Role of microglia in age-related changes to the nervous system

TheScientificWorldJournal

Volumn 9, Issue , 2009, Pages 1061-1071

  Brown, David R ^a  

^a University of Bath   (United Kingdom)

Author keywords

Amyloid; Iron; Microglia; Neurodegeneration; Neuron; Prion

Indexed keywords

NONSTEROID ANTIINFLAMMATORY AGENT;

ALZHEIMER DISEASE; CELL AGING; CELL FUNCTION; CELL LOSS; COGNITIVE DEFECT; DYSTROPHY; HUMAN; MICROGLIA; NERVE CELL NECROSIS; NERVE DEGENERATION; NEUROPROTECTION; NONHUMAN; PRION DISEASE; REVIEW;

AGING; ALZHEIMER DISEASE; ANIMALS; COGNITION DISORDERS; HUMANS; MICROGLIA; NERVE DEGENERATION; NERVOUS SYSTEM; PRION DISEASES; PRPSC PROTEINS;

EID: 77649239863     PISSN: None     EISSN: 1537744X     Source Type: Journal    
DOI: 10.1100/tsw.2009.111     Document Type: Review

References (90)

1. Kreutzberg, G.W. (1996) Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318.
2. Liu, B. and Hong, J.S. (2003) Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304, 1-7.
3. Streit, W.J., Graeber, M.B. and Kreutzberg, G.W. (1988) Functional plasticity of microglia: a review. Glia 1, 301-307.
4. Streit, W.J., Walter, S.A., and Pennell, N.A. (1999) Reactive microgliosis. Prog. Neurobiol. 57, 563-581.
5. Graeber, M.B., Streit, W.J., and Kreutzberg, G.W. (1988). The microglial cytoskeleton: vimentin is localized within activated cells in situ. J. Neurocytol. 17, 573-580.
6. Oehmichen, W. and Gencic, M. (1975). Experimental studies on kinetics and functions of monuclear phagozytes of the central nervous system. Acta Neuropathol. Suppl. 6, 285-290.
7. Colton, C.A. and Gilbert, D.L. (1987) Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett. 223, 284-288.
8. Liu, B., Gao, H.M., Wang, J.Y., Jeohn, G.H., Cooper, C.L. and Hong, J.S. (2002) Role of nitric oxide in inflammation-mediated neurodegeneration. Ann. N. Y. Acad. Sci. 962, 318-331.
9. Moss, D.W. and Bates, T.E. (2001) Activation of murine microglial cell lines by lipopolysaccharide and interferongamma causes NO-mediated decreases in mitochondrial and cellular function. Eur. J. Neurosci. 13, 529-538.
10. Sawada, M., Kondo, N., Suzumura, A., and Marunouchi, T. (1989) Production of tumor necrosis factor-alpha by microglia and astrocytes in culture. Brain Res. 491, 394-397.
11. Lee, S.C., Liu, W., Dickson, D.W., Brosnan, C.F., and Berman, J.W. (1993) Cytokine production by human fetal microglia and astrocytes. Differential induction by lipopolysaccharide and IL-1 beta. J. Immunol. 150, 2659-2667.
12. Meda, L., Cassatella, M.A., Szendrei, G.I., Otvos, L., Jr., Baron, P., Villalba, M., Ferrari, D., and Rossi, F. (1995) Activation of microglial cells by beta-amyloid protein and interferon-gamma. Nature 374, 647-650.
13. Brown, D.R., Schmidt, B., and Kretzschmar, H.A. (1996) Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380, 345-347.
14. Sparkman, N.L. and Johnson, R.W. (2008) Neuroinflammation associated with aging sensitizes the brain to the effects of infection or stress. Neuroimmunomodulation 15, 323-330.
15. Liao, H., Bu, W.Y., Wang, T.H., Ahmed, S., and Xiao, Z.C. (2005) Tenascin-R plays a role in neuroprotection via its distinct domains that coordinate to modulate the microglia function. J. Biol. Chem. 280, 8316-8323.
16. Morgan, S.C., Taylor, D.L., and Pocock, J.M. (2004) Microglia release activators of neuronal proliferation mediated by activation of mitogen-activated protein kinase, phosphatidylinositol-3-kinase/Akt and delta-Notch signalling cascades. J. Neurochem. 90, 89-101.
17. Polazzi, E., Gianni, T., and Contestabile, A. (2001) Microglial cells protect cerebellar granule neurons from apoptosis: evidence for reciprocal signaling. Glia 36, 271-280.
18. McGeer, P.L. and McGeer, E.G. (2008) Glial reactions in Parkinson's disease. Mov. Disord. 23, 474-483.
19. Carnevale, D., De Simone, R., and Minghetti, L. (2007) Microglia-neuron interaction in inflammatory and degenerative diseases: role of cholinergic and noradrenergic systems. CNS Neurol. Disord. Drug Targets 6, 388-397.
20. Dewil, M., Van Den Bosch, L., and Robberecht, W. (2007) Microglia in amyotrophic lateral sclerosis. Acta Neurol. Belg. 107, 63-70.
21. Hill, K.E., Zollinger, L.V., Watt, H.E., Carlson, N.G., and Rose, J.W. (2004) Inducible nitric oxide synthase in chronic active multiple sclerosis plaques: distribution, cellular expression and association with myelin damage. J. Neuroimmunol. 151, 171-179.
22. Rose, J.W., Hill, K.E., Watt, H.E., and Carlson, N.G. (2004) Inflammatory cell expression of cyclooxygenase-2 in the multiple sclerosis lesion. J. Neuroimmunol. 149, 40-49.
23. Schönrock, L.M., Kuhlmann, T., Adler, S., Bitsch, A., and Bruck, W. (1998) Identification of glial cell proliferation in early multiple sclerosis lesions. Neuropathol. Appl. Neurobiol. 24, 320-330.
24. Banati, R.B., Newcombe, J., Gunn, R.N., Cagnin, A., Turkheimer, F., Heppner, F., Price, G., Wegner, F., Giovannoni, G., Miller, D.H., Perkin, G.D., Smith, T., Hewson, A.K., Bydder, G., Kreutzberg, G.W., Jones, T., Cuzner, M.L., and Myers, R. (2000) The peripheral benzodiazepine binding site in the brain in multiple sclerosis: quantitative in vivo imaging of microglia as a measure of disease activity. Brain 123, 2321-2337.
25. Matsumoto, Y., Ohmori, K., and Fujiwara, M. (1992) Microglial and astroglial reactions to inflammatory lesions of experimental autoimmune encephalomyelitis in the rat central nervous system. J. Neuroimmunol. 37, 23-33.
26. Mack, C.L., Vanderlugt-Castaneda, C.L., Neville, K.L., and Miller, S.D. (2003) Microglia are activated to become competent antigen presenting and effector cells in the inflammatory environment of the Theiler's virus model of multiple sclerosis. J. Neuroimmunol. 144, 68-79.
27. Olson, E.E. and McKeon, R.J. (2004) Characterization of cellular and neurological damage following unilateral hypoxia/ischemia. J. Neurol. Sci. 227, 7-19.
28. Morioka, T., Kalehua, A.N., and Streit, W.J. (1993) Characterization of microglial reaction after middle cerebral artery occlusion in rat brain. J. Comp. Neurol. 327, 123-132.
29. Hall, E.D., Oostveen, J.A., and Gurney, M.E. (1998) Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23, 249-256.
30. Tsuda, M., Mizokoshi, A., Shigemoto-Mogami, Y., Koizumi, S., and Inoue, K. (2004) Activation of p38 mitogenactivated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 45, 89-95.
31. Zhang, W., Wang, T., Pei, Z., Miller, D.S., Wu, X., Block, M.L., Wilson, B., Zhang, W., Zhou, Y., Hong, J.S., and Zhang, J. (2005) Aggregated alpha-synuclein activates microglia: a process leading to disease progression in Parkinson's disease. FASEB J. 19, 533-542.
32. Loeffler, D.A., DeMaggio, A.J., Juneau, P.L., Havaich, M.K., and LeWitt, P.A. (1994) Effects of enhanced striatal dopamine turnover in vivo on glutathione oxidation. Clin. Neuropharmacol. 17, 370-379.
33. Kim, W.G., Mohney, R.P., Wilson, B., Jeohn, G.H., Liu, B., and Hong, J.S. (2000) Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 20, 6309-6316.
34. Betarbet, R., Sherer, T.B., MacKenzie, G., Garcia-Osuna, M., Panov, A.V., and Greenamyre, J.T. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3, 1301-1306.
35. Gao, H.M., Hong, J.S., Zhang, W., and Liu, B. (2002) Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 22, 782-790.
36. Thiruchelvam, M., McCormack, A., Richfield, E.K., Baggs, R.B., Tank, A.W., Di Monte, D.A., and Cory-Slechta, D.A. (2003) Age-related irreversible progressive nigrostriatal dopaminergic neurotoxicity in the paraquat and maneb model of the Parkinson's disease phenotype. Eur. J. Neurosci. 18, 589-600.
37. Qin, L., Liu, Y., Wang, T., Wei, S.J., Block, M.L., Wilson, B., Liu, B. and Hong, J.S. (2004) NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J. Biol. Chem. 279, 1415-1421.
38. Wu, X., Block, M.L., Zhang, W., Qin, L., Wilson, B., Zhang, W., Veronesi, B., and Hong, J.S. (2005) The role of microglia in paraquat-induced dopaminergic neurotoxicity. Antioxid. Redox. Signal. 7, 654-661.
39. Prusiner, S.B. (1998) Prions. Proc. Natl. Acad. Sci. U. S. A. 95, 13363-13383.
40. Brown, D.R. (2001) Microglia and prion disease. Microscop. Res. Tech. 54, 71-80.
41. Brown, D.R. (2005) Neurodegeneration and oxidative stress: prion disease results from loss of antioxidant defence. Folia Neuropathol. 43, 229-243.
42. Mühleisen, H., Gehrmann, J., and Meyermann, R. (1995) Reactive microglia in Creutzfeldt-Jakob disease. Neuropathol. Appl. Neurobiol. 21, 505-517.
43. Williams, A.E., Lawson, L.J., Perry, V.H., and Fraser, H. (1994) Characterization of the microglial response in murine scrapie. Neuropathol. Appl. Neurobiol. 20, 47-55.
44. Williams, A., Lucassen, P.J., Ritchie, D., and Bruce, M. (1997) PrP deposition, microglial activation, and neuronal apoptosis in murine scrapie. Exp. Neurol. 144, 433-438.
45. Giese, A., Brown, D.R., Groschup, M.H., Feldmann, C., Haist, I., and Kretzschmar, H.A. (1998) Role of microglia in neuronal cell death in prion disease. Brain Pathol. 8, 449-457.
46. Herms, J.W., Madlung, A., Brown, D.R., and Kretzschmar, H.A. (1997) Increase of intracellular free Ca2+ in microglia activated by prion protein fragment. Glia 21, 253-257.
47. Brown, D.R., Besinger, A., Herms, J.W., and Kretzschmar, H.A. (1998) Microglial expression of the prion protein. Neuroreport 9, 1425-1429.
48. Hafiz, F. and Brown, D.R. (2000) A model for the mechanism of astrogliosis in prion disease. Mol. Cell. Neurosci. 16, 221-232.
49. Peyrin, J.M., Lasmézas, C.I., Haïk, S., Tagliavini, F., Salmona, M., Williams, A., Richie, D., Deslys, J.P., and Dormont, D. (1999) Microglial cells respond to amyloidogenic PrP peptide by the production of inflammatory cytokines. Neuroreport 10, 723-729.
50. Bate, C., Reid, S., and Williams, A. (2001) Killing of prion-damaged neurones by microglia. Neuroreport 12, 2589-2594.
51. Marella, M. and Chabry, J. (2004) Neurons and astrocytes respond to prion infection by inducing microglia recruitment. J. Neurosci. 24, 620-627.
52. Bate, C., Kempster, S., and Williams, A. (2006) Prostaglandin D2 mediates neuronal damage by amyloid-beta or prions which activates microglial cells. Neuropharmacology 50, 229-237.
53. Sassoon, J., Daniels, M., and Brown, D.R. (2004) Astrocytic regulation of NMDA receptor subunit composition modulates the toxicity of prion peptide PrP106-126. Mol. Cell. Neurosci. 25, 181-191.
54. Sawada, M., Sawada, H., and Nagatsu, T. (2008) Effects of aging on neuroprotective and neurotoxic properties of microglia in neurodegenerative diseases. Neurodegener. Dis. 5, 54-56.
55. Sierra, A., Gottfried-Blackmore, A.C., McEwen, B.S., and Bulloch, K. (2007) Microglia derived from aging mice exhibit an altered inflammatory profile. Glia 55, 412-424.
56. Nicholas, R. St. J., Compston, A., and Brown. D.R. (2001) Inhibition of TNFa-induced NF-kB p52 converts the metabolic effects of microglia-derived TNFα on mouse cerebellar neurons to neurotoxicity. J. Neurochem. 76, 1431-1438.
57. Davis, J.B., McMurray, H.F., and Schubert, D. (1992) The amyloid beta-protein of Alzheimer's disease is chemotactic for mononuclear phagocytes. Biochem. Biophys. Res. Commun. 189, 1096-1100.
58. Sasaki, A., Yamaguchi, H., Ogawa, A., Sugihara, S., and Nakazato, Y. (1997). Microglial activation in early stages of amyloid beta protein deposition. Acta Neuropathol. (Berl.) 94, 316-322.
59. Ii, M., Sunamoto, M., Ohnishi, K., and Ichimori, Y. (1996) beta-Amyloid protein-dependent nitric oxide production from microglial cells and neurotoxicity. Brain Res. 720, 93-100.
60. Dheen, S.T., Jun, Y., Yan, Z., Tay, S.S., and Ang Ling, E. (2005) Retinoic acid inhibits expression of TNF-alpha and iNOS in activated rat microglia. Glia 50, 21-31.
61. Qin, L., Liu, Y., Cooper, C., Liu, B., Wilson, B., and Hong, J.S. (2002) Microglia enhance beta-amyloid peptideinduced toxicity in cortical and mesencephalic neurons by producing reactive oxygen species. J. Neurochem. 83, 973-983.
62. Akiyama, H., Barger, S., Barnum, S., Bradt, B., Bauer, J., Cole, G.M., Cooper, N.R., Eikelenboom, P., Emmerling, M., Fiebich, B.L., Finch, C.E., Frautschy, S., Griffin, W.S., Hampel, H., Hull, M., Landreth, G., Lue, L., Mrak, R., Mackenzie, I.R., McGeer, P.L., O'Banion, M.K., Pachter, J., Pasinetti, G., Plata-Salaman, C., Rogers, J., Rydel, R., Shen, Y., Streit, W., Strohmeyer, R., Tooyoma, I., Van Muiswinkel, F.L., Veerhuis, R., Walker, D., Webster, S., Wegrzyniak, B., Wenk, G., and Wyss-Coray, T. (2000) Inflammation and Alzheimer's disease. Neurobiol. Aging 21, 383-421.
63. Giulian, D., Haverkamp, L.J., Yu, J.H., Karshin, W., Tom, D., Li, J., Kirkpatrick, J., Kuo, L.M., and Roher, A.E. (1996) Specific domains of beta-amyloid from Alzheimer plaque elicit neuron killing in human microglia. J. Neurosci. 16, 6021-6037.
64. Bate, C., Veerhuis, R., Eikelenboom, P., and Williams, A. (2004) Microglia kill amyloid-beta1-42 damaged neurons by a CD14-dependent process. Neuroreport 15, 1427-1430.
65. Koenigsknecht, J. and Landreth, G. (2004) Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrindependent mechanism. J. Neurosci. 24, 9838-9846.
66. Bamberger, M.E., Harris, M.E., McDonald, D.R., Husemann, J., and Landreth, G.E. (2003) A cell surface receptor complex for fibrillar beta-amyloid mediates microglial activation. J. Neurosci. 23, 2665-2674.
67. Craft, J.M., Watterson, D.M., Frautschy, S.A., and Van Eldik, L.J. (2004) Aminopyridazines inhibit beta-amyloid-induced glial activation and neuronal damage in vivo. Neurobiol. Aging 25, 1283-1292.
68. Yan, Q., Zhang, J., Liu, H., Babu-Khan, S., Vassar, R., Biere, A.L., Citron, M., and Landreth, G. (2003) Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease. J. Neurosci. 23, 7504-7509.
69. Liu, B., Gao, H.M., and Hong, J.S. (2003) Parkinson's disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ. Health Perspect. 111, 1065-1073.
70. McGeer, P.L. and McGeer, E.G. (1996) Anti-inflammatory drugs in the fight against Alzheimer's disease. Ann. N. Y. Acad. Sci. 777, 213-220.
71. Perry, N.S., Bollen, C., Perry, E.K., and Ballard, C. (2003) Salvia for dementia therapy: review of pharmacological activity and pilot tolerability clinical trial. Pharmacol. Biochem. Behav. 75, 651-659.
72. Szekely, C.A., Thorne, J.E., Zandi, P.P., Ek, M., Messias, E., Breitner, J.C., and Goodman, S.N. (2004) Nonsteroidal anti-inflammatory drugs for the prevention of Alzheimer's disease: a systematic review. Neuroepidemiology 23, 159-169.
73. Mandrekar, S., Jiang, Q., Lee, C.Y., Koenigsknecht-Talboo, J., Holtzman, D.M., and Landreth, G.E. (2009) Microglia mediate the clearance of soluble Abeta through fluid phase macropinocytosis. J. Neurosci. 29, 4252-4262.
74. Rogers, J. and Lue, L.F. (2001) Microglial chemotaxis, activation, and phagocytosis of amyloid beta-peptide as linked phenomena in Alzheimer's disease. Neurochem. Int. 39, 333-340.
75. Floden, A.M. and Combs, C.K. (2006) Beta-amyloid stimulates murine postnatal and adult microglia cultures in a unique manner. J. Neurosci. 26, 4644-4648.
76. Streit, W.J., Sammons, N.W., Kuhns, A.J., and Sparks, D.L. (2004) Dystrophic microglia in the aging human brain. Glia 45, 208-212.
77. Lopes, K.O., Sparks, D., and Streit, W.J. (2008) Microglial dystrophy in the aged and Alzheimer's disease brain is associated with ferritin immunoreactivity. Glia 56, 1048-1060.
78. Tanaka, M., Sotomatsu, A., Yoshida, T., Hirai, S., and Nishida, A. (1994) Detection of superoxide production by activated microglia using a sensitive and specific chemiluminescence assay and microglia-mediated PC12h cell death. J. Neurochem. 63, 266-270.
79. Biemond, P., van Eijk, H.G., Swaak, A.J.G., and Koster, J.F. (1984) Iron mobilization from ferritin by superoxide derived from stimulated polymorphonuclear leukocytes. J. Clin. Invest. 73, 1576-1579.
80. Yoshida, T., Tanaka, M., Sotomatsu, A., and Hirai, S. (1995) Activated microglia cause superoxide-mediated release of iron from ferritin. Neurosci. Lett. 190, 21-24.
81. Agrawal, R., Sharma, P.K., and Rao, G.S. (2001) Release of iron from ferritin by metabolites of benzene and superoxide radical generating agents. Toxicology 168, 223-230.
82. Thomas, C.E., Morehouse, L.A., and Aust, S.D. (1985) Ferritin and superoxide-dependent lipid peroxidation. J. Biol. Chem. 260, 3275-3280.
83. Roskams, A.J. and Connor, J.R. (1994) Iron, transferrin, and ferritin in the rat brain during development and aging. J. Neurochem. 63, 709-716.
84. Brown, D.R. (2003) Prion protein expression modulates neuronal copper content. J. Neurochem. 87, 377-385.
85. Bartzokis, G., Tishler, T.A., Lu, P.H., Villablanca, P., Altshuler, L.L., Carter, M., Huang, D., Edwards, N., and Mintz, J. (2007) Brain ferritin iron may influence age- and gender-related risks of neurodegeneration. Neurobiol. Aging 28, 414-423.
86. Nakanishi, H. and Wu, Z. (2009) Microglia-aging: roles of microglial lysosome- and mitochondria-derived reactive oxygen species in brain aging. Behav. Brain Res. 201, 1-7.
87. Hayashi, Y., Yoshida, M., Yamato, M., Ide, T., Wu, Z., Ochi-Shindou, M., Kanki, T., Kang, D., Sunagawa, K., Tsutsui, H., and Nakanishi, H. (2008) Reverse of age-dependent memory impairment and mitochondrial DNA damage in microglia by an overexpression of human mitochondrial transcription factor a in mice. J. Neurosci. 28, 8624-8634.
88. Lawson, L.J., Perry, V.H., and Gordon, S. (1992) Turnover of resident microglia in the normal adult mouse brain. Neuroscience 48, 405-415.
89. Kanki, T., Ohgaki, K., Gaspari, M., Gustafsson, C.M., Fukuoh, A., Sasaki, N., Hamasaki, N., and Kang, D. (2004) Architectural role of mitochondrial transcription factor A in maintenance of human mitochondrial DNA. Mol. Cell. Biol. 24, 9823-9834.
90. Ikeuchi, M., Matsusaka, H., Kang, D., Matsushima, S., Ide, T., Kubota, T., Sunagawa, K., Kinugawa, S., and Tsutsui, H. (2006) Overexpression of mitochondrial transcription factor A ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation 112, 683-690.