. Chem. 263:17205-17208, 1988. (Pubitemid 19029311)
27. Kern, T.S., Kowluru, RA, and Engerman, RL. Abnormalities of retinal metabolism in diabetes or galactosemia: ATPases and glutathione. Invest. Ophthalmol. Vis. Sci. 35:2962-2967, 1994. (Pubitemid 24186397)
28. Kowluru, R.A., Kern, T.S., and Engerman, R.L. Abnormal-ities of retinal metabolism in diabetes or galactosemia II. Comparison of γ-glutamyl transpeptidase in retina and ce-rebral cortex, and effects of antioxidant therapy. Curr. Eye Res. 13:891-896, 1994.
29. Agardh, C.D., Agardh, E., Qian, Y., and Hultberg, B. Glu-tathione levels are reduced in diabetic rat retina but are not influenced by ischemia followed by recirculation. Metabolism 47:269-272, 1998. (Pubitemid 28108772)
30. Obrosova, I.G., Minchenko, A.G., Vasupuram, R., White, L., Abatan, O.I., Kumagai, A.K., and Frank, R.M. Aldose re-ductase inhibitor fidarestat prevents retinal oxidative stress and vascular endothelial growth factor over expression in streptozotocin-diabetic rats. Diabetes 52:864-871, 2003. (Pubitemid 36323597)
31. Obrosova, I.G., Drel, V.R, Kumagai, A.K., Szábo, C., Pacher, P., and Stevens, M.J. Early diabetes-induced biochemical changes in the retina: comparison of rat and mouse models. Diabetologia 49:2525-2533, 2006. (Pubitemid 44359115)
32. Limb, G.A., Chignell, A.H., Green, W., LeRoy, F., and Du-monde, D.C. Distribution of TNF alpha and its reactive vascular adhesion molecules in fibrovascular membranes of proliferative diabetic retinopathy. Br. J. Ophthalmol. 80:168-173, 1996. (Pubitemid 26058553)
33. Hawrami, K., Hitman, G.A., Rema, M., Snehalatha, C., Vis-wanathan, M., Ramachandran, A., and Mohan, V. An asso-ciation in non-insulin-dependent diabetes mellitus subjects between susceptibility to retinopathy and tumor necrosis factor polymorphism. Hum Immunol 46:49-54,1996. (Pubitemid 26131461)
34. Kacimi, R, Karliner, J.S., Koudssi, F., and Long, C.S. Ex-pression and regulation of adhesion molecules in cardiac cells by cytokines: response to acute hypoxia. Circ Res. 82:576-586, 1998. (Pubitemid 28129028)
35. Wright, P.S., Cooper, J.R, Kropp, K.E., and Busch, S.J. In-duction of vascular cell adhesion molecule-1 expression by IL-4 in human aortic smooth muscle cells is not associated with increased nuclear NF-kappaB levels. J. Cell. Physiol. 180:381-389, 1999. (Pubitemid 29334839)
36. Wallach, D. Cell death induction by TNF: a matter of self control. Trends Biochem. Sci. 22:107-109, 1997. (Pubitemid 27156937)
37. Amrani, Y., Lazaar, A.L., and Panettieri, R.A. Up-regulation of ICAM-1 by cytokines in human tracheal smooth muscle cells involves an NF-kappa B-dependent signaling pathway that is only partially sensitive to dexamethasone. J. Immunol. 163:2128-2134, 1999. (Pubitemid 29382219)
38. Amore, A., Cirina, P., Conti, G., Peruzzi, L., and Coppo, R Possible role of glycated albumin filtered during diabetic glomerulopathy, in the activation of tubular cells and pro-gression of diabetic nephropathy. J. Am. Soc Nephrol. 11:634A, 2000.
39. El-Remessy, A.B., Al-Shabrawey, M., Khalifa, Y., Tsai, N.T., Caldwell, RB., and Liou, G.I. Neuroprotective and blood-retinal barrier-preserving effects of cannabidiol in experi-mental diabetes. Am. J. Pathol. 168:235-244, 2006. (Pubitemid 43062576)
40. Joussen, A.M., Poulaki, V., Mitsiades, N., Kirchhof, B., Koi-zumi, K., Dohmen, S., and Adamis, A.P. Nonsteroidal anti-inflammatory drugs prevent early diabetic retinopathy via TNF-alpha suppression. FASEB J. 16:438-440, 2002.
41. Kim, K.H., Park, HY., Nam, J.H., Park, J.E., Kim, JY., Park, M.I., Chung, K.O., Park, KY., and Koo, JY. The inhibitory effect of curcumin on the growth of human colon cancer cells (HT-29, WiDr) in vitro. Korean J. Gastroenterol. 45:277-284, 2005.
42. Martens, F.M., Visseren, F.L., Lemay, J., de Koning, E.J., and Rabelink, T.J. Metabolic and additional vascular effects of thioazolidinediones. Drugs 62:1463-1480, 2002. (Pubitemid 34804155)
43. Aiello, L.P., Bursell, S.E., Clermont, A., Duh, E., Ishii, H., Takagi, C., Mori, F., Ciulla, T.A., Ways, K., Jirousek, M., Smith, L.E., and King, GL. Vascular endothelial growth factor-induced retinal permeability is mediated by protein kinase C in vivo and suppressed by an orally effective β-isoform selective inhibitor. Diabetes 46:1473-1480, 1997. (Pubitemid 27369086)
44. Vinores, S.A., Youssri, A.I., Luna, J.D., Chen, Y.S., Bhargave, S., Vinores, M.A., Schoenfeld, C.L., Peng, B., Chan, C.C., LaRochelle, W., Green, W.R., and Campochiaro, P.A. Up-regulation of vascular endothelial growth factor in ischemic and nonischemic human and experimental retinal disease. Histol. Histopathol. 12:99-109, 1997 (Pubitemid 27106924)
45. Qaum, T., Xu, Q., Joussen, A.M., Clemens, M.W., Qin, W., Miyamoto, K., Hassessian, H., Wiegand, S.J., Rudge, J., Yancopoulos, G.D., and Adamis, A.P. VEGF-initiated blood-retinal barrier breakdown in early diabetes. Invest. Ophthal-mol. Vis. Sci. 42:2408-2413, 2001. (Pubitemid 32848873)
46. Mrudula, T., Suryanarayana, P., Srinivas, P.N.B.S., and Bha-nuprakash Reddy, G Effect of curcumin on hyperglycemia-induced vascular endothelial growth factor expression in streptozotocin-induced diabetic rat retina. Biochem. Biophys. Res. Commun. 361:528-532, 2007. (Pubitemid 47187290)
47. Lambert, J., Aarsen, M., Donker, A.J., and Stehouwer, C.D. Endothelium-dependent and-independent vasodilation of large arteries in normoalbuminuric insulin-dependent diabe-tes mellitus. Arterioscler. Thromb. Vasc Biol. 16:705-711, 1996. (Pubitemid 26153116)
48. Roy, S., Maiello, M., and Lorenzi, M. Increased expression of basement membrane collagen in human diabetic retinopa-thy. J. Clin. Invest. 93:438-442, 1994. (Pubitemid 24030866)
49. Roy, S., and Lorenzi, M. Early biosynthetic changes in the diabetic-like retinopathy of galactose-fed rats. Diabetologia 39:735-738, 1996. (Pubitemid 26157631)
50. Roy, S., and Sate, T. Role of vascular basement membrane components in diabetic microangiopathy. Drug News Per-spect. 13:91-98, 2000. (Pubitemid 30414562)
51. Roy, S., Sato, T., Paryani, G., and Kao, R Downregulation of fibronectin overexpression reduces basement membrane thickening and vascular lesions in retinas of galactose-fed rats. Diabetes 52:1229-1234, 2003. (Pubitemid 36523361)
52. Siperstein, M.D., Unger, R.H., and Madison, L.L. Studies of muscle capillary basement membranes in normal subjects, diabetic, and prediabetic patients. J. Clin. Invest. 47:1973-1999, 1968.
53. Yamashita, T., and Becker, B. The basement membrane in the human diabetic eye. Diabetes 10:167-174, 1961.
54. Cagliero, E., Roth, T., Roy, S., and Lorenzi, M., Character-istics and mechanisms of high-glucose-induced over-expression of basement membrane components in cultured human endothelial cells. Diabetes 40:102-110, 1991.
55. Cagliero, E., Maiello, M., Boeri, D., Roy, S., and Lorenzi, M. Increased expression of basement membrane components in human endothelial cells cultured in high glucose. J. Clin. Invest. 82:735-738, 1998.
56. Hua, H., Goldberg, H.J., Fantus, I.G., and Whiteside, C.I., High glucose-enhanced mesangial cell extracellular signal regulated protein kinase activation and α1 (IV) collagen expression in response to endothelin-1: role of specific pro-tein kinase C isozymes. Diabetes 50:2376-2383, 2001. (Pubitemid 33641925)
57. Nishikawa, T., Giardino, I., Edelstein, D., and Brownlee, M. Changes in diabetic retinal matrix protein mRNA levels in a common transgenic mouse strain. Curr. Eye Res. 21:581-587, 2000.
58. D'Amore, P.A. Mechanisms of retinal and choroidal neo-vascularization Invest. Ophthalmol. Vis. Sci. 35:3974-3979,1994. (Pubitemid 24350660)
59. McAvoy, J.W., and Chamberlain, C.G Growth factors in the eye. Prog. Growth Factor Res. 2:29-43, 1990. (Pubitemid 120040339)
60. Ljubimov, A.V., Burgeson, R.E., Butkowski, RJ., John, R., Coucman, J.R, Zardi, L., Minomiya, Y., Sado, Y., Huang, Z.S., Nesburn, A.B., and Kenney, M.C. Basement membrane abnormalities in human eyes with diabetic retinopathy. J. Histochem. Cytochem. 44:1469-1479, 1996.
61. Meghana, K., Sanjeev, G., and Ramesh, B. Curcumin pre-vents streptozotocin-induced islet damage by scavenging free radicals: a prophylactic and protective role. Eur. J. Pharmacol. 577:183-191, 2007 (Pubitemid 47632529)
62. Fujiwara, H., Hosokawa, M., Zhou, X., Fujimoto, S., Fukuda, K., Toyoda, K., Nishi, Y., Fujita, Y., Yamada, K., Yamada, Y., Seino, Y., and Inagaki, N. Curcumin inhibits glucose pro-duction in isolated mice hepatocytes. Diabetes Res. Clin. Pract. 80:185-191, 2008.
63. Hardie, D.G, and Hawley, S.A. AMP-activated protein ki-nase: the energy charge hypothesis revisited. Bioessays 23:1112-1119, 2001.
64. Maiti, K., Mukherjee, K., Gantait, A., Saha, B.P., and Mu-kherjee, P.K. Curcumin-phospholipid complex: preparation, therapeutic evaluation and pharmacokinetic study in rats. Int. J. Pharm. 330:155-163, 2007 (Pubitemid 46097368)
65. Li, L., Braiteh, F.S., and Kurzrock, R Liposome-encapsulated curcumin: in vitro and in vivo effects on proliferation, apo-ptosis, signaling, and angiogenesis. Cancer 104:1322-1331, 2005. (Pubitemid 41282806)
66. Bisht, S., Feldmann, G., Soni, S., Ravi, R., Karikar, C., Maitra, A., and Maitra, A. Polymeric nanoparticle-encapsulated curcumin (" nanocurcumin"): a novel strategy for human cancer therapy. J. Nanobiotech. 5:3, 2007.
67. Shoba, G., Joy, D., Joseph, T., Majeed, M., Rajendran, R., and Srinivas, P.S. Influence of piperine on the pharmacokinetics of curcumin in animals and human volunteers. Planta Med. 64:353-356, 1998. (Pubitemid 28234275)