NeuroAIDS: Contributions of the human immunodeficiency virus-1 proteins Tat and gp120 as well as CD40 to microglial activation

Journal of Neuroscience Research

Volumn 81, Issue 3, 2005, Pages 436-446

  D'Aversa, T G ^a,b   Eugenin, E A ^a   Berman, Joan W ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b Division of Natural Sciences   (United States)

Author keywords

Alzheimer's disease; Chemokines; Migration; Multiple sclerosis; Neurotoxicity

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; CHEMOKINE; GLYCOPROTEIN GP 120; TRANSACTIVATOR PROTEIN; VIRUS PROTEIN;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ALZHEIMER DISEASE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CENTRAL NERVOUS SYSTEM; DISEASE COURSE; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; MACROPHAGE; MICROGLIA; MULTIPLE SCLEROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; REVIEW;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANIMALS; ANTIGENS, CD40; CENTRAL NERVOUS SYSTEM; CHEMOKINES; GENE PRODUCTS, TAT; HIV ENVELOPE PROTEIN GP120; HIV-1; HUMANS; MICROGLIA;

EID: 25444487187     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20486     Document Type: Review

References (132)

1. Adams CW, Poston RN, Buk SJ. 1989. Pathology, histochemistry and immunocytochemistry of lesions in acute multiple sclerosis. J Neurol Sci 92:291-306.
2. Aksenov MY, Hasselrot U, Wu G, Nath A, Anderson C, Mactutus CF, Booze RM. 2003. Temporal relationships between HIV-1 Tat-induced neuronal degeneration, OX-42 immunoreactivity, reactive astrocytosis, and protein oxidation in the rat striatum. Brain Res 987:1-9.
3. Albini A, Benelli R, Giunciuglio D, Cai T, Mariani G, Ferrini S, Noonan DM. 1998a. Identification of a novel domain of HIV tat involved in monocyte chemotaxis. J Biol Chem 273:15895-15900.
4. Albini A, Ferrini S, Benelli R, Sforzini S, Giunciuglio D, Aluigi MG, Proudfoot AE, Alouani S, Wells TN, Mariani G, Rabin RL, Farber JM, Noonan DM. 1998b. HIV-1 Tat protein mimicry of chemokines. Proc Natl Acad Sci U S A 95:13153-13158.
5. Albright AV, Shieh JT, Itoh T, Lee B, Pleasure D, O'Connor MJ, Doms RW, Gonzalez-Scarano F. 1999. Microglia express CCR5, CXCR4, and CCR3, but of these, CCR5 is the principal coreceptor for human immunodeficiency virus type 1 dementia isolates. J Virol 73:205-213.
6. Alkhatib G, Combadiere C, Broder CC, Feng Y, Kennedy PE, Murphy PM, Berger EA. 1996. CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272:1955-1958.
7. Armitage RJ, Fanslow WC, Strockbine L, Sato TA, Clifford KN, Macduff BM, Anderson DM, Gimpel SD, Davis-Smith T, Maliszewski CR, Clark EA, Smith CA, Grabstein KH, Cosman D, Spriggs MK. 1992. Molecular and biological characterization of a murine ligand for CD40. Nature 357:80-82.
8. Arya SK, Guo C, Josephs SF, Wong-Staal F. 1985. Trans-activator gene of human T-lymphotropic virus type III (HTLV-III). Science 229:69-73.
9. Asensio VC, Campbell IL. 1999. Chemokines in the CNS: plurifunctional mediators in diverse states. Trends Neurosci 22:504-512.
10. Asensio VC, Maier J, Milner R, Boztug K, Kincaid C, Moulard M, Phillipson C, Lindsley K, Krucker T, Fox HS, Campbell IL. 2001. Interferon-independent, human immunodeficiency virus type 1 gp120-mediated induction of CXCL10/IP-10 gene expression by astrocytes in vivo and in vitro. J Virol 75:7067-7077.
11. Bachis A, Mocchetti I. 2004. The chemokine receptor CXCR4 and not the N-methyl-D-aspartate receptor mediates gp120 neurotoxicity in cerebellar granule cells. J Neurosci Res 75:75-82.
12. Bakri Y, Mannioui A, Ylisastigui L, Sanchez F, Gluckman JC, Benjouad A. 2002. CD40-activated macrophages become highly susceptible to X4 strains of human immunodeficiency virus type 1. AIDS Res Hum Retroviruses 18:103-113.
13. Bansal AK, Mactutus CF, Nath A, Maragos W, Hauser KF, Booze RM. 2000. Neurotoxicity of HIV-1 proteins gp120 and Tat in the rat striatum. Brain Res 879:42-49.
14. Becher B, Prat A, Antel JP. 2000. Brain-immune connection: immunoregulatory properties of CNS-resident cells. Glia 29:293-304.
15. Bergamini A, Bolacchi F, Pesce CD, Carbone M, Cepparulo M, Demin F, Rocchi G. 2002. Increased CD4 and CCR5 expression and human immunodeficiency virus type 1 entry in CD40 ligand-stimulated macrophages. J Infect Dis 185:1567-1577.
16. Bonavia R, Bajetto A, Barbero S, Albini A, Noonan DM, Schettini G. 2001. HIV-1 Tat causes apoptotic death and calcium homeostasis alterations in rat neurons. Biochem Biophys Res Commun 288:301-308.
17. Bornemann MA, Verhoef J, Peterson PK. 1997. Macrophages, cytokines, and HIV. J Lab Clin Med 129:10-16.
18. Bragg DC, Hudson LC, Liang YH, Tompkins MB, Fernandes A, Meeker RB. 2002. Choroid plexus macrophages proliferate and release toxic factors in response to feline immunodeficiency virus. J Neurovirol 8:225-239.
19. Bruce-Keller AJ, Barger SW, Moss NI, Pham JT, Keller JN, Nath A. 2001. Pro-inflammatory and pro-oxidant properties of the HIV protein Tat in a microglial cell line: attenuation by 17 beta-estradiol. J Neurochem 78:1315-1324.
20. Buttini M, Westland CE, Masliah E, Yafeh AM, Wyss-Coray T, Mucke L. 1998. Novel role of human CD4 molecule identified in neurodegeneration. Nat Med 4:441-446.
21. Cafaro A, Caputo A, Fracasso C, Maggiorella MT, Goletti D, Baroncelli S, Pace M, Sernicola L, Koanga-Mogtomo ML, Betti M, Borsetti A, Belh R, Akerblom L, Corrias F, Butto S, Heeney J, Verani P, Titti F, Ensoh B. 1999. Control of SHIV-89.6P-infection of cynomolgus monkeys by HIV-1 Tat protein vaccine. Nat Med 5:643-650.
22. Calingasan NY, Erdely HA, Altar CA. 2002. Identification of CD40 ligand in Alzheimer's disease and in animal models of Alzheimer's disease and brain injury. Neurobiol Aging 23:31-39.
23. Chang HC, Samaniego F, Nair BC, Buonaguro L, Ensoli B. 1997. HIV-1 Tat protein exits from cells via a leaderless secretory pathway and binds to extracellular matrix-associated heparan sulfate proteoglycans through its basic region. AIDS 11:1421-1431.
24. Chirmule N, Than S, Khan SA, Pahwa S. 1995. Human immunodeficiency virus Tat induces functional unresponsiveness in T cells. J Virol 69:492-498.
25. Conant K, Garzino-Demo A, Nath A, McArthur JC, Halliday W, Power C, Gallo RC, Major EO. 1998. Induction of monocyte chemoattractant protein-1 in HIV-1 Tat-stimulated astrocytes and elevation in AIDS dementia. Proc Natl Acad Sci U S A 95:3117-3121.
26. Cosenza MA, Zhao ML, Si Q, Lee SC. 2002. Human brain parenchymal microglia express CD14 and CD45 and are productively infected by HIV-1 in HIV-1 encephalitis. Brain Pathol 12:442-455.
27. D'Aversa TG, Weidenheim KM, Berman JW. 2002. CD40-CD40L interactions induce chemokine expression by human microglia: implications for human immunodeficiency virus encephalitis and multiple sclerosis. Am J Pathol 160:559-567.
28. D'Aversa TG, Yu KOA, Berman JW. 2004. Expression of chemokines by human fetal microglia after treatment with the human immunodeficiency virus type 1 protein Tat. J Neurovirol 10:86-97.
29. Doranz BJ, Rucker J, Yi Y, Smyth RJ, Samson M, Peiper SC, Parmentier M, Collman RG, Doms RW. 1996. A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85:1149-1158.
30. + cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667-673.
31. Ehrlich LC, Hu S, Sheng WS, Sutton RL, Rockswold GL, Peterson PK, Chao CC. 1998. Cytokine regulation of human microglial cell IL-8 production. J Immunol 160:1944-1948.
32. Ensoli B, Buonaguro L, Barillari G, Fiorelli V, Gendelman R, Morgan RA, Wingfield P, Gallo RC. 1993. Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 67:277-287.
33. Eugenin EA, D'Aversa TG, Lopez L, Calderon TM, Berman JW. 2003. MCP-1 (CCL2) protects human neurons and astrocytes from NMDA or HIV-tat-induced apoptosis. J Neurochem 85:1299-1311.
34. Eugenin EA, Dyer G, Calderon TM, Berman JW. 2005. HIV-1 tat protein induces a migratory phenotype in human fetal microglia by a CCLP(MCP-1)- dependent mechanism: possible role in NeuroAIDS. Glia 49:501-510.
35. Feng Y, Broder CC, Kennedy PE, Berger EA. 1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877.
36. Fisher AG, Feinberg MB, Josephs SF, Harper ME, Marselle LM, Reyes G, Gonda MA, Aldovini A, Debouk C, Gallo RC, Wong-Staal F. 1986. The trans-activator gene of HTLV-III is essential for virus replication. Nature 320:367-371.
37. Garden GA. 2002. Microglia in human immunodeficiency virus-associated neurodegeneration. Glia 40:240-251.
38. Gebicke-Haerter PJ, Van Calker D, Norenberg W, Illes P. 1996. Molecular mechanisms of microglial activation. A. Implications for regeneration and neurodegenerative diseases. Neurochem Int 29:1-12.
39. Gerritse K, Laman JD, Noelle RJ, Aruffo A, Ledbetter JA, Boersma WJ, Claassen E. 1996. CD40-CD40 ligand interactions in experimental allergic encephalomyelitis and multiple sclerosis. Proc Natl Acad Sci USA 93:2499-2504.
40. Ghorpade A, Persidskaia R, Suryadevara R, Che M, Liu XJ, Persidsky Y, Gendelman HE. 2001. Mononuclear phagocyte differentiation, activation, and viral infection regulate matrix metalloproteinase expression: implications for human immunodeficiency virus type 1-associated dementia. J Virol 75:6572-6583.
41. Glass JD, Wesselingh SL, Seines OA, McArthur JC. 1993. Clinical-neuropathologic correlation in HIV-associated dementia. Neurology 43: 2230-2237.
42. Glass JD, Fedor H, Wesselingh SL, McArthur JC. 1995. Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann Neurol 38:755-762.
43. Glenner GG, Wong CW. 1984. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120:885-890.
44. Gray F, Adle-Biassette H, Brion F, Ereau T, le Maner I, Levy V, Corcket G. 2000. Neuronal apoptosis in human immunodeficiency virus infection. J Neurovirol 6(Suppl 1):S38-S43.
45. Grewal IS, Foellmer HG, Grewal KD, Xu J, Hardardottir F, Baron JL, Janeway CA Jr, Flavell RA. 1996. Requirement for CD40 ligand in costimulation induction, T cell activation, and experimental allergic encephalomyelitis. Science 273:1864-1867.
46. Haga S, Akai K, Ishii T. 1989. Demonstration of microglial cells in and around senile (neuritic) plaques in the Alzheimer brain. An immunohistochemical study using a novel monoclonal antibody. Acta Neuropathol 77:569-575.
47. Haughey NJ, Nath A, Mattson MP, Slevin JT, Geiger JD. 2001. HIV-1 Tat through phosphorylation of NMDA receptors potentiates glutamate excitotoxicity. J Neurochem 78:457-467.
48. He J, Chen Y, Farzan M, Choe H, Ohagen A, Gartner S, Busciglio J, Yang X, Hofmann W, Newman W, Mackay CR, Sodroski J, Gabuzda D. 1997. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385:645-649.
49. Helland DE, Welles JL, Caputo A, Haseltine WA. 1991. Transcellular transactivation by the human immunodeficiency virus type 1 tat protein. J Virol 65:4547-4549.
50. Herrmann H, Aebi U. 2000. Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol 12:79-90.
51. Hesselgesser J, Horuk R. 1999. Chemokine and chemokine receptor expression in the central nervous system. J Neurovirol 5:13-26.
52. Ho DD, Sarngadharan MG, Resnick L, Dimarzoveronese F, Rota TR, Hirsch MS. 1985. Primary human T-lymphotropic virus type III infection. Ann Intern Med 103:880-883.
53. Ishizuka K, Kimura T, Igata-yi R, Katsuragi S, Takamatsu J, Miyakawa T. 1997. Identification of monocyte chemoattractant protein-1 in senile plaques and reactive microglia of Alzheimer's disease. Psychiatry Clin Neurosci 51:135-138.
54. Jones MV, Bell JE, Nath A. 2000. Immunolocalization of HIV envelope gp120 in HIV encephalitis with dementia. AIDS 14:2709-2713.
55. Kanmogne GD, Kennedy RC, Grammas P. 2002. HIV-1 gp120 proteins and gp160 peptides are toxic to brain endothelial cells and neurons: possible pathway for HIV entry into the brain and HIV-associated dementia. J Neuropathol Exp Neurol 61:992-1000.
56. Kaul M, Garden GA, Lipton SA. 2001. Pathways to neuronal injury and apoptosis in HIV-associated dementia. Nature 410:988-994.
57. Kehry MR. 1996. CD40-mediated signaling in B cells. Balancing cell survival, growth, and death. J Immunol 156:2345-2348.
58. Kielian T. 2004. Microglia and chemokines in infectious diseases of the nervous system: views and reviews. Front Biosci 9:732-750.
59. Kielian T, Barry B, Hickey WF. 2001. CXC chemokine receptor-2 ligands are required for neutrophil-mediated host defense in experimental brain abscesses. J Immunol 166:4634-4643.
60. Kim BO, Liu Y, Ruan Y, Xu ZC, Schantz L, He JJ. 2003. Neuropathologies in transgenic mice expressing human immunodeficiency virus type 1 Tat protein under the regulation of the astrocyte-specific glial fibrillary acidic protein promoter and doxycycline. Am J Pathol 162: 1693-1707.
61. Kremlev SG, Roberts RL, Palmer C. 2004. Differential expression of chemokines and chemokine receptors during microglial activation and inhibition. J Neuroimmunol 149:1-9.
62. Kruman II, Nath A, Mattson MP. 1998. HIV-1 protein Tat induces apoptosis of hippocampal neurons by a mechanism involving caspase activation, calcium overload, and oxidative stress. Exp Neurol 154:276-288.
63. Kruman II, Nath A, Maragos WF, Chan SL, Jones M, Rangnekar VM, Jakel RJ, Mattson MP. 1999. Evidence that Par-4 participates in the pathogenesis of HIV encephalitis. Am J Pathol 155:39-46.
64. Kutsch O, Levy DN, Kosloff BR, Shaw GM, Benveniste EN. 2003. CD154-CD40-induced reactivation of latent HIV-1 infection. Virology 314:261-270.
65. Lafreme RM, Wahl LM, Epstein JS, Hewlett IK, Yamada KM, Dhawan S. 1996. HIV-1-Tat protein promotes chemotaxis and invasive behavior by monocytes. J Immunol 157:974-977.
66. Lane P, Traunecker A, Hubele S, Inui S, Lanzavecchia A, Gray D. 1992. Activated human T cells express a ligand for the human B cell-associated antigen CD40 which participates in T cell-dependent activation of B lymphocytes. Eur J Immunol 22:2573-2578.
67. Lavi E, Strizki JM, Ulrich AM, Zhang W, Fu L, Wang Q, O'Connor M, Hoxie JA, Gonzalez-Scarano F. 1997. CXCR-4 (Fusin), a coreceptor for the type 1 human immunodeficiency virus (HIV-1), is expressed in the human brain in a variety of cell types, including microglia and neurons. Am J Pathol 151:1035-1042.
68. + T cells that induces contact-dependent B cell differentiation (help). J Exp Med 175:1091-1101.
69. Lee SC, Hatch WC, Liu W, Kress Y, Lyman WD, Dickson DW. 1993. Productive infection of human fetal microglia by HIV-1. Am J Pathol 143:1032-1039.
70. Lipsky PE, Attrep JF, Grammer AC, McIlraith MJ, Nishioka Y. 1997. Analysis of CD40-CD40 ligand interactions in the regulation of human B cell function. Ann N Y Acad Sci 815:372-383.
71. Lipton SA. 1991. HIV-related neurotoxicity. Brain Pathol 1:193-199.
72. Lipton SA. 1992. Requirement for macrophages in neuronal injury induced by HIV envelope protein gp120. Neuroreport 3:913-915.
73. Lipton SA. 1994a. HIV-related neuronal injury. Potential therapeutic intervention with calcium channel antagonists and NMDA antagonists. Mol Neurobiol 8:181-196.
74. Lipton SA. 1994b. Neuronal injury associated with HIV-1 and potential treatment with calcium-channel and NMDA antagonists. Dev Neurosci 16:145-151.
75. Lipton SA. 1998. Neuronal injury associated with HIV-1: approaches to treatment. Annu Rev Pharmacol Toxicol 38:159-177.
76. Lokensgard JR, Hu S, Hegg CC, Thayer SA, Gekker G, Peterson PK. 2001. Diazepam inhibits HIV-1 Tat-induced migration of human microglia. J Neurovirol 7:481-486.
77. Mach F, Schonbeck U, Sukhova GK, Bourcier T, Bonnefoy JY, Pober JS, Libby P. 1997. Functional CD40 ligand is expressed on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for CD40-CD40 ligand signaling in atherosclerosis. Proc Natl Acad Sci U S A 94:1931-1936.
78. Maragos WF, Tillman P, Jones M, Bruce-Keller AJ, Roth S, Bell JE, Nath A. 2003. Neuronal injury in hippocampus with human immunodeficiency virus transactivating protein, Tat. Neuroscience 117:43-53.
79. Marcuzzi A, Weinberger J, Weinberger OK. 1992. Transcellular activation of the human immunodeficiency virus type 1 long terminal repeat in cocultured lymphocytes. J Virol 66:4228-4232.
80. Matsumoto T, Miike T, Nelson RP, Trudeau WL, Lockey RF, Yodoi J. 1993. Elevated serum levels of IL-8 in patients with HIV infection. Clin Exp Immunol 93:149-151.
81. May RC, Machesky LM. 2001. Phagocytosis and the actin cytoskeleton. J Cell Sci 114:1061-1077.
82. McManus CM, Weidenheim K, Woodman SE, Nunez J, Hesselgesser J, Nath A, Berman JW. 2000. Chemokine and chemokine-receptor expression in human glial elements: induction by the HIV protein, Tat, and chemokine autoregulation. Am J Pathol 156:1441-1453.
83. Miller RJ, Meucci O. 1999. AIDS and the brain: is there a chemokine connection? Trends Neurosci 22:471-479.
84. Minghetti L, Visentin S, Patrizio M, Franchini L, Ajmone-Cat MA, Levi G. 2004. Multiple actions of the human immunodeficiency virus type-1 Tat protein on microglial cell functions. Neurochem Res 29:965-978.
85. Mitchison TJ, Cramer LP. 1996. Actin-based cell motility and cell locomotion. Cell 84:371-379.
86. Mucke L, Masliah E, Campbell IL. 1995. Transgenic models to assess the neuropathogenic potential of HIV-1 proteins and cytokines. Curr Top Microbiol Immunol 202:187-205.
87. Nath A, Geiger J. 1998. Neurobiologjcal aspects of human immunodeficiency virus infection: neurotoxic mechanisms. Prog Neurobiol 54:19-33.
88. Nath A, Conant K, Chen P, Scott C, Major EO. 1999. Transient exposure to HIV-1 Tat protein results in cytokine production in macrophages and astrocytes. A hit and run phenomenon. J Biol Chem 274: 17098-17102.
89. Nath A, Haughey NJ, Jones M, Anderson C, Bell JE, Geiger JD. 2000. Synergistic neurotoxicity by human immunodeficiency virus proteins Tat and gp120: protection by memantine. Ann Neurol 47:186-194.
90. Navia BA, Cho ES, Petito CK, Price RW. 1986. The AIDS dementia complex: II. Neuropathology. Ann Neurol 19:525-535.
91. Nelson PT, Soma LA, Lavi E. 2002. Microglia in diseases of the central nervous system. Ann Med 34:491-500.
92. Noonan D, Albini A. 2000. From the outside in: extracellular activities of HIV Tat. Adv Pharmacol 48:229-250.
93. Notarangelo LD, Peitsch MC. 1996. CD401base: a database of CD40L gene mutations causing X-linked hyper-IgM syndrome. Immunol Today 17:511-516.
94. Nottet HS, Persidsky Y, Sasseville VG, Nukuna AN, Bock P, Zhai QH, Sharer LR, McComb RD, Swindells S, Soderland C, Gendelman HE. 1996. Mechanisms for the transendothelial migration of HIV-1-infected monocytes into brain. J Immunol 156:1284-1295.
95. Palmer DL, Hjelle BL, Wiley CA, Allen S, Wachsman W, Mills RG, Davis LE, Merlin TL. 1994. HIV-1 infection despite immediate combination antiviral therapy after infusion of contaminated white cells. Am J Med 97:289-295.
96. Patrizio M, Colucci M, Levi G. 2001. Human immunodeficiency virus type 1 Tat protein decreases cyclic AMP synthesis in rat microglia cultures. J Neurochem 77:399-407.
97. Perry VH, Gordon S. 1991. Macrophages and the nervous system. Int Rev Cytol 125:203-244.
98. Polazzi E, Levi G, Minghetti L. 1999. Human immunodeficiency virus type 1 Tat protein stimulates inducible nitric oxide synthase expression and nitric oxide production in microglial cultures. J Neuropathol Exp Neurol 58:825-831.
99. Prendergast MA, Rogers DT, Mulholland PJ, Littleton JM, Wilkins LH, Jr., Self RL, Nath A. 2002. Neurotoxic effects of the human immunodeficiency virus type-1 transcription factor Tat require function of a polyamine sensitive-site on the N-methyl-D-aspartate receptor. Brain Res 954:300-307.
100. Prineas JW, Raine CS. 1976. Electron microscopy and immunoperoxidase studies of early multiple sclerosis lesions. Neurology 26:29-32.
101. Prineas JW, Wright RG. 1978. Macrophages, lymphocytes, and plasma cells in the perivascular compartment in chronic multiple sclerosis. Lab Invest 38:409-421.
102. Rezaie P, Trillo-Pazos G, Everall IP, Male DK. 2002. Expression of beta-chemokines and chemokine receptors in human fetal astrocyte and microglial co-cultures: potential role of chemokines in the developing CNS. Glia 37:64-75.
103. Rogers J, Luber-Narod J, Styren SD, Civin WH. 1988. Expression of immune system-associated antigens by cells of the human central nervous system: relationship to the pathology of Alzheimer's disease. Neurobiol Aging 9:339-349.
104. Rohr O, Lecestre D, Chasserot-Golaz S, Marban C, Avram D, Aunis D, Leid M, Schaeffer E. 2003. Recruitment of Tat to heterochromatin protein HP1 via interaction with CTIP2 inhibits human immunodeficiency virus type 1 replication in microglial cells. J Virol 77:5415-5427.
105. Rollins BJ. 1997. Chemokines. Blood 90:909-928.
106. + T cells. J Immunol 151:2497-2510.
107. Sanders VJ, Pittman CA, White MG, Wang G, Wiley CA, Achim CL. 1998. Chemokines and receptors in HIV encephalitis. AIDS 12:1021-1026.
108. Sasseville VG, Smith MM, Mackay CR, Pauley DR, Mansfield KG, Ringler DJ, Lackner AA. 1996. Chemokine expression in simian immunodeficiency virus-induced AIDS encephalitis. Am J Pathol 149: 1459-1467.
109. Schmidtmayerova H, Nottet HS, Nuovo G, Raabe T, Flanagan CR, Dubrovsky L, Gendelman HE, Cerami A, Bukrinsky M, Sherry B. 1996. Human immunodeficiency virus type 1 infection alters chemokine beta peptide expression in human monocytes: implications for recruitment of leukocytes into brain and lymph nodes. Proc Natl Acad Sci U S A 93:700-704.
110. Schneider J, Kaaden O, Copeland TD, Oroszlan S, Hunsmann G. 1986. Shedding and interspecies type sero-reactivity of the envelope glycopolypeptide gp120 of the human immunodeficiency virus. J Gen Virol 67:2533-2538.
111. Seguin R, Biemacki K, Prat A, Wosik K, Kim HJ, Blain M, McCrea E, Bar-Or A, Antel JP. 2003. Differential effects of Th1 and Th2 lymphocyte supernatants on human microglia. Glia 42:36-45.
112. Selkoe DJ. 1991. The molecular pathology of Alzheimer's disease. Neuron 6:487-498.
113. Sheng WS, Hu S, Hegg CC, Thayer SA, Peterson PK. 2000. Activation of human microglial cells by HIV-1 gp41 and Tat proteins. Clin Immunol 96:243-251.
114. Si Q, Kim MO, Zhao ML, Landau NR, Goldstein H, Lee S. 2002. Vpr- and Nef-dependent induction of RANTES/CCL5 in microglial cells. Virology 301:342-353.
115. Sodroski J, Patarca R, Rosen C, Wong-Staal F, Haseltine W. 1985. Location of the trans-activating region on the genome of human T-cell lymphotropic virus type III. Science 229:74-77.
116. Sopper S, Demuth M, Stahl-Hennig C, Hunsmann G, Plesker R, Coulibaly C, Czub S, Ceska M, Koutsilieri E, Riederer P, Brinkmann R, Katz M, ter Meulen V. 1996. The effect of simian immunodeficiency virus infection in vitro and in vivo on the cytokine production of isolated microglia and peripheral macrophages from rhesus monkey. Virology 220:320-329.
117. Stoll G, Jander S. 1999. The role of microglia and macrophages in the pathophysiology of the CNS. Prog Neurobiol 58:233-247.
118. Styren SD, Civin WH, Rogers J. 1990. Molecular, cellular, and pathologic characterization of HLA-DR immunoreactivity in normal elderly and Alzheimer's disease brain. Exp Neurol 110: 93-104.
119. Tan J, Town T, Paris D, Mori T, Suo Z, Crawford F, Mattson MP, Flavell RA, Mullan M. 1999. Microglial activation resulting from CD40-CD40L interaction after beta-amyloid stimulation. Science 286:2352-2355.
120. Toggas SM, Masliah E, Rockenstein EM, Rail GF, Abraham CR, Mucke L. 1994. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367: 188-193.
121. Togo T, Akiyama H, Kondo H, Ikeda K, Kato M, Iseki E, Kosaka K. 2000. Expression of CD40 in the brain of Alzheimer's disease and other neurological diseases. Brain Res 885:117-121.
122. Tyor WR, Wesselingh SL, Griffin JW, McArthur JC, Griffin DE. 1995. Unifying hypothesis for the pathogenesis of HIV-associated dementia complex, vacuolar myelopathy, and sensory neuropathy. J Acquir Immune Defic Syndr Hum Retrovirol 9:379-388.
123. Vallat AV, De Girolami U, He J, Mhashilkar A, Marasco W, Shi B, Gray F, Bell J, Keohane C, Smith TW, Gabuzda D. 1998. Localization of HIV-1 co-receptors CCR5 and CXCR4 in the brain of children with AIDS. Am J Pathol 152:167-178.
124. Wang EJ, Sun J, Pettoello-Mantovani M, Anderson CM, Osiecki K, Zhao ML, Lopez L, Lee SC, Berman JW, Goldstein H. 2003. Microglia from mice transgenic for a provirus encoding a monocyte-tropic HIV type 1 isolate produce infectious virus and display in vitro and in vivo up-regulation of lipopolysaccharide- induced chemokine gene expression. AIDS Res Hum Retroviruses 19:755-765.
125. Weiss JM, Nath A, Major EO, Berman JW. 1999. HIV-1 Tat induces monocyte chemoattractant protein-1-mediated monocyte transmigration across a model of the human blood-brain barrier and up-regulates CCR5 expression on human monocytes. J Immunol 163:2953-2959.
126. Westendorp MO, Frank R, Ochsenbauer C, Stricker K, Dhein J, Walczak H, Debatin KM, Krammer PH. 1995. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375:497-500.
127. Wieland U, Kuhn JE, Jassoy C, Rubsamen-Waigmann H, Wolber V, Braun RW. 1990. Antibodies to recombinant HIV-1 vif, tat, and nef proteins in human sera. Med Microbiol Immunol 179:1-11.
128. Wiley CA, Schrier RD, Nelson JA, Lampert PW, Oldstone MB. 1986. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc Natl Acad Sci U S A 83:7089-7093.
129. Wiley CA, Achim CL, Christopherson C, Kidane Y, Kwok S, Masliah E, Mellors J, Radhakrishnan L, Wang G, Soontornniyomkij V. 1999. HIV mediates a productive infection of the brain. AIDS 13:2055-2059.
130. Xu Y, Kulkosky J, Acheampong E, Nunnari G, Sullivan J, Pomerantz RJ. 2004. HIV-1-mediated apoptosis of neuronal cells: Proximal molecular mechanisms of HIV-1-induced encephalopathy. Proc Natl Acad Sci U S A 101:7070-7075.
131. Yi Y, Lee C, Liu QH, Freedman BD, Collman RG. 2004. Chemokine receptor utilization and macrophage signaling by human immunodeficiency virus type 1 gp120: Implications for neuropathogenesis. J Neurovirol 10(Suppl 1):91-96.
132. Zink MC, Coleman GD, Mankowski JL, Adams RJ, Tarwater PM, Fox K, Clements JE. 2001. Increased macrophage chemoattractant protein-1 in cerebrospinal fluid precedes and predicts simian immunodeficiency virus encephalitis. J Infect Dis 184:1015-1021.