Astaxanthin attenuates the apoptosis of retinal ganglion cells in db/db mice by inhibition of oxidative stress

Marine Drugs

Volumn 11, Issue 3, 2013, Pages 960-974

  Dong, Ling Yan ^a   Jin, Jie ^a   Lu, Gao ^b   Kang, Xiao Li ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b NORTHEAST AGRICULTURAL UNIVERSITY   (China)

Author keywords

Apoptosis; Astaxanthin; Oxidative stress; Retinal ganglion cells (RGCs)

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ASTAXANTHIN; HYDROGEN PEROXIDE; MALONALDEHYDE; MANGANESE SUPEROXIDE DISMUTASE; SUPEROXIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; APOPTOSIS; ARTICLE; CELL TRANSFORMATION; CONTROLLED STUDY; DIABETIC RETINOPATHY; DRUG EFFECT; ENZYME ACTIVITY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; RAT; RETINA GANGLION CELL;

ALGAE; MUS; RATTUS;

EID: 84875760496     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md11030960     Document Type: Article

References (43)

1. Antonetti, D.A.; Barber, A.J.; Bronson, S.K.; Freeman, W.M.; Gardner, T.W.; Jefferson, L.S.; Kester, M.; Kimball, S.R.; Krady, J.K.; LaNoue, K.F.; et al. Diabetic retinopathy: Seeing beyond glucose-induced microvascular disease. Diabetes 2006, 55, 2401-2411.
2. Ghirlanda, G.; Di Leo, M.A.; Caputo, S.; Cercone, S.; Greco, A.V. From functional to microvascular abnormalities in early diabetic retinopathy. Diabetes Metab. Rev. 1997, 13, 15-35.
3. Kowluru, R.A.; Chan, P.S. Oxidative stress and diabetic retinopathy. Exp. Diabetes Res. 2007, 2007, 43603.
4. Gurler, B.; Vural, H.; Yilmaz, N.; Oguz, H.; Satici, A.; Aksoy, N. The role of oxidative stress in diabetic retinopathy. Eye (Lond.) 2000, 14, 730-735.
5. Madsen-Bouterse, S.A.; Kowluru, R.A. Oxidative stress and diabetic retinopathy: Pathophysiological mechanisms and treatment perspectives. Rev. Endocr. Metab. Disord. 2008, 9, 315-327.
6. Cui, Y.; Xu, X.; Bi, H.; Zhu, Q.; Wu, J.; Xia, X.; Qiushi, R.; Ho, P.C. Expression modification of uncoupling proteins and MnSOD in retinal endothelial cells and pericytes induced by high glucose: The role of reactive oxygen species in diabetic retinopathy. Exp. Eye Res. 2006, 83, 807-816.
7. El-Remessy, A.B.; Bartoli, M.; Platt, D.H.; Fulton, D.; Caldwell, R.B. Oxidative stress inactivates VEGF survival signaling in retinal endothelial cells via PI 3-kinase tyrosine nitration. J. Cell Sci. 2005, 118, 243-252.
8. Gil, J.; Almeida, S.; Oliveira, C.R.; Rego, A.C. Cytosolic and mitochondrial ROS in staurosporine-induced retinal cell apoptosis. Free Radic. Biol. Med. 2003, 35, 1500-1514.
9. Carmody, R.J.; Cotter, T.G. Oxidative stress induces caspase-independent retinal apoptosis in vitro. Cell Death Differ. 2000, 7, 282-291.
10. Sanvicens, N.; Cotter, T.G. Ceramide is the key mediator of oxidative stress-induced apoptosis in retinal photoreceptor cells. J. Neurochem. 2006, 98, 1432-1444.
11. Naguib, Y.M. Antioxidant activities of astaxanthin and related carotenoids. J. Agric. Food Chem. 2000, 48, 1150-1154.
12. Leite, M.F.; Lima, A.M.; Massuyama, M.M.; Otton, R. Astaxanthin restores the enzymatic antioxidant profile in salivary gland of alloxan-induced diabetic rats. Arch. Oral Biol. 2010, 55, 479-485.
13. Nakajima, Y.; Inokuchi, Y.; Shimazawa, M.; Otsubo, K.; Ishibashi, T.; Hara, H. Astaxanthin, a dietary carotenoid, protects retinal cells against oxidative stress in vitro and in mice in vivo. J. Pharm. Pharmacol. 2008, 60, 1365-1374.
14. Kim, Y.J.; Kim, Y.A.; Yokozawa, T. Protection against oxidative stress, inflammation, and apoptosis of high-glucose-exposed proximal tubular epithelial cells by astaxanthin. J. Agric. Food Chem. 2009, 57, 8793-8797.
15. Moeller, S.M.; Parekh, N.; Tinker, L.; Ritenbaugh, C.; Blodi, B.; Wallace, R.B.; Mares, J.A. Associations between intermediate age-related macular degeneration and lutein and zeaxanthin in the Carotenoids in Age-related Eye Disease Study (CAREDS): Ancillary study of the Women's Health Initiative. Arch. Ophthalmol. 2006, 124, 1151-1162.
16. Krinsky, N.I.; Johnson, E.J. Carotenoid actions and their relation to health and disease. Mol. Aspects Med. 2005, 26, 459-516.
17. Winklhofer-Roob, B.M.; Rock, E.; Ribalta, J.; Shmerling, D.H.; Roob, J.M. Effects of vitamin E and carotenoid status on oxidative stress in health and disease. Evidence obtained from human intervention studies. Mol. Aspects Med. 2003, 24, 391-402.
18. Li, G.Y.; Fan, B.; Su, G.F. Acute energy reduction induces caspase-dependent apoptosis and activates p53 in retinal ganglion cells (RGC-5). Exp. Eye Res. 2009, 89, 581-589.
19. Ji, Y.; Lu, G.; Chen, G.; Huang, B.; Zhang, X.; Shen, K.; Wu, S. Microcystin-LR induces apoptosis via NF-κB/iNOS pathway in INS-1 cells. Int. J. Mol. Sci. 2011, 12, 4722-4734.
20. Kowluru, V.; Kowluru, R.A. Increased oxidative stress in diabetes regulates activation of a small molecular weight G-protein, H-Ras, in the retina. Mol. Vis. 2007, 13, 602-610.
21. Van Reyk, D.M.; Gillies, M.C.; Davies, M.J. The retina: Oxidative stress and diabetes. Redox Rep. 2003, 8, 187-192.
22. Burnaugh, L.; Sabeur, K.; Ball, B.A. Generation of superoxide anion by equine spermatozoa as detected by dihydroethidium. Theriogenology 2007, 67, 580-589.
23. Pan, H.Z.; Zhang, H.; Chang, D.; Li, H.; Sui, H. The change of oxidative stress products in diabetes mellitus and diabetic retinopathy. Br. J. Ophthalmol. 2008, 92, 548-551.
24. Miranda, M.; Muriach, M.; Roma, J.; Bosch-Morell, F.; Genoves, J.M.; Barcia, J.; Araiz, J.; Diaz-Llospis, M.; Romero, F.J. Oxidative stress in a model of experimental diabetic retinopathy: The utility of peroxinytrite scavengers. Arch. Soc. Esp. Oftalmol. 2006, 81, 27-32.
25. Choi, H.D.; Kim, J.H.; Chang, M.J.; Kyu-Youn, Y.; Shin, W.G. Effects of astaxanthin on oxidative stress in overweight and obese adults. Phytother. Res. 2011, 25, 1813-1818.
26. Yuan, J.P.; Peng, J.; Yin, K.; Wang, J.H. Potential health-promoting effects of astaxanthin: A high-value carotenoid mostly from microalgae. Mol. Nutr. Food Res. 2011, 55, 150-165.
27. Liu, X.; Osawa, T. Astaxanthin protects neuronal cells against oxidative damage and is a potent candidate for brain food. Forum Nutr. 2009, 61, 129-135.
28. Uchiyama, K.; Naito, Y.; Hasegawa, G.; Nakamura, N.; Takahashi, J.; Yoshikawa, T. Astaxanthin protects β-cells against glucose toxicity in diabetic db/db mice. Redox Rep. 2002, 7, 290-293.
29. Naito, Y.; Uchiyama, K.; Aoi, W.; Hasegawa, G.; Nakamura, N.; Yoshida, N.; Maoka, T.; Takahashi, J.; Yoshikawa, T. Prevention of diabetic nephropathy by treatment with astaxanthin in diabetic db/db mice. Biofactors 2004, 20, 49-59.
30. Poitout, V.; Briaud, I.; Kelpe, C.; Hagman, D. Gluco-lipotoxicity of the pancreatic β cell. Ann. Endocrinol. (Paris) 2004, 65, 37-41.
31. Drews, G.; Krippeit-Drews, P.; Dufer, M. Oxidative stress and β-cell dysfunction. Pflugers Arch. 2010, 460, 703-718.
32. Yoon, I.H.; Shiroyama, N.; Miyake, Y.; Awaya, S. Oscillatory potentials of local macular ERG in diabetic retinopathy. Korean J. Ophthalmol. 1990, 4, 40-45.
33. Iizuka, Y.; Hong, S.; Kim, C.Y.; Kim, S.K.; Seong, G.J. Agmatine pretreatment protects retinal ganglion cells (RGC-5 cell line) from oxidative stress in vitro. Biocell 2008, 32, 245-250.
34. Maher, P.; Hanneken, A. Flavonoids protect retinal ganglion cells from oxidative stress-induced death. Invest. Ophthalmol. Vis. Sci. 2005, 46, 4796-4803.
35. Byeon, S.H.; Lee, S.C.; Choi, S.H.; Lee, H.K.; Lee, J.H.; Chu, Y.K.; Kwon, O.W. Vascular endothelial growth factor as an autocrine survival factor for retinal pigment epithelial cells under oxidative stress via the VEGF-R2/PI3K/Akt. Invest. Ophthalmol. Vis. Sci. 2010, 51, 1190-1197.
36. Tian, X.Y.; Wong, W.T.; Xu, A.; Chen, Z.Y.; Lu, Y.; Liu, L.M.; Lee, V.W.; Lau, C.W.; Yao, X.; Huang, Y. Rosuvastatin improves endothelial function in db/db mice: Role of angiotensin II type 1 receptors and oxidative stress. Br. J. Pharmacol. 2011, 164, 598-606.
37. Kitada, M.; Kume, S.; Imaizumi, N.; Koya, D. Resveratrol improves oxidative stress and protects against diabetic nephropathy through normalization of Mn-SOD dysfunction in AMPK/SIRT1-independent pathway. Diabetes 2011, 60, 634-643.
38. Xiao, C.; He, M.; Nan, Y.; Zhang, D.; Chen, B.; Guan, Y.; Pu, M. Physiological effects of superoxide dismutase on altered visual function of retinal ganglion cells in db/db mice. PLoS One 2012, 7, e30343.
39. Martin, B.T.; List, E.O.; Kopchick, J.J.; Sauve, Y.; Harvey, S. Selective inner retinal dysfunction in growth hormone transgenic mice. Growth Horm. IGF Res. 2011, 21, 219-227.
40. Rousseau, S.; Lachapelle, P. The electroretinogram recorded at the onset of dark-adaptation: Understanding the origin of the scotopic oscillatory potentials. Doc. Ophthalmol. 1999, 99, 135-150.
41. Yu, M.; Peachey, N.S. Attenuation of oscillatory potentials in nob2 mice. Doc. Ophthalmol. 2007, 115, 173-186.
42. Wang, Y.; Gao, L.; Li, Y.; Chen, H.; Sun, Z. Nifedipine protects INS-1 β-cell from high glucose-induced ER stress and apoptosis. Int. J. Mol. Sci. 2011, 12, 7569-7580.
43. He, S.Q.; Zhang, Y.H.; Venugopal, S.K.; Dicus, C.W.; Perez, R.V.; Ramsamooj, R.; Nantz, M.H.; Zern, M.A.; Wu, J. Delivery of antioxidative enzyme genes protects against ischemia/ reperfusion-induced liver injury in mice. Liver Transpl. 2006, 12, 1869-1879.