Determinants of syncytium formation in microglia by human immunodeficiency virus type 1: Role of the V1/V2 domains

Journal of Virology

Volumn 74, Issue 2, 2000, Pages 693-701

  Shieh, Joseph T C ^a   Martín, Julio ^a   Baltuch, Gordon ^a   Malim, Michael H ^a   González Scarano, Francisco ^a,b  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CD4 ANTIGEN; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CCR5; GLYCOPROTEIN GP 120; VIRUS ENVELOPE PROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; CONTROLLED STUDY; DEMENTIA; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MICROGLIA; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SYNCYTIUM; VIRUS REPLICATION;

ADULT; ANTIGENS, CD4; CELL FUSION; CELL LINE, TRANSFORMED; CELLS, CULTURED; CHROMOSOME MAPPING; GENE PRODUCTS, ENV; GIANT CELLS; HIV-1; HUMANS; LEUKOCYTES, MONONUCLEAR; MICROGLIA; PHENOTYPE; RECEPTORS, CCR5; RECOMBINATION, GENETIC; TUMOR CELLS, CULTURED; VIRUS REPLICATION;

EID: 0033986315     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.2.693-701.2000     Document Type: Article

References (76)

1. Albright, A. V., J. T. C. Shieh, T. Itoh, B. Lee, D. Pleasure, M. J. O'Connor, R. W. Doms, and F. Gonzalez-Scarano. 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.
2. Andersen, K. B. 1994. A domain of murine retrovirus surface protein gp70 mediates fusion, as shown in a novel SC-1 cell fusion system. J. Virol. 68: 3175-3182.
3. Atchison, R. E., J. Gosling, F. S. Monteclaro, C. Franci, L. Digilio, I. F. Charo, and M. A. Goldsmith. 1996. Multiple extracellular elements of CCR5 and HIV-1 entry: dissociation from response to chemokines. Science 274: 1924-1926.
4. Bieniasz, D., R. A. Fridell, I. Aramori, S. S. G. Ferguson, M. G. Caron, and B. R. Cullen. 1997. HIV-1-induced cell fusion is mediated by multiple regions within the viral envelope and the CCR-5 co-receptor. EMBO J. 16: 2599-2609.
5. Boyd, M. T., G. R. Simpson, A. J. Cann, M. A. Johnson, and R. A. Weiss. 1993. A single amino acid substitution in the V1 loop of human immunodeficiency virus type 1 gp120 alters cellular tropism. J. Virol. 67:3649-3652.
6. Brew, B. J., L. Evans, C. Byrne, L. Pemberton, and L. Hurren. 1996. The relationship between AIDS dementia complex and the presence of macrophage tropic and non syncytium inducing isolates of human immunodeficiency virus type 1 in the cerebrospinal fluid. J. Neuruvirol. 2:152-157.
7. Cao, J., N. Sullivan, E. Desjardin, C. Parolin, J. Robinson, R. Wyatt, and J. Sodroski. 1997. Replication and neutralization of human immunodeficiency virus type 1 lacking the V1 and V2 variable loops of the gp120 envelope glycoprotein. J. Virol. 71:9808-9812.
8. Carillo, A., and L. Ratner. 1996. Cooperative effects of the human immunodeficiency virus type 1 envelope variable loops V1 and V3 in mediating infectivity for T cells. J. Virol. 70:1310-1316.
9. Chackerian, B., E. M. Long, P. A. Luciw, and J. Overbaugh. 1997 Human immunodeficiency virus type 1 coreceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 71:3932-3939.
10. Chan, S. Y., R. F. Speck, C. Power, S. L. Gaffen, B. Chesebro, and M. A. Goldsmith. 1999. V3 recombinants indicate a central role for CCR5 as a coreceptor in tissue infection by human immunodeficiency virus type 1. J. Virol. 73:2350-2358.
11. SF33A variant in vivo by virtue of sequence changes in the extracellular envelope glycoprotein that modify N-linked glycosylation. J. Virol. 73:5294-5300.
12. Choe, H., M. Farzan, Y. Sun, N. Sullivan, B. Rollins, P. D. Ponath, J. Wu, C. R. Mackay, G. LaRosa, W. Newman, N. Gerard, C. Gerard, and J. Sodroski. 1996. The b-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85:1135-1148.
13. Clark, S. J., M. S. Saag, W. D. Decker, S. Campbell-Hill, J. L. Roberson, P. J. Veldkamp, J. C. Kappes, B. H. Hahn, and G. M. Shaw. 1991. High titers of cytopathic virus in plasma of patients with symptomatic primary HIV-1 infection. N. Engl. J. Med. 324:954-960.
14. Clavel, F., and P. Charneau. 1994. Fusion from without directed by human immunodeficiency virus particles. J. Virol. 68:1179-1185.
15. Collman, R., J. W. Balliet, S. A. Gregory, H. Friedman, D. L. Kolson, N. Nathanson, and A. Srinivasan. 1992. An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. J. Virol. 66:7517-7521.
16. Deng, H., R. Liu, W. Ellmeier, S. Choe, D. Unutmaz, M. Burkhart, P. Di Marzio, S. Marmon, R. E. Sutton, C. M. Hill, C. B. Davis, S. C. Peiper, T. J. Schall, D. R. Littman, and N. R. Landau. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666.
17. Dick, A. D., M. Pell, B. J. Brew, E. Foulcher, and J. D. Sedgwick. 1997. Direct ex vivo flow cytometric analysis of human microglial cell CD4 expression: examination of central nervous system biopsy specimens from HIV-seropositive patients and patients with other neurological disease. AIDS 11:1699-1708.
18. Di Stefano, M., S. Wilt, F. Gray, M. Dubois-Dalcq, and F. Chiodi. 1996. HIV type 1 V3 sequences and the development of dementia during AIDS. AIDS Res. Hum. Retrovir. 12:471-476.
19. Dragic, T., A. Trkola, S. W. Lin, K. A. Nagashima, F. Kajumo, L. Zhao, W. C. Olson, L. Wu, C. R. Mackay, G. P. Allaway, T. P. Sakmar, J. P. Moore, and P. J. Maddon. 1998. Amino-terminal substitutions in the CCR5 coreceptor impair gp120 binding and human immunodeficiency virus type 1 entry. J. Virol. 72:279-285.
20. Dumonceaux, J., S. Nisole, C. Chanel, L. Quivet, A. Amara, F. Baleux, P. Briand, and U. Hazan. 1998. Spontaneous mutations in the env gene of the human immunodeficiency virus type 1 NDK isolate are associated with a CD4-independent entry phenotype. J. Virol. 72:512-519.
21. Edinger, A. L., J. L. Mankowski, B. J. Doranz, B. J. Margulies, B. Lee, J. Rucker, M. Sharron, T. L. Hoffman, J. F. Berson, M. C. Zink, V. M. Hirsch, J. E. Clements, and R. W. Doms. 1997. CD4-independent, CCR5-dependent infection of brain capillary endothelial cells by a neurovirulent simian immunodeficiency virus strain. Proc. Nail. Acad. Sci. USA 94:14742-14747.
22. Endres, M. J., P. R. Clapham, M. Marsh, M. Ahuja, J. D. Turner, A. McKnight, J. F. Thomas, B. Stoebenau-Haggerty, S. Choe, P. J. Vance, T. N. Wells, C. A. Power, S. S. Sutterwala, R. W. Doms, N. R. Landau, and J. A. Hoxie. 1996. CD4-independent infection by HIV-2 is mediated by fusin/ CXCR4. Cell 87:745-756.
23. Epstein, L. G., C. Kuiken, B. M. Blumberg, S. Hartman, L. R. Sharer, M. Clement, and J. Goudsmit. 1991. HIV-1 V3 domain variation in brain and spleen of children with AIDS: tissue-specific evolution within host-determined quasispecies. Virology 180:583-590.
24. Farzan, M., T. Mirzabekov, P. Kolchinsky, R. Wyatt, M. Cayabyab, N. P. Gerard, C. Gerard, J. Sodroski, and H. Choe. 1999. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96:667-676.
25. Gabuzda, D., J. He, A. Ohagen, and A. V. Vallat. 1998. Chemokine receptors in HIV-1 infection of the central nervous system. Semin. Immunol. 10: 203-213.
26. Ghorpade, A., M. Q. Xia, B. T. Hyman, Y. Persidsky, A. Nukuna, P. Bock, M. Che, J. Limoges, H. E. Gendelman, and C. R. MacKay. 1998. Role of the beta-chemokine receptors CCR3 and CCRS in human immunodeficiency virus type 1 infection of monocytes and microglia. J. Virol. 72:3351-3361.
27. Glass, J. D., S. L. Wesselingh, O. A. Selnes, and J. C. McArthur. 1993. Clinical-neuropathological correlation in HIV-associated dementia. Neurology 43:2230-2237.
28. Gonzalez-Scarano, F., N. Pobjecky, and N. Nathanson. 1984. La Crosse bunyavirus can mediate pH-dependent fusion from without. Virology 132: 222-225.
29. Harrington, R. D., and A. P. Geballe. 1993. Cofactor requirement for human immunodeficiency virus type 1 entry into a CD4-expressing human cell line. J. Virol. 67:5939-5947.
30. He, J., Y. Chen, M. Farzan, H. Choe, A. Ohagen, S. Gatner, J. Busciglio, X. Yang, W. Hofmann, W. Newman, C. R. Mackay, J. Sodroski, and D. Gabuzda. 1997. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385:645-649.
31. Hoffman, T. L., C. C. LaBranche, W. Zhang, G. Canziani, J. Robinson, I. Chaiken, J. A. Hoxie, and R. W. Doms. 1999. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein. Proc. Natl. Acad. Sci. USA 96:6359-6364.
32. Hoffman, T. L., E. B. Stephens, O. Narayan, and R. W. Doms. 1998. HIV type 1 envelope determinants for use of the CCR2b, CCR3, STRL33, and APJ coreceptors. Proc. Natl. Acad. Sci. USA 95:11360-11365.
33. Hwang, S. S., T. J. Boyle, H. K. Lyerly, and B. R. Cullen. 1991. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science 253:71-74.
34. Ioannidis, J. P. A., S. Reichlin, and P. R. Skolnik. 1995. Long-term productive human immunodeficiency virus-1 infection in human infant microglia. Am. J. Pathol. 147:1200-1206.
35. Keys, B., J. Karis, B. Fadeel, A. Valentin, G. Norkrans, L. Hagberg, and F. Chiodi. 1993. V3 sequences of paired HIV-1 isolates from blood and CSF cluster according to host and show variation related to the clinical stage of disease. Virology 196:475-483.
36. Koito, A., G. Harrowe, J. A. Levy, and C. Cheng-Mayer. Functional role of the V1/V2 region of human immunodeficiency virus type 1 envelope glycoprotein in infection of primary macrophages and soluble CD4 neutralization. J. Virol. 68:2253-2259.
37. Korber, B. T. M., K. J. Kunstman, B. K. Patterson, M. Furtado, M. M. McEvilly, R. Levy, and S. M. Wolinsky. 1994. Genetic differences between blood-and brain-derived viral sequences from human immunodeficiency virus type 1-infected patients: evidence of conserved elements in the V3 region of the envelope protein of brain-derived sequences. J. Virol. 68: 7467-7481.
38. Koyanagi, Y., S. Miles, R. T. Mitsuyasu, J. T. Merrill, H. V. Vinters, and I. S. Y. Chen. 1987. Dual infection of the central nervous system by AIDS virus with distinct cellular tropisms. Science 236:819-822.
39. Kozak, S. L, E. J. Platt, N. Madani, F. E. Ferro, K. Peden, and D. Kabat. 1997. CD4, CXCR-4, and CCR-5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1. J Virol. 71:873-882.
40. LaCasse, R. A., K. E. Follis, M. Trahey, J. D. Scarborough, D. R. Liftman, and J. H. Nunnerg. 1999. Fusion-competent vaccines: broad neutralization of primary isolates of HIV. Science 283:357-362.
41. Lee, B., M. Sharron, C. Blanpain, B. J. Doranz, J. Vakili, P. Setoh, E. Berg, G. Liu, H. R. Guy, S. R. Drell, M. Parmentier, C. N. Chang, K. Price, M. Tsang, and R. W. Doms. 1999. Epitope mapping of CCR5 reveals multiple conformational states and distinct overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274:9617-9626.
42. Lee, S. C., C. Hatch, W. Liu, Y. Kress, B. D. Lyman, and D. W. Dickson. 1993. Productive infection of human fetal microglia by HIV-1. Am. J. Pathol. 143:1032-1039.
43. Lipton, S. A., and H. E. Gendelman. 1995. Dementia associated with the acquired immunodeficiency syndrome. N. Engl. J. Med. 332:934-940.
44. Mondor, I., M. Moulard, S. Ugolini, P. J. Klasse, J. Hoxie, A. Amara, T. Delaunay, K. Wyatt, J. Sodroski, and Q. J. Sattentau. 1998. Interactions among HIV gp120, CD4, and CXCR4: dependence on CD4 expression level, gp120 viral origin, conservation of the gp120 COOH-and NH2-termini and V1/V2 and V3 loops, and sensitivity to neutralizing antibodies. Virology 248: 394-405.
45. Morikita, T., Y. Maeda, S.-I. Fujii, S. Matsushita, K. Obaru, and K. Takatsuki. 1997. The VI/V2 region of Human Immunodeficiency Virus type 1 modulates the sensitivity to neutralization by soluble CD4 and cellular tropism. AIDS Res. Hum. Retrovir. 13:1291-1298.
46. Nussbaum, O., C. C. Broder, and E. A. Berger. 1994. Fusogenic mechanisms of enveloped-virus glycoproteins analyzed by a novel recombinant vaccinia virus-based assay quantitating cell fusion-dependent reporter gene activation. J. Virol. 68:5411-5418.
47. Palmer, C., P. Balfe, D. Fox, J. C. May, R. Frederiksson, E.-M. Fenyo, and J. A. McKeating. 1996. Functional characterization of the V1V2 region of Human Immunodeficiency Virus type 1. Virology 220:436-449.
48. Platt, E. J., N. Madani. S. L. Kozak, and D. Kabat. 1997. Infectious properties of human immunodeficiency virus type 1 mutants with distinct affinities for the CD4 receptor. J. Virol. 71:883-890.
49. 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.
50. Power, C., J. C. McArthur, A. Nath, K. Wehrly, M. Mayne, J. Nishio, T. Langelier, R. T. Johnson, and B. Chesebro. 1998. Neuronal death induced by brain-derived human immunodeficiency virus type 1 envelope genes differs between demented and nondemented AIDS patients. J. Virol. 72:9045-9053.
51. Price, R. W., B. Brew, J. Sidtis, J. Rosenblum, A. C. Scheck, and P. Cleary. 1988. The brain in AIDS: central nervous system HIV-1 infection and AIDS dementia complex. Science 239:586-591.
52. Reeves, J. D., and T. F. Schulz. 1997. The CD4-independent tropism of HIV-2 involves several regions of the envelope protein and correlates with a reduced activation threshold for envelope-mediated fusion. J. Virol. 71: 1453-1465.
53. Rizzuto, C. D., R. Wyatt, N. Hernandez-Ramos, Y. Sun, P. D. Kwong, W. A. Hendrickson, and J. Sodroski. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science 280:1949-1953.
54. Rucker, J., B. J. Doranz, A. L. Edinger, D. Long, J. F. Berson, and R. W. Doms. 1997. Cell-cell fusion assay to study role of chemokine receptors in Human Immunodeficiency Virus type 1 entry. Methods Enzymol. 288:118-133.
55. Rucker, J., M. Samson, B. J. Doranz, F. Libert, J. F. Berson, Y. Yi, R. J. Smyth, R. G. Collman, C. C. Broder, G. Vassart, R. W. Doms, and M. Parmentier. 1996. Regions in b-chemokine receptors CCR5 and CCR2b that determine HIV-1 cofactor specificity. Cell 87:437-446.
56. Saharkhiz-Langroodi, A., and T. C. Holland. 1997. Identification of the fusion-from-without determinants of Herpes Simplex Virus type 1 glycoprotein B. Virology 227:153-159.
57. Sharpless, N. E., W. A. O'Brien, E. Verdin, C. V. Kufla, I. S. Y. Chen, and M. Dubois-Dalcq. 1992. Human immunodeficiency virus type 1 tropism for brain microglial cells is determined by a region of the env glycoprotein that also controls macrophage tropism. J. Virol. 66:2588-2593.
58. Shieh, J. T. C., A. V. Albright, M. Sharron, S. Gartner, J. Strizki, R. W. Doms, and F. Gonzalez-Scarano. 1998. Chemokine receptor utilization by HIV-1 isolates that replicate in microglia. J. Virol. 72:4243-4249.
59. Siess, D. C., S. L. Kozak, and D. Kabat. 1996. Exceptional fusogenicity of Chinese hamster ovary cells with murine retroviruses suggests roles for cellular factor(s) and receptor clusters in the membrane fusion process. J. Virol. 70:3432-3439.
60. 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.
61. Sullivan, N., Y. Sun, Q. Sattentau, M. Thali, D. Wu, G. Denisova, J. Gershoni, J. Robinson, J. Moore, and J. Sodroski. 1998. CD4-induced conformational changes in the human immunodeficiency virus type 1 gp120 glycoprotein: consequences for virus entry and neutralization, J. Virol. 72: 4694-4703.
62. Sullivan, N., M. Thali, C. Furman, D. D. Ho, and J. Sodroski. 1993. Effect of amino acid changes in the V1/V2 region of the human immunodeficiency virus type 1 gp120 glycoprotein on subunit association, syncytium formation, and recognition by a neutralizing antibody. J. Virol. 67:3674-3679.
63. 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 immunocytochcmistry Ann. Neurol. 39:705-711.
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. Trkola, A., T. Dragic, J. Arthos, J. M. Binley, W. C. Olson, G. P. Allaway, C. Cheng-Mayer, J. Robinson, P. J. Maddon, and J. P. Moore. 1996. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR5. Nature 14:184-187.
66. Vodicka, M. A., W. C. Goh, L. I. Wu, M. E. Rogel, S. R. Bartz, V. L. Schweickart, C. J. Raport, and M. Emerman. 1997. Indicator cell lines for detection of primary strains of human and simian immunodeficiency viruses. Virology 233:193-198.
67. Watkins, B. A., H. H. Dorn, W. B. Kelly, R. C. Armstrong, B. J. Potts, F. Michaels, C. V. Kufta, and M. Dubois-Dalq. 1990. Specific tropism of HIV-1 for microglial cells in primary human brain cultures. Science 249:549-552.
68. Wiley, C. A., and C. L. Achim. 1994. Human immunodeficiency virus encephalitis is the pathological correlate of dementia in acquired immunodeficiency syndrome. Ann. Neurol. 36:673-676.
69. Wiley, C. A., R. D. Schrier, J. A. Nelson, P. W. Lampert, and M. B. A. 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.
70. Wong, J. K., C. C. Ignacio, F. Torriani, D. Havlir, N. J. S. Fitch, and D. D. Richman. 1997. In vivo compartmentalization of human immunodeficiency virus: evidence from the examination of pol sequences from autopsy tissues. J. Virol. 71:2059-2071.
71. Wu, L., W. A. Paxton, N. Kassam, N. Ruffing, J. B. Rottman, N. Sullivan, H. Choe, J. Sodroski. W. Newman, R. A. Koup, and C. R. Mackay. 1997. CCR5 levels and expression pattern correlate with infectability by macrophagetropic HIV-1, in vitro. J. Exp. Med. 185:1681-1691.
72. Wu, Z., S. C. Kayman, W. Honnen, K. Revesz, H. Chen, S. Vijh-Warrier, S. A. Tilley, J. McKeating, C. Shotton, and A. Pinter. 1995. Characterization of neutralization epitopes in the V2 region of human immunodeficiency virus type 1 gp120: role of glycosylation in the correct folding of the V1/V2 domain. J. Virol. 69:2271-2278.
73. Wyatt, R., P. D. Kwong, E. Desjardins, R. W. Sweet, J. Robinson, W. A. Hendrickson, and J. G. Sodroski. 1998. The antigenic structure of the HIV gp120 envelope glycoprotein. Nature 393:705-711.
74. Wyatt, R., J. Moore, M. Accola, E. Desjardin, J. Robinson, and J. Sodroski. 1995. Involvement of the V1/V2 variable loop structure in the exposure of human immunodeficiency virus type 1 gp120 epitopes induced by receptor binding. J. Virol. 69:5723-5733.
75. Yong, V. W., and J. P. Antel. 1992. Culture of glial cells from human brain biopsies, p. 81-96. In S. Fedoroff and A. Richardson (ed.), Protocols for neural cell culture. Humana Press, Totowa, N.J.
76. Zhang, Y. J., and J. P. Moore. 1999. Will multiple coreceptors need to be targeted by inhibitors of human immunodeficiency virus type 1 entry? J. Virol. 73:3443-3448.