Astaxanthin Attenuates Oxidative Damage in Retina by Potentiation of the Antioxidant Capacity in Experimental Model of Diabetic Retinopathy

Mojarrab, Shahnaz; Bahrami, Farideh; Mohammadi, Mohammad Taghi; Khoshbaten, Ali; Salem, Fatemeh; Norozzadeh, Ali

doi:10.30483/RIJM.2018.26

Astaxanthin Attenuates Oxidative Damage in Retina by Potentiation of the Antioxidant Capacity in Experimental Model of Diabetic Retinopathy

Document Type : Original Article

Authors

¹ Department of Physiology and Biophysics, Faculty of Medicine, Baqiyatallah University of Medical Sciences, Tehran, Iran

² Neuroscience Research Center, Baqiyatallah University of Medical Sciences, Tehran, Iran

10.30483/RIJM.2018.26

Abstract

Background: Astaxanthin is a natural carotenoid, which is belonged to the Xanthophylls family. Previously, the powerful antioxidant properties of this compound have been demonstrated in several biological environments.

Objectives: As overproduction of reactive oxygen species (ROS) has a critical role in the pathophysiology of diabetic retinopathy (DR), we aimed to evaluate the effects of astaxanthin on the antioxidant capacity of retina in experimental model of DR.

Methods: Forty eight rats were randomly divided into four groups (n=12 for each group); normal, diabetic, and two treated normal and diabetic groups. Diabetes was induced by a single intravenous injection of streptozotocin (50 mg/kg). Rats with blood glucose >500 mg/dL were selected as diabetic animals. Treatment groups were treated with astaxanthin (20 mg/kg/day, orally) for six weeks. At the end, the eyeballs were removed under deep anesthesia and then the retinal tissues were quickly frozen for assessment of the glutathione and malondialdehyde contents as well as superoxide dismutase (SOD) activity.

Results: Malondialdehyde levels of the retina in diabetic rats increased significantly (16%), whereas the glutathione levels decreased (85%), (P<0.05). Astaxanthin significantly increased the glutathione content of retina in treated diabetic rats by 77% compared to untreated rats (P<0.05). Diabetes also increased the activity of SOD in retina. Treatment with astaxanthin enhanced the SOD activity both in treated normal and diabetic rats (P<0.05).

Conclusion: Our findings reveal that astaxanthin can decrease oxidative damage of retina by improving the antioxidant capacity in diabetic rats, which may ultimately delay the appearance of DR.

Keywords

Open Access Policy: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/

References

1.Cunha-Vaz J, Ribeiro L, Lobo C. Phenotypes and biomarkers of diabetic retinopathy. Prog Retin Eye Res. 2014;41: 90-111. [PubMed:24680929]. https://doi.org/10.1016/j.preteyeres.2014.03.003 PMid:24680929

2. Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004;27(5):1047-53. [PubMed: 15111519]. https://doi.org/10.2337/diacare.27.5.1047 PMid:15111519

3. Obrosova IG, Julius UA. Role for poly (ADP-ribose) polymerase activation in diabetic nephropathy, neuropathy and retinopathy. Curr Vasc Pharmacol. 2005;3(3):267-83. [PubMed: 16026323]. https://doi.org/10.2174/1570161054368634 PMid:16026323

4. Brownlee M. The pathobiology of diabetic complications: a unifying mechanism. Diabetes. 2005;54(6):1615. [PubMed: 15919781]. https://doi.org/10.2337/diabetes.54.6.1615 PMid:15919781

5. 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(8):3805-11. [PubMed: 17652755]. https://doi.org/10.1167/iovs.06-1280 PMid:17652755

6. Kowluru RA, Chan PS. Oxidative stress and diabetic retinopathy. Exp Diabetes Res. 2007;2007:43603. [PubMed: 17641741]. https://doi.org/10.1155/2007/43603 PMid:17641741 PMCid:PMC1880867

7. Madsen-Bouterse SA, Kowluru RA. Oxidative stress and diabetic retinopathy: Pathophysiological mechanisms and treatment perspectives. Rev Endocr Metab Disord. 2008; 9(4):315-27. [PubMed: 18654858]. https://doi.org/10.1007/s11154-008-9090-4 PMid:18654858

8. Riahi S, Mohammadi MT, Sobhani V, Ababzadeh S. Chronic aerobic exercise decreases lectin-like low density lipoprotein (LOX-1) receptor expression in heart of diabetic rat. Iran Biomed J. 2016;20(1):26-32. [PubMed: 26432573].

9. Coucha M, Elshaer SL, Eldahshan WS, Mysona BA, El-Remessy AB. Molecular mechanisms of diabetic retinopathy: potential therapeutic targets. Middle East Afr J Ophthalmol. 2015; 22(2):135-44. [PubMed:25949069]. https://doi.org/10.4103/0974-9233.154386 PMid:25949069 PMCid:PMC4411608

10. Lai AK, Lo AC. Animal models of diabetic retinopathy: Mojarrab S et al.48 Razavi Int J Med. 2018

6(3):e46865. summary and comparison. J Diabetes Res. 2013;2013:106594 [PubMed: 24286086].

11. Kedziora‐Kornatowska K, Luciak M, Paszkowski J. Lipid peroxidation and activities of antioxidant enzymes in the diabetic kidney: effect of treatment with angiotensin convertase inhibitors. IUBMB Life. 2000;49(4):303-7. [PubMed: 10995033]. https://doi.org/10.1080/15216540050033177 PMid:10995033

12. Kowluru R, Kern TS, Engerman RL. Abnormalities of retinal metabolism in diabetes or galactosemia II. Comparison of γglutamyl transpeptidase in retina and cerebral cortex, and effects of antioxidant therapy. Curr Eye Res. 1994;13(12):891-6. [PubMed: 7720397]. https://doi.org/10.3109/02713689409015092 PMid:7720397

13. Kowluru RA, Kern TS, Engerman RL. Abnormalities of retinal metabolism in diabetes or experimental galactosemia. IV. Antioxidant defense system. Free Radic Biol Med. 1996; 22(4):587-92. [PubMed: 9013121]. https://doi.org/10.1016/S0891-5849(96)00347-4 PMid:9013121

14. Pashkow FJ, Watumull DG, Campbell CL. Astaxanthin: a novel potential treatment for oxidative stress and inflammation in cardiovascular disease. Am J Cardiol. 2008;101(10A): 58D-68D. [PubMed:18474276]. https://doi.org/10.1016/j.amjcard.2008.02.010 PMid:18474276

15. Otton R, Marin DP, Bolin AP, Santos Rde C, Polotow TG, Sampaio SC, et al. Astaxanthin ameliorates the redox imbalance in lymphocytes of experimental diabetic rats. Chem Biol Interact. 2010;3(186):306-15. [PubMed: 20513374]. https://doi.org/10.1016/j.cbi.2010.05.011 PMid:20513374

16. Leite MF, Lima AM, Massuyama MM, Otton R. Astaxanthin restores the enzymatic antioxidant profile in salivary gland of alloxan-induced diabetic rats. Arch Oral Biol. 2010;55(7):479-85. [PubMed: 20510163]. https://doi.org/10.1016/j.archoralbio.2010.04.006 PMid:20510163

17. McNulty H, Jacob RF, Mason RP. Biologic activity of carotenoids related to distinct membrane physicochemical interactions. Am J Cardiol. 2008;10(101):20D-9D. [PubMed: 18474269]. https://doi.org/10.1016/j.amjcard.2008.02.004 PMid:18474269

18. Curek GD, Cort A, Yucel G, Demir N, Ozturk S, Elpek GO, et al. Effect of astaxanthin on hepatocellular injury following ischemia/reperfusion. Toxicology. 2010;267(1-3):147-53. [PubMed: 19900500]. https://doi.org/10.1016/j.tox.2009.11.003 PMid:19900500

19. Palozza P, Torelli C, Boninsegna A, Simone R, Catalano A, Mele MC, et al. Growth-inhibitory effects of the astaxanthin-rich alga Haematococcus pluvialis in human colon cancer cells. Cancer Lett. 2009;283(1):108. [PubMed: 19423215]. https://doi.org/10.1016/j.canlet.2009.03.031 PMid:19423215

20. Cort A, Ozturk N, Akpinar D, Unal M, Yucel G, Ciftcioglu A, et al. Suppressive effect of astaxanthin on retinal injury induced by elevated intraocular pressure. Regul Toxicol Pharmacol. 2010;58(1):121-30. [PubMed:20457203]. https://doi.org/10.1016/j.yrtph.2010.05.001 PMid:20457203

21. Yuan JP, Peng J, Yin K, Wang JH. Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae. Mol Nutr Food Res. 2011;55(1):150-65. [PubMed: 21207519]. https://doi.org/10.1002/mnfr.201000414 PMid:21207519

22. Tso MO, Lam TT. Method of retarding and ameliorating central nervous system and eye damage. US Patent.1996;5:527-33.

23. Wolf A, Asoh S, Hiranuma H, Ohsawa I, Iio K, Satou A, et al. Astaxanthin protects mitochondrial redox state and functional integrity against oxidative stress. J Nutr Biochem. 2010;21(5):381-9. [PubMed: 19423317] https://doi.org/10.1016/j.jnutbio.2009.01.011 PMid:19423317

24. Dong LY, Jin J, Lu G, Kang XL. Astaxanthin attenuates the apoptosis of retinal ganglion cells in db/db mice by inhibition of oxidative stress. Mar Drugs. 2013;11(3):960-74. [PubMed: 23519150]. https://doi.org/10.3390/md11030960 PMid:23519150 PMCid:PMC3705382

25. Tietze F. Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem. 1969;27(3):502-22. [PubMed: 4388022]. https://doi.org/10.1016/0003-2697(69)90064-5 PMid:4388022

26. Winterbourn CC, Hawkins RE, Brian M, Carrell RW. The estimation of red cell superoxide dismutase activity. J Lab Clin Med. 1975;85(2):337-41. [PubMed: 803541].

27. Satoh K. Serum lipid peroxide in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta. 1978;90(1):37-43. [PubMed: 719890]. https://doi.org/10.1016/0009-8981(78)90081-5 PMid:719890

28. Kruger NJ. The Bradford method for protein quantitation. In: Walker JM, editor. The protein protocols handbook. New York: Humana Press; 2009. P. 17-24. https://doi.org/10.1007/978-1-59745-198-7_4

29. Santocono M, Zurria M, Berrettini M, Fedeli D, Falcioni G. Influence of astaxanthin, zeaxanthin and lutein on DNA damage and repair in UVA-irradiated cells. J Photochem Photobiol B. 2006;85(3):205-15.[PubMed: 16962787]. https://doi.org/10.1016/j.jphotobiol.2006.07.009 PMid:16962787

30. Tiwari BK, Pandey KB, Abidi A, Rizvi SI. Markers of oxidative stress during diabetes mellitus. J Biomark. 2013;2013:378790. [PubMed: 26317014]. https://doi.org/10.1155/2013/378790 PMid:26317014 PMCid:PMC4437365

31. Bandeira Sde M, Guedes Gda S, da Fonseca LJ, Pires AS, Gelain DP, Moreira JC, et al. Characterization of blood oxidative stress in type 2 diabetes mellitus patients: increase in lipid peroxidation and SOD activity. Oxid Med Cell Longev. 2012;2012:819310. [PubMed: 23259029]. https://doi.org/10.1155/2012/819310 PMid:23259029 PMCid:PMC3509371

32. Yamagishi S, Matsui T. Advanced glycation end products (AGEs), oxidative stress and diabetic retinopathy. Curr Pharm Biotechnol. 2011;12(3):362-8. [PubMed: 20939798]. https://doi.org/10.2174/138920111794480534 PMid:20939798

33. Yoshida K, Hirokawa J, Tagami S, Kawakami Y, Urata Y, Kondo T. Weakened cellular scavenging activity against oxidative stress in diabetes mellitus: regulation of glutathione synthesis and efflux. Diabetologia. 1995;38(2):201-10. [PubMed: 7713315]. https://doi.org/10.1007/BF00400095 PMid:7713315

34. Jackson H, Braun CL, Ernst H. The chemistry of novel xanthophyll carotenoids. Am J Cardio. 2008;101(10A):50D-57D. [PubMed: 18474275]. 35. Marin DP, Bolin AP, Macedo Rde C, Sampaio SC, Otton R. Ros production in neutrophils from alloxan-induced diabetic rats treated in vivo with astaxanthin. Int Immunopharmacol. 2011;11(1):103-9. [PubMed:21055504]. https://doi.org/10.1016/j.intimp.2010.10.013 PMid:21055504

36. Breithaupt DE. Modern application of xanthophylls in animal feeding-a review. Trends Food Sci Technol. 2007;18(10):501-6. https://doi.org/10.1016/j.tifs.2007.04.009

37. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol. 2007;39(1):44-84. [PubMed: 16978905]. https://doi.org/10.1016/j.biocel.2006.07.001 PMid:16978905

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Astaxanthin Attenuates Oxidative Damage in Retina by Potentiation of the Antioxidant Capacity in Experimental Model of Diabetic Retinopathy

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Volume 6, Issue 3
July 2018
Pages 1-6

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Astaxanthin Attenuates Oxidative Damage in Retina by Potentiation of the Antioxidant Capacity in Experimental Model of Diabetic Retinopathy

References

Volume 6, Issue 3July 2018Pages 1-6

Files

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Volume 6, Issue 3
July 2018
Pages 1-6