Beneficial effects of blueberries in experimental autoimmune encephalomyelitis

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 23, 2012, Pages 5743-5748

  Xin, Junping ^a,b   Feinstein, Douglas L ^c   Hejna, Matthew J ^a,b   Lorens, Stanley A ^b   McGuire, Susan O ^a,c  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b LOYOLA UNIVERSITY CHICAGO   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

blueberry; dietary supplementation; EAE; experimental autoimmune encephalomyelitis; MOG; mouse; myelin; PLP; Vaccinium ashei

Indexed keywords

BLUEBERRY; DIETARY SUPPLEMENTATION; EAE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; MOG; MOUSE; MYELIN; PLP; VACCINIUM ASHEI;

NEURODEGENERATIVE DISEASES;

MAMMALS;

ANIMAL; ARTICLE; BLUEBERRY; C57BL MOUSE; DISEASE MODEL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FOOD HANDLING; FREEZE DRYING; FRUIT; METABOLISM; METHODOLOGY; MOUSE; MYELIN SHEATH; PATHOLOGY; SPINAL CORD;

ANIMALS; BLUEBERRY PLANT; DISEASE MODELS, ANIMAL; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FOOD HANDLING; FREEZE DRYING; FRUIT; MICE; MICE, INBRED C57BL; MYELIN SHEATH; SPINAL CORD;

ANIMALIA; MUS; VACCINIUM; VACCINIUM VIRGATUM;

EID: 84862189427     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf203611t     Document Type: Article

References (47)

1. Baxter, A. G. The origin and application of experimental autoimmune encephalomyelitis Nat. Rev. Immunol. 2007, 7, 904-912
2. Dittel, B. N. CD4 T cells: balancing the coming and going of autoimmune-mediated inflammation in the CNS Brain, Behav. Immun. 2008, 22, 421-430
3. Friese, M. A.; Montalban, X.; Willcox, N.; Bell, J. I.; Martin, R.; Fugger, L. The value of animal models for drug development in multiple sclerosis Brain 2006, 129, 1940-1952
4. Gold, R.; Linington, C.; Lassmann, H. Understanding pathogenesis and therapy of MS via animal models: 70 years of merits and culprits in EAE research Brain 2006, 129, 1953-1971
5. Miller, S. D.; Karpus, W. J.; Davidson, T. S. Experimental autoimmune encephalomyelitis in the mouse. In Current Protocols in Immunology; Coligan, J. E.; Bierer, B. E.; Marguilies, D. J.; Shevach, E. M.; Strober, W., Eds.; Wiley Interscience: Somerset, NJ, 2010; Unit 15.1.
6. Racke, M. K. Experimental autoimmune encephalomyelitis (EAE). Curr. Protoc. Neurosci. 2001, unit 9.7-9.7.11.
7. Miyake, M.; Sasaki, K.; Ide, K.; Matsukura, Y.; Shijima, K.; Fujiwara, D. Highly oligomeric procyanidins ameliorate experimental autoimmune encephalomyelitis via suppression of Th1 immunity J. Immunol. 2006, 176, 5797-5804
8. Hendriks, J. J. A.; Alblas, J.; van der Pol, S. M.; van Tol, E. A.; Dijkstra, C. D.; de Vries, H. E. Flavonoids influence monocytic GTPase activity and are protective in experimental allergic encephalitis J. Exp. Med. 2004, 200, 1667-1672
9. Imler, T. J.; Petro, T. M. Decreased severity of EAE during resveratrol administration is associated with increased IL17+IL10+ T cells, CD4-INFg+ cells, and decreased macrophage IL6 expression Int. Immunopharm. 2009, 9, 134-143
10. Muthian, G.; Bright, J. J. Quercetin, a flavonoid phytoestrogen, ameliorates EAE by blocking IL12 signaling through JAK-STAT pathway in T lymphocytes J. Clin. Immunol. 2004, 24, 542-552
11. Natarajan, C.; Bright, J. J. Curcumin inhibits experimental allergic encephalomyelitis by blocking IL12 signaling through Janus Kinse-STAT patheway in T lymphocytes J. Immunol. 2002, 169, 6506-6513
12. Aktas, O.; Prozorovski, T.; Smorodchenko, A.; Savaskan, N. E.; Lauster, R.; Kloetzel, P. M.; Infante-Duarte, C.; Brocke, S.; Zipp, F. Green tea epigallocatechine-3-gallate mediates T cellular NFκB inhibition and exerts neuroprotection in autoimmune encephalomyelitis J. Immunol. 2004, 173, 5794-5800
13. Verbeek, R; van Tol, E. A.; van Noort, J. M. Oral flavonoids delay recovery from EAE in SJL mice Biochem. Pharmacol. 2005, 70, 220-228
14. Galli, R. L.; Shukitt-Hale, B.; Youdim, K. A.; Joseph, J. A. Fruit polyphenolic and brain aging Ann. N.Y. Acad. Sci. 2002, 959, 128-132
15. Gemma, C.; Mesches, M. J.; Sepesi, B.; Choo, K.; Holmes, D. B.; Bickford, P. C. Diets enriched in foods with high antioxidant activity reverse age-induced decreases in cerebellar beta-adrenergic function and increases in proinflammatory cytokines J. Neurosci. 2002, 22, 6114-6120
16. Joseph, J. A.; Shukitt-Hale, B.; Denisova, N. A.; Bielinski, D.; Martin, A.; McEwen, J. J.; Bickford, P. C. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation J. Neurosci. 1999, 19, 8114-8121
17. Joseph, J. A.; Shukitt-Hale, B.; Casadesus, G. Reversing the deleterious effects of aging on neuronal communication and behavior: beneficial properties of fruit polyphenolic compounds Am. J. Clin. Nutr. 2005a, 81, 313S-316S
18. Joseph, J. A.; Shukitt-Hale, B.; Casadesus, G.; Fisher, D. Oxidative stress and inflammation in brain aging: nutritional considerations Neurochem. Res. 2005b, 30, 927-935
19. Joseph, J. A.; Shukitt-Hale, B.; Willis, L. M. Grape juice, berries, and walnuts affect brain aging and behavior J. Nutr. 2009, 139, 1813S-1817S
20. Spencer, J. P. E. Beyond antioxidants: the cellular and molecular interactions of flavonoids and how these underpin their actions on the brain Proc. Nutr. Soc. 2010, 69, 244-260
21. McGuire, S. O.; Sortwell, C. E.; Shukitt-Hale, B.; Joseph, J. A.; Hejna, M. J.; Collier, T. J. Dietary supplementation with blueberry extract improves survival of transplanted dopamine neurons Nutr. Neurosci. 2006, 9, 251-258
22. Ahmet, I.; Spangler, E.; Shukitt-Hale, B.; Juhaszova, M.; Sollott, S. J.; Joseph, J. A.; Ingram, D. K.; Talan, M. Blueberry-enriched diet protects rat heart from ischemic damage PLoS One 2009, 4 (6) e5954
23. 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, 427-431
24. Wang, Y.; Chang, C. F.; Chou, J.; Chen, H. L.; Deng, X.; Harvey, B. K.; Cadet, J. L.; Bickford, P. C. Dietary supplementation with blueberries, spinach, or spirulina reduces ischemic brain damage Exp. Neurol. 2005, 193, 75-84
25. Bickford, P. C.; Gould, T.; Breiderick, L.; Chadman, K.; Pollock, A.; Young, D.; Shukitt-Hale, B.; Joseph, J. A. Antioxidant-rich diets improve cerebellar physiology and motor learning in aged rats Brain Res. 2000, 866, 211-217
26. Cao, G.; Shukitt-Hale, B.; Bickford, P. D.; Joseph, J. A.; McEwen, J.; Prior, R. L. Hyperoxia-induced changes in antioxidant capacity and the effect of dietary antioxidants J. Appl. Physiology 1999, 86, 1817-1822
27. Goyarzu, P.; Halin, D. H.; Lau, F. C.; Taglialatela, G.; Moon, W. D.; Jennings, R.; Moy, E.; Lippold, S.; Shukitt-Hale, B.; Joseph, J. A. Blueberry supplemented diet: effects on object recognition memory and nuclear factor-κB levels in aged rats Nutr. Neurosci. 2004, 7, 75-83
28. Nijveldt, T. J.; van Nood, E.; van Hoorn, D. E.; Boelens, P. G.; van Norren, K.; van Leeuwen, P. A. M. Flavonoids: a review of probable mechanisms of action and potential applications Am. J. Clin. Nutr. 2001, 74, 418-425
29. Youdim, K. A.; Shukitt-Hale, B.; Martin, A.; Wang, H.; Denisova, N.; Bickford, P. C.; Joseph, J. A. Short-term dietary supplementation of blueberry polyphenolics: beneficial effects on aging brain performance and peripheral tissue function Nutr. Neurosci. 2000, 3, 383-397
30. Youdim, K. A.; McDonald, J.; Kalt, W.; Joseph, J. A. Potential role of dietary flavonoids in reducing microvascular endothelium vulnerability to oxidative and inflammatory insults J. Nutr. Biochem. 2002, 13, 282-288
31. Williams, R. J.; Spencer, J. P. E.; Rice-Evans, C. Flavonoids: antioxidants or signaling molecules Free Radical Biol. Med. 2004, 36, 838-849
32. 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, 675-683
33. Calder, P. C.; Kew, S. The immune system: a target for functional foods? Br. J. Nutr. 2002, 88, S165-S176
34. Cartford, M. C.; Gemma, C; Bickford, P. C. Eighteen-month-old F344 rats fed a spinach-enriched diet show improved delay classical eyeblink conditioning and reduced expression of TNFα and TNFβ in the cerebellum J. Neurosci. 2002, 22, 5813-5816
35. Lau, F. C.; Bielinski, D. F.; Joseph, J. A. Inhibitory effects of blueberry extract on the production of inflammatory mediators in lipopolysaccharide-activated BV2 microglia J. Neurosci. Res. 2007, 85, 1010-1017
36. Lau, F.; Joseph, J. A.; Mcdonald, J. E.; Kalt, W. Attenuation of iNOS and COX2 by blueberry polyphenols is mediated through the suppression of NF-κB activation J. Funct. Foods 2009, 1, 274-283
37. Willis, L. M.; Freeman, L.; Bickford, P. C.; Quintero, E. M.; Umphlet, C. D.; Moore, A. B.; Goetzl, L.; Granholm, A. C. Blueberry supplementation attenuates microglial activation in hippocampal intraocular grafts to aged host Glia 2010, 58, 679-690
38. Polak, P. E.; Kalinin, S.; Feinstein, D. L. Locus coeruleus damage and noradrenaline reductions in multiple sclerosis and experimental autoimmune encephalomyelitis Brain 2011, 134, 665-677
39. Simonini, M. V.; Polak, P. E.; Boullerne, A. I.; Peters, J. M.; Richardson, J. C.; Feinstein, D. L. Regulation of oligodendrocyte progenitor cell maturation by PPARδ: effects on bone morphogenetic proteins ASN NEURO 2010, 2, e00025-e00033
40. McGuire, S. O.; Ling, Z. D.; Lipton, J. W.; Sortwell, C. E.; Collier, T. J.; Carvey, P. M. Tumor necrosis factor alpha is toxic to embryonic dopamine neurons Exp. Neurol. 2001, 169, 219-230
41. Clarke, D. J.; Branton, R. L. A role for tumor necrosis factor α in death of dopaminergic neurons following neuronal transplantation Exp. Neurol. 2002, 176, 154-162
42. Shukitt-Hale, B.; Lau, F. C.; Carey, A. N.; Galli, R. L.; Spangler, E. L.; Ingram, D. K.; Joseph, J. A. Blueberry polyphenols attenuate kainic acid-induced decrements in cognition and alter inflammatory gene expression in rat hippocampus Nutr. Neurosci. 2008, 11, 172-182
43. Wang, Y. J.; Zheng, Y. L.; Lu, J.; Chen, G. Q.; Wang, X. H.; Feng, J.; Ruan, J.; Sun, X.; Li, C. X.; Sun, Q. J. Purple sweet potato color suppresses lipopolysaccharide-induced acute inflammatory response in mouse brain Neurochem. Int. 2010, 56, 424-430
44. Lee, H.; Kim, Y. O.; Kim, H.; Kim, S. Y.; Noh, H. S.; Kang, S. S.; Cho, G. J.; Choi, W. S.; Suk, K. Flavonoid wogonin from medicinal herb is neuroprotective by inhibiting inflammatory activation of microglia FASEB J. 2003, 17, 1973-1944
45. Williams, C. M.; El Mohsen, M. A.; Vauzour, D.; Rendeiro, C.; Butler, L. T.; Ellis, J. A.; Whiteman, M.; Spencer, J. P. Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels Free Radical Biol. Med. 2008, 45, 295-305
46. Ruggieri, M.; Avolio, C.; Livrea, P.; Trojano, M. Glatiramer acetate in multiple sclerosis: a review CNS Drug Rev. 2007, 13, 178-191
47. Wekerle, H. Lessons from MS: models, concepts, observations Ann. Rheum. Dis. 2008, 67, 56-60