Primary human immunodeficiency virus type 2 (HIV-2) isolates infect CD4- negative cells via CCR5 and CXCR4: Comparison with HIV-1 and simian immunodeficiency virus and relevance to cell tropism in vivo

Journal of Virology

Volumn 73, Issue 9, 1999, Pages 7795-7804

  Reeves, Jacqueline D ^a   Hibbitts, Sam ^a   Simmons, Graham ^a   McKnight, Áine ^a   Azevedo Pereira, José M ^b   Moniz Pereira, José ^b   Clapham, Paul R ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b RESEARCH INSTITUTE FOR MEDICINES IMED ULISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4;

ARTICLE; COMPARATIVE STUDY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; SIMIAN IMMUNODEFICIENCY VIRUS; STRAIN DIFFERENCE; VIRUS ADSORPTION; VIRUS INFECTIVITY; VIRUS ISOLATION; VIRUS STRAIN;

EID: 0032856713     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.9.7795-7804.1999     Document Type: Article

References (90)

1. Albritton, L. M., L. Tseng, D. Scadden, and J. M. Cunningham. 1989. A putative murine ecotropic retrovirus receptor gene encodes a multiple membrane-spanning protein and confers susceptibility to virus infection. Cell 57:659-666.
2. Alkhatib, G., F. Liao, E. A. Berger, J. M. Farber, and K. W. Peden. 1997. A new SIV co-receptor, STRL33. Nature 388:238.
3. Babu, P. G., N. K. Saraswathi, F. Devapriya, and T. J. John. 1993. The detection of HIV-2 infection in southern India. Indian J. Med. Res. 97:49-52.
4. Baier, M., A. Werner, K. Cichutek, C. Garber, C. Müller, G. Kraus, F. J. Ferdinand, S. Hartung, T. S. Papas, and R. Kurth. 1989. Molecularly cloned simian immunodeficiency virus SIVagm3 is highly divergent from other SIVagm isolates and is biologically active in vitro and in vivo. J. Virol. 63:5119-5123.
5. Bieniasz, P. D., R. A. Fridell, I. Aramori, S. S. Ferguson, M. G. Caron, and B. R. Cullen. 1997. HIV-1-induced cell fusion is mediated by multiple regions within both the viral envelope and the CCR-5 co-receptor. EMBO J. 16:2599-2609.
6. Björndal, Å., H. Deng, M. Jansson, J. R. Fiore, C. Colognesi, A. Karlsson, J. Albert, G. Scarlatti, D. R. Littman, and E. M. Fenyö, 1997. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J. Virol. 71:7478-7487.
7. Bleul, C. C., M. Farzan, H. Choe, C. Parolin, I. Clark Lewis, J. Sodroski, and T. A. Springer. 1996. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature 382:829-833.
8. Brojatsch, J., J. Naughton, M. M. Rolls, K. Zingler, and J. A. Young. 1996. CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosis-sarcoma viruses and mediates apoptosis. Cell 87:845-855.
9. Bron, R., P. J. Klasse, D. Wilkinson, P. R. Clapham, A. Pelchen-Matthews, C. Power, T. N. C. Wells, J. Kim, S. C. Peiper, J. A. Hoxie, and M. Marsh. 1997. Promiscuous use of CC and CXC chemokine receptors in cell-to-cell fusion mediated by a human immunodeficiency virus type 2 envelope protein. J. Virol. 71:8405-8415.
10. Cecilia, D., V. N. KewalRamani, J. O'Leary, B. Volsky, P. Nyambi, S. Burda, S. Xu, D. R. Littman, and S. Zolla Pazner. 1998. Neutralization profiles of primary human immunodeficiency virus type 1 isolates in the context of coreceptor usage. J. Virol. 72:6988-6996.
11. Chen, Z., A. Gettie, D. D. Ho, and P. A. Marx. 1993. Primary SIVsm isolates use the CCR5 coreceptor from sooty mangabeys naturally infected in west Africa: a comparison of coreceptor usage of primary SIVsm, HIV-2 and SIVmac. Virology 246:113-124.
12. Clapham, P. R. 1991. Human immunodeficiency virus infection of nonhaematopoietic cells. The role of CD4-independent infection. Rev. Med. Virol. 1:51-58.
13. - cells, vol. 5. ESCOM Science Publishers B. V., Leiden, The Netherlands.
14. Clapham, P. R., A. McKnight, and R. A. Weiss. 1992. Human immunodeficiency virus type 2 infection and fusion of CD4-negative human cell lines: induction and enhancement by soluble CD4. J. Virol. 66:3531-3537.
15. Clapham, P. R., and R. A. Weiss. 1997. Immunodeficiency viruses. Spoilt for choice of co-receptors. Nature 388:230-231.
16. Clavel, F., D. Guetard, F. Brun Vezinet, S. Chamaret, M. A. Rey, M. O. Santos Ferreira, A. G. Laurent, C. Dauguet, C. Katiama, C. Rouzioux, et al. 1986. Isolation of a new human retrovirus from West African patients with AIDS. Science 233:343-346.
17. Clavel, F., M. Guyader, D. Guetard, M. Salle, L. Montagnier, and M. Alizon. 1986. Molecular cloning and polymorphism of the human immune deficiency virus type 2. Nature 324:691-695.
18. Cranage, M., J. Stott, K. Mills, T. Ashworth, F. Taffs, G. Farrar, L. Chan, M. Dennis, P. Putkonen, G. Biberfeld, et al. 1992. Vaccine studies with the 32H reisolate of SIVmac251: an overview. AIDS Res. Hum. Retroviruses 8:1479-1481.
19. Crandell, R. A., C. G. Fabricant, and W. A. Nelson Rees. 1973. Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro 9:176-185.
20. Damico, R. L., J. Crane, and P. Bates. 1998. Receptor-triggered membrane association of a model retroviral glycoprotein. Proc. Natl. Acad. Sci. USA 95:2580-2585.
21. Daniel, M. D., N. L. Letvin, N. W. King, M. Kannagi, P. K. Sehgal, R. D. Hunt, P. J. Kanki, M. Essex, and R. C. Desrosiers. 1985. Isolation of T-cell tropic HTLV-III-like retrovirus from macaques. Science 228:1201-1204.
22. Deng, H. K., D. Unutmaz, V. N. KewalRamani, and D. R. Littman. 1997. Expression cloning of new receptors used by simian and human immunodeficiency viruses. Nature 388:295-300.
23. Dittmar, M. T., G. Simmons, S. Hibbitts, M. O'Hare, S. Louisirirotchanakul, S. Beddows, J. Weber, P. R. Clapham, and R. A. Weiss. 1997. Langerhans cell tropism of human immunodeficiency virus type 1 subtype A through F isolates derived from different transmission groups. J. Virol. 71: 8008-8013.
24. Donzella, G. A., D. Schols, S. W. Lin, J. A. Este, K. A. Nagashima, P. J. Maddon, G. P. Allaway, T. P. Sakmar, G. Henson, E. De Clercq, and J. P. Moore. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
25. Edinger, A. L., C. Blanpain, K. J. Kunstman, S. M. Wolinsky, M. Parmentier, and R. W. Doms. 1999. Functional dissection of CCR5 coreceptor function through the use of CD4-independent simian immunodeficiency virus strains. J. Virol. 73:4062-4073.
26. 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. Natl. Acad. Sci. USA 94:14742-14747.
27. Endres, M. J., P. R. Clapham, M. Marsh, M. Ahuja, J. D. Turner, A. McKnight, J. F. Thomas, B. Stoebenau Haggarty, 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.
28. Farzan, M., H. Choe, K. Martin, L. Marcon, W. Hofmann, G. Karlsson, Y. Sun, P. Barrett, N. Marchand, N. Sullivan, N. Gerard, C. Gerard, and J. Sodroski. 1997. Two orphan seven-transmembrane segment receptors which are expressed in CD4-positive cells support simian immunodeficiency virus infection. J. Exp. Med. 186:405-411.
29. 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.
30. Gao, F., L. Yue, A. T. White, P. G. Pappas, J. Barchue, A. P. Hanson, B. M. Greene, P. M. Sharp, G. M. Shaw, and B. H. Hahn. 1992. Human infection by genetically diverse SIVSM-related HIV-2 in west Africa. Nature 358:495-499.
31. Groenink, M., R. A. M. Fouchler, R. E. Y. de Goede, F. de Wolf, R. A. Gruters, H. T. M. Cuypers, H. G. Huisman, and M. Tersmette. 1991. Phenotypic heterogeneity in a panel of infectious molecular human immunodeficiency virus type 1 clones derived from a single individual. J. Virol. 65: 1968-1975.
32. Guillon, C., M. E. van der Ende, P. H. M. Boers, R. A. Gruters, M. Schutten, and A. D. M. E. Osterhaus. 1998. Coreceptor usage of human immunodeficiency virus type 2 primary isolates and biological clones is broad and does not correlate with their syncytium-inducing capacities. J. Virol. 72:6260-6263.
33. Healey, D., L. Dianda, J. P. Moore, J. S. McDougal, M. J. Moore, P. Estess, D. Buck, P. D. Kwong, P. C. Beverley, and Q. J. Sattentau. 1990. Novel anti-CD4 monoclonal antibodies separate human immunodeficiency virus infection and fusion of CD4+ cells from virus binding. J. Exp. Med. 172: 1233-1242.
34. Hernandez, L. D., R. J. Peters, S. E. Delos, J. A. Young, D. A. Agard, and J. M. White. 1997. Activation of a retroviral membrane fusion protein: soluble receptor-induced liposome binding of the ALSV envelope glycoprotein. J. Cell Biol. 139:1455-1464.
35. 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.
36. Hoxie, J. A., C. C. LaBranche, M. J. Endres, J. D. Turner, J. F. Berson, R. W. Doms, and T. J. Matthews. 1998. CD4-independent utilization of the CXCR4 chemokine receptor by HIV-1 and HIV-2. J. Reprod. Immunol. 41:197-211.
37. Johann, S. V., J. J. Gibbons, and B. O'Hara. 1992. GLVR1, a receptor for gibbon ape leukemia virus, is homologous to a phosphate permease of Neurospora crassa and is expressed at high levels in the brain and thymus. J. Virol. 66:1635-1640.
38. ROD envelope glycoprotein modulate fusion. J. Virol. 67:6253-6258.
39. Kent, K. A., L. Gritz, G. Stallard, M. P. Cranage, C. Collignon, C. Thiriart, T. Corcoran, P. Silvera, and E. J. Stott. 1991. Production of monoclonal antibodies to simian immunodeficiency virus envelope glycoproteins. AIDS 5:829-836.
40. Kent, K. A., E. Rud, T. Corcoran, C. Powell, C. Thiriart, C. Collignon, and E. J. Stott. 1992. Identification of two neutralizing and 8 non-neutralizing epitopes on simian immunodeficiency virus envelope using monoclonal antibodies. AIDS Res. Hum. Retroviruses 8:1147-1151.
41. Kledal, T. N., M. M. Rosenkilde, F. Coulin, G. Simmons, A. H. Johnsen, S. Alouani, C. A. Power, H. R. Luttichau, J. Gerstoft, P. R. Clapham, I. Clark Lewis, T. N. C. Wells, and T. W. Schwartz. 1997. A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma-associated herpesvirus. Science 277:1655-1659.
42. Koot, M., I. P. Keet, A. H. Vos, R. E. de Goede, M. T. Roos, R. A. Coutinho, F. Miedema, P. T. Schellekens, and M. Tersmette. 1993. Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4+ cell depletion and progression to AIDS. Ann. Intern. Med. 118:681-688.
43. Kulkarni, S., M. Thakar, J. Rodrigues, and K. Banerjee. 1992. HIV-2 antibodies in serum samples from Maharashtra state. Indian J. Med. Res. 95: 213-215.
44. Kurane, I., B. L. Innis, S. Nimmannitya, A. Nisalak, A. Meager, J. Janus, and F. A. Ennis. 1991. Activation of T lymphocytes in dengue virus infections. High levels of soluble interleukin 2 receptor, soluble CD4, soluble CD8, interleukin 2, and interferon-gamma in sera of children with dengue. J. Clin. Investig. 88:1473-1480.
45. Kwong, P. D., R. Wyatt, J. Robinson, R. W. Sweet, J. Sodroski, and W. A. Hendrickson. 1998. Structure of an HIV gp120 envelope glycoprotein in complex with the CD4 receptor and a neutralizing human antibody. Nature 393:648-659.
46. Lapham, C. K., M. B. Zaitseva, S. Lee, T. Romanstseva, and H. Golding. 1999. Fusion of monocytes and macrophages with HIV-1 correlates with biochemical properties of CXCR4 and CCR5. Nat. Med. 5:303-308.
47. Lee, B., M. Sharron, C. Blanpain, B. J. Doranz, J. Vakill, P. Setoh, E. Berg, G. Liu, H. R. Guy, S. R. Durell, M. Parmentier, C. N. Chang, K. Price, M. Tsang, and R. W. Doms. 1999. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274:9617-9626.
48. Liao, F., G. Alkhatib, K. W. Peden, G. Sharma, E. A. Berger, and J. M. Farber. 1997. STRL33, a novel chemokine receptor-like protein, functions as a fusion cofactor for both macrophage-tropic and T cell line-tropic HIV-1. J. Exp. Med. 185:2015-2023.
49. Loetscher, M., A. Amara, E. Oberlin, N. Brass, D. Legler, P. Loetscher, D. A. M. E. Meese, D. Rousset, J. L. Virelizier, M. Baggiolini, F. Arenzana Seisdedos, and B. Moser. 1997. TYMSTR, a putative chemokine receptor selectively expressed in activated T cells, exhibits HIV-1 coreceptor function. Curr. Biol. 7:652-660.
50. Martin, K. A., R. Wyatt, M. Farzan, H. Choe, L. Marcon, E. Desjardins, J. Robinson, J. Sodroski, C. Gerard, and N. P. Gerard. 1997. CD4-independent binding of SIV gp120 to rhesus CCR5. Science 278:1470-1473.
51. McKnight, A., M. T. Dittmar, J. Moniz-Periera. K. Ariyoshi, J. D. Reeves, S. Hibbitts, D. Whitby, E. Aarons, A. E. I. Proudfoot, H. Whittle, and P. R. Clapham. 1998. A broad range of chemokine receptors are used by primary isolates of human immunodeficiency virus type 2 as coreceptors with CD4. J. Virol. 72:4065-4071.
52. McKnight, A., C. Shotton, J. Cordell, I. Jones, G. Simmons, and P. R. Clapham. 1996. Location, exposure, and conservation of neutralizing and nonneutralizing epitopes on human immunodeficiency virus type 2 SU glycoprotein. J. Virol. 70:4598-4606.
53. McKnight, A., D. Wilkinson, G. Simmons, S. Talbot, L. Picard, M. Ahuja, M. Marsh, J. A Hoxie, and P. R. Clapham. 1997. Inhibition of human immunodeficiency virus fusion by a monoclonal antibody to a coreceptor (CXCR4) is both cell type and virus strain dependent. J. Virol. 71:1692-1696.
54. Miller, D. G., R. H. Edwards, and A. D. Miller. 1994. Cloning of the cellular receptor for amphotropic murine retroviruses reveals homology to that for gibbon ape leukemia virus. Proc. Natl. Acad. Sci. USA 91:78-82.
55. + cells. J. Virol. 66:4784-4793.
56. Murphey Corb, M., L. N. Martin, S. R. Rangan, G. B. Baskin, B. J. Gormus, R. H. Wolf, W. A. Andes, M. West, and R. C. Montelaro. 1986. Isolation of an HTLV-III-related retrovirus from macaques with simian AIDS and its possible origin in asymptomatic mangabeys. Nature 321:435-437.
57. Oberlin, E., A. Amara, F. Bachelerie, C. Bessia, J. L. Virelizier, F. Arenzana Seisdedos, O. Schwartz, J. M. Heard, I. Clark Lewis, D. F. Legler, M. Loetscher, M. Baggiolini, and B. Moser. 1996. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 382:833-835.
58. Owen, S. M., D. Ellenberger, M. Rayfield, S. Wiktor, P. Michel, M. H. Grieco, F. Gao, B. H. Hahn, and R. B. Lal. 1998. Genetically divergent strains of human immunodeficiency virus type 2 use multiple coreceptors for viral entry. J. Virol. 72:5425-5432.
59. Picard, L., G. Simmons, C. A. Power, A. Meyer, R. A. Weiss, and P. R. Clapham. 1997. Multiple extracellular domains of CCR-5 contribute to human immunodeficiency virus type 1 entry and fusion. J. Virol. 71:5003-5011.
60. Popovic, M., M. G. Sarngadharan, E. Read, and R. C. Gallo. 1984. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science 224:497-500.
61. Potempa, S., L. Picard, J. D. Reeves, D. Wilkinson, R. A. Weiss, and S. J. Talbot. 1997. CD4-independent infection by human immunodeficiency virus type 2 strain ROD/B: the role of the N-terminal domain of CXCR-4 in fusion and entry. J. Virol. 71:4419-4424.
62. Ratner, L., A. Fisher, L. L. Jagodzinski, H. Mitsuya, R. S. Liou, R. C. Gallo, and F. Wong Staal. 1987. Complete nucleotide sequences of functional clones of the AIDS virus. AIDS Res. Hum. Retroviruses 3:57-69.
63. Reeves, J. D., A. McKnight, S. Potempa, G. Simmons, P. W. Gray, C. A. Power, T. Wells, R. A. Weiss, and S. J. Talbot. 1997. CD4-independent infection by HIV-2 (ROD/B): use of the 7-transmembrane receptors CXCR-4, CCR-3, and V28 for entry. Virology 231:130-134.
64. Reeves, J. D., and T. F. Schulz. 1997. The CD4-independent tropism of human immunodeficiency virus type 2 involves several regions of the envelope protein and correlates with a reduced activation threshold for envelope-mediated fusion. J. Virol. 71:1453-1465.
65. Rey-Cuillé, M.-A., J.-L. Berthier, M.-C. Bomsel Demontoy, Y. Chaduc, L. Montagnier, A. G. Hovanessian, and L. A. Chakrabarti. 1998. Simian immunodeficiency virus replicates to high levels in sooty mangabeys without inducing disease. J. Virol. 72:3872-3886.
66. 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.
67. Rubsamen Waigmann, H., H. V. Briesen, J. K. Maniar, P. K. Rao, C. Scholz, and A. Pfutzner. 1991. Spread of HIV-2 in India. Lancet 337:550-551.
68. Saito, Y., L. R. Sharer, L. G. Epstein, J. Michaels, M. Mintz, M. Louder, K. Golding, T. A. Cvetkovich, and B. M. Blumberg. 1994. Overexpression of nef as a marker for restricted HIV-1 infection of astrocytes in postmortem pediatric central nervous tissues. Neurology 44:474-481.
69. Sauermann, U., J. Schneider, J. Mous, U. Brunckhorst, I. Schedel, K. D. Jentsch, and G. Hunsmann. 1990. Molecular cloning and characterization of a German HIV-1 isolate. AIDS Res. Hum. Retroviruses 6:813-823.
70. Schall, T. J., J. Jongstra, B. J. Dyer, J. Jorgensen, C. Clayberger, M. M. Davis, and A. M. Krensky. 1988. A human T cell-specific molecule is a member of a new gene family. J. Immunol. 141:1018-1025.
71. Schols, D., J. A. Este, G. Henson, and E. De Clercq. 1997. Bicyclams, a class of potent anti-HIV agents, are targeted at the HIV coreceptor fusin/CXCR-4. Antiviral Res. 35:147-156.
72. Schols, D., S. Struyf, J. Van Damme, J. A. Este, G. Henson, and E. De Clercq. 1997. Inhibition of T-tropic HIV strains by selective antagonization of the chemokine receptor CXCR4. J. Exp. Med. 186:1383-1388.
73. Schulz, T. F., D. Whitby, J. G. Hoad, T. Corrah, H. Whittle, and R. A. Weiss. 1990. Biological and molecular variability of human immunodeficiency virus type 2 isolates from The Gambia. J. Virol. 64:5177-5182.
74. Sharer, L. R., Y. Saito, L. G. Epstein, and B. M. Blumberg. 1994. Detection of HIV-1 DNA in pediatric AIDS brain tissue by two-step ISPCR. Adv. Neuroimmunol. 4:283-285.
75. Simmons, G., P. R. Clapham, L. Picard, R. E. Offord, M. M. Rosenkilde, T. W. Schwartz, R. Buser, T. N. C. Wells, and A. E. Proudfoot. 1997. Potent inhibition of HIV-1 infectivity in macrophages and lymphocytes by a novel CCR5 antagonist. Science 276:276-279.
76. Simmons, G., J. D. Reeves, A. McKnight, N. Dejucq, S. Hibbitts, C. A. Power, E. Aarons, D. Schols, E. De Clercq, A. E. I. Proudfoot, and P. R. Clapham. 1998. CXCR4 as a functional coreceptor for human immunodeficiency virus type 1 infection of primary macrophages. J. Virol. 72:8453-8457.
77. Simmons, G., D. Wilkinson, J. D. Reeves, M. T. Dittmar, S. Beddows, J. Weber, G. Carnegie, U. Desselberger, P. W. Gray, R. A. Weiss, and P. R. Clapham. 1996. Primary, syncytium-inducing human immunodeficiency virus type 1 isolates are dual-tropic and most can use either Lestr or CCR5 as coreceptors for virus entry. J. Virol. 70:8355-8360.
78. Sol, N., F. Ferchal, J. Braun, O. Pleskoff, C. Tréboute, I. Ansart, and M. Alizon. 1997. Usage of the coreceptors CCR-5, CCR-3, and CXCR-4 by primary and cell line-adapted human immunodeficiency virus type 2. J. Virol. 71:8237-8244.
79. Stratton, M. R., B. R. Reeves, and C. S. Cooper. 1989. Misidentified cell. Nature 337:311-312.
80. Takeuchi, Y., M. Akutsu, K. Murayama, N. Shimizu, and H. Hoshino. 1991. Host range mutant of human immunodeficiency virus type 1: modification of cell tropism by a single point mutation at the neutralization epitope in the env gene. J. Virol. 65:1710-1718.
81. Takeuchi, Y., R. G. Vile, G. Simpson, B. O'Hara, M. K. L. Collins, and R. A. Weiss. 1992. Feline leukemia virus subgroup B uses the same cell surface receptor as gibbon ape leukemia virus. J. Virol. 66:1219-1222.
82. Talbot, S. J., R. A. Weiss, and T. F. Schulz. 1995. Reduced glycosylation of human cell lines increases susceptibility to CD4-independent infection by human immunodeficiency virus type 2 (LAV-2/B). J. Virol. 69:3399-3406.
83. Tornatore, C., A. Nath, K. Amemiya, and E. O. Major. 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. 65:6094-6100.
84. Whittle, H., J. Morris, J. Todd, T. Corrah, S. Sabally, J. Bangali, P. T. Ngom, M. Rolfe, and A. Wilkins. 1994. HIV-2-infected patients survive longer than HIV-1-infected patients. AIDS 8:1617-1620.
85. Willett, B. J., M. J. Hosie, J. C. Neil, J. D. Turner, and J. A. Hoxie. 1997. Common mechanism of infection by lentiviruses. Nature 385:587.
86. Willett, B. J., L. Picard, M. J. Hosie, J. D. Turner, K. Adema, and P. R. Clapham. 1997. Shared usage of the chemokine receptor CXCR4 by the feline and human immunodeficiency viruses. J. Virol. 71:6407-6415.
87. Wu, L., G. LaRosa, N. Kassam, C. J. Gordon, H. Heath, N. Ruffing, H. Chen, J. Humblias, M. Samson, M. Parmentier, J. P. Moore, and C. R. Mackay. 1997. Interaction of chemokine receptor CCR5 with its ligands: multiple domains for HIV-1 gp120 binding and a single domain for chemokine binding. J. Exp. Med. 186:1373-1381.
88. 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.
89. Yamanaka, R., R. Tanaka, and S. Yoshida. 1993. Effects of irradiation on cytokine production in glioma cell lines. Neurol. Med. Chir. Tokyo 33:744-748.
90. Young, J. A. T., P. Bates, and H. E. Varmus. 1993. Isolation of a chicken gene that confers susceptibility to infection by subgroup A avian leukosis and sarcoma viruses. J. Virol. 67:1811-1816.