Neuronal death induced by brain-derived human immunodeficiency virus type 1 envelope genes differs between demented and nondemented AIDS patients

Journal of Virology

Volumn 72, Issue 11, 1998, Pages 9045-9053

  Power, C ^a,f   Mcarthur, J C ^b,c   Nath, A ^d   Wehrly, K ^e   Mayne, M ^a   Nishio, J ^e   Langelier, T ^a   Johnson, R T ^b   Chesebro, B ^e  

^a UNIVERSITY OF MANITOBA   (Canada)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^f UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NERVE DEGENERATION; PRIORITY JOURNAL; VIRUS DETECTION; VIRUS ENVELOPE; VIRUS GENOME; VIRUS REPLICATION;

EID: 0031690759     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.11.9045-9053.1998     Document Type: Article

References (71)

1. Adamson, D. C., T. M. Dawson, M. C. Zink, J. E. Clements, and V. L. Dawson. 1996. Neurovirulent simian immunodeficiency virus infection induces neuronal, endothelial, and glial apoptosis. Mol. Med. 2:417-428.
2. Adamson, D. C., B. Wildemann, M. Sasaki, J. D. Glass, J. C. McArthur, V. I. Christov, T. M. Dawson, and V. L. Dawson. 1996. Immunologic NO synthase: elevation in severe AIDS dementia and induction by HIV-1 gp41. Science 274:1917-1921.
3. Barks, J. D. E., X.-H. Liu, R. Sun, and F. S. Silverstein. 1996. gp120, a human immunodeficiency virus-1 coat protein, augments excitotoxic hippocampal injury in perinatal rats. Neuroscience 76:397-409.
4. Bell, J. E., A. Busuttil, J. W. Ironside, S. Rebus, Y. K. Donaldson, P. Simmonds, and J. F. Peutherer. 1993. Human immunodeficiency virus and the brain: investigations of virus load and neuropathologic changes in pre-AIDS subjects. J. Infect. Dis. 168:818-824.
5. Cheng-Mayer, C., R. Liu, N. R. Landau, and L. Stamalatos. 1997. Macrophage tropism and human immunodeficiency virus type 1 and utilization of the CC-CKR5 coreceptor. J. Virol. 71:1657-1661.
6. Chesebro, B., J. Nishio, S. Perryman, A. Cann, W. O'Brien, I. S. Y. Chen, and K. Wehrly. 1991. Identification of human immunodeficiency virus envelope gene sequences influencing viral entry into CD4-positive HeLa cells, T-leukemia cells, and macrophages. J. Virol. 65:5782-5789.
7. Chesebro, B., and K. Wehrly. 1988. Development of a sensitive quantitative focal assay for human immunodeficiency virus infectivity. J. Virol. 62:3779-3788.
8. Chesebro, B., K. Wehrly, J. Metcalf, and D. E. Griffin. 1991. Use of a new CD4-positive HeLa cell clone for direct quantification of infectious human immunodeficiency virus from blood cells of AIDS patients. J. Infect. Dis. 163:64-70.
9. Chesebro, B., K. Wehrly, J. Nishio, and S. Perryman. 1992. Macrophagetropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism. J. Virol. 66:6547-6554.
10. Chesebro, B., K. Wehrly, J. Nishio, and S. Perryman. 1996. Mapping of independent V3 envelope determinants of human immunodeficiency virus type 1 macrophage tropism and syncytium formation in lymphocytes. J. Virol. 70:9055-9059.
11. Cunningham, A. L., H. Naif, N. Saksena, G. Lynch, J. Chang, S. Li, R. Jozwiak, M. Alali, B. Wang, W. Fear, A. Sloane, L. Pemberton, and B. Brew. 1996. HIV-1 infection of macrophages and pathogenesis of AIDS dementia complex: interaction of the host cell and viral genotype. J. Leukoc. Biol. 62:117-125.
12. Dawson, V. L., T. M. Dawson, G. R. Uhl, and S. H. Snyder. 1993. Human immunodeficiency virus type 1 coat protein neurotoxicity mediated by nitric oxide in primary cortical cultures. Proc. Natl. Acad. Sci. USA 90:3256-3259.
13. Dietzschold, B., W. H. Wunner, T. J. Wiktor, A. D. Lopes, M. Lafon, C. L. Smith, and H. Koprowski. 1983. Characterization of an antigenic determinant of the glycoprotein that correlates with pathogenicity of rabies virus. Proc. Natl. Acad. Sci. USA 80:70-74.
14. Dreyer, E. B., P. K. Kaiser, J. T. Offermann, and S. A. Lipton. 1990. HIV-1 coat protein neurotoxicity prevented by calcium channel antagonists. Science 248:364-367.
15. Ferrari, G., A. Batistatou, and L. A. Greene. 1993. Ganglosides rescue neuronal cells from death after factor deprivation. J. Neurosci. 13:1879-1887.
16. Gartner, S., P. Markovits, D. M. Markovitz, M. H. Kaplan, R. C. Gallo, and M. Popovic. 1986. The role of mononuclear phagocytes in HTLV-III/LAV infection. Science 233:215-219.
17. Giulian, D., K. Vaga, and C. A. Noonan. 1990. Secretion of neurotoxins by mononuclear phagocytes infected with HIV-1. Science 250:1593-1596.
18. Giulian, D., E. Wendt, K. Vaca, and C. A. Noonan. 1993. The envelope glycoprotein of human immunodeficiency virus type 1 stimulates release of neurotoxins from monocytes. Proc. Natl. Acad. Sci. USA 90:2769-2773.
19. Giulian, D., J. Yu, X. Li, D. Tom, J. Li, E. Wendt, S. N. Lin, R. Schwarcz, and C. Noonan. 1996. Study of receptor-mediated neurotoxins released by HIV-1-infected mononuclear phagocytes found in human brain. J. Neurosci. 16: 3139-3153.
20. Glass, J. D., H. Fedor, S. L. Wesselingh, and J. C. McArthur. 1995. Immunocytochemical quantitation of human immunodeficiency virus in the brain: correlations with dementia. Ann. Neurol. 38:755-762.
21. Groenink, M., R. A. M. Fouchier, S. Broersen, C. H. Baker, M. Koot, A. B. van't Wout, H. G. Huisman, F. Miedema, M. Tersmette, and H. Schuitemaker. 1993. Relation of phenotype evolution of HIV-1 to envelope V2 configuration. Science 260:1533-1516.
22. Hasenkrug, K. J., S. J. Robertson, J. Porti, F. McAtee, J. Nishio, and B. Chesebro. 1996. Two separate envelope regions influence induction of brain disease by a polytropic murine retrovirus (FMCF98). J. Virol. 70:4825-4828.
23. Jordan, C. A., B. A. Watkins, C. Kufta, and M. Dubois-Dalcq. 1991. Infection of brain microglial cells by human immunodeficiency virus type 1 is CD4 dependent. J. Virol. 65:736-742.
24. Karlsson, A. K., E. Parsmyr, E. Sandstrom, E. M. Fenyo, and J. Albert. 1994. MT-2 cell tropism as prognostic marker for disease progression in human immunodeficiency virus type 1 infection. J. Clin. Microbiol. 32:364-370.
25. Kodama, T., K. Mori, T. Kawahara, D. J. Ringler, and R. C. Desrosiers. 1993. Analysis of simian immunodeficiency virus sequence variation in tissues of rhesus macaques with simian AIDS. J. Virol. 67:6522-6534.
26. Koenig, S., H. E. Gendelman, J. M. Orenstein, M. C. Dal Canto, G. H. Pezeshpour, M. Yungbluth, K. Janotta, A. Akasimit, M. A. Martin, and A. S. Fauci. 1986. Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089-1093.
27. Koito, A., G. Harrowe, J. A. Levy, and C. Cheng-Mayer. 1994. Functional role of the V1/V2 region of human immunodeficiency virus type 1 envelope glycoprotein gp120 in infection of primary macrophages and soluble CD4 neutralization. J. Virol. 68:2253-2259.
28. Kong, L.-Y., B. C. Wilson, M. K. McMillian, G. Bing, P. M. Hudson, and J.-S. Hong. 1996. The effects of the HIV-1 envelope protein gp120 on the production of nitric oxide and proinflammatory cytokines in mixed glial cell cultures. Cell. Immunol. 172:77-83.
29. Koyanagi, Y., S. Miles, R. T. Mitsuyasu, J. E. Merrill, H. V. Vinters, and I. S. Y. Chen. 1987. Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236:819-822.
30. Kumar, S., K. Tamura, and M. Nei. 1994. MEGA: Molecular Evolutionary Genetics Analysis software for microcomputers. Comput. Appl. Biosci. 10: 189-191.
31. Lane, T. E., M. J. Buchmeier, D. D. Watry, D. B. Jakubowski, and H. S. Fox. 1995. Serial passage of microglial SIV results in selection of homogeneous env quasispecies in the brain. Virology 212:458-465.
32. Lipton, S. D., and H. E. Gendelman. 1995. Dementia associated with the acquired immunodeficiency syndrome. N. Engl. J. Med. 332:934-940.
33. Mankowski, J. L., M. T. Flaherty, J. P. Spelman, D. A. Hauer, P. J. Didier, A. M. Amadee, M. Murphey-Corb, L. M. Kirstein, A. Munoz, J. E. Clements, and M. C. Zink. 1997. Pathogenesis of simian immunodeficiency virus encephalitis: viral determinants of neurovirulence. J. Virol. 71:6055-6060.
34. Masuda, M., C. A. Hanson, W. G. Alvord, P. M. Hoffman, S. K. Ruscetti, and M. Masuda. 1996. Effects of subtle changes in the SU protein of ecotropic murine leukemia virus on its capillary endothelial cell tropism and interference proteins. Virology 215:142-151.
35. McArthur, J. C., D. R. Hoover, H. Bacellar, E. N. Miller, B. A. Cohen, J. T. Becker, N. M. H. Graham, J. H. McArthur, O. A. Seines, L. P. Jacobson, B. R. Visscher, M. Concha, and A. Saab. 1993. Dementia in AIDS patients: incidence and risk factors. Neurology 43:2245-2252.
36. McNearney, T., Z. Hornickova, R. Markham, A. Birdwell, M. Arens, A. Saah, and L. Ratner. 1992. Relationship of human immunodeficiency virus type 1 sequence heterogeneity to stage of disease. Proc. Natl. Acad. Sci. USA 89:10247-10251.
37. Meeker, R., R. English, and M. Tompkins. 1996. Enhanced excitoxicity in primary feline neural cultures exposed to feline immunodeficiency virus (FIV). J. NeuroAIDS 1:1-27.
38. Myers, G. 1995. Human retroviruses and AIDS. A compilation and analysis of nucleic acid and amino acid sequences. Theoretical Biology and Biophysics Group T-10, Los Alamos National Library, Los Alamos, N.Mex.
39. Namboodiri, A. M., C. N. Venkateshan, R. Narayanan, K. Blinder, J. R. Moffett, D. C. Gajdusek, M. Gravell, and C. J. Gibbs, Jr. 1996. Increased quinolinate immunoreactivity in the peripheral blood monocytes/macrophages from SIV-infected monkeys. J. Neurovirol. 2:433-438.
40. Nath, A., K. Psooy, C. Martin, B. Knudsen, D. S. Magnuson, N. Haughey, and J. D. Geiger. 1996. Identification of a human immunodeficiency virus type 1 Tat epitope that is neuroexcitatory and neurotoxic. J. Virol. 70:1475-1480.
41. O'Brien, W. A., Y. Koyanagi, A. Namazie, J. Q. Zhao, A. Diagne, K. Idler, J. A. Zack, and I. S. Y. Chen. 1990. HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 348:69-73.
42. Paquette, Y., Z. Hanna, P. Savard, R. Brousseau, Y. Robitaille, and P. Jolicoeur. 1989. Retrovirus-induced murine motor neuron disease: mapping the determinant of spongiform degeneration within the envelope gene. Proc. Natl. Acad. Sci. USA 86:3896-3900.
43. Pawley, A. C., S. Flesher, R. J. Beninger, and K. H. Jhamamanda. 1996. Different actions of NMDA antagonists on cholinergic neurotoxicity produced by N-methyl-D-aspartate and quiniolinc acid. Br. J. Pharmacol. 117: 1059-1064.
44. Platt, E. J., K. Wehrly, S. E. Kuhmann, B. Chesebro, and D. Kabat. 1998. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophage-tropic isolates of human immunodeficiency virus type 1. J. Virol. 72:2855-2864.
45. Poulsen, D. J., S. J. Robertson, C. A. Favara, J. L. Portis, and B. Chesebro. 1998. Mapping of a neurovirulence determinant within the envelope protein of a polytropic murine retrovirus: induction of CNS disease by low levels of virus. Virology 248:199-207.
46. Power, C., P. A. Kong, T. O. Crawford, S. Wesselingh, J. D. Glass, J. C. McArthur, and B. D. Trapp. 1993. Cerebral white matter changes in acquired immunodeficiency syndrome dementia: alterations in the blood-brain barrier. Ann. Neurol. 34:339-350.
47. Power, C., J. C. McArthur, R. T. Johnson, D. E. Griffin, J. D. Glass, R. Dewey, and B. Chesebro. 1995. Distinct HIV-1 env sequences are associated with neurotropism and neurovirulence. Curr. Top. Microbiol. Immunol. 202: 89-104.
48. Power, C., J. C. McArthur, R. T. Johnson, D. E. Griffin, J. D. Glass, S. Perryman, and B. Chesebro. 1994. Demented and nondemented patients with AIDS differ in brain-derived human immunodeficiency virus type 1 envelope sequences. J. Virol. 68:4643-4649.
49. Price, R. W., and B. J. Brew. 1988. The AIDS dementia complex. J. Infect. Dis. 158:1079-1083.
50. Pulliam, L., B. G. Herndier, N. M. Tang, and M. S. McGrath. 1991. Human immunodeficiency virus-infected macrophages produce soluble factors that cause histological and neurochemical alterations in cultured human brains. J. Clin. Investig. 87:503-512.
51. Reddy, R. T., C. L. Achim, D. A. Sirko, S. Tehranchi, F. G. Kraus, F. Wong Staal, and C. A. Wiley. 1996. Sequence analysis of the V3 loop in brain and spleen of patients with HIV encephalitis. AIDS Res. Hum. Retroviruses 12:477-482.
52. Robertson, S., K. Hasenkrug, B. Chesebro, and J. Portis. 1997. Neurologic disease induced by polytropic murine retroviruses: neurovirulence determined by efficiency of spread to microglial cells. J. Virol. 71:5287-5294.
53. Schuitemaker, H. M., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. de Goede, R. P. van Steenwijk, J. M. Lange, J. K. Schttenkerk, F. Miedema, and M. Tersmette. 1992. Biological phenotype of human immunodeficiency virus type 1 variants detectable at all stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus populations. J. Virol. 66:1354-1360.
54. Shioda, T., J. A. Levy, and C. Cheng-Mayer. 1992. Small amino acid changes in the V3 hypervariable region of gp120 can affect the T-cell-line and macrophage tropism of human immunodeficiency virus type 1. Proc. Natl. Acad. Sci. USA 89:9434-9438.
55. Shioda, T., S. Oka, X. Xin, H. Liu, R. Harukuni, A. Kurotani, M. Fukushima, M. K. Hasan, T. Shiino, Y. Takebe, A. Iwamoto, and Y. Nagai. 1997. In vivo sequence variability of human immunodeficiency virus type 1 envelope gp120: association of V2 extension with slow disease progression. J. Virol. 71:4871-4881.
56. Speck, R., K. Wehrly, E. J. Platt, R. E. Atchison, I. F. Charo, D. Kabat, B. Chesebro, and M. Goldsmith. 1997. Selective employment of chemokine receptors as human immunodeficiency virus type 1 coreceptors determined by individual amino acids within the envelope V3 loop. J. Virol. 71:7136-7139.
57. Stephens, E. B., S. Mukherjee, M. Sahni, W. Zhuge, R. Raghavan, D. K. Singh, K. Leung, B. Atkinson, Z. Li, S. V. Joag, Z. Q. Liu, and O. Narayan. 1997. A cell-free stock of simian-human immunodeficiency virus that causes AIDS in pig-tailed macaques has a limited number of amino acid substitutions in both SIVmac and HIV-1 regions of the genome and has altered cytotropism. Virology 231:313-321.
58. Stoler, M. H., T. A. Eskin, S. Benn, R. C. Angerer, and L. M. Angerer. 1986. Human T-cell lymphotropic virus type III infection of the central nervous system. A preliminary in situ analysis. JAMA 256:2360-2364.
59. Strizki, J. M., A. V. Albright, H. Sheng, M. O'Connor, L. Perrin, and F. Gonzalez-Scarano. 1996. Infection of primary human microglia and monocyte-derived macrophages with human immunodeficiency virus type 1 isolates: evidence of differential tropism. J. Virol. 70:7654-7662.
60. env alters the neurovirulence of ts1, a mutant of Moloney murine leukemia virus TB. J. Virol. 54:5241-5249.
61. Takahashi, K., S. L. Wesselingh, D. E. Griffin, J. C. McArthur, R. T. Johnson, and J. D. Glass. 1996. Localization of HIV-1 in human brain using polymerase chain reaction/in situ hybridization and immunocytochemistry. Ann. Neurol. 39:705-711.
62. Thomas, F. P., C. Chalk, R. Lalonde, Y. Robitaille, and P. Jolicoeur. 1994. Expression of human immunodeficiency virus type 1 in the nervous system of transgenic mice leads to neurological disease. J. Virol. 68:7099-7107.
63. Toggas, S. M., E. Masliah, E. M. Rockenstein, G. F. Rall, C. R. Abraham, and L. Mucke. 1994. Central nervous system damage produced by expression of the HIV-1 coat protein gp120 in transgenic mice. Nature 367:188-193.
64. Toohey, K., K. Wehrly, J. Nishio, S. Perryman, and B. Chesebro. 1995. Human immunodeficiency virus envelope V1 and V2 regions influence replication efficiency in macrophages by affecting virus spread. Virology 213: 70-79.
65. Tucker, P. C., E. G. Strauss, R. J. Kuhn, J. H. Strauss, and D. E. Griffin. 1993. Viral determinants of age-dependent virulence of Sindbis virus for mice. J. Virol. 67:4605-4610.
66. Tyor, W. R., C. Power, H. E. Gendelman, and R. B. Markham. 1993. A model of human immunodeficiency virus encephalitis in SCID mice. Proc. Natl. Acad. Sci. USA 90:8658-8662.
67. Wang, W. K., M. Essex, and T. H. Lee. 1995. The highly conserved aspartic acid residue between hypervariable regions 1 and 2 of human immunodeficiency virus type 1 gp120 is important for early stages of virus replication. J. Virol. 69:538-542.
68. Wesselingh, S. L., C. Power, J. D. Glass, W. R. Tyor, J. C. McArthur, J. M. Farber, J. W. Griffin, and D. E. Griffin. 1993. Intracerebral cytokine messenger RNA expression in acquired immunodeficiency syndrome dementia. Ann. Neurol. 33:576-582.
69. Westervelt, P., D. B. Trowbridge, L. G. Epstein, B. M. Blumberg, Y. Li, B. H. Hahn, G. M. Shaw, R. W. Price, and L. Ratner. 1992. Macrophage tropism determinants of human immunodeficiency virus type 1 in vivo. J. Virol. 66:2577-2582.
70. Wiley, C. A., R. D. Schrier, J. A. Nelsen, P. W. Lampert, and M. B. Oldstone. 1986. Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proc. Natl. Acad. Sci. USA 83:7089-7093.
71. Wong, P. K., E. Floyd, and Szurek. 1991. High susceptibility of FV/N mice to the paralytic disease induced by ts1, a mutant of Moloney murine leukemia virus TB. Virology 180:365-371.