Unwelcomed guests with master keyes: How HIV uses chemokine receptors for cellular entry

Virology

Volumn 235, Issue 2, 1997, Pages 179-190

  Doms, Robert W ^a   Peiper, Stephen C ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR; VIRUS RECEPTOR;

ANTIVIRAL ACTIVITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; REVIEW; VIRUS CELL INTERACTION; VIRUS INFECTION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0030770546     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1997.8703     Document Type: Article

References (108)

1. Alkhatib G., Broder C. C., Berger E. A. Cell type-specific cofactors determine human immunodeficiency virus type 1 tropism for T-cel lines versus primary macrophages. J. Virol. 70:1996a;5487-5494.
2. Alkhatib G., Combadiere C., Broder C. C., Feng Y., Kennedy P. E., Murphy P. M., Berger E. A. CC CKR5: A RANTES, MIP-1α, MIP-1β receptor as a fusion cofactor for macrophage-tropic HIV-1. Science. 272:1996b;1955-1958.
3. Aramori I., Ferguson S. S. G., Bieniasz P. D., Cullen B. R., Caron M. G. Molecular mechanism of desensitization of the chemokine receptor CCR5: Receptor signaling and internalization are dissociable from its role as an HIV-1 co-receptor. EMBO J. 1997.
4. Arenzanaseisdos F., Virelizier J. L., Rousset D., ClarkLewis I., Loetscher P., Moser B., Baggiolini M. HIV blocked by chemokine antagonist. Nature. 383:1996;400.
5. Ashorn P. A., Berger E. A., Moss B. Human immunodeficiency virus envelope glycoprotein/CD4-mediated fusion of nonprimate cells with human cell. J. Virol. 64:1990;2149-2156.
6. Atchison R. E., Gosling J., Monteclaro F. S., Franci C., Digilio L., Charo I. F., Goldsmith M. Multiple extracellular elements of CCR5 and HIV-1 entry: Dissociation from response to chemokines. Science. 274:1996;1924-1926.
7. Baggiolini M., Dewald B., Moser B. Human chemokines: An update. Annu. Rev. Immunol. 15:1997;675-705.
8. Berson J. F., Long D., Doranz B. J., Rucker J., Jirik F. R., Doms R. W. A seven transmembrane domain receptor involved in fusion and entry of T-cell tropic human immunodeficiency virus type-1 strains. J. Virol. 70:1996;6288-6295.
9. Bieniasz P. D., Fridell R. A., Aramori I., Ferguson S. S. G., Caron M. G., Cullen B. R. HIV-1 induced cell fusion is mediated by multiple regions within both the viral envelope and the CCR-5 coreceptor. EMBO J. 16:1997;2599-2609.
10. Biti R., French R., Young J., Bennetts B., Stewart G. HIV-1 infection in an individual homozygous for the CCR5 deletion mutant. Nature Med. 3:1997;252-253.
11. Bleul C. C., Farazan M., Choe H., Parolin C., Clark-Lewis I., Sodroski J., Springer T. A. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/Fusin and blocks HIV-1 entry. Nature. 382:1996;829-833.
12. Bleul C. C., Wu L., Hoxie J. A., Springer T. A., Mackay C. R. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. USA. 94:1997;1925-1930.
13. Brelot A., Heveker N., Pleskoff O., Sol N., Alizon M. Role of the first and third extracellular domains of CXCR-4 in human immunodeficiency virus coreceptor activity. J. Virol. 71:1997;4744-4751.
14. Broder C. C., Dimitrov D. S., Blumenthal R., Berger E. A. The block to HIV-1 envelope glycoprotein-mediated membrane fusion in animal cells expressing human CD4 can be overcome by a human cell component(s). Virology. 193:1993;483-491.
15. Chackerian B., Long E. M., Luciw P. A., Overbaugh J. Human immunodeficiency virus type 1 coreceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 71:1997;3932-3939.
16. Chan D. C., Fass D., Berger J. M., Kim P. S. Core structure of gp41 from the HIV envelope glycoprotein. Cell. 89:1997;263-273.
17. Chen Z., Zhou P., Ho D. D., Landau N. R., Marx P. A. Genetically divergent strains of simian immunodeficiency virus use CCR5 as a coreceptor for entry. J. Virol. 71:1997;2705-2714.
18. Cheng-Mayer C., Quiroga M., Tung J. W., Dina D., Levy J. A. Viral determinants of human immunodeficiency virus type 1 T-cell or macrophage tropism, cytopathogenicity, and CD4 antigen. J. Virol. 64:1990;4390-4398.
19. Cheng-Mayer C., Seto D., Tateno M., Levy J. A. Biological features of HIV that correlate with virulence in the host. Science. 240:1988;80-82.
20. Chesebro B., Buller R., Portis J., Wehrly K. Failure of human immunodeficiency virus entry and infection in CD4-positive human brain and skin cells. J. Virol. 64:1990;215-221.
21. Choe H., Farzan M., Sun Y., Sullivan N., Rollins B., Ponath P. D., Wu L., Mackay C. R., LaRosa G., Newman W., Gerard N., Gerard C., Sodroski J. The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell. 85:1996;1135-1148.
22. Clapham P. R., Blanc D., Weiss R. A. Specific cell surface requirements for infection of CD4-positive cells by human immunodeficiency virus type 1, type 2 and simian immunodeficiency virus. Virology. 181:1991;703-715.
23. +. Science. 270:1995;1811-1815.
24. Cocchi F., DeVico A. L., Garzino-Demo A., Cara A., Gallo R. C., Lusso P. The V3 domain of the HIV-1 gp120 envelope glycoprotein is critical for chemokine-mediated blockade of infection. Nature Med. 2:1996;1244-1247.
25. Collman R., Balliet J. W., Gregory S. A., Friedman H., Kolson D. L., Nathanson N., Srinivasan A. An infectious molecular clone of an unusual macrophage-tropic and highly cytopathic strain of human immunodeficiency virus type 1. J. Virol. 66:1992;7517-7521.
26. Connor R. I., Mohri H., Cao Y., Ho D. D. Increased viral burden and cytopathicity correlate temporally with CD4+ T-lymphocyte decline and clinical progression in human immunodeficiency virus type 1-infected individuals. J. Virol. 67:1993;1772-1777.
27. Connor R. I., Paxton W. A., Sheridan K. E., Koup R. A. Macrophages and CD4+ T-lymphocytes from two multiply exposed, uninfected individuals resist infection with primary NSI isolates of human immunodeficiency virus type-1. J. Virol. 70:1996;8758-8764.
28. Connor R. I., Sheridan K. E., Ceradini D., Choe S., Landau N. R. Change in coreceptor use correlates with disease progression in HIV-1 infected individuals. J. Exp. Med. 185:1997;621-628.
29. Dalgleish A. G., Beverley P. C. L., Clapham P. R., Crawford D. H., Greaves M. F., Weiss R. A. The CD4 (T4) antigen is an essential component of the receptor of the AIDS retrovirus. Nature. 312:1984;763-767.
30. Dean M., Carrington M., Winkler C., Huttley G. A., Smith M. W., Allikmets R., Goedert J. J., Buchbinder S. P., Vittinghoff E., Gomperts E., Donfield S., Vlahov D., Kaslow R., Saah A., Rinaldo C., Detels R., O'Brien S. J. Genetic resistance of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Science. 273:1996;1856-1862.
31. DeJong J.-J., Goudsmit J., Keulen W., Klaver B., Krone W., Tersmette M., deRonde A. Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium fromation and replication capacity. J. Virol. 66:1992;757-765.
32. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Marzio P. D., Marmon S., Sutton R. E., Hill C. M., Davis C. B., Peiper S. C., Schall T. J., Littman D. R., Landau N. R. Identification of a major co-receptor for primary isolates of HIV-1. Nature. 381:1996;661-666.
33. Doranz B. J., Lu Z., Rucker J., Zhang T., Sharron M., Cen Y., Wang Z., Guo H., Du J., Accavitti M. A., Doms R. W., Peiper S. C. Structural determinants of CCR5 coreceptor function for HIV-1. J. Virol. 1997.
34. Doranz B. J., Rucker J., Yi Y., Smyth R. J., Samson M., Peiper S. C., Parmentier M., Collman R. G., Doms R. W. A dual-tropic primary HIV-1 isolate that uses fusin and the β-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell. 85:1996;1149-1158.
35. Dragic T., Charneau P., Clavel F., Alizon M. Complementation of murine cells for human immunodeficiency virus envelope/CD4-mediated fusion in human/murine heterokaryons. J. Virol. 66:1992;4794-4802.
36. 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. HIV-1 entry into CD4+ cells is mediated by the chemokine receptor CC-CKR-5. Nature. 381:1996;667-673.
37. Edinger A. L., Amedee A., Miller K., Doranz B. J., Endres M., Sharron M., Samson M., Lu Z.-H., Clements J. E., Murphey-Corb M., Peiper S. C., Parmentier M., Broder C. C., Doms R. W. Differential utilization of CCR5 by macrophage and T-cell tropic SIV strains. Proc. Natl. Acad. Sci. USA. 94:1997;4005-4010.
38. Endres M. J., Clapham P. R., Marsh M., Ahuja M., Turner J. D., McKnight A., Thomas J. F., Stoebenau-Haggarty B., S. Choe P. J. V., Wells T. N. C., Power C. A., Sutterwala S. S., Doms R. W., Landau N. R., Hoxie J. A. CD4-independent infection by HIV-2 is mediated by fusin/CXCR4. Cell. 87:1996;745-765.
39. Farzan M., Choe H., Martin K. A., Sun Y., Sidelko M., Mackay C. R., Gerard N. P., Sodroski J., Gerard C. HIV-1 entry and macrophage inflammatory protein 1β-mediated signaling are independent functions of the chemokine receptor CCR5. J. Biol. Chem. 272:1997;6854-6857.
40. Fauci A. Host factors and the pathogenesis of HIV-induced disease. Nature. 384:1996;529-534.
41. Federsppiel B., Melhado I. G., Duncan A. M. V., Delaney A., Schappert K., Clark-Lewis I., Jirik F. R. Molecular cloning of the cDNA and chromosomal localization of the gene for a putative seven-transmembrane segment (7-TMS) receptor isolated from human spleen. Genomics. 16:1993;707-712.
42. Feng Y., Broder C. C., Kennedy P. E., Berger E. A. HIV-1 entry cofactor: Functional cDNA cloning of a seven-transmembrane domain, G-protein coupled receptor. Science. 272:1996;872-877.
43. Fenyö E., Morfeldt-Mason L., Chiodi F., Lind B., VonGegerfelt A., Albert J., Åsjö B. Distinctive replicative and cytopathic characteristics of human immunodeficiency virus isolates. J. Virol. 62:1988;4414-4419.
44. Fouchier R. A. M., Groenink M., Kootstra N. A., Tersmette M., Huisman H. G., Miedema F., Schuitemaker H. Phenotype-associated sequence variation in the third variable domain of the human immunodeficiency virus type 1 gp120 molecule. J. Virol. 66:1992;3183-3187.
45. Gosling J., Monteclaro F. S., Atchison R. E., Arai H., Tsou C., Goldsmith M. A., Charo I. F. Molecular uncoupling of C-C chemokine receptor 5-induced chemotaxis and singnal transduction from HIV-1 coreceptor activity. Proc. Natl. Acad. Sci. USA. 94:1997;5061-5066.
46. He J., Chen Y., Farzan M., Choe H., Ohagen A., Gartner S., Busciglio J., Yang X., Hofmann W., Newman W., Mackay C. R., Sodroski J., Babuzda D. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature. 385:1997;645-649.
47. Hesselgesser J., Halks-Miller M., DelVecchio V., Peiper S. C., Hoxie J., Kolson D. L., Taub D., Horuk R. CD4-independent association between HIV-1 gp120 and CXCR4: Functional chemokine receptors are expressed in human neurons. Curr. Biol. 7:1997;112-121.
48. Horuk R. Molecular properties of the chemokine receptor family. Trends Pharmacol. Sci. 15:1994;159-165.
49. Huang Y., Paxton W. A., Wolinsky S. M., Neumann A. U., Zhang L., He T., Kang S., Ceradini D., Jin Z., Yazdanbakhsh K., Kuntsman K., Erickson D., Dragon E., Landau N. R., Phair J., Ho D. D., Koup R. A. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nature Med. 2:1996;1240-1243.
50. Hwang S. S., Boyle T. J., Lyerly H. K., Cullen B. R. Identification of the envelope V3 loop as the primary determinant of cell tropism in HIV-1. Science. 253:1991;71-74.
51. Jansson M., Popovic M., Karlsson A., Cocchi F., Rossi P., Albert J., Wigzell H. Sensitivity to inhibition by β-chemokines correlates with biological phenotypes of primary HIV-1 isolates. Proc. Natl. Acad. Sci. USA. 93:1996;15382-15387.
52. Kim F. M., Kolson D. L., Balliet J. W., Srinivasan A., Collman R. G. V3-independent determinants of macrophage tropism in a primary human immunodeficiency virus type 1 isolate. J. Virol. 69:1995;1755-1761.
53. Klatzman D., Champagne E., Chamaret S., Gruest J., Guetard D., Hercend T., Gluckman J. C., Montagnier L. T-lymphocyte T4 molecule behaves as the receptor for human retrovirus LAV. Nature. 312:1984;767-768.
54. Koito A., Harrowe G., Levy J. A., Cheng-Mayer C. 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. 68:1994;2253-2259.
55. Kozak S. L., Platt E. J., Madani N., Ferro F. E., Peden K., Kabat D. CD4, CXCR-4, and CCR5 dependencies for infections by primary patient and laboratory-adapted isolates of human immunodeficiency virus type 1. J. Virol. 71:1997;873-882.
56. Lapham C. K., Ouyang J., Chandrasekhar B., Nguyen N. Y., Dimitrov D. S., Golding H. Evidence for cell-surface association between Fusin and the CD4-gp120 complex in human cell lines. Science. 274:1996;602-605.
57. Levy J. A. HIV pathogenesis and long-term survival. AIDS. 7:1993;1401-1410.
58. Liao F., Alkhatib G., Peden K. W. C., Sharma G., Berger E. A., Farber J. M. 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. 185:1997;2015-2023.
59. 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. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell. 86:1996;367-377.
60. Liu Z.-Q., Wood C., Levy J. A., Cheng-Mayer C. The viral envelope gene is involved in macrophage tropism of a human immunodeficiency virus type 1 strain isolated from brain tissue. J. Virol. 67:1990;6148-6153.
61. Lu Z., Berson J. F., Chen Y., Turner J. D., Zhang T., Sharron M., Jenks M. H., Wang Z., Kim J., Rucker J., Hoxie J. A., Peiper S. C., Doms R. W. Evolution of HIV-1 coreceptor usage through interactions with distinct CCR5 and CXCR4 domains. Proc. Natl. Acad. Sci. USA. 94:1997;6426-6431.
62. Maddon P. J., Dalgleish A. G., McDougal J. S., Clapham P. R., Weiss R. A., Axel R. A. The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell. 47:1986;333-385.
63. Marcon L., Choe H., Martin K. A., Farzan M., Ponath P. D., Wu L., Newman W., Gerard N., Gerard C., Sodroski J. Utilization of C-C chemokine receptor 5 by the envelope glycoproteins of a pathogenic simian immunodeficiency virus, SIVmac239. J. Virol. 71:1997;2522-2527.
64. McDougal J. S., Kennedy M. S., Sligh J. M., Cort S. P., Mawle A., Nicholson J. K. A. Binding of HTLV-III/LAV to T4+ T cells by a complex of the 110K viral protein and the T4 molecule. Science. 231:1986;382-385.
65. McKnight A., Wilkinson D., Simmons G., Talbot S., Picard L., Ahuja M., Marsh M., Hoxie J. A., Clapham P. R. Inhibition of human immunodeficiency virus fusion by a monoclonal antibody to a coreceptor (CXCR4) is both cell type and virus strain dependent. J. Virol. 71:1997;1692-1696.
66. Michael N. L., Chang G., Louis L. G., Mascola J. R., Dondero D., Birx D. L., Sheppard H. W. The role of viral phenotype and CCR-5 gene defects in HIV-1 transmission and disease progression. Nature Med. 3:1997;338-340.
67. Miller L. H., Mason S. J., Dvorak J. A., McGinniee M. H., Rothman I. K. Erythrocyte receptors for plasmodium knowlesi malaria: Duffy blood group determinants. Science. 189:1975;561-563.
68. Moore J., Jameson B., Weiss R., Sattentau Q. The HIV-cell fusion reaction. Viral Fusion Mechanisms. 1993;CRC Press, Boca Raton. p. 233-289.
69. Moore J. P. Coreceptors: Implications for HIV pathogenesis and therapy. Science. 276:1997;51-52.
70. Mori K., Ringler D. J., Desrosiers R. C. Restricted replication of simian immunodeficiency virus strain 239 in macrophages is determined by env but is not due to restricted entry. J. Virol. 67:1993;2807-2814.
71. Mori K., Ringler D. J., Kodama T., Derosiers R. C. Complex determinants of macrophage tropism in env of simian immunodeficiency virus. J. Virol. 66:1992;2067-2075.
72. Nagasawa T., Hirota S., Tachibana K., Takakura N., Nishikawa S., Kitamura Y., Yoshida N., Kikutani H., Kishimoto T. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1. Nature. 382:1996;635-638.
73. O'Brien T. R., Winkler C., Dean M., Nelson J. A. E., Carr. HIV-1 infection in a man homozygous for CCR5Δ32. Lancet. 349:1997;1219.
74. O'Brien W. A., Koyanagi Y., Namazie A., Zhao J.-Q., Diagne A., Idler K., Zack J. A., Chen I. S. Y. HIV-tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature. 348:1990;69-73.
75. Oberlin E., Amara A., Bachelerie F., Bessia C., Virelizier J.-L., Arenzana-Seisdedos F., Schwartz O., Heard J.-M., Clark-Lewis I., Legler D. F., Loetscher M., Baggiolini M., Moser B. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell line-adapted HIV-1. Nature. 382:1996;833-835.
76. Pantaleo G., Graziosi C., Fauci A. S. New concepts in the immunopathogenesis of human immunodeficiency virus infection. N. Engl. J. Med. 328:1993;327-335.
77. Paxton W. A., Martin S. R., Tse D., O'Brien T. R., Skurnick J., VanDevanter N. L., Padian N., Braun J. F., Kotler D. P., Wolinsky S. M., Koup R. A. Relative resistance to HIV-1 infection of CD4 lymphocytes from persons who remain uninfected despite multiple high-risk sexual exposures. Nature Med. 2:1996;412-417.
78. Peiper S. C., Wang Z.-X., Neote K., Martin A. W., Showell H. J., Conklyn M. J., Ogborne K., Hadley T. J., Lu Z.-H., Hesselgesser J., Horuk R. The Duffy antigen/receptor for chemokines (DARC) is expressed in endothelial cells of Duffy negative individuals who lack the erythrocyte receptor. J. Exp. Med. 181:1995;1311-1317.
79. Picard L., Wilkinson D. A., McKnight A., Gray P. W., Hoxie J. A., Clapham P. R., Weiss R. A. Role of the amino-terminal extracellular domain of CXCR4 in human immunodeficiency virus type 1 entry. Virology. 231:1997;105-111.
80. Pleskoff O., Sol N., Labrosse B., Alizon M. Human immunodeficiency virus strains differ in their ability to infect CD4+ cells expressing the rat homolog of CXCR-4 (Fusin). J. Virol. 71:1997;3259-3262.
81. Rana S., Besson G., Cook D. G., Rucker J., Smyth R. J., Yi Y., Turner J., Guo H., Du J.-G., Peiper S. C., Lavi E., Samson M., Libert F., Liesnard C., Vassart G., Doms R. W., Parmentier M., Collman R. G. Role of CCR5 in infection of primary macrophages and lymphocytes by M-tropic strains of HIV: Resistance to patient-derived and prototype isolates resulting from theΔccr5. J. Virol. 71:1997;3219-3227.
82. Raport C. J., Gosling J., Schweickart V. L., Gray P. W., Charo I. F. Molecular cloning and functional characterization of a novel human CC chemokine receptor (CCR5) for RANTES, MIP-1β, and MIP-1α J. Biol. Chem. 271:1996;17161-17166.
83. Reeves J. D., McKnight A., Potempa S., Simmons G., Gray P. W., Power C. A., Wells T., Weiss R. A., Talbot S. J. CD4-independent infection by HIV-2 (ROD/B): Use of the 7-transmembrane receptors CXCR-4, CCR-3, and V28 for entry. Virology. 231:1997;130-134.
84. Roos M. T. L., Lange J. M. A., Goede R. E. Y. d., Coutinho R. A., Schellekens P. T. A., Miedema F., Tersmette M. Viral phenotype and immune response in primary human immunodeficiency virus type 1 infection. J. Infect. Dis. 165:1992;427-432.
85. Rubbert A., Weissman D., Combadiere C., Pettrone K. A., Daucher J. A., Murphy P. M., Fauci A. S. Multifactorial nature of noncytolytic CD8+ T-cell-mediated suppression of HIV replication: β-chemokine-dependent and -independent effects. AIDS Res. Human Retroviruses. 13:1997;63-69.
86. Rucker J., Samson M., Doranz B. J., Libert F., Berson J., Yi Y., Collman R. G., Vassart G., Broder C. C., Doms R. W., Parmentier M. Regions in β-chemokine receptors CKR-5 and CKR-2b that determine HIV-1 cofactor specificity. Cell. 87:1996;437-446.
87. Samson M., Labbe O., Mollereau C., Vassart G., Parmentier M. Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry. 35:1996a;3362-3367.
88. Samson M., Libert F., Doranz B. J., Rucker J., Liesnard C., Farber C.-M., Saragosti S., Lapoum roulie C., Cogniaux J., Forceille C., Muyldermans G., Verhofstede C., Burtonboy G., Georges M., Imai T., Rana S., Yi Y., Smyth R. J., Collman R. G., Doms R. W., Vassart G., Parmentier M. Resistance to HIV-1 infection of Caucasian individuals bearing mutant alleles of the CCR5 chemokine receptor gene. Nature. 382:1996b;722-725.
89. Schnittman S. M., Lane H. C., Greenhouse J., Justement J. S., Baseler M., Fauci A. S. Preferential infection of CD4+ memory T cells by human immunodeficiency virus type 1: Evidence for a role in the selective T-cell functional defects observed in infected individuals. Proc. Natl. Acad. Sci. USA. 87:1990;6058-6062.
90. Schuitemaker H., Koot M., Koostra N. A., Dercksen M. W., Goede R. E. Y. d., Steenwijk R. P. v., Lange J. M. A., Schattenkerk J. K. M. E., Miedema F., Tersmette M. Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: Progression of disease is associated with a shift from monocytotropic to T-cell tropic populations. J. Virol. 66:1992;1354-1360.
91. Shioda T., Levy J. A., Cheng-Meyer C. Macrophage and T-cell line tropisms of HIV-1 are determined by specific regions of the envelope gp120 gene. Nature. 349:1991;167-169.
92. Simmons G., Clapham P. R., Picard L., Offord R. E., Rosenkilde M. M., Schwartz T. W., Buser R., Wells T. N. C., Proudfoot W. E. I. Potent inhibition of HIV-1 infectivity in macrophages and lymphocytes by a novel CCR5 antagonist. Science. 276:1997;276-279.
93. Simmons G., Wilkinson D., Reeves J. D., Dittman M. T., Beddows S., Weber J., Carnegis G., Gesselberger U., Gray P. W., Weiss R. A., Clapham P. R. 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. 70:1996;8355-8360.
94. Stephens E. B., McClure H. M., Narayan O. The proteins of lymphocyte-tropic and macrophage-tropic strains of simian immunodeficiency virus are processed differently in macrophages. Virology. 206:1995;535-544.
95. Tachibana K., Nakajima T., Sato A., Igarashi K., Shida H., Iizasa H., Yoshida N., Yoshie O., Kishimoto T., Nagasawa T. CXCR4/fusin is not a species-specific barrier in murine cells for HIV-1 entry. J. Exp. Med. 185:1997;1865-1870.
96. Tersmette M., deGoede R. E. Y., Ai B. J. M., Winkel I. N., Gruters R. A., Cuypers H. T., Huisman H. G., Miedema F. Differential syncytium-inducing capacity of human immunodeficiency virus isolates: Frequent detection of syncytium-inducing isolates in patients with acquired immunodeficiency virus syndrome (AIDS) and AIDS-related complex. J. Virol. 62:1988;2026-2032.
97. Tersmette M., Gruters R., Wolf F. d., Goede R. E. Y. d., Lange J. M. A., Schellekens P. T. A., Goudsmit J., Huisman H. G., Meidema F. Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency virus syndrome: Studies on sequential isolates. J. Virol. 63:1989a;2118-2125.
98. Tersmette M., Lange J. M. A., Goed R. E. Y. d., Wolf F. d., Schattenkerk J. K. M. E., Schellekens P. T. A., Coutinho R. A., Huisman H. G., Goudsmit J., Meidema F. Association between biological properties of human immunodeficiency virus variants and risk for AIDS and AIDS mortality. Lancet. i:1989b;983-985.
99. Theodorou I., Meyer L., Magierowska M., Katlana C., Rouzioux C. HIV-1 infection in an individual homozygous for CCR5Δ32. Lancet. 349:1997;1219.
100. Tournamille C., Colin Y., Cartron J. P., Kim C. L. Disruption of a GATA motif in the Duffy gene promoter abolishes erythroid gene expression in Duffy negative individuals. Nature Genet. 10:1995;224-228.
101. Trkola A., Drajic T., Arthos J., Binley J. M., Olson W. C., Allaway G. P., Cheng-Mayer C., Robinson J., Maddon P. J., Moore J. P. CD4-dependent, antibody-sensitive interactions between HIV-1 and its coreceptor CCR-5. Nature. 384:1996;184-187.
102. Walker C. M., Levy J. A. A diffusable lymphokine produced by CD8+ T lymphocytes suppresses HIV replication. Immunology. 66:1989;628-630.
103. Walker C. M., Moody D. J., Sites D. P., Levy J. A. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 234:1986;1563-1566.
104. Weissenhorn W., Dessen A., Harrison S. C., Skehel J. J., Wiley D. C. Atomic structure of the ectodomain from HIV-1 gp41. Nature. 387:1997;426-430.
105. Westervelt P., Trowbridge D. B., Epstein L. G., Blumberg B. M., Li X., Hahn B. H., Shaw G. M., Price R. W., Ratner L. Macrophage tropism determinants of human immunodeficiency virus type 1 in vivo. J. Virol. 66:1992;2577-2582.
106. 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. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5. Nature. 384:1996;179-183.
107. Wu L., Paxton W. A., Kassam N., Ruffing N., Rottman J. B., Sullivan N., Choe H., Sodroski J., Newman W., Koup R. A., Mackay C. R. CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J. Exp. Med. 185:1997;1681-1691.
108. Zhu T., Mo H., Wang N., Nam D. S., Cao Y., Koup R. A., Ho D. D. Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science. 261:1993;1179-1181.