Blueberry supplementation attenuates microglial activation in hippocampal intraocular grafts to aged hosts

GLIA

Volumn 58, Issue 6, 2010, Pages 679-690

  Willis, Lauren M ^a   Freeman, Linnea ^a   Bickford, Paula C ^b,c   Quintero, E Matthew ^a   Umphlet, Claudia D ^a   Moore, Alfred B ^a   Goetzl, Laura ^a   Granholm, Ann Charlotte ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Aging; Blueberry; Glial activation; Hippocampus; Oxidative stress; Transplantation

Indexed keywords

ANTHOCYANIN; CYTOKINE; INTERLEUKIN 6;

AGED; AGING; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTOSIS; BLUEBERRY; BRAIN; CONTROLLED STUDY; CYTOKINE PRODUCTION; DEGENERATIVE DISEASE; DIET SUPPLEMENTATION; FETAL TISSUE TRANSPLANTATION; FETUS; HIPPOCAMPUS; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATION; MICROGLIA; NERVE TRANSPLANTATION; NEUROLOGIC DISEASE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; STROKE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; BLUEBERRY PLANT; BRAIN TISSUE TRANSPLANTATION; DIETARY SUPPLEMENTS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GLIAL FIBRILLARY ACIDIC PROTEIN; GRAFT SURVIVAL; HIPPOCAMPUS; HISTOCOMPATIBILITY ANTIGENS CLASS II; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MICROGLIA; PLANT EXTRACTS; RATS; RATS, INBRED F344;

EID: 77950898188     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.20954     Document Type: Article

References (58)

1. Bagga V, Dunnett SB, Fricker-Gates RA. 2008. Ascorbic acid increases the number of dopamine neurons in vitro and in transplants to the 6-OHDA-lesioned rat brain.Cell Transplant 17:763-773.
2. Bal-Price A, Brown GC. 2001. Inflammatory neurodegeneration mediated by nitric oxide fromactivated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity. JNeurosci 21:6480-6491. (Pubitemid 32781092)
3. Bastian D, Tamburstuen MV, Lyngstadaas SP, Reikeras O. 2008. Systemic and local cytokine kinetics after total hip replacement surgery. Eur Surg Res 41:334-340.
4. Beattie MS. 2004. Inflammation and apoptosis: Linked therapeutic targets in spinal cord injury. Trends Mol Med 10:580-583. (Pubitemid 39573147)
5. Bi XL, Yang JY, Dong YX, Wang JM, Cui YH, Ikeshima T, Zhao YQ, Wu CF. 2005. Resveratrol inhibits nitric oxide and TNF-alpha production by lipopolysaccharide-activatedmicroglia. Int Immunopharmacol 5:185-193. (Pubitemid 39626704)
6. Brundin P, Bjorklund A. 1987. Survival, growth and function of dopaminergic neurons grafted to the brain. Prog Brain Res 71:293-308.
7. Casadesus G, Shukitt-Hale B, Stellwagen HM, Zhu X, Lee HG, Smith MA, Joseph JA. 2004. Modulation of hippocampal plasticity and cognitive behavior by short-term blueberry supplementation in aged rats. Nutr Neurosci 7:309-316. (Pubitemid 40123781)
8. Collier TJ, Sortwell CE, Daley BF. 1999. Diminished viability, growth, and behavioral efficacy of fetal dopamine neuron grafts in aging rats with long-term dopamine depletion: An argument for neurotrophic supplementation. J Neurosci 19:5563-5573.
9. Cotrina ML, Nedergaard M. 2002. Astrocytes in the aging brain. J Neurosci Res 67:1-10.
10. Dong Y, Benveniste EN. 2001. Immune function of astrocytes. Glia 36:180-190.
11. Duan WM, Zhao LR, Westerman M, Lovick D, Furcht LT, McCarthy JB, Low WC. 2000. Enhancement of nigral graft survival in rat brain with the systemic administration of synthetic fibronectin peptide V. Neuroscience 100:521-530.
12. Ekdahl CT, Claasen JH, Bonde S, Kokaia Z, Lindvall O. 2003. Inflammation is detrimental for neurogenesis in adult brain. Proc Natl Acad Sci USA 100:13632-13637. (Pubitemid 37444791)
13. Eriksdotter-Nilsson M, Bjorklund H, Dahl D, Olson L. 1986. Growth and development of intraocular fetal cortex cerebri grafts in rats of different ages. Brain Res 393:75-84. (Pubitemid 16036313)
14. Eriksdotter-Nilsson M, Olson L. 1989. Growth of brain tissue grafts is dependent upon host age. Mech Ageing Dev 49:1-22. (Pubitemid 19173327)
15. Ershler WB. 1993. Interleukin-6: A cytokine for gerontologists. J Am Geriatr Soc 41:176-181.
16. Evans ZP, Ellett JD, Fariss MW, Schnellmann RG, Schmidt MG, Chavin K. 2008. Vitamin E succinate reduces ischemia/reperfusion injury in steatotic livers. Transplant Proc 40:3327-3329.
17. Fassett RG, Healy H, Driver R, Robertson IK, Geraghty DP, Sharman JE, Coombes JS. 2008. Astaxanthin vs. placebo on arterial stiffness, oxidative stress and inflammation in renal transplant patients (Xanthin): a randomised controlled trial.BMC Nephrol 9:17
18. Gerhardt GA, Palmer MR, Granholm AC. 1991. Age-induced changes in single locus coeruleus brain transplants grown in oculo: An in vivo electrochemical study. Neurobiol Aging 12:487-494.
19. Granholm AC, Seiger A. 1981. Thyroid hormone dependency in immature but not mature grafted locus coeruleus neurons. Evidence from intraocular innervation of iris transplants. Med Biol 59:51-57.
20. Granholm A-Ch, Ford KA, Hyde LA, Bimonte HA, Hunter CL, Nelson M, Albeck D, Sanders LA, Mufson EJ, Crnic LS. 2002. Estrogen restores cognition and cholinergic phenotype in an animalmodel of Downs Syndrome. Physiol Behav 77:371-385. (Pubitemid 35373893)
21. Heine VM, Maslam S, Joels M, Lucassen PJ. 2004. Prominent decline of newborn cell proliferation, differentiation, and apoptosis in the aging dentate gyrus, in absence of an age-related hypothalamus-pituitary-adrenal axis activation.Neurobiol Aging 25:361-375.
22. Ideguchi M, Shinoyama M, Gomi M, Hayashi H, Hashimoto N, Takahashi J. 2008. Immune or inflammatory response by the host brain suppresses neuronal differentiation of transplanted ES cell-derived neural precursor cells. J Neurosci Res 86:1936-1943.
23. Johann V, Schiefer J, Sass C, Mey J, Brook G, Kruttgen A, Schlangen C, Bernreuther C, Schachner M, Dihne M, Kosinski CM. 2007. Time of transplantation and cell preparation determine neural stem cell survival in a mousemodel of Huntington's disease. Exp Brain Res 177:458-470. (Pubitemid 46339598)
24. Joseph JA, Arendash G, Gordon M, Diamond D, Shukitt-Hale B, Morgan D. 2003.Blueberry supplementation enhances signaling and prevents behavioral deficits in an Alzheimer disease model. Nutr Neurosci 6:153-162. (Pubitemid 36656693)
25. Joseph JA, Shukitt-Hale B, Denisova NA, Bielinski D, Martin A, McEwen JJ, Bickford PC. 1999. Reversals of age-related declines in neuronal signal transduction, cognitive, and motor behavioral deficits with blueberry, spinach, or strawberry dietary supplementation. J Neurosci 19:8114-8121. (Pubitemid 30225807)
26. Kelly KM, Nadon NL, Morrison JH, Thibault O, Barnes CA, Blalock EM. The neurobiology of aging. Epilepsy Res 2006; 68(Suppl 1):S5-S20.
27. Kempermann G, Neumann H. 2003. Neuroscience. Microglia: The enemy within? Science 302:1689-1690.
28. Kempermann G,Wiskott L, Gage FH. 2004. Functional significance of adult neurogenesis. Curr Opin Neurobiol 14:186-191.
29. Kordower JH, Brundin P. 2009. Lewy body pathology in long-term fetal nigral transplants: Is Parkinson's disease transmitted from one neural systemto another?Neuropsychopharmacology 34:254.
30. Krabbe KS, Pedersen M, Bruunsgaard H. 2004. Inflammatory mediators in the elderly. Exp Gerontol 39:687-699.
31. Kuhn HG, Dickinson-Anson H, Gage FH. 1996. Neurogenesis in the dentate gyrus of the adult rat: Age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027-2033. (Pubitemid 26144015)
32. Lau FC, Bielinski DF, Joseph JA. 2007. Inhibitory effects of blueberry extract on the production of inflammatory mediators in lipopolysaccharide- activated BV2 microglia. J Neurosci Res 85:1010-1017.
33. Lau FC, Shukitt-Hale B, Joseph JA. The beneficial effects of fruit polyphenols on brain aging. Neurobiol Aging 2005;26(Suppl 1):128-132.
34. Li R, Huang YG, Fang D, Le WD. 2004. (-)-Epigallocatechin gallate inhibits lipopolysaccharide-induced microglial activation and protects against inflammation-mediated dopaminergic neuronal injury. J Neurosci Res 78:723-731.
35. Little AR, O'Callagha JP. 2001. Astrogliosis in the adult and developing CNS: Is there a role for proinflammatory cytokines? Neurotoxicology 22:607-618.
36. Lohachoompol V, George S, John C. 2004. The change of total Anthocyanins in blueberries and their antioxidant effect after drying and freezing. J Biomed Biotechnol 2004:248-252. (Pubitemid 40389463)
37. Mazurova Y, Latr I, Osterreicher J, Guncova I. 2006. Progressive reparative gliosis in aged hosts and interferences with neural grafts in an animal model of Huntington's disease. Cell Mol Neurobiol 26:1423-1441. (Pubitemid 44924056)
38. Monje ML, Toda H, Palmer TD. Inflammatory blockade restores adult hippocampal neurogenesis. Science 2003; 302:1760-1765. (Pubitemid 37505739)
39. Nakanishi M, Niidome T, Matsuda S, Akaike A, Kihara T, Sugimoto H. 2007. Microglia-derived interleukin-6 and leukaemia inhibitory factor promote astrocytic differentiation of neural stem/progenitor cells. Eur J Neurosci 25:649-658. (Pubitemid 46271169)
40. Nakashima K, Taga T. 2002. Mechanisms underlying cytokine-mediated cell-fate regulation in the nervous system. Mol Neurobiol 25:233-244. (Pubitemid 34665092)
41. Okano H, Okada S, Nakamura M, Toyama Y. 2005. Neural stem cells and regeneration of injured spinal cord. Kidney Int 68:1927-1931. (Pubitemid 43117763)
42. Olson L, Freedman R, Seiger A,Hoffer B. 1977. Electrophysiology and cytology of hippocampal formation transplants in the anterior chamber of the eye. I. Intrinsic organization. Brain Res 119:87-106.
43. Paxinos G, Watson C. 2007. The rat brain in stereotaxic coordinates. New York: Elsevier.
44. Perry VH, Matyszak MK, Fearn S. 1993. Altered antigen expression of microglia in the aged rodent CNS. Glia 7:60-67.
45. Rohl C, Lucius R, Sievers J. 2007. The effect of activated microglia on astrogliosis parameters in astrocyte cultures. Brain Res 1129:43-52. (Pubitemid 46048779)
46. Sheridan KM, Distasi MR, Witzmann FA, Dalsing MC, Miller SJ, Unthank JL. 2007. Impact of genetic background and aging on mesenteric collateral growth capacity in Fische 344, Brown Norway, and Fisched 344 x Brown Norway hybrid rats. Am J Physiol 293:H3498-H3505.
47. Shukitt-Hale B, Lau FC, Carey AC, Galli RL, Spangler EL, Ingram DK, Joseph JA. 2008. Blueberry polyphenols prevent kainic acid-induced decrements in cognition and alter inflammatory gene expression in rat hippocampus. Nutr Neurosci 11:172-182.
48. Sortwell CE, Camargo MD, Pitzer MR, Gyawali S, Collier TJ. 2001. Diminished survival of mesencephalic dopamine neurons grafted into aged hosts occurs during the immediate postgrafting interval. Exp Neurol 169:23-29. (Pubitemid 32424318)
49. Spaulding CC, Walford RL, Effros RB. 1997. Calorie restriction inhibits the age-related dysregulation of the cytokines TNF-alpha and IL-6 in C3B10RF1 mice. Mech Ageing Dev 93:87-94.
50. Stromberg I, Gemma C, Vila J, Bickford PC. 2005. Blueberry- and spirulinaenriched diets enhance striatal dopamine recovery and induce a rapid, transient microglia activation after injury of the rat nigrostriatal dopamine system. Exp Neurol 196:298-307. (Pubitemid 41607818)
51. Tian DS, Dong Q, Pan DJ,He Y, Yu ZY, Xie MJ, Wang W. 2007. Attenuation of astrogliosis by suppressing of microglial proliferation with the cell cycle inhibitor olomoucine in rat spinal cord injury model. Brain Res 1154:206-214. (Pubitemid 46856341)
52. Tilleux S, Berger J, Hermans E. 2007. Induction of astrogliosis by activated microglia is associated with a down-regulation of metabotropic glutamate receptor 5. JNeuroimmunol 189:23-30. (Pubitemid 47379423)
53. Virgili M, Monti B, Polazzi E, Angiolini G, Contestabile A. 2001. Topography of neurochemical alterations in the CNS of aged rats. Int J Dev Neurosci 19:109-116. (Pubitemid 32156978)
54. Williams CM, El Mohsen MA, Vauzour D, Rendeiro C, Butler LT, Ellis JA, Whiteman M, Spencer JP. 2008. Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Radic Biol Med 45:295-305.
55. Willis L, Bickford P, Zaman V, Moore A, Granholm AC. 2005. Blueberry extract enhances survival of intraocular hippocampal transplants. Cell Transplant 14:213-223. (Pubitemid 40677151)
56. Willis LM, Small BJ, Bickford PC, Umphlet CD, Moore AB, Granholm AC. 2008. Dietary blueberry supplementation affects growth but not vascularization of neural transplants. J Cereb Blood Flow Metab 28:1150-1164.
57. Ye SM, Johnson RW. 1999. Increased interleukin-6 expression by microglia frombrain of agedmice. J Neuroimmunol 93:139-148.
58. Zhang SC, Goetz BD, Duncan ID. Suppression of activated microglia promotes survival and function of transplanted oligodendroglial progenitors. Glia 2003;41:191-198.