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Oxidative Medicine and Cellular Longevity
Volume 2013, Article ID 213505, 11 pages
http://dx.doi.org/10.1155/2013/213505
Research Article

Effect of Lutein and Antioxidant Supplementation on VEGF Expression, MMP-2 Activity, and Ultrastructural Alterations in Apolipoprotein E-Deficient Mouse

1Experimental Ophthalmology Laboratory, Clínica Universidad de Navarra, School of Medicine, University of Navarra, ES-31008 Pamplona, Spain
2Department of Ophthalmology, Clínica Universidad de Navarra, School of Medicine, University of Navarra, Pio XII 36, ES-31008 Pamplona, Spain
3Atherothrombosis Research Laboratory, Division of Cardiovascular Sciences, Center for Applied Medical Research (CIMA), University of Navarra, ES-31008 Pamplona, Spain

Received 7 February 2013; Revised 5 April 2013; Accepted 8 April 2013

Academic Editor: Kota V. Ramana

Copyright © 2013 Patricia Fernández-Robredo et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. A. Curcio, M. Johnson, J. D. Huang, and M. Rudolf, “Aging, age-related macular degeneration, and the response-to-retention of apolipoprotein B-containing lipoproteins,” Progress in Retinal and Eye Research, vol. 28, no. 6, pp. 393–422, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. X. Ding, M. Patel, and C. C. Chan, “Molecular pathology of age-related macular degeneration,” Progress in Retinal and Eye Research, vol. 28, no. 1, pp. 1–18, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. G. S. Hageman, K. Gehrs, S. Lejnine et al., “Clinical validation of a genetic model to estimate the risk of developing choroidal neovascular age-related macular degeneration,” Human Genomics, vol. 5, no. 5, pp. 420–440, 2011. View at Publisher · View at Google Scholar
  4. G. J. McKay, C. C. Patterson, U. Chakravarthy et al., “Evidence of association of APOE with age-related macular degeneration-a pooled analysis of 15 studies,” Human Mutation, vol. 32, no. 12, pp. 1407–1416, 2011. View at Publisher · View at Google Scholar
  5. R. H. Guymer and E. W. T. Chong, “Modifiable risk factors for age-related macular degeneration,” Medical Journal of Australia, vol. 184, no. 9, pp. 455–458, 2006. View at Google Scholar · View at Scopus
  6. J. Ambati, B. K. Ambati, S. H. Yoo, S. Ianchulev, and A. P. Adamis, “Age-related macular degeneration: etiology, pathogenesis, and therapeutic strategies,” Survey of Ophthalmology, vol. 48, no. 3, pp. 257–293, 2003. View at Publisher · View at Google Scholar · View at Scopus
  7. W. R. Green, “Histopathology of age-related macular degeneration,” Molecular Vision, vol. 5, p. 27, 1999. View at Google Scholar · View at Scopus
  8. P. S. Mettu, A. R. Wielgus, S. S. Ong, and S. W. Cousins, “Retinal pigment epithelium response to oxidant injury in the pathogenesis of early age-related macular degeneration,” Molecular Aspects of Medicine, vol. 33, no. 4, pp. 376–398, 2012. View at Publisher · View at Google Scholar
  9. B. Falsini, M. Piccardi, G. Iarossi, A. Fadda, E. Merendino, and P. Valentini, “Influence of short-term antioxidant supplementation on macular function in age-related maculopathy: a pilot study including electrophysiologic assessment,” Ophthalmology, vol. 110, no. 1, pp. 51–60, 2003. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Dithmar, C. A. Curcio, N. A. Le, S. Brown, and H. E. Grossniklaus, “Ultrastructural changes in Bruch's membrane of apolipoprotein E- deficient mice,” Investigative Ophthalmology and Visual Science, vol. 41, no. 8, pp. 2035–2042, 2000. View at Google Scholar · View at Scopus
  11. D. Praticò, R. K. Tangirala, D. J. Rader, J. Rokach, and G. A. Fitzgerald, “Vitamin E suppresses isoprostane generation in vivo and reduces atherosclerosis in ApoE-deficient mice,” Nature Medicine, vol. 4, no. 10, pp. 1189–1192, 1998. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Kliffen, E. Lutgens, M. J. A. P. Daemen, E. D. De Muinck, C. M. Mooy, and P. T. V. M. De Jong, “The APOE3-Leiden mouse as an animal model for basal laminar deposit,” British Journal of Ophthalmology, vol. 84, no. 12, pp. 1415–1419, 2000. View at Publisher · View at Google Scholar · View at Scopus
  13. J. M. Ong, N. C. Zorapapel, K. A. Rich et al., “Effects of cholesterol and apolipoprotein E on retinal abnormalities in ApoE-deficient mice,” Investigative Ophthalmology and Visual Science, vol. 42, no. 8, pp. 1891–1900, 2001. View at Google Scholar · View at Scopus
  14. E. Applegate, “Introduction: nutritional and functional roles of eggs in the diet,” Journal of the American College of Nutrition, vol. 19, supplement 5, pp. 495S–498S, 2000. View at Google Scholar · View at Scopus
  15. E. W. T. Chong, T. Y. Wong, A. J. Kreis, J. A. Simpson, and R. H. Guymer, “Dietary antioxidants and primary prevention of age related macular degeneration: systematic review and meta-analysis,” British Medical Journal, vol. 335, no. 7623, pp. 755–759, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. E. Loane, J. M. Nolan, O. O'Donovan, P. Bhosale, P. S. Bernstein, and S. Beatty, “Transport and retinal capture of lutein and zeaxanthin with reference to age-related macular degeneration,” Survey of Ophthalmology, vol. 53, no. 1, pp. 68–81, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. J. T. Landrum, R. A. Bone, H. Joa, M. D. Kilburn, L. L. Moore, and K. E. Sprague, “A one year study of the macular pigment: the effect of 140 days of a lutein supplement,” Experimental Eye Research, vol. 65, no. 1, pp. 57–62, 1997. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Pratt, “Dietary prevention of age-related macular degeneration,” Optometry, vol. 70, no. 1, pp. 39–47, 1999. View at Google Scholar · View at Scopus
  19. D. M. Snodderly, “Evidence for protection against age-related macular degeneration by carotenoids and antioxidant vitamins,” American Journal of Clinical Nutrition, vol. 62, supplement 6, pp. 1448S–1461S, 1995. View at Google Scholar · View at Scopus
  20. L. M. Rapp, S. S. Maple, and J. H. Choi, “Lutein and zeaxanthin concentrations in rod outer segment membranes from perifoveal and peripheral human retina,” Investigative Ophthalmology and Visual Science, vol. 41, no. 5, pp. 1200–1209, 2000. View at Google Scholar · View at Scopus
  21. P. Fernandez-Robredo, D. Moya, J. A. Rodriguez, and A. Garcia-Layana, “Vitamins C and E reduce retinal oxidative stress and nitric oxide metabolites and prevent ultrastructural alterations in porcine hypercholesterolemia,” Investigative Ophthalmology and Visual Science, vol. 46, no. 4, pp. 1140–1146, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Fernández-Robredo, S. Recalde, G. Arnáiz et al., “Effect of zeaxanthin and antioxidant supplementation on vascular endothelial growth factor (VEGF) expression in apolipoprotein-e deficient mice,” Current Eye Research, vol. 34, no. 7, pp. 543–552, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. P. Fernandez-Robredo, S. R. Maestre, J. Zarranz-Ventura, H. H. Mulero, A. Salinas-Alaman, and A. Garcia-Layana, “Myopic choroidal neovascularization genetics,” Ophthalmology, vol. 115, no. 9, pp. 1632–e1, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. P. Fernández-Robredo, J. A. Rodríguez, L. M. Sádaba, S. Recalde, and A. García-Layana, “Egg yolk improves lipid profile, lipid peroxidation and retinal abnormalities in a murine model of genetic hypercholesterolemia,” Journal of Nutritional Biochemistry, vol. 19, no. 1, pp. 40–48, 2008. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Conti, P. C. Morand, P. Levillain, and A. Lemonnier, “Improved fluorometric determination of malonaldehyde,” Clinical Chemistry, vol. 37, no. 7, pp. 1273–1275, 1991. View at Google Scholar · View at Scopus
  26. S. Archer, “Measurement of nitric oxide in biological models,” FASEB Journal, vol. 7, no. 2, pp. 349–360, 1993. View at Google Scholar · View at Scopus
  27. M. Marzinzig, A. K. Nussler, J. Stadler et al., “Improved methods to measure end products of nitric oxide in biological fluids: nitrite, nitrate, and S-nitrosothiols,” Nitric Oxide, vol. 1, no. 2, pp. 177–189, 1997. View at Publisher · View at Google Scholar · View at Scopus
  28. P. A. M. Snoek-van Beurden and J. W. Von Den Hoff, “Zymographic techniques for the analysis of matrix metalloproteinases and their inhibitors,” BioTechniques, vol. 38, no. 1, pp. 73–83, 2005. View at Google Scholar · View at Scopus
  29. D. G. Espinosa-Heidmann, J. Sall, E. P. Hernandez, and S. W. Cousins, “Basal laminar deposit formation in APO B100 transgenic mice: complex interactions between dietary fat, blue light, and vitamin E,” Investigative Ophthalmology and Visual Science, vol. 45, no. 1, pp. 260–266, 2004. View at Publisher · View at Google Scholar · View at Scopus
  30. M. V. Miceli, D. A. Newsome, D. J. Tate, and T. G. Sarphie, “Pathologic changes in the retinal pigment epithelium and Bruch's membrane of fat-fed atherogenic mice,” Current Eye Research, vol. 20, no. 1, pp. 8–16, 2000. View at Google Scholar · View at Scopus
  31. S. Dithmar, N. A. Sharara, C. A. Curcio et al., “Murine high-fat diet and laser photochemical model of basal deposits in bruch membrane,” Archives of Ophthalmology, vol. 119, no. 11, pp. 1643–1649, 2001. View at Google Scholar · View at Scopus
  32. A. N. Witmer, G. F. J. M. Vrensen, C. J. F. Van Noorden, and R. O. Schlingemann, “Vascular endothelial growth factors and angiogenesis in eye disease,” Progress in Retinal and Eye Research, vol. 22, no. 1, pp. 1–29, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. T. T. L. Wong, C. Sethi, J. T. Daniels, G. A. Limb, G. Murphy, and P. T. Khaw, “Matrix metalloproteinases in disease and repair processes in the anterior segment,” Survey of Ophthalmology, vol. 47, no. 3, pp. 239–256, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. H. Nagaset and J. F. Woessner, “Matrix metalloproteinases,” Journal of Biological Chemistry, vol. 274, no. 31, pp. 21491–21494, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. I. A. Bhutto, T. Baba, C. Merges, D. S. McLeod, and G. A. Lutty, “Low nitric oxide synthases (NOSs) in eyes with age-related macular degeneration (AMD),” Experimental Eye Research, vol. 90, no. 1, pp. 155–167, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. J. M. Seddon, U. A. Ajani, R. D. Sperduto et al., “Dietary carotenoids, vitamins A, C, and E, and advanced age-related macular degeneration,” Journal of the American Medical Association, vol. 272, no. 18, pp. 1413–1420, 1994. View at Publisher · View at Google Scholar · View at Scopus
  37. C. R. Gale, N. F. Hall, D. I. W. Phillips, and C. N. Martyn, “Lutein and zeaxanthin status and risk of age-related macular degeneration,” Investigative Ophthalmology and Visual Science, vol. 44, no. 6, pp. 2461–2465, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. R. Kannan, N. Zhang, P. G. Sreekumar et al., “Stimulation of apical and basolateral vascular endothelial growth factor-A and vascular endothelial growth factor-C secretion by oxidative stress in polarized retinal pigment epithelial cells,” Molecular Vision, vol. 12, pp. 1649–1659, 2006. View at Google Scholar · View at Scopus
  39. R. Arias, Efecto de la homocisteína sobre la expresión vascular del TIMP-1 y la Metaloproteinasa-2. Implicaciones en la aterosclerosis [Ph.D. thesis], Universidad de Navarra, Pamplona, Spain, 2002.
  40. B. Nespereira, M. Pérez-Ilzarbe, P. Fernández, A. M. Fuentes, J. A. Páramo, and J. A. Rodríguez, “Vitamins C and E downregulate vascular VEGF and VEGFR-2 expression in apolipoprotein-E-deficient mice,” Atherosclerosis, vol. 171, no. 1, pp. 67–73, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. G. Hashimoto, I. Inoki, Y. Fujii, T. Aoki, E. Ikeda, and Y. Okada, “Matrix metalloproteinases cleave connective tissue growth factor and reactivate angiogenic activity of vascular endothelial growth factor 165,” Journal of Biological Chemistry, vol. 277, no. 39, pp. 36288–36295, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. Y. J. Roh, C. Moon, S. Y. Kim et al., “Glutathione depletion induces differential apoptosis in cells of mouse retina, in vivo,” Neuroscience Letters, vol. 417, no. 3, pp. 266–270, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. P. Maher and A. Hanneken, “Flavonoids protect retinal ganglion cells from oxidative stress-induced death,” Investigative Ophthalmology and Visual Science, vol. 46, no. 12, pp. 4796–4803, 2005. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Miranda, E. Arnal, S. Ahuja et al., “Antioxidants rescue photoreceptors in rd1 mice: relationship with thiol metabolism,” Free Radical Biology and Medicine, vol. 48, no. 2, pp. 216–222, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Kijlstra, Y. Tian, E. R. Kelly, and T. T. Berendschot, “Lutein: more than just a filter for blue light,” Progress in Retinal and Eye Research, vol. 31, no. 4, pp. 303–315, 2012. View at Publisher · View at Google Scholar
  46. K. Izumi-Nagai, N. Nagai, K. Ohgami et al., “Macular pigment lutein is antiinflammatory in preventing choroidal neovascularization,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 27, no. 12, pp. 2555–2562, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. Z. Sun, J. Liu, X. Zeng et al., “Protective actions of microalgae against endogenous and exogenous advanced glycation endproducts (AGEs) in human retinal pigment epithelial cells,” Food and Function, vol. 2, no. 5, pp. 251–258, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. D. G. Espinosa-Heidmann, I. J. Suner, P. Catanuto, E. P. Hernandez, M. E. Marin-Castano, and S. W. Cousins, “Cigarette smoke-related oxidants and the development of sub-RPE deposits in an experimental animal model of dry AMD,” Investigative Ophthalmology and Visual Science, vol. 47, no. 2, pp. 729–737, 2006. View at Publisher · View at Google Scholar · View at Scopus
  49. S. W. Cousins, D. G. Espinosa-Heidmann, A. Alexandridou, J. Sall, S. Dubovy, and K. Csaky, “The role of aging, high fat diet and blue light exposure in an experimental mouse model for basal laminar deposit formation,” Experimental Eye Research, vol. 75, no. 5, pp. 543–553, 2002. View at Publisher · View at Google Scholar · View at Scopus