Molecular and biological mechanisms in the development of AIDS dementia complex (ADC)

Bulletin de l'Institut Pasteur

Volumn 96, Issue 3, 1998, Pages 171-187

  Saksena, Nitin K ^a   Jozwiak, R ^a   Wang, B ^a  

^a WESTMEAD HOSPITAL   (Australia)

Author keywords

ADC; AIDS; HIV; Molecular and biological mechanisms; Neuropathogenesis; Review; Therapy

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; BRAIN DISEASE; DEMENTIA; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MACROPHAGE; MORTALITY; NEUROPATHOLOGY; PARALYSIS; REVIEW;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0032126292     PISSN: 00202452     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0020-2452(98)80012-2     Document Type: Review

References (95)

1. [1] Price, RW., Brew, B., Sidtis, J., Rosenblum, M., Scheck, A.C. & Cleary, P. (1988), The brain in AIDS : central nervous system HIV-1 infection and AIDS dementia complex. Science, 239 (4840), 586-592.
2. [2] Resnick, L., Berger, J.R., Shapshak, P. & Tourtellotte, W.W. (1988), Early penetration of the blood-brain-barrier by HIV. Neurology, 38 (1), 9-14.
3. [3] Davis, L.E., Hjelle, B.L., Miller, V.E., Palmer, D.L., Llewellyn, A.L., Merlin, T.L., Young, S.A., Mills, R.G., Wachsman, W. & Wiley, C.A. (1992), Early viral brain invasion in iatrogenic human immunodeficiency virus infection. Neurology, 42 (9), 1736-1739.
4. [4] Atwood, W.A. & Berger, J.A. (1993), HIV-1 infection of brain. Clin. Microbiol. Rev., 6, 3339-3366.
5. [5] McArthur, J.C., McClernon, D.R., Cronin, M.F., Nance-Sproson T.E., Saah, A.J., St. Clair, M. & Lanier, E.R. (1997), Relationship between HIV associated with dementia and viral load in CSF and brain. Ann. Neurol., 42 (5), 689-698.
6. [6] Michaels, J., Sharer, L.R. & Epstein, L.G. (1988), Human immunodeficiency virus type 1 (HIV-1) infection of the nervous system: a review. Immunodefic. Rev., 1 (1), 71-104.
7. [7] Price, R.W., Brew, B., Sidtis, J., Rosenblum, M. & Scheck, A.C. (1987), The brain in AIDS: CNS HIV-1 infection in ADC. N. Engl. J. Med., 317, 278-286.
8. [8] Gendelman, H.E., Lipton, S.A., Tardieu, M., Bukrinsky, M.I. & Nottet, H.S. (1994), The neuropathogenesis of HIV-1 infection. J. Leukocyte Biol., 56 (3), 389-398.
9. [9] Brew, B. (1993), The neuroscience of HIV infection. Venerol., 6, 129-132.
10. [10] Saksena, N.K. (1996), Recent Advances in AIDS Research. Kaleidoscopio (Ed. Sergio Rassu, Italy) 5, 1-110.
11. [11] Narayan, O. & Clements, J.E. (1990), Lentiviruses, in "Virology" (B.N. Fields and D.M. Kuipel) (pp. 1571-1589). Raven Press Ltd., New York.
12. [12] Navia, BA., Cho, ES., Petito, CK. & Price, RW. (1986), The AIDS dementia complex: II. Neuropathol. Ann. Neurol, 19(6), 525-535.
13. [13] Wiley, C.A. & Budka, H. (1991), HIV-1 induced CNS lesions. Brain pathol., 1, 153-154.
14. [14] Everall, I.P., Luthert, P.J. & Lantos, P.L. (1991, Neuronal loss in the frontal cortex in HIV infection. Lancet, 337 (8750), 1119-1121.
15. [15] Holtzman, D.M., Kaku, DA. & So, Y.T. (1989), New-onset seizures associated with human immunodeficiency virus infection : causation and clinical features in 100 cases. Am. J. Med., 87 (2), 173-177.
16. [16] Norman, S.E., Chediak, AD., Kiel, M. & Cohn, M.A. (1990), Sleep disturbances in HIV-infected homosexual men. AIDS, 4 (8), 775-781.
17. [17] Parisi, A., Strosselli, M., Di Perri, G., Cairoli, S., Minoli, L., Bono, G., Moglia, A. & Nappi, G. (1989), Electroencephalography in the early diagnosis of HIV-related subacute encephalitis: analysis of 185 patients. Clin. Electroencephalogr., 20 (1), 1-5.
18. [18] Merrill, PT., Paige, GD., Abrams, RA., Jacoby, RG. & Clifford, D.B. (1991), Ocular motor abnormalities in human immunodeficiency virus infection. Ann. Neurol., 30 (2), 130-138.
19. [19] Arendt, G., Hefter, H., Elsing, C., Strohmeyer, G. & Freund, H.J. (1990), Motor dysfunction in HIV-infected patients without clinically detectable central-nervous deficit. J. Neurol., 237 (6), 362-368.
20. [20] Jordan, C.A., Watkins, B.A., Kufta, C. & Dubois-Dalcq, M. (1991), Infection of brain microglial cells by human immunodeficiency virus type 1 is CD4 dependent. J. Virol., 65 (2), 736-742.
21. [21] Koenig, S., Gendelman, H.E., Orenstein, J.M., dal canto, M.C., Pezeshkpour, G.H., Yungbluth, M., Janotta, F., Aksamit, A., Martin, M.A. & Fauci, A.S. (1986), Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science, 233, 1089-1093.
22. [22] Schweitzer, C., Keller, F., Schmitt, M.P., Jaeck, D., Adloff, M., Schmitt, C., Royer, C., Kirn, A. & Aubertin, A.M. (1991), Morphine stimulates HIV replication in primary cultures of human Kupffer cells. Res. Virol., 142 (2-3), 189-195.
23. [23] Meltzer, M.S., Skillman, D.R., Gomatos, P.J., Kalter D.C. & Gendelman, H.E. (1990), Role of mononuclear phagocytes in the pathogenesis of human immunodeficiency virus infection. Annu. Rev. Immunol., 8, 169-194.
24. [24] Lewis, S.H., Reynolds-Kohler, C., Fox, H.E. & Nelson, J.A. (1990), HIV-1 in trophoblastic and villous Hofbauer cells, and haematological precursors in eight-week fetuses. Lancet, 335 (8689), 565-568.
25. [25] Collman, R., Hassan, N.F., Walker, R., Godfrey B., Cutilli J., Hastings, J.C., Friedman, H., Douglas, S.D. & Nathanson, N. (1989), Infection of monocyte-derived macrophages with human immunodeficiency virus type 1 (HIV-1). Monocyte-tropic and lymphocyte-tropic strains of HIV-1 show distinctive patterns of replication in a panel of cell types. J. Exp. Med., 170 (4), 1149-1163.
26. [26] Eilbott, D.J., Peress, N., Burger, H., LaNeve, D., Orenstein, J., Gendelman, H.E., Seidman, R. & Weiser, B. (1989), Human immunodeficiency virus type 1 in spinal cords of acquired immunodeficiency syndrome patients with myelopathy: expression and replication in macrophages. Proc. Natl. Acad. Sci. USA, 86 (9), 3337-3341.
27. [27] De La Monte, S.M., Ho, D.D., Schooley, R.T., Hirsh, M.S. & Richardson, E.P. (1987), Subacute encephalomyelitis of AIDS and its relation to HTLV-III infection. Neurology, 37, 562-569.
28. [28] Michaels, J., Price, R.W. & Rosenblum, M.K. (1988), Microglia in the giant cell encephalitis of acquired immune deficiency syndrome: proliferation, infection and fusion. Acta Neuropathol., 76 (4), 373-379.
29. [29] Kunsch, C., Hartle, H.T. & Wigddahl, B. (1989), Infection of human fetal dorsal root ganglonglial cells with HIV-1 involves an entry mechanism independent of the CD4 T4A epitope. J. Virol., 63, 5054-5061.
30. [30] Tornatore, C., Nath, A., Amemiya, K. & Major, E.O. (1991), Persistent human immunodeficiency virus type 1 infection in human fetal glial cells reactivated by T-cell factor(s) or by the cytokines tumor necrosis factor alpha and interleukin-1 beta. J. Virol., 65 (11), 6094-6100.
31. [31] Merrill, J.E . (1992), Cytokines and retroviruses. Clin. Immunol. Immunopathol., 64(1), 23-27.
32. [32] Giulian, D., Baker, T.J., Shih, L.C. & Lachman, L.B. (1986), Interleukin 1 of the central nervous system is produced by ameboid microglia. J. Exp. Med., 164(2), 594-604.
33. [33] Gallo, P., Piccinno, M.G., Krzalic, L. & Tavolato, B. (1989), Tumor necrosis factor alpha and neurological diseases. Failure in detecting TNF alpha in the cerebrospinal fluid from patients with multiple sclerosis, AIDS dementia complex, and brain tumors. J. Neuroimmunol., 23, 41-44.
34. [34] Achim, C.L., Heyes, M.P. & Wiley, C.A. (1993), Quantitation of human immunodeficiency virus, immune activation factors, and quinolinic acid in AIDS brains. J. Clin. Invest., 91 (6), 2769-2775.
35. [35] Trkola, A., Dragic, T., Arthos, J., Binley, J.M., Olson, W.C., Allaway, G.P., Cheng-Mayer, C., Robinson, J., Maddon, P.J. & Moore, J.P. (1996), CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature, 384 (6605), 184-187.
36. [36] Yoshioka, M., Shapshak, P., Srivastava, A.K., Stewart, R.V., Nelson, S.J., Bradley, W.G., Berger, J.R., Rhodes, R.H., Sun, N.C. & Nakamura, S. (1994), Expression of HIV-1 and interleukin-6 in lumbosacral dorsal root ganglia of patients with AIDS. Neurology, 44 (6), 1120-1130.
37. [37] Masliah, E., Achim, C.L., Ge, N., DeTeresa, R., Terry, R.D. & Wiley, C.A. (1994), Spectrum of human immunodeficiency virus-associated neocortical damage. Ann. Neurol., 32 (3), 321-329.
38. [38] Swingler, S., Easton, A. & Morris, A. (1992), Cytokine augmentation of HIV-1 LTR-driven gene expression in neural cells. AIDS Res. Hum. Retroviruses, 8 (4), 487-493.
39. [39] Yeung, M.C., Pulliam, L. & Lau, A.S. (1995), The HIV envelope protein gp120 is toxic to human brain-cell cultures through the induction of interleukin-6 and tumor necrosis factor-alpha. AIDS, 9 (2), 137-143.
40. [40] Wahl, L.M., Corcoran, M.L., Pyle, S.W., Arthur, L.O., Harel-Bellan, A. & Farrar, W.L. (1989), Human immunodeficiency virus glycoprotein (gp120) induction of monocyte arachidonic acid metabolites and interleukin 1. Proc. Natl. Acad. Sci. USA, 86 (2), 621-625.
41. [41] Tardieu, M., Henry, C., Peudenier, S., Boespflug, O. & Montagnier, L. (1992), Human immunodeficiency virus type 1-infected monocytic cells can destroy human neural cells after cell-to-cell adhesion. Ann. Neurol., 32 (1), 11-17.
42. [42] Pulliam, L., Clarke, J.A., McGrath, M.S., Moore, D. & McGuire, D. (1996), Monokine products as predictors of AIDS dementia. AIDS, 10 (13), 1495-1500.
43. [43] Pulliam, L., Gascon, R., Stubblebine, M., McGuire, D. & McGrath, M.S. (1997), Unique monocyte subset in patients with AIDS dementia. Lancet, 349 (9053), 692-695.
44. [44] Kawano, H., Rostaphshov, V., Rosen, L. & Lai, J.C. (1993), Genetic determinants of Dengue type 4 Virus neurovirulence for mice. J. Virol., 67, 6567-6575.
45. [45] Hwang, S.S., Boyle, T.J., Lyerly, H.K. & Cullen, B.R. (1991), Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science, 253, 202-209.
46. [46] Chesebro, B., Wehrly, K., Nishio, J. & Perryman, S. (1992), Macrophage tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence heterogeneity in comparison with T-cell tropic isolates: Definition of critical amino acids involved in cell tropism. J. Virol., 253, 202-209.
47. [47] Power, C., McArthur, J.C., Johnson, R.T., Griffin, D.E., Glass, J.D., Perryman, S. & Chesebro, B. (1994), Demented and nondemented patients with AIDS differ in brain-derived human immunodeficiency virus type 1 envelope sequences. J. Virol., 68 (7), 4643-4649.
48. [48] Korber, B.T.M., Kunstman, K.J., Patterson, B.K., Furtado, M.J., McEvilly, M.M., Levy, R. & Wolinsky, S.M. (1994), Genetic differences between blood- and brain-derived viral sequences from HIV-1 infected patients. J. Virol., 68, 7467-7481.
49. [49] DiStefano, M., Wilt, S., Gray, F., Dubois-Dalc, M. & Chiodi, R. (1996), HIV-1 type 1 V3 sequences and the development of dementia during AIDS. AIDS Res. Hum. Retroviruses, 12, 471-476.
50. [50] Monken, C., Wu, B. & Srinivasan, A. (1995), High resolution analysis of HIV-1 quasispecies in the brain. AIDS, 9, 345-349.
51. [51] Chang, J., Jozwiak, R., Wang, B., Ng, T., Ge, Y.C., Bolton, W., Dwyer, D.E., Randle, C., Osborn, R. & Saksena, N.K. (1998), Unique HIV type 1 V3 region sequences derived from six different regions of brain : Region-specific evolution within host-determined quasispecies. AIDS Res. Hum. Retroviruses, 14, 25-30.
52. [52] O'Brien, W.A. (1992), Viral determinants of cellular tropism. pathobiology, 60, 225-233.
53. [53] Saksena, N.K., Wang, B., Ge, Y.C., Chang, J., Dwyer, D.E., Xiang, S.H., Packham, D.R. & Randle, C. (1997), Region-specific changes, gene duplications, and random deletions in the nef gene from HIV-1 infected brain tissues and blood of a demented patient. AIDS Res. Hum. Retroviruses, 13 (1), 111-116.
54. [54] New, D.R., Ma, M., Epstein, L.G., Nath, A. & Gelbard, H.A. (1997), Human immunodeficiency virus type 1 Tat protein induces death by apoptosis in primary human neuron cultures. J. Neurovirol., 3 (2), 168-173.
55. [55] Annamari, R., Nyberg, M., Vladimir, O., Haltia, M., Elovaara, I., Raininko, R., Haapasalo, H. & Krohn, K. (1995), Abundant expression of HIV Nef and Rev proteins in brain astrocytes in vivo is associated with dementia. AIDS, 9, 1001-1008.
56. [56] Sabatier, J-M., Vives, E. & Mabrouk, K. (1991), Evidence for neurotoxic activity of tat from HIV-1. J. Virol., 65, 961-967.
57. [57] Harouse, J, M., Bhat, S., Spitalnik, S.L., Laughlin, M., Stefano, K., Silberberg, D.H. & Gonzalez-Scarano, F. (1991), Inhibition of entry of HIV-1 in neural cell lines by antibodies against galactosyl ceramide. Science, 253 (5017), 320-323.
58. [58] Feng, Y., Broder, C.C., Kennedy, P.E. & Berger, E.A. (1996), HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science, 272 (5263), 872-877.
59. [59] Dragic, T., Litwin, V., Allaway, G.P., Martin, S.R., Huang, Y., Nagashima, K.A., Cayanan, C., Maddon, P.J., Koup, R.A., Moore, J.P. & Paxton, W.A. (1996), HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature, 381 (6584), 667-673.
60. [60] Liu, R., Paxton, W.A., Choe, S., Ceradini, D., Martin, S.R., Horuk, R., MacDonald, M.E., Stuhlmann, H., Koup, R.A. & Landau, N.R. (1996), Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell, 86 (3), 367-377.
61. [61] Choe, H., Farzan, M., Sun, Y., Sullivan, N., Rollins, B., Ponath, PD., Wu, L., Mackay, C.R., LaRosa, G., Newman, W., Gerard, N., Gerard, C. & Sodroski, J. (1996), The beta-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell, 85 (7), 1135-1148.
62. [62] Doranz, B.J., Rucker, J., Yi, Y., Smyth, R.J., Samson, M., Peiper, S.C., Parmentier, M., Collman, R.G. & Doms, R.W. (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 (7), 1149-1158.
63. [63] Wu, L., Gerard, N.P., Wyatt, R., Choe, H., Parolin, C., Ruffing, N., Borsetti, A., Cardoso, A.A., Desjardin, E., Newman, W., Gerard, C. & Sodroski, J. (1996), CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature, 384 (6605), 179-183.
64. [64] 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 (6617), 645-659.
65. [65] Lavi, E., Strizki, J.M., Ulrich, A.M., Zhang, W., Fu, L., Wang, Q., O'Connor, M., Hoxie, J.A. & 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 (4), 1035-1042.
66. [66] Strizki, J.M., Albright, A.V., Sheng, H., O'Connor, M., Perrin, L. & Gonzalez-Scarano, F. (1996), Infection of primary human microglia and monocyte-derived macrophages with human immunodeficiency virus type 1 isolates: evidence of differential tropism. J. Virol., 70 (11), 7654-7662.
67. [67] Peluso, R., Hasse, A., Stowring, L., Edwards, M. & Ventura, P. (1985), A trojan-horse mechanism for the spread of visna virus in monocytes. Viroloy, 147, 231-236.
68. [68] Lassman, H., Schmied, M., Vass, K. & Hickey, W.F. (1993), Bone marrow derived elements and resident microglia in brain inflammation. Glia, 7, 19-24.
69. [69] Springer, T.A. (1994), Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell, 76 (2), 301-314.
70. [70] Bevilacqua, MP., Schleef, R.R., Gimbrone, M.A., Jr. & Loskutoff, D.J. (1986), Regulation of the fibrinolytic system of cultured human vascular endothelium by interleukin 1. J. Clin. Invest., 78 (2), 587-591.
71. [71] Dustin, M.L., Rothlein, R., Bhan, A.K., Dinarello, C.A. & Springer, T.A. (1986), J Induction by IL 1 and interferon-gamma: tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). Immunology, 137 (1), 245-254.
72. [72] Selmaj, K.W., Farooq, M., Norton, W.T., Raine, C.S. & Brosnan, C.F. (1990), Proliferation of astrocytes in vitro in response to cytokines. A primary role for tumor necrosis factor. J. Immunol., 144 (1), 129-135.
73. [73] Taub, D.D., Turcovski-Corrales, S.M., Key, M.L., Longo, D.L. & Murphy, W.J. (1996), Chemokines and T lymphocyte activation : I. Beta chemokines costimulate human T lymphocyte activation in vitro. J. Immunol., 156 (6), 2095-2103.
74. [74] Cocchi, F., DeVico, A.L., Garzino-Demo, A., Arya, S.K., Gallo, R.C. & Lusso, P . (1995), Identification of RANTES, MIP-1 alpha, and MIP-1 beta as the major HIV-suppressive factors produced by CD8+T cells. Science, 270 (5243), 1811-1815.
75. [75] Paxton, W.A., Dragic, T., Koup, R.A. & Moore, J.P. (1996), The beta-chemokines, HIV type 1 second receptors, and exposed uninfected persons. AIDS Res. Hum. Retroviruses, 12 (13), 1203-1207.
76. [76] Sasseville, V.G., Smith. M.M., Mackay, C.R., Pauley, D.R., Mansfield, K.G., Ringler, D.J. & Lackner, A.A. (1996), Chemokine expression in simian immunodeficiency virus-induced AIDS encephalitis. Am. J. Pathol., 149 (5), 1459-1467.
77. [77] Koch, A.E., Kunkel, S.L., Harlow, L.A., Mazarakis, D.D., Haines, G.K., Burdick, M.D., Pope, R.M. & Strieter, R.M. (1994), Macrophage inflammatory protein-1 alpha. A novel chemotactic cytokine for macrophages in rheumatoid arthritis. J. Clin. Invest., 93 (3), 921-928.
78. [78] Bell, J.E., Busuttil, A., Ironside, J.W., Rebus, S., Donaldson, Y.K., Simmonds, P. & Peutherer, J.F. (1993), HIV-1 and the brain: Investigation of virus load and neuropathologic changes in pre-AIDS subjects. J. Infect. Dis., 168, 818-824.
79. [79] Moses, A.V., Stenglein, S.G., Strussberg, J.G., Wehrly K., Chesebro, B. & Nelson, J.A.(1996), Sequences regulating tropism of HIV-1 for brain capillary endothelial cells map to a unique region on the viral genome. J. Virol., 6, 3401-3406.
80. [80] Connor, R.I. & Ho, D.D. (1994), Human immunodeficiency virus type 1 variants with increased replicative capacity develop during the asymptomatic stage before disease progression. J. Virol., 68 (7), 4400-4408.
81. [81] Mellors, J.W., Munoz, A., Giorgi, J.V., Margolick, J.B., Tassoni, C.J., Gupta, P., Kingsley, L.A., Todd, J.A., Saah, A.J., Detels, R., Phair, J.P. & Rinaldo, C.R., Jr. (1997), Plasma viral load and CD4+ lymphocytes as prognostic markers of HIV-1 infection. Ann. Intern. Med., 126 (12), 946-954.
82. [82] Toggas, S.M. & Mucke, L. (1998), Transgenic models to assess the potential of viral products in HIV-1 associated CNS disease, in "Neurology of AIDS" (Howard Gendelman et al.) (pp. 156-167). Chapman & Hall.
83. [83] Lazarini, F., Seilhean, D., Rosenblum, O., Suarez, S., Conquy, L. & Uchihara, T. (1997), HIV-1 DNA and RNA load in brains of demented and non-demented patients with AIDS. J. Neurovirol., 3 (4) 299-303.
84. [84] Epstein, L.G & Gendelman, H.E. (1993), Human immunodeficiency virus type 1 infection of the nervous system: Pathogenic mechanisms. Ann. Neurol., 33, 429-436.
85. [85] Toggas, S.M., Masliah, E., Rockenstein, E.M., Rall, G.F., Abraham, C.R. & Mucke, L. (1994), Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature, 367 (6459), 188-193.
86. [86] Brenneman, D.E., Westbrook, G.L. & Fitzgerald, S.P. (1988), Neuronal cell killing by the envelope protein of HIV and its prevention by vasoactive intestinal peptide. Nature, 355, 639-642.
87. [87] Lipton, S.A., Sucher, N.J., Kaiser, P.K. & Dreyer, E.B. (1991), Synergistic effects of HIV coat protein and NMDA receptor-mediated neurotoxicity. Neuron, 7 (1), 111-118.
88. [88] Savio, T. & Levi, G. (1993), Neurotoxicity of HIV coat protein gp120, NMDA receptors, and protein kinase C: a study with rat cerebellar granule cell cultures. J. Neurosci. Res., 34 (3), 265-272.
89. [89] Aggoun-Zouaoui, D., Charriaut-Marlangue, C., Rivera, S., Jorquera, I., Ben-Ari, Y. & Represa, A. (1996), The HIV-1 envelope protein gp120 induces neuronal apoptosis in hippocampal slices. Neuroreport, 1 (2), 433-436.
90. [90] Brooke, S., Chan, R., Howard, S. & Sapolsky, R. (1997), Endocrine-modulation of the neurotoxicity of gp120: implications for AIDS related dementia complex. PNAS, 94 (17), 9457-9462.
91. [91] Robbins, D.S., Shirazi, Y., Drysdale, B.E., Lieberman, A., Shin, H.S. & Shin, M.L. (1987), Production of cytotoxic factor for oligodendrocytes by stimulated astrocytes. J. Immunol., 139 (8), 2593-2597.
92. [92] Selmaj, KW. & Raine, C.S. (1988), Tumor necrosis factor mediates myelin and oligodendrocyte damage in vitro. Ann. Neurol., 23 (4), 339-346.
93. [93] Rutka, J.T. & Smith, S.L. (1993), Transfection of human astrocytoma cells with glial fibrillary acidic protein complementary DNA : analysis of expression, proliferation, and tumorigenicity. Cancer Res., 53 (15), 3624-3631.
94. [94] Selmaj, K., Shafit-Zagardo, B., Aquino, D.A., Farooq, M., Raine, C.S., Norton, W.T. & Brosnan, C.F. (1991), Tumor necrosis factor-induced proliferation of astrocytes from mature brain is associated with down-regulation of glial fibrillary acidic protein mRNA. J. Neurochem., 57 (3), 823-830.
95. [95] Tyor, W.R., Glass, J.D., Baumrind, N., McArthur, J.C., Griffin, J.W., Becker, P.S. & Griffin, D.E. (1993), Cytokine expression of macrophages in HIV-1-associated vacuolar myelopathy. Neurology, 43 (5), 1002-1009.