Microglia and Alzheimer's disease

Current Opinion in Hematology

Volumn 6, Issue 1, 1999, Pages 15-24

  Kalaria, Rajesh N ^a  

^a NEWCASTLE GENERAL HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; CYTOKINE; NITROGEN DERIVATIVE; REACTIVE OXYGEN METABOLITE;

ALZHEIMER DISEASE; ANTIGEN PRESENTING CELL; HISTIOCYTE; HUMAN; LEUKOCYTE; MACROPHAGE; MICROGLIA; PHAGOCYTE; PRIORITY JOURNAL; REVIEW;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; ANTIBODY FORMATION; ANTIGEN-PRESENTING CELLS; CELL DIFFERENTIATION; CYTOKINES; HUMANS; MICROGLIA;

EID: 0032904130     PISSN: 10656251     EISSN: None     Source Type: Journal    
DOI: 10.1097/00062752-199901000-00004     Document Type: Review

References (105)

1. 1 McGeer PL, McGeer EG: The inflammatory reponse system of brain: implications for therapy of Alzheimer's and other neurodegenerative diseases. Brain Res Brain Res Rev 1995, 21:195-218.
2. 2 Eikelenboom P, Veerhuis R: The role of complement and activated microglia in the pathogenesis of Alzheimer's disease. Neurobiol Aging 1996, 17:673-680.
3. 3 Rogers J, Webster S, Lue LF, Brachova L, Civin WH, Emmerling M, et al.: Inflammation and Alzheimer's disease pathogenesis. Neurobiol Aging 1996, 17:681-686.
4. 4 Kalaria RN: The immunopathology of Alzheimer's disease. Brain Pathol 1993, 3:333-347.
5. 5 del Rio Hortega P: Microglia. In Cytology and Cellular Pathology of the Nervous System. Edited by Penfield W. New York: Hoeber; 1932:481-534.
6. 6 Barron KD: The microglial cell: a historical review. J Neural Sci 1995, 134(suppl):57-68.
7. 7 Streit WJ, Kincaid-Colton CA: The brain's immune system. Sci Am 1995, 273:38-43.
8. 8 Kruetzberg GW: Microglia: a sensor for pathological events in the CNS. Trends Neurosci 1996, 19:312-318.
9. 9 McRae A, Dahlstrom A, Ling EA: Microglia in neurodegenerative disorders: emphasis on Alzheimer's disease. Gerontology 1997, 43:95-108.
10. 10 Lassman H, Schmied M, Vass K, Mickey WF: Bone marrow derived elements and resident microglia in brain inflammation. Glia 1993, 7:19-24.
11. 11 Morshead CM, Kooy D van der: Separate blood and brain origins of proliferating cells during gliosis in adult brains. Brain Res 1990, 535:237-244.
12. 12 Kennedy DW, Abkowitz JL: Kinetics of central nervous system microglial and macrophage engraftment: analysis using a transgenic bone marrow transplantation model. Blood 1997, 90:986-993. This study provides clear evidence that recruitment of circulating macrophages in the quiescent brain are limited to at most 30%, which subsequently reside as perivascular cells. The data show that these microglia derive from bone marrow precursors but turn over at a significantly lower rate than other tissue macrophages.
13. 13 Masliah E, Mallory M, Hansen L, Alford M, Albright T, Terry R, et al.: Immunoreactivity of CD45, a protein phosphotyrosine phosphatase, in Alzheimer's disease. Acta Neuropathol 1991, 83:12-20.
14. 14 Kalaria RN, Cohen DL, Premkumar DR: Cellular aspects of the inflammatory response in Alzheimer's disease. Neurodegeneration 1996, 5:497-503.
15. 15 Sheng JG, Mrak RE, Griffin WS: Neuritic plaque evolution in Alzheimer's disease is accompanied by transition of activated microglia from primed to enlarged to phagocytic forms. Acta Neuropathol 1997, 94:1-5.
16. 16 Sasaki A, Yamaguchi H, Ogawa A, Sugihara S, Nakazato Y: Microglial activation in early stages of amyloid β protein deposition. Acta Neuropathol 1997, 94:316-322.
17. 17 Uchihara T, Kondo H, Akiyama H, Ikeda K: White matter amyloid in Alzheimer's disease brain. Acta Neuropathol 1995, 90:51-56.
18. 18 Tomimoto H, Akiguchi I, Suenaga T, Nishimura M, Wakita H, Nakamura S, Kimura J: Alterations of the blood-brain barrier and glial cells in white-matter lesions in cerebrovascular and Alzheimer's disease patients. Stroke 1996, 27:2069-2074.
19. 19 Groom GN, Junck L, Foster NL, Frey KA, Kuhl DE: PET of peripheral benzodiazepine binding sites in the microgliosis of Alzheimer's disease. J Nucl Med 1995, 36:2207-2210.
20. 20 Sugaya K, Reeves M, McKinney M: Topographic associations between DNA fragmentation and Alzheimer's disease neuropathology in the hippocampus. Neurochem Intl 1997, 31:275-281.
21. 21 Su JH, Deng G, Cotman CW: Bax protein expression is increased in Alzheimer's brain: correlations with DNA damage, Bcl-2 expression, and brain pathology. J Neuropathol Exp Neurol 1997, 56:86-93.
22. 22 Drache B, Diehl GE, Beyreuther K, Perlmutter LS, Konig G: Bcl-xl-specific antibody labels activated microglia associated with Alzheimer's disease and other pathological states. J Neurosci Res 1997, 47:98-108.
23. 23 Griffin WS, Sheng JS, Royston MC, Gentleman SM, McKenzie JE, Graham DI, et al: Glial-neuronal interactions in Alzheimer's disease: the potential role of a "cytokine cycle" in disease progression. Brain Pathol 1998, 8:65-72. This review suggests an elegant mechanism whereby perpetual activation of microglia and neuronal injury are caused by release of cytokines such as IL-1 in the brains of patients with Alzheimer's disease.
24. 24 Mackenzie IR, Hao C, Munoz DG: Role of microglia in senile plaque formation. Neurobiol Aging 1995, 16:797-804.
25. 25 Kalaria RN, Perry G: Amyloid P component and other acute phase proteins in cerebellar Aβ deposits of Alzheimer's disease. Brain Res 1993, 631:151-155.
26. 26 Roe MT, Dawson DV, Hulette CM, Einstein G, Grain BJ: Microglia are not exclusively associated with plaque-rich regions of the dentate gyrus in Alzheimer's disease. J Neuropathol Exp Neurol 1996, 55:366-371.
27. 27 Fukumoto H, Asami-Odaka A, Suzuki N, Iwatsubo T: Association of A beta 40-positive senile plaques with microglial cells in the brains of patients with Alzheimer's disease and in non-demented aged individuals. Neurodegeneration 1996, 5:13-17.
28. 28 Mann DM, Iwatsubo T, Fukumoto H, Ihara Y, Odaka A, Suzuki N: Microglial cells and amyloid β protein (A beta) deposition: association with A beta 40-containing plaques. Acta Neuropathol 1995, 90:472-477.
29. 29 Akiyama H, Schwab C, Kondo H, Mori H, Kametani F, Ikeda K, McGeer PL: Granules in glial cells of patients with Alzheimer's disease are immunopositive for C-terminal sequences of beta-amyloid protein. Neurosci Lett 1996, 206:169-172.
30. 30 Uchihara T, Akiyama H, Kondo H, Ikeda K: Activated microglial cells are colocalized with perivascular deposits of amyloid-beta protein in Alzheimer's disease brain. Stroke 1997, 28:1948-1951.
31. 31 Uchihara T, Kondo H, Akiyama H, Ikeda K: Single-laser three-color immuno-labeling of a histological section by laser scanning microscopy: application to senile plaque-related structures in post-mortem human brain tissue. J Histochem Cytochem 43:103-106.
32. 32 Miller JD, Cummings J, Maresh GA, Walker DG, Castillo GM, Ngo C, et al.: Localization of perlecan (or a perlecan-related macromolecule) to isolated microglia in vitro and to microglia/macrophages following infusion of beta-amyloid protein into rodent hippocampus. Glia 1997, 21:228-243.
33. 33 Wisniewski HM, Wegiel J, Kotula L: Some neuropathological aspects of Alzheimer's disease and its relevance to other disciplines. Neuropathol Appl Neurobiol 1996, 22:3-11.
34. 34 Bauer J, Konig G, Stauss S, Jonas U, Ganter U, Weidsmann A, et al.: In-vitro matured human macrophages express Alzheimer's beta A4-amyloid precursor protein indicating synthesis in microglial cells. FEBS Lett 1991, 282:335-340.
35. 35 Haass C, Hung AY, Selkoe DJ: Processing of beta-amyloid precursor protein in microglia and astrocytes favors an internal localization over constitutive secretion. J Neurosci 1992, 11:3783-3793.
36. 36 Frackowiak J, Wisniewski HM, Wegiel J, Merz GS, Iqbal K, Wang K-C: Ultrastructure of the microglia that phagocytose amyloid and microglia that produce β-amyloid fibrils. Acta Neuropathol 1992, 84:225-233.
37. 37 LeBlanc AC, Xue R, Gambetti PG: Amyloid precursor protein metabolism in primary cell cultures of neurons, astrocytes and microglia. J Neurochem 1996, 66:2300-2310.
38. 38 Monning U, Sandbrink R, Weidemann A, Banati RB, Masters CL, Beyreuther K: Extracellular matrix influences the biogenesis of amyloid precursor protein in microglial cells. J Biol Chem 1995, 270:7104-7110.
39. 39 Banati RB, Gehrmann J, Lannes-Vieira J, Wekerle H, Kreutzberg GW: Inflammatory reaction in experimental autoimmune encephalomyelitis (EAE) is accompanied by a microglial expression of the beta A4-amyloid precursor protein (APP). Glia 1995, 14:209-215.
40. 40 Bitting L, Naidu A, Cordell B, Murphy GM Jr: Beta-amyloid peptide secretion by a microglial cell line is induced by beta-amyloid-(25-35) and lipopolysaccharide. J Biol Chem 1996, 271:16084-16089.
41. 41 LeBlanc AC, Papadopoulos M, Belair C, Chu W, Crosato M, Powell J, Goodyer CG: Processing of amyloid precursor protein in human primary neuron and astrocyte cultures. J Neurochem 1997, 68:1183-1190. This study provides the first evidence of its kind to show that human microglial cells produce small carboxyl terminal fragments of the amyloid β precursor protein rather than Aβ.
42. 42 Scott SA, Johnson SA, Zarow C, Perlmutter LS: Inability to detect β-amyloid protein precursor mRNA in Alzheimer's plaque-associated microglia. Exp Neurol 1992, 121:113-118.
43. 43 Lue LF, Brachova L, Walker DG, Rogers J: Characterization of glial cultures from rapid autopsies of Alzheimer's and control patients. Neurobiol Aging 1996, 17:421-419.
44. 44 Ard MD, Cole GM, Wei J, Mehrle AP, Fratkin JD: Scavenging of Alzheimer's amyloid β-protein by microglia in culture. J Neurosci Res 1996, 43:190-202.
45. 45 Shaffer LM, Dority MD, Gupta-Bansal R, Frederickson RC, Younkin SG, Brunden KR: Amyloid β protein (Aβ) removal by neuroglial cells in culture. Neurobiol Aging 1995, 16:737-745.
46. 46 Paresce DM, Chung H, Maxfield FR: Slow degradation of aggregates of the Alzheimer's disease amyloid β-protein by microglial cells. J Biol Chem 1997, 272:29390-29397. This paper shows that microglia can degrade limited amounts of Aβ. The authors imply that in Alzheimer's disease, degrading mechanisms within microglia are overwhelmed by the increased Aβ.
47. 47 Giulian D, Haverkamp LJ, Li J, Karshin WL, Yu J, Tom D, et al.: Senile plaques stimulate microglia to release a neurotoxin found in Alzheimer's brain. Neurochem Int 1995, 27:119-137.
48. 48 Giulian D, Haverkamp LJ, Yu JH, Karshin W, Tom D, Li J, et al.: Specific domains of beta-amyloid from Alzheimer's plaque elicit neuron killing in human microglia. J Neurosci 1996, 16:6021-6037.
49. 49 Roher AE, Chaney MO, Kuo YM, Webster SD, Stine WB, Haverkamp LJ, et al.: Morphology and toxicity of Abeta-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease. J Biol Chem 1996, 271:20630-20635.
50. 50 Qiu WQ, Ye Z, Kholodenko D, Seubert P, Selkoe DJ: Degradation of amyloid β-protein by a metalloprotease secreted by microglia and other neural and non-neural cells. J Biol Chem 272:6641-6646.
51. 51 Gottschall PE, Deb S: Regulation of matrix metalloproteinase expressions in astrocytes, microglia and neurons. Neuroimmunomodulation 1996, 3:69-75.
52. 52 Gottschall PE: beta-Amyloid induction of gelatinase B secretion in cultured microglia: inhibition by dexamethasone and indomethacin. Neuroreport 1996, 7:3077-3080.
53. 53 Yamada T, Yoshiyama Y, Sato H, Seiki M, Shinagawa A, Takahashi M: White matter microglia produce membrane-type matrix metalloprotease, an activator of gelatinase A, in human brain tissues. Acta Neuropathol 1995, 90:421-424.
54. 54 Rozovsky I, Finch CE, Morgan TE: Age-related activation of microglia and astrocytes: in vitro studies show persistent phenotypes of aging, increased proliferation, and resistance to downregulation. Neurobiol Aging 1998, 19:97-103.
55. 55 Van Dyke K: The possible role of peroxynitrite in Alzheimer's disease: a simple hypothesis that could be tested more thoroughly. Med Hypotheses 1997, 48:375-380.
56. 56 Hensley K, Hall N, Subramaniam R, Cole P, Harris M, Aksenov M, et al.: Brain regional correspondence between Alzheimer's disease histopathology and biomarkers of protein oxidation. J Neurochem 1995, 65:2146-2156.
57. 57 Klegeris A, Walker DG, McGeer PL: Activation of macrophages by Alzheimer's β amyloid peptide. Biochem Biophys Res Commun 1994, 199:984-991.
58. 58 Weldon DT, Maggio JE, Mantyh PW: New insights into the neuropathology and cell biology of Alzheimer's disease. Geriatrics 1997, 52(suppl 2):S13-16.
59. 59 Vodovotz Y, Lucia MS, Flanders KC, Chesler L, Xie QW, Smith TW, et al.: Inducible nitric oxide synthase in tangle-bearing neurons of patients with Alzheimer's disease. J Exp Med 1996, 184:1425-1433.
60. 60 Vitek MP, Snell J, Dawson H, Colton CA: Modulation of nitric oxide production in human macrophages by apolipoprotein-E and amyloid-beta peptide. Biochem Biophys Res Commun 1997, 240:391-394.
61. 61 Ii M, Sunamoto M, Ohnishi K, Ichimori Y: beta-Amyloid protein-dependent nitric oxide production from microglial cells and neurotoxicity. Brain Res 1996, 720:93-100.
62. 62 Van Muiswinkel FL, Veerhuis R, Eikelenboom P: Amyloid β protein primes cultured rat microglial cells for an enhanced phorbol 12-myristate 13-acetate-induced respiratory burst activity. J Neurochem 1996, 66:2468-2476.
63. 63 McMillian M, Kong LY, Sawin SM, Wilson B, Das K, Hudson P, et al.: Selective killing of cholinergic neurons by microglial activation in basal fore-brain mixed neuronal/glial cultures. Biochem Biophys Res Commun 1995, 215:572-577.
64. 64 Goodwin JL, Uemura E, Cunnick JE: Microglial release of nitric oxide by the synergistic action of beta-amyloid and IFN-gamma. Brain Res 1995, 692:207-214.
65. 65 Meda L, Cassatella MA, Szendrei GI, Otvos L Jr, Baron P, Villalba M, et al.: Activation of microglial cells by beta-amyloid protein and interferon gamma. Nature 1995, 374:647-650.
66. 66 Goodwin JL, Kehrli ME Jr, Uemura E: Integrin Mac-1 and beta-amyloid in microglial release of nitric oxide. Brain Res 1997, 768:279-286.
67. 67 Barger SW, Harmon AD: Microglial activation by Alzheimer's amyloid precursor protein and modulation by apolipoprotein E. Nature 1997, 388:878-881.
68. 68 Paresce DM, Ghosh RN, Maxfield FR: Microglial cells internalize aggregates of the Alzheimer's disease amyloid β-protein via a scavenger receptor. Neuron 1996, 17:553-665.
69. 69 El Khoury J, Hickman SE, Thomas CA, Cao L, Silverstein SC, Loike JD: Scavenger receptor-mediated adhesion of microglia to beta-amyloid fibrils. Nature 1996, 382:716-719.
70. 70 Yan SD, Chen X, Fu J, Chen M, Zhu H, Roher A, et al.: RAGE and amyloid-beta peptide neurotoxicity in Alzheimer's disease. Nature 1996, 382:685-691.
71. 71 Christie RH, Freeman M, Hyman BT: Expression of the macrophage scavenger receptor, a multifunctional lipoprotein receptor, in microglia associated with senile plaques in Alzheimer's disease. Am J Pathol 1996, 148:399-403.
72. 72 McDonald DR, Brunden KR, Landreth GE: Amyloid fibrils activate tyrosine kinase-dependent singaling and supoeroxide production in microglia. J Neurosci 1997, 17:2284-2294. This study was the first to suggest that phosphorylation by tyrosine kinases is a key step in the action fo fibrillar Aβ on human microglial equivalents, the THP-1 macrophages.
73. 73 McDonald DR, Bamberger ME, Combs CK, Landreth GE: β-Amyloid fibrils activate parallel mitogen-activated protein kinase pathways in microglia and THP1 monocytes. J Neurosci 1998, 18:4451-4460. This paper provides evidence for the involvement of mitogen-activated protein kinases and related downstream effects upon microglial activation by fibrillar Aβ.
74. 74 Bonaiuto C, McDonald PP, Rossi F, Cassatella MA: Activation of nuclear factor-kappa B by beta-amyloid peptides and interferon gamma in murine microglia. J Neuroimmunol 1997, 77:51-56. This study shows that Aβ peptides can activate nuclear factor κ B in microglia. Nuclear factor κ B activation might constitute one of the mechanisms underlying the inducible expression of κ B-dependent genes and altering nuclear expression in microglia.
75. 75 Mattson MP, Barger SW, Furukawa K, Bruce AJ, Wyss-Coray T, Mark RJ, Mucke L: Cellular signaling roles of TGF beta, TNF alpha and beta APP in brain injury responses and Alzheimer's disease. Brain Res Brain Res Rev 1997, 23:47-61.
76. 76 Forloni G, Mangiarotti F, Angeretti N, Lucca E, De Simoni MG: Beta-amyloid fragment potentiates IL-6 and TNF-alpha secretion by LPS in astrocytes but not in microglia. Cytokine 1997, 9:759-762.
77. 77 Klegeris A, Walker DG, McGeer PL: Interaction of Alzheimer's beta-amyloid peptide with the human monocytic cell line THP-1 results in a protein kinase C-dependent secretion of tumor necrosis factor-alpha. Brain Res 1997, 747:114-121.
78. 78 Lorton D: beta-Amyloid-induced IL-1 beta release from an activated human monocyte cell line is calcium-and G-protein-dependent. Mech Ageing Develop 1997, 94:199-211.
79. 79 Lorton D, Kocsis JM, King L, Madden K, Brunden KR: beta-Amyloid induces increased release of interleukin-1 beta from lipopolysaccharide-activated human monocytes. J Neuroimmunol 1996, 67:21-29.
80. 80 Bell MD, Taub DD, Perry VH: Overriding the brain's intrinsic resistance to leukocyte recruitment with intraparenchymal injections of recombinant chemokines. Neurosci 1996, 74:283-292.
81. 81 Peress NS, Perillo E: Differential expression of TGF-beta 1, 2 and 3 isotypes in Alzheimer's disease: a comparative immunohistochemical study with cerebral infarction, aged human and mouse control brains. J Neuropathol Exp Neurol 1995, 54:802-811.
82. 82 Ferrer I, Alcantara S, Ballabriga J, Olive M, Blanco R, Rivera R, et al.: Transforming growth factor-alpha (TGF-alpha) and epidermal growth factor-receptor (EGF-R) immunoreactivity in normal and pathologic brain. Prog Neurobiol 1996, 49:99-123.
83. 83 Yamada T, Yamanaka I: Microglial localization of alpha-interferon receptor in human brain tissues. Neurosci Lett 1995, 189:73-76.
84. 84 Meda L, Bernasconi S, Bonaiuto C, Sozzani S, Zhou D, Otvos L Jr, et al.: Beta-amyloid (25-35) peptide and IFN-gamma synergistically induce the production of the chemotactic cytokine MCP-1/JE in monocytes and microglial cells. J Immunol 1996, 157:1213-1218.
85. 85 Ishizuka K, Kimura T, Igata-yi R, Katsuragi S, Takamatsu J, Miyakawa T: Identification of monocyte chemoattractant protein-1 in senile plaques and reactive microglia of Alzheimer's disease. Psychiatry Clin Neurosci 1997, 51:135-138.
86. 86 Stone DJ, Rozovsky I, Morgan TE, Anderson CP, Hajian H, Finch CE: Astrocytes and microglia respond to estrogen with increased apoE mRNA in vivo and in vitro. Exp Neurol 1997, 143:313-318.
87. 87 Uchihara T, Duyckaerts C, He Y, Kobayashi K, Seilhean D, Amouyel P, Hauw JJ: ApoE immunoreactivity and microglial celts in Alzheimer's disease brain. Neurosci Lett 1995, 195:5-8.
88. 88 Christie RH, Chung H, Rebeck GW, Strickland D, Hyman BT: Expression of the very low-density lipoprotein receptor (VLDL-r), an apolipoprotein-E receptor, in the central nervous system and in Alzheimer's disease. J Neuropathol Exp Neurol 1996, 55:491-498.
89. 89 Hollister RD, Kisiel W, Hyman BT: Immunohistochemical localization of tissue factor pathway inhibitor-1 (TFPI-1), a Kunitz proteinase inhibitor, in Alzheimer's disease. Brain Res 1996, 728:13-19.
90. 90 Akiyama H, Kondo H, Ikeda K, Arai T, Kato M, McGleer PL: Immunohistochemical detection of coagulation factor XIIIa in postmortem human brain tissue. Neurosci Lett 1996, 202:29-32.
91. 91 Tsirka SE, Gualandris A, Amaral DG, Strickland S: Excitotoxin-induced neuronal degeneration and seizure are mediated by tissue plasminogen activator. Nature 1995, 377:340-344.
92. 92 Jefferies WA, Food MR, Gabathuler R, Rothenberger S, Yamada T, Yasuhara O, McGeer PL: Reactive microglia specifically associated with amyloid plaques in Alzheimer's disease brain tissue express melanotransferrin. Brain Res 1996, 712:122-126.
93. 93 Matsuo A, Walker DG, Terai K, McGeer PL: Expression of CD43 in human microglia and its downregulation in Alzheimer's disease. J Neuroimmunol 1996, 71:81-86.
94. 94 Fiebich BL, Biber K, Lieb K, van Calker D, Berger M, Bauer J, Gebicke-Haerter PJ: Cyclooxygenase-2 expression in rat microglia is induced by adenosine A2a-receptors. Glia 1996, 18:152-160.
95. 95 Smith MA, Richey PL, Kalaria RN, Perry G: Elastase is associated with the neurofibrillary pathology of Alzheimer's disease: a putative link between proteoplytic imbalance and oxidative stress. Res Neurol Neurosci 1996, 9:213-217.
96. 96 Oda T, Lehrer-Graiwer J, Finch CE, Pasinetti GM: Complement and β-amyloid (Aβ) neurotoxicity in vitro: a model for Alzheimer's disease. Alzheimer Res 1995, 1:29-34.
97. 97 Korotzer AR, Watt J, Cribbs D, Tenner AJ, Burdick D, Glabe C, Cotman CW: Cultured rat microglia express C1q and receptor for C1q: implications for amyloid effects on microglia. Exp Neurol 1995, 134:214-221.
98. 98 Afagh A, Cummings BJ, Cribbs DH, Cotman CW, Tenner AJ: Localization and cell association of C1q in Alzheimer's disease brain. Exp Neurol 1996, 138:22-32.
99. 99 DeNagel DC, Pierce SK: A case for chaperons in antigen processing. Immunol Today 1991, 13:86-89.
100. 100 De Simone R, Giampaolo A, Giometto B, Gallo P, Levi G, Peschle C, Aloisi F: The costimulatory molecule B7 is expressed on human microglia in culture and in multiple sclerosis acute lesions. J Neuropathol Exp Neurol 1995, 54:175-187.
101. 101 Ford AL, Foulcher E, Lemckert FA, Sedgwick JD: Microglia induce CD4 T lymphocyte final effector function and death. J Exp Med 1996, 184:1737-1745.
102. 102 Mayer B, Funke I, Seed B, Riethmuller G, Weiss E: Expression of the CD6 T lymphocyte differentiation antigen in normal human brain. J Neuroimmunol 1990, 29:193-202.
103. 103 Dhib-Jalbut S, Kufta CV, Flerlage M, Shimojo N, McFarland HF: Adult human glial cells can present target antigens to HLA-restricted cytotoxic T-cells. J Neuroimmunol 1990, 29:203-211.
104. 104 Schubert P, Ogata T, Rudolphi K, Marchini C, McRae A, Ferroni S: Support of homeostatic glial cell signaling: a novel therapeutic approach by propentofylline. Ann N Y Acad Sci 1997, 826:337-347. This review provides an account of the potential beneficial effects of a xanthine derivative, propentofylline, by inhibition of adenosine uptake. These actions suppress the cytotoxic functions of activated microglia and prove useful in treating Alzheimer's disease.
105. 105 Debol SM, Herron MJ, Nelson RD: Anti-inflammatory action of dapsone: inhibition of neutrophil adherence is associated with inhibition of chemoattractant-induced signal transduction. J Leukoc Biol 1997, 62:827-836.