Prophylactic neuroprotection by blueberry-enriched diet in a rat model of light-induced retinopathy

Journal of Nutritional Biochemistry

Volumn 24, Issue 4, 2013, Pages 647-655

  Tremblay, François ^a   Waterhouse, Jenna ^a   Nason, Janette ^a   Kalt, Wilhelmina ^b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Anthocyanin; Blueberry; Light induced retinal degeneration; Neuroprotection; Photoreceptor; Retina

Indexed keywords

BLUEBERRY EXTRACT; CHLOROGENIC ACID; CYANIDIN 3 GLUCOSIDE; GALLIC ACID; PHENOL; PLACEBO; RHODOPSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; ELECTRORETINOGRAPHY; HISTOPATHOLOGY; LIGHT INDUCED RETINAL DEGENERATION; NEUROPROTECTION; NONHUMAN; PIGMENT EPITHELIUM; RAT; RETINA INJURY; RETINOPATHY; TREATMENT DURATION;

ANIMALS; BLUEBERRY PLANT; DISEASE MODELS, ANIMAL; ELECTRORETINOGRAPHY; LIGHT; NEUROPROTECTIVE AGENTS; RATS; RATS, WISTAR; RETINAL DISEASES;

RATTUS; RATTUS NORVEGICUS; VACCINIUM;

EID: 84875073072     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2012.03.011     Document Type: Article

References (82)

1. Kalt W., Ryan D.A., Duy J.C., Prior R.L., Ehlenfeldt M.K., Vander Kloet S.P. Interspecific variation in anthocyanins, phenolics, and antioxidant capacity among genotypes of highbush and lowbush blueberries (Vaccinium section cyanococcus spp.). J Agric Food Chem 2001, 49(10):4761-4767.
2. Wang S.Y., Chen C.T., Sciarappa W., Wang C.Y., Camp M.J. Fruit quality, antioxidant capacity, and flavonoid content of organically and conventionally grown blueberries. J Agric Food Chem 2008, 56(14):5788-5794.
3. Brambilla A., Lo Scalzo R., Bertolo G., Torreggiani D. Steam-blanched highbush blueberry (Vaccinium corymbosum L.) juice: phenolic profile and antioxidant capacity in relation to cultivar selection. J Agric Food Chem 2008, 56(8):2643-2648.
4. Bagchi D., Sen C.K., Bagchi M., Atalay M. Anti-angiogenic, antioxidant, and anti-carcinogenic properties of a novel anthocyanin-rich berry extract formula. Biochemistry (Mosc) 2004, 69(1):75-80.
5. Wang L.S., Stoner G.D. Anthocyanins and their role in cancer prevention. Cancer Lett 2008, 269(2):281-290.
6. Ziberna L., Lunder M., Moze S., Vanzo A., Tramer F., Passamonti S., Drevensek G. Acute cardioprotective and cardiotoxic effects of bilberry anthocyanins in ischemia-reperfusion injury: beyond concentration-dependent antioxidant activity. Cardiovasc Toxicol 2010, 10(4):283-294.
7. Shin W.H., Park S.J., Kim E.J. Protective effect of anthocyanins in middle cerebral artery occlusion and reperfusion model of cerebral ischemia in rats. Life Sci 2006, 79(2):130-137.
8. Spencer J.P. Flavonoids and brain health: multiple effects underpinned by common mechanisms. Genes Nutr 2009, 4(4):243-250.
9. Krikorian R., Shidler M.D., Nash T.A., Kalt W., Vinqvist-Tymchuk M.R., Shukitt-Hale B., Joseph J.A. Blueberry supplementation improves memory in older adults. J Agric Food Chem 2009, 58(7):3996-4000.
10. Rossi A., Serraino I., Dugo P., Di Paola R., Mondello L., Genovese T., et al. Protective effects of anthocyanins from blackberry in a rat model of acute lung inflammation. Free Radic Res 2003, 37(8):891-900.
11. DeFuria J., Bennett G., Strissel K.J., Perfield J.W., Milbury P.E., Greenberg A.S., Obin M.S. Dietary blueberry attenuates whole-body insulin resistance in high fat-fed mice by reducing adipocyte death and its inflammatory sequelae. J Nutr 2009, 139(8):1510-1516.
12. Roy S., Khanna S., Alessio H.M., Vider J., Bagchi D., Bagchi M., Sen C.K. Anti-angiogenic property of edible berries. Free Radic Res 2002, 36(9):1023-1031.
13. Shin D.Y., Lee W.S., Lu J.N., Kang M.H., Ryu C.H., Kim G.Y., et al. Induction of apoptosis in human colon cancer HCT-116 cells by anthocyanins through suppression of Akt and activation of p38-MAPK. Int J Oncol 2009, 35(6):1499-1504.
14. Zikri N.N., Riedl K.M., Wang L.S., Lechner J., Schwartz S.J., Stoner G.D. Black raspberry components inhibit proliferation, induce apoptosis, and modulate gene expression in rat esophageal epithelial cells. Nutr Cancer 2009, 61(6):816-826.
15. Canter P.H., Ernst E. Anthocyanosides of Vaccinium myrtillus (bilberry) for night vision - a systematic review of placebo-controlled trials* 1. Surv Ophthalmol 2004, 49(1):38-50.
16. Jayle G.E., Aubert L. Action des glucosides d'anthocyanes sur la vision scotopique et mesopique du suject normal. Therapie 1964, 171:171-175.
17. Kalt W., Hanneken A., Milbury P., Tremblay F. Recent research on polyphenolics in vision and eye health. J Agric Food Chem 2010, 58(7):4001-4007.
18. Matsumoto H., Nakamura Y., Tachibanaki S., Kawamura S., Hirayama M. Stimulatory effect of cyanidin 3-glycosides on the regeneration of rhodopsin. J Agric Food Chem 2003, 51(12):3560-3563.
19. Tronche P., Bastide P. Effet des glycosides 'anthocyanes sur la cinetique de regeneration du pourpre retinien chez le lapin. C.R. Soc Biol 1967, 161:2473-2476.
20. Tirupula K.C., Balem F., Yanamala N., Klein-Seetharaman J. Ph-dependent interaction of rhodopsin with cyanidin-3-glucoside. 2. Functional aspects. Photochem Photobiol 2009, 85(2):463-470.
21. Johnson J., Maher P., Hanneken A. The flavonoid, eriodictyol, induces long-term protection in ARPE-19 cells through its effects on nrf2 activation and phase 2 gene expression. Invest Ophthalmol Vis Sci 2009, 50(5):2398-2406.
22. Yanamala N., Tirupula K.C., Balem F., Klein-Seetharaman J. Ph-dependent interaction of rhodopsin with cyanidin-3-glucoside. 1. Structural aspects. Photochem Photobiol 2009, 85(2):454-462.
23. Ponte F, Lauricella M. Effect of Vaccinium myrtillus total extract on the recovery in the dark of the human electroretinogram. Atti VII Simposio ISCERG Istambul 1969; 355-66.
24. Sbrozzi F., Landini J., Zago M. Night vision affected by anthocyanosides. An electroretinographic test. Minerva Oftalmol 1983, 24:189-193.
25. Penn J.S., Thum L.A. A comparison of the retinal effects of light damage and high illuminance light history. Prog Clin Biol Res 1987, 247:425-438.
26. O'Steen W.K., Shear C.R., Anderson K.V. Retinal damage after prolonged exposure to visible light. A light and electron microscopic study. Am J Anat 1972, 134(1):5-21.
27. Wenzel A., Grimm C., Samardzija M., Reme C.E. Molecular mechanisms of light-induced photoreceptor apoptosis and neuroprotection for retinal degeneration. Prog Retin Eye Res 2005, 24(2):275-306.
28. Li F., Cao W., Anderson R.E. Protection of photoreceptor cells in adult rats from light-induced degeneration by adaptation to bright cyclic light. Exp Eye Res 2001, 73(4):569-577.
29. Organisciak D.T., Darrow R.M., Barsalou L., Kutty R.K., Wiggert B. Circadian-dependent retinal light damage in rats. Invest Ophthalmol Vis Sci 2000, 41(12):3694-3701.
30. Vaughan D.K., Coulibaly S.F., Darrow R.M., Organisciak D.T. A morphometric study of light-induced damage in transgenic rat models of retinitis pigmentosa. Invest Ophthalmol Vis Sci 2003, 44(2):848.
31. Reme C.E., Grimm C., Hafezi F., Marti A., Wenzel A. Apoptotic cell death in retinal degenerations. Prog Retin Eye Res 1998, 17(4):443-464.
32. Roh S., Weiter J.J. Light damage to the eye. J Fla Med Assoc 1994, 81(4):248-251.
33. Noell W.K., Walker V.S., Kang B.S., Berman S. Retinal damage by light in rats. Invest Ophthalmol 1966, 5(5):450-473.
34. Hafezi F., Marti A., Munz K., Reme C.E. Light-induced apoptosis: differential timing in the retina and pigment epithelium. Exp Eye Res 1997, 64(6):963-970.
35. Rapp L.M., Tolman B.L., Koutz C.A., Thum L.A. Predisposing factors to light-induced photoreceptor cell damage: retinal changes in maturing rats. Exp Eye Res 1990, 51(2):177-184.
36. Joly S., Pernet V., Dorfman A.L., Chemtob S., Lachapelle P. Light-induced retinopathy: comparing adult and juvenile rats. Invest Ophthalmol Vis Sci 2006, 47(7):3202-3212.
37. Ranchon I., Gorrand J.M., Cluzel J., Vennat J.C., Doly M. Light-induced variations of retinal sensitivity in rats. Curr Eye Res 1998, 17(1):14-23.
38. Maccarone R., Di Marco S., Bisti S. Saffron supplement maintains morphology and function after exposure to damaging light in mammalian retina. Invest Ophthalmol Vis Sci 2008, 49(3):1254-1261.
39. Mandal M.N., Patlolla J.M., Zheng L., Agbaga M.P., Tran J.T., Wicker L., et al. Curcumin protects retinal cells from light-and oxidant stress-induced cell death. Free Radic Biol Med 2009, 46(5):672-679.
40. Tanaka J., Nakanishi T., Ogawa K., Tsuruma K., Shimazawa M., Shimoda H., Hara H. Purple rice extract and anthocyanidins of the constituents protect against light-induced retinal damage in vitro and in vivo. J Agric Food Chem 2011, 59(2):528-536.
41. Imai S., Inokuchi Y., Nakamura S., Tsuruma K., Shimazawa M., Hara H. Systemic administration of a free radical scavenger, edaravone, protects against light-induced photoreceptor degeneration in the mouse retina. Eur J Pharmacol 2010, 642(1-3):77-85.
42. Costa B.L., Fawcett R., Li G.Y., Safa R., Osborne N.N. Orally administered epigallocatechin gallate attenuates light-induced photoreceptor damage. Brain Res Bull 2008, 76(4):412-423.
43. Boatright J.H., Moring A.G., McElroy C., Phillips M.J., Do V.T., Chang B., et al. Tool from ancient pharmacopoeia prevents vision loss. Mol Vis 2006, 12:1706-1714.
44. Collier, Patel, Martin, Dembinska, Hellberg, Krueger, et al. Agonists at the serotonin receptor (5HT1A) protect the retina from severe photo- oxidative stress. IOVS 2011.
45. Kunchithapautham K., Coughlin B., Lemasters J.J., Rohrer B. Differential effects of rapamycin on rods and cones during light-induced stress in albino mice. Invest Ophthalmol Vis Sci 2011, 52(6):2967-2975.
46. Sanders R.D., Ma D., Maze M. Anaesthesia induced neuroprotection. Best Pract Res Clin Anaesthesiol 2005, 19(3):461-474.
47. Singleton V.L., Rossi J.A. Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture 1965, 16(3):144.
48. Castelluccio C., Paganga G., Melikian N., Bolwell G.P., Pridham J., Sampson J., Rice-Evans C. Antioxidant potential of intermediates in phenylpropanoid metabolism in higher plants. FEBS Lett 1995, 368(1):188-192.
49. Fulton A.B., Hansen R.M. Scotopic stimulus/response relations of the b-wave of the electroretinogram. Doc Ophthalmol 1988, 68(3-4):293-304.
50. Manach C., Williamson G., Morand C., Scalbert A., Rémésy C. Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies. Am J Clin Nutr 2005, 81(1 Suppl):230S-242S.
51. Del Bò C., Ciappellano S., Klimis-Zacas D., Martini D., Gardana C., Riso P., Porrini M. Anthocyanin absorption, metabolism, and distribution from a wild blueberry-enriched diet (Vaccinium angustifolium) is affected by diet duration in the Sprague-Dawley rat. J Agric Food Chem 2010, 58(4):2491-2497.
52. Mazza G., Kay C.D., Cottrell T., Holub B.J. Absorption of anthocyanins from blueberries and serum antioxidant status in human subjects. J Agric Food Chem 2002, 50(26):7731-7737.
53. Kalt W., Blumberg J.B., McDonald J.E., Vinqvist-Tymchuk M.R., Fillmore S.A., Graf B.A., et al. Identification of anthocyanins in the liver, eye, and brain of blueberry-fed pigs. J Agric Food Chem 2008, 56(3):705-712.
54. Andres-Lacueva C., Shukitt-Hale B., Galli R.L., Jauregui O., Lamuela-Raventos R.M., Joseph J.A. Anthocyanins in aged blueberry-fed rats are found centrally and may enhance memory. Nutr Neurosci 2005, 8(2):111-120.
55. Sweeney M.I., Kalt W., MacKinnon S.L., Ashby J., Gottschall-Pass K.T. Feeding rats diets enriched in lowbush blueberries for six weeks decreases ischemia-induced brain damage. Nutr Neurosci 2002, 5(6):427-431.
56. Galli R.L., Bielinski D.F., Szprengiel A., Shukitt-Hale B., Joseph J.A. Blueberry supplemented diet reverses age-related decline in hippocampal HSP70 neuroprotection. Neurobiol Aging 2006, 27(2):344-350.
57. Galli R.L., Shukitt-Hale B., Youdim K.A., Joseph J.A. Fruit polyphenolics and brain aging: nutritional interventions targeting age-related neuronal and behavioral deficits. Ann N Y Acad Sci 2002, 959:128-132.
58. Dulebohn R.V., Yi W., Srivastava A., Akoh C.C., Krewer G., Fischer J.G. Effects of blueberry (Vaccinium ashei) on DNA damage, lipid peroxidation, and phase II enzyme activities in rats. J Agric Food Chem 2008, 56(24):11700-11706.
59. Maeda A., Maeda T., Golczak M., Chou S., Desai A., Hoppel C.L., et al. Involvement of all-trans-retinal in acute light-induced retinopathy of mice. J Biol Chem 2009, 284(22):15173-15183.
60. Rózanowska M., Sarna T. Light-induced damage to the retina: role of rhodopsin chromophore revisited. Photochem Photobiol 2005, 81(6):1305-1330.
61. Xie Z., Wu X., Gong Y., Song Y., Qiu Q., Li C. Intraperitoneal injection of ginkgo biloba extract enhances antioxidation ability of retina and protects photoreceptors after light-induced retinal damage in rats. Curr Eye Res 2007, 32(5):471-479.
62. Wiegand R.D., Giusto N.M., Rapp L.M., Anderson R.E. Evidence for rod outer segment lipid peroxidation following constant illumination of the rat retina. Invest Ophthalmol Vis Sci 1983, 24(10):1433.
63. Hafezi F., Steinbach J.P., Marti A., Munz K., Wang Z.Q., Wagner E.F., et al. The absence of c-fos prevents light-induced apoptotic cell death of photoreceptors in retinal degeneration in vivo. Nat Med 1997, 3(3):346-349.
64. Wenzel A., Grimm C., Marti A., Kueng-Hitz N., Hafezi F., Niemeyer G., Remé C.E. C-Fos controls the "private pathway" of light-induced apoptosis of retinal photoreceptors. J Neurosci 2000, 20(1):81-88.
65. Organisciak D.T., Vaughan D.K. Retinal light damage: mechanisms and protection. Prog Retin Eye Res 2010, 29(2):113-134.
66. O'Steen W.K., Anderson K.V., Shear C.R. Photoreceptor degeneration in albino rats: dependency on age. Invest Ophthalmol 1974, 13(5):334-339.
67. Youdim K.A., Shukitt-Hale B., MacKinnon S., Kalt W., Joseph J.A. Polyphenolics enhance red blood cell resistance to oxidative stress: in vitro and in vivo. Biochim Biophys Acta 2000, 1523(1):117-122.
68. Zafra-Stone S., Yasmin T., Bagchi M., Chatterjee A., Vinson J.A., Bagchi D. Berry anthocyanins as novel antioxidants in human health and disease prevention. Mol Nutr Food Res 2007, 51(6):675-683.
69. Stone J., Maslim J., Valter-Kocsi K., Mervin K., Bowers F., Chu Y., et al. Mechanisms of photoreceptor death and survival in mammalian retina. Prog Retin Eye Res 1999, 18(6):689-736.
70. Chen L., Wu W., Dentchev T., Wong R., Dunaief J.L. Increased metallothionein in light damaged mouse retinas. Exp Eye Res 2004, 79(2):287-293.
71. Matsumoto H., Nakamura Y., Iida H., Ito K., Ohguro H. Comparative assessment of distribution of blackcurrant anthocyanins in rabbit and rat ocular tissues. Exp Eye Res 2006, 83(2):348-356.
72. Ishizawa Y., Sharp R., Liebman P.A., Eckenhoff R.G. Halothane binding to a G protein coupled receptor in retinal membranes by photoaffinity labeling. Biochemistry 2000, 39(29):8497-8502.
73. Keller C., Grimm C., Wenzel A., Hafezi F., Reme C. Protective effect of halothane anesthesia on retinal light damage: inhibition of metabolic rhodopsin regeneration. Invest Ophthalmol Vis Sci 2001, 42(2):476-480.
74. Hanneken A., Harris R., Olson A., Crouch R., Cornwall C., Kono M. Modulation of opsin signalling by flavonoids. Invest Ophthalmol Vis Sci 2009, 50. (E-Abstract 2722).
75. Albert D.M., Neekhra A., Wang S., Darjatmoko S.R., Sorenson C.M., Dubielzig R.R., Sheibani N. Development of choroidal neovascularization in rats with advanced intense cyclic light-induced retinal degeneration. Arch Ophthalmol 2010, 128(2):212-222.
76. Wasowicz M., Morice C., Ferrari P., Callebert J., Versaux-Botteri C. Long-term effects of light damage on the retina of albino and pigmented rats. Invest Ophthalmol Vis Sci 2002, 43(3):813-820.
77. O'steen W.K., Donnelly J.E. Chronologic analysis of variations in retinal damage in two strains of rats after short-term illumination. Invest Ophthalmol Vis Sci 1982, 22(2):252.
78. LaVail M.M., Gorrin G.M., Repaci M.A., Thomas L.A., Ginsberg H.M. Genetic regulation of light damage to photoreceptors. Invest Ophthalmol Vis Sci 1987, 28(7):1043-1048.
79. Wenzel A., Reme C.E., Williams T.P., Hafezi F., Grimm C. The rpe65 leu450met variation increases retinal resistance against light-induced degeneration by slowing rhodopsin regeneration. J Neurosci 2001, 21(1):53-58.
80. Grimm C., Wenzel A., Hafezi F., Yu S., Redmond T.M., Reme C.E. Protection of rpe65-deficient mice identifies rhodopsin as a mediator of light-induced retinal degeneration. Nat Genet 2000, 25(1):63-66.
81. Penn J.S., Tolman B.L., Thum L.A., Koutz C.A. Effect of light history on the rat retina: timecourse of morphological adaptation and readaptation. Neurochem Res 1992, 17(1):91-99.
82. Remé C.E., Malnoë A., Jung H.H., Wei Q., Munz K. Effect of dietary fish oil on acute light-induced photoreceptor damage in the rat retina. Invest Ophthalmol Vis Sci 1994, 35(1):78-90.