Effective activation alleviates the replication block of CCR5-tropic HIV-1 in chimpanzee CD4+ lymphocytes

Virology

Volumn 394, Issue 1, 2009, Pages 109-118

  Decker, Julie M ^a   Zammit, Kenneth P ^a   Easlick, Juliet L ^a   Santiago, Mario L ^c   Bonenberger, Denise ^d   Hahn, Beatrice H ^a,b   Kutsch, Olaf ^a   Bibollet Ruche, Frederic ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d EMORY UNIVERSITY   (United States)

Author keywords

Activation; CCR5; CD4+ lymphocytes; Chimpanzee; HIV 1

Indexed keywords

CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; HLA DR ANTIGEN;

ANIMAL CELL; ARTICLE; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CHIMPANZEE; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE CULTURE; NONHUMAN; PRIORITY JOURNAL; VIRUS REPLICATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; HIV CORE PROTEIN P24; HIV-1; HLA-DR ANTIGENS; HUMANS; L-SELECTIN; LYMPHOCYTE ACTIVATION; PAN TROGLODYTES;

HUMAN IMMUNODEFICIENCY VIRUS 1; PAN;

EID: 70350128797     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.08.027     Document Type: Article

References (90)

1. Alter H.J., Eichberg J.W., Masur H., Saxinger W.C., Gallo R., Macher A.M., Lane H.C., and Fauci A.S. Transmission of HTLV-III infection from human plasma to chimpanzees: an animal model for AIDS. Science 226 4674 (1984) 549-552
2. Annunziato F., Galli G., Nappi F., Cosmi L., Manetti R., Maggi E., Ensoli B., and Romagnani S. Limited expression of R5-tropic HIV-1 in CCR5-positive type 1-polarized T cells explained by their ability to produce RANTES, MIP-1alpha, and MIP-1beta. Blood 95 4 (2000) 1167-1174
3. Bamshad M.J., Mummidi S., Gonzalez E., Ahuja S.S., Dunn D.M., Watkins W.S., Wooding S., Stone A.C., Jorde L.B., Weiss R.B., and Ahuja S.K. A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc. Natl. Acad. Sci. U. S. A. 99 16 (2002) 10539-10544
4. Barnaba V., Watts C., de Boer M., Lane P., and Lanzavecchia A. Professional presentation of antigen by activated human T cells. Eur. J. Immunol. 24 1 (1994) 71-75
5. Bavari S., Hunt R.E., and Ulrich R.G. Divergence of human and nonhuman primate lymphocyte responses to bacterial superantigens. Clin. Immunol. Immunopathol. 76 3 Pt. 1 (1995) 248-254
6. Beaumier C.M., Harris L.D., Goldstein S., Klatt N.R., Whitted S., McGinty J., Apetrei C., Pandrea I., Hirsch V.M., and Brenchley J.M. CD4 downregulation by memory CD4+ T cells in vivo renders African green monkeys resistant to progressive SIVagm infection. Nat. Med. 15 8 (2009) 879-885
7. Beaumont T., Broersen S., van Nuenen A., Huisman H.G., de Roda Husman A.M., Heeney J.L., and Schuitemaker H. Increased neutralization sensitivity and reduced replicative capacity of human immunodeficiency virus type 1 after short-term in vivo or in vitro passage through chimpanzees. J. Virol. 74 17 (2000) 7699-7707
8. Benton P.A., Lee D.R., and Kennedy R.C. Sequence comparisons of non-human primate HIV-1 coreceptor homologues. Mol. Immunol. 35 2 (1998) 95-101
9. Benton P.A., Timanus D.K., Shearer M.H., White G.L., Lee D.R., and Kennedy R.C. Analysis of nonhuman primate peripheral blood mononuclear cells for susceptibility to HIV-1 infection and HIV coreceptor expression. Dev. Comp. Immunol. 23 1 (1999) 97-105
10. Bhardwaj N., Young J.W., Nisanian A.J., Baggers J., and Steinman R.M. Small amounts of superantigen, when presented on dendritic cells, are sufficient to initiate T cell responses. J. Exp. Med. 178 2 (1993) 633-642
11. Bibollet-Ruche F., Gao F., Bailes E., Saragosti S., Delaporte E., Peeters M., Shaw G.M., Hahn B.H., and Sharp P.M. Complete genome analysis of one of the earliest SIVcpzPtt strains from Gabon (SIVcpzGAB2). AIDS Res. Hum. Retroviruses 20 12 (2004) 1377-1381
12. Bibollet-Ruche F., McKinney B.A., Duverger A., Wagner F.H., Ansari A.A., and Kutsch O. The quality of chimpanzee T cell activation and SIV/HIV susceptibility achieved via antibody-mediated TCR/CD3 stimulation is a function of the anti-CD3 antibody isotype. J. Virol. (2008)
13. Bleul C.C., Wu L., Hoxie J.A., Springer T.A., and Mackay C.R. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 94 5 (1997) 1925-1930
14. Bogers W.M., Koornstra W.H., Dubbes R.H., ten Haaft P.J., Verstrepen B.E., Jhagjhoorsingh S.S., Haaksma A.G., Niphuis H., Laman J.D., Norley S., Schuitemaker H., Goudsmit J., Hunsmann G., Heeney J.L., and Wigzell H. Characteristics of primary infection of a European human immunodeficiency virus type 1 clade B isolate in chimpanzees. J. Gen. Virol. 79 Pt. 12 (1998) 2895-2903
15. Bonecchi R., Bianchi G., Bordignon P.P., D'Ambrosio D., Lang R., Borsatti A., Sozzani S., Allavena P., Gray P.A., Mantovani A., and Sinigaglia F. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med. 187 1 (1998) 129-134
16. Boshell M., McLeod J., Walker L., Hall N., Patel Y., and Sansom D. Effects of antigen presentation on superantigen-induced apoptosis mediated by Fas/Fas ligand interactions in human T cells. Immunology 87 4 (1996) 586-592
17. Cayota A., Vuillier F., Scott-Algara D., Feuillie V., and Dighiero G. Differential requirements for HIV-1 replication in naive and memory CD4 T cells from asymptomatic HIV-1 seropositive carriers and AIDS patients. Clin. Exp. Immunol. 91 2 (1993) 241-248
18. Cho M.W., Shibata R., and Martin M.A. Infection of chimpanzee peripheral blood mononuclear cells by human immunodeficiency virus type 1 requires cooperative interaction between multiple variable regions of gp120. J. Virol. 70 10 (1996) 7318-7321
19. Chun T.W., Carruth L., Finzi D., Shen X., DiGiuseppe J.A., Taylor H., Hermankova M., Chadwick K., Margolick J., Quinn T.C., Kuo Y.H., Brookmeyer R., Zeiger M.A., Barditch-Crovo P., and Siliciano R.F. Quantification of latent tissue reservoirs and total body viral load in HIV-1 infection. Nature 387 6629 (1997) 183-188
20. Conley A.J., Kessler II J.A., Boots L.J., McKenna P.M., Schleif W.A., Emini E.A., Mark III G.E., Katinger H., Cobb E.K., Lunceford S.M., Rouse S.R., and Murthy K.K. The consequence of passive administration of an anti-human immunodeficiency virus type 1 neutralizing monoclonal antibody before challenge of chimpanzees with a primary virus isolate. J. Virol. 70 10 (1996) 6751-6758
21. Creson J.R., Lin A.A., Li Q., Broad D.F., Roberts M.R., and Anderson S.J. The mode and duration of anti-CD28 costimulation determine resistance to infection by macrophage-tropic strains of human immunodeficiency virus type 1 in vitro. J. Virol. 73 11 (1999) 9337-9347
22. Damaj B., Mourad W., and Naccache P.H. Superantigen-mediated human monocyte-T lymphocyte interactions are associated with an MHC class II-, TCR/CD3-, and CD4-dependent mobilization of calcium in monocytes. J. Immunol. 149 5 (1992) 1497-1503
23. de Groot N.G., and Bontrop R.E. The major histocompatibility complex class II region of the chimpanzee: towards a molecular map. Immunogenetics 50 3-4 (1999) 160-167
24. Dejucq N., Simmons G., and Clapham P.R. Expanded tropism of primary human immunodeficiency virus type 1 R5 strains to CD4(+) T-cell lines determined by the capacity to exploit low concentrations of CCR5. J. Virol. 73 9 (1999) 7842-7847
25. Derdeyn C.A., Decker J.M., Sfakianos J.N., Wu X., O'Brien W.A., Ratner L., Kappes J.C., Shaw G.M., and Hunter E. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120. J. Virol. 74 18 (2000) 8358-8367
26. Dragic T., Trkola A., Lin S.W., Nagashima K.A., Kajumo F., Zhao L., Olson W.C., Wu L., Mackay C.R., Allaway G.P., Sakmar T.P., Moore J.P., and Maddon P.J. Amino-terminal substitutions in the CCR5 coreceptor impair gp120 binding and human immunodeficiency virus type 1 entry. J. Virol. 72 1 (1998) 279-285
27. Eichberg J.W., Zarling J.M., Alter H.J., Levy J.A., Berman P.W., Gregory T., Lasky L.A., McClure J., Cobb K.E., Moran P.A., et al. T-cell responses to human immunodeficiency virus (HIV) and its recombinant antigens in HIV-infected chimpanzees. J. Virol. 61 12 (1987) 3804-3808
28. Fischer U.B., Jacovetty E.L., Medeiros R.B., Goudy B.D., Zell T., Swanson J.B., Lorenz E., Shimizu Y., Miller M.J., Khoruts A., and Ingulli E. MHC class II deprivation impairs CD4 T cell motility and responsiveness to antigen-bearing dendritic cells in vivo. Proc. Natl. Acad. Sci. U. S. A. 104 17 (2007) 7181-7186
29. Gendelman H.E., Ehrlich G.D., Baca L.M., Conley S., Ribas J., Kalter D.C., Meltzer M.S., Poiesz B.J., and Nara P. The inability of human immunodeficiency virus to infect chimpanzee monocytes can be overcome by serial viral passage in vivo. J. Virol. 65 7 (1991) 3853-3863
30. Ghosh S.K., Fultz P.N., Keddie E., Saag M.S., Sharp P.M., Hahn B.H., and Shaw G.M. A molecular clone of HIV-1 tropic and cytopathic for human and chimpanzee lymphocytes. Virology 194 2 (1993) 858-864
31. Gonzalez E., Kulkarni H., Bolivar H., Mangano A., Sanchez R., Catano G., Nibbs R.J., Freedman B.I., Quinones M.P., Bamshad M.J., Murthy K.K., Rovin B.H., Bradley W., Clark R.A., Anderson S.A., O'Connell R.J., Agan B.K., Ahuja S.S., Bologna R., Sen L., Dolan M.J., and Ahuja S.K. The influence of CCL3L1 gene-containing segmental duplications on HIV-1/AIDS susceptibility. Science 307 5714 (2005) 1434-1440
32. Herman A., Croteau G., Sekaly R.P., Kappler J., and Marrack P. HLA-DR alleles differ in their ability to present staphylococcal enterotoxins to T cells. J. Exp. Med. 172 3 (1990) 709-717
33. Herrmann T., Accolla R.S., and MacDonald H.R. Different staphylococcal enterotoxins bind preferentially to distinct major histocompatibility complex class II isotypes. Eur. J. Immunol. 19 11 (1989) 2171-2174
34. Hewitt C.R., Lamb J.R., Hayball J., Hill M., Owen M.J., and O'Hehir R.E. Major histocompatibility complex independent clonal T cell anergy by direct interaction of Staphylococcus aureus enterotoxin B with the T cell antigen receptor. J. Exp. Med. 175 6 (1992) 1493-1499
35. Kakimoto W.M., Gettie A., Smith S., Donahoe S.M., Jin X., Marx P., Connor R., and Nixon D.F. Comparison of restimulation methods to elicit SIV specific cytotoxic T-lymphocytes (CTL) in vitro: Staphylococcal enterotoxin B (SEB) provides a novel method for the quantification of SIV specific CTL precursors. Immunol. Lett. 66 1-3 (1999) 135-140
36. Kayagaki N., Kawasaki A., Ebata T., Ohmoto H., Ikeda S., Inoue S., Yoshino K., Okumura K., and Yagita H. Metalloproteinase-mediated release of human Fas ligand. J. Exp. Med. 182 6 (1995) 1777-1783
37. Koller C.A., King G.W., Hurtubise P.E., Sagone A.L., and LoBuglio A.F. Characterization of glass adherent human mononuclear cells. J. Immunol. 111 5 (1973) 1610-1612
38. Kratovac Z., Virgen C.A., Bibollet-Ruche F., Hahn B.H., Bieniasz P.D., and Hatziioannou T. Primate lentivirus capsid sensitivity to TRIM5 proteins. J. Virol. 82 13 (2008) 6772-6777
39. Kruisbeek A.M., Shevach E., and Thornton A.M. Proliferative assays for T cell function. Curr. Protoc. Immunol. (2004) Chapter 3, Unit 3 12
40. LaSalle J.M., Ota K., and Hafler D.A. Presentation of autoantigen by human T cells. J. Immunol. 147 3 (1991) 774-780
41. Lee B., Sharron M., Montaner L.J., Weissman D., and Doms R.W. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc. Natl. Acad. Sci. U. S. A. 96 9 (1999) 5215-5220
42. Lin Y.L., Mettling C., Portales P., Reynes J., Clot J., and Corbeau P. Cell surface CCR5 density determines the postentry efficiency of R5 HIV-1 infection. Proc. Natl. Acad. Sci. U. S. A. 99 24 (2002) 15590-15595
43. Loffredo J.T., Sidney J., Wojewoda C., Dodds E., Reynolds M.R., Napoe G., Mothe B.R., O'Connor D.H., Wilson N.A., Watkins D.I., and Sette A. Identification of seventeen new simian immunodeficiency virus-derived CD8+ T cell epitopes restricted by the high frequency molecule, Mamu-A*02, and potential escape from CTL recognition. J. Immunol. 173 8 (2004) 5064-5076
44. Mack M., Luckow B., Nelson P.J., Cihak J., Simmons G., Clapham P.R., Signoret N., Marsh M., Stangassinger M., Borlat F., Wells T.N., Schlondorff D., and Proudfoot A.E. Aminooxypentane-RANTES induces CCR5 internalization but inhibits recycling: a novel inhibitory mechanism of HIV infectivity. J. Exp. Med. 187 8 (1998) 1215-1224
45. Margolis L.B., Glushakova S., Grivel J.C., and Murphy P.M. Blockade of CC chemokine receptor 5 (CCR5)-tropic human immunodeficiency virus-1 replication in human lymphoid tissue by CC chemokines. J. Clin. Invest. 101 9 (1998) 1876-1880
46. Martin K.A., Wyatt R., Farzan M., Choe H., Marcon L., Desjardins E., Robinson J., Sodroski J., Gerard C., and Gerard N.P. CD4-independent binding of SIV gp120 to rhesus CCR5. Science 278 5342 (1997) 1470-1473
47. Martinson J.J., Chapman N.H., Rees D.C., Liu Y.T., and Clegg J.B. Global distribution of the CCR5 gene 32-basepair deletion. Nat. Genet. 16 1 (1997) 100-103
48. Mengozzi M., Malipatlolla M., De Rosa S.C., Herzenberg L.A., Herzenberg L.A., and Roederer M. Naive CD4 T cells inhibit CD28-costimulated R5 HIV replication in memory CD4 T cells. Proc. Natl. Acad. Sci. U. S. A. 98 20 (2001) 11644-11649
49. Mills G.B., Lee J.W., Cheung R.K., and Gelfand E.W. Characterization of the requirements for human T cell mitogenesis by using suboptimal concentrations of phytohemagglutinin. J. Immunol. 135 5 (1985) 3087-3093
50. Muller-Trutwin M.C., Corbet S., Hansen J., Georges-Courbot M.C., Diop O., Rigoulet J., Barre-Sinoussi F., and Fomsgaard A. Mutations in CCR5-coding sequences are not associated with SIV carrier status in African nonhuman primates. AIDS Res. Hum. Retroviruses 15 10 (1999) 931-939
51. Muller-Trutwin M.C., Corbet S., Souquiere S., Roques P., Versmisse P., Ayouba A., Delarue S., Nerrienet E., Lewis J., Martin P., Simon F., Barre-Sinoussi F., and Mauclere P. SIVcpz from a naturally infected Cameroonian chimpanzee: biological and genetic comparison with HIV-1 N. J. Med. Primatol. 29 3-4 (2000) 166-172
52. Mummidi S., Bamshad M., Ahuja S.S., Gonzalez E., Feuillet P.M., Begum K., Galvis M.C., Kostecki V., Valente A.J., Murthy K.K., Haro L., Dolan M.J., Allan J.S., and Ahuja S.K. Evolution of human and non-human primate CC chemokine receptor 5 gene and mRNA. Potential roles for haplotype and mRNA diversity, differential haplotype-specific transcriptional activity, and altered transcription factor binding to polymorphic nucleotides in the pathogenesis of HIV-1 and simian immunodeficiency virus. J. Biol. Chem. 275 25 (2000) 18946-18961
53. Nguyen D.H., Hurtado-Ziola N., Gagneux P., and Varki A. Loss of Siglec expression on T lymphocytes during human evolution. Proc. Natl. Acad. Sci. U. S. A. 103 20 (2006) 7765-7770
54. Ondoa P., Kestens L., Davis D., Vereecken C., Willems B., Fransen K., Vingerhoets J., Zissis G., ten Haaft P., Heeney J., and van der Groen G. Longitudinal comparison of virus load parameters and CD8 T-cell suppressive capacity in two SIVcpz-infected chimpanzees. J. Med. Primatol. 30 5 (2001) 243-253
55. Ondoa P., Davis D., Kestens L., Vereecken C., Garcia Ribas S., Fransen K., Heeney J., and van der Groen G. In vitro susceptibility to infection with SIVcpz and HIV-1 is lower in chimpanzee than in human peripheral blood mononuclear cells. J. Med. Virol. 67 3 (2002) 301-311
56. Oswald-Richter K., Grill S.M., Leelawong M., Tseng M., Kalams S.A., Hulgan T., Haas D.W., and Unutmaz D. Identification of a CCR5-expressing T cell subset that is resistant to R5-tropic HIV infection. PLoS Pathog. 3 4 (2007) e58
57. Pischinger K., Zimmermann K., Eibl M.M., and Mannhalter J.W. Comparison of early events during infection of human and chimpanzee peripheral blood mononuclear cells with HIV-1. Arch. Virol. 143 11 (1998) 2065-2076
58. Platt E.J., Wehrly K., Kuhmann S.E., Chesebro B., and Kabat D. Effects of CCR5 and CD4 cell surface concentrations on infections by macrophagetropic isolates of human immunodeficiency virus type 1. J. Virol. 72 4 (1998) 2855-2864
59. Preece G., Murphy G., and Ager A. Metalloproteinase-mediated regulation of L-selectin levels on leucocytes. J. Biol. Chem. 271 20 (1996) 11634-11640
60. Pretet J.L., Zerbib A.C., Girard M., Guillet J.G., and Butor C. Chimpanzee CXCR4 and CCR5 act as coreceptors for HIV type 1. AIDS Res. Hum. Retroviruses 13 18 (1997) 1583-1587
61. Riley J.L., Carroll R.G., Levine B.L., Bernstein W., St Louis D.C., Weislow O.S., and June C.H. Intrinsic resistance to T cell infection with HIV type 1 induced by CD28 costimulation. J. Immunol. 158 11 (1997) 5545-5553
62. Riley J.L., Levine B.L., Craighead N., Francomano T., Kim D., Carroll R.G., and June C.H. Naive and memory CD4 T cells differ in their susceptibilities to human immunodeficiency virus type 1 infection following CD28 costimulation: implicatip6s for transmission and pathogenesis. J. Virol. 72 10 (1998) 8273-8280
63. Sabbe R., Picchio G.R., Pastore C., Chaloin O., Hartley O., Offord R., and Mosier D.E. Donor- and ligand-dependent differences in C-C chemokine receptor 5 reexpression. J. Virol. 75 2 (2001) 661-671
64. Samson M., Labbe O., Mollereau C., Vassart G., and Parmentier M. Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry 35 11 (1996) 3362-3367
65. Sawyer S.L., Emerman M., and Malik H.S. Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol. 2 9 (2004) E275
66. Schuitemaker H., Meyaard L., Kootstra N.A., Dubbes R., Otto S.A., Tersmette M., Heeney J.L., and Miedema F. Lack of T cell dysfunction and programmed cell death in human immunodeficiency virus type 1-infected chimpanzees correlates with absence of monocytotropic variants. J. Infect. Dis. 168 5 (1993) 1140-1147
67. Shao W., Tang J., Song W., Wang C., Li Y., Wilson C.M., and Kaslow R.A. CCL3L1 and CCL4L1: variable gene copy number in adolescents with and without human immunodeficiency virus type 1 (HIV-1) infection. Genes. Immun. 8 3 (2007) 224-231
68. Shibata R., Hoggan M.D., Broscius C., Englund G., Theodore T.S., Buckler-White A., Arthur L.O., Israel Z., Schultz A., Lane H.C., et al. Isolation and characterization of a syncytium-inducing, macrophage/T-cell line-tropic human immunodeficiency virus type 1 isolate that readily infects chimpanzee cells in vitro and in vivo. J. Virol. 69 7 (1995) 4453-4462
69. Sodora D.L., Allan J.S., Apetrei C., Brenchley J.M., Douek D.C., Else J.G., Estes J.D., Hahn B.H., Hirsch V.M., Kaur A., Kirchhoff F., Muller-Trutwin M., Pandrea I., Schmitz J.E., and Silvestri G. Toward an AIDS vaccine: lessons from natural simian immunodeficiency virus infections of African nonhuman primate hosts. Nat. Med. 15 8 (2009) 861-865
70. Song B., Javanbakht H., Perron M., Park D.H., Stremlau M., and Sodroski J. Retrovirus restriction by TRIM5alpha variants from Old World and New World primates. J. Virol. 79 7 (2005) 3930-3937
71. Song K., Rabin R.L., Hill B.J., De Rosa S.C., Perfetto S.P., Zhang H.H., Foley J.F., Reiner J.S., Liu J., Mattapallil J.J., Douek D.C., Roederer M., and Farber J.M. Characterization of subsets of CD4+ memory T cells reveals early branched pathways of T cell differentiation in humans. Proc. Natl. Acad. Sci. U. S. A. 102 22 (2005) 7916-7921
72. Spertini F., Spits H., and Geha R.S. Staphylococcal exotoxins deliver activation signals to human T-cell clones via major histocompatibility complex class II molecules. Proc. Natl. Acad. Sci. U. S. A. 88 17 (1991) 7533-7537
73. Takehisa J., Kraus M.H., Ayouba A., Bailes E., Van Heuverswyn F., Decker J.M., Li Y., Rudicell R.S., Learn G.H., Neel C., Ngole E.M., Shaw G.M., Peeters M., Sharp P.M., and Hahn B.H. Origin and biology of simian immunodeficiency virus in wild-living western gorillas. J. Virol. 83 4 (2009) 1635-1648
74. Takehisa J., Kraus M.H., Decker J.M., Li Y., Keele B.F., Bibollet-Ruche F., Zammit K.P., Weng Z., Santiago M.L., Kamenya S., Wilson M.L., Pusey A.E., Bailes E., Sharp P.M., Shaw G.M., and Hahn B.H. Generation of infectious molecular clones of simian immunodeficiency virus from fecal consensus sequences of wild chimpanzees. J. Virol. 81 14 (2007) 7463-7475
75. Tang J., Rivers C., Karita E., Costello C., Allen S., Fultz P.N., Schoenbaum E.E., and Kaslow R.A. Allelic variants of human beta-chemokine receptor 5 (CCR5) promoter: evolutionary relationships and predictable associations with HIV-1 disease progression. Genes. Immun. 1 1 (1999) 20-27
76. ten Haaft P.J., Murthy K.K., Verstrepen B.E., Eichberg J.W., and Heeney J.L. Intact CCR-5 coreceptors in HIV-1-infected chimpanzees. Aids 11 10 (1997) 1291-1293
77. ten Haaft P., Murthy K., Salas M., McClure H., Dubbes R., Koornstra W., Niphuis H., Davis D., van der Groen G., and Heeney J. Differences in early virus loads with different phenotypic variants of HIV-1 and SIV(cpz) in chimpanzees. Aids 15 16 (2001) 2085-2092
78. Trkola A., Dragic T., Arthos J., Binley J.M., Olson W.C., Allaway G.P., Cheng-Mayer C., Robinson J., Maddon P.J., and Moore J.P. CD4-dependent, antibody-sensitive interactions between HIV-1 and its co-receptor CCR-5. Nature 384 6605 (1996) 184-187
79. Trkola A., Paxton W.A., Monard S.P., Hoxie J.A., Siani M.A., Thompson D.A., Wu L., Mackay C.R., Horuk R., and Moore J.P. Genetic subtype-independent inhibition of human immunodeficiency virus type 1 replication by CC and CXC chemokines. J. Virol. 72 1 (1998) 396-404
80. Unutmaz D., KewalRamani V.N., Marmon S., and Littman D.R. Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J. Exp. Med. 189 11 (1999) 1735-1746
81. Vicenzi E., and Poli G. Infection of CD4+ primary T cells and cell lines, generation of chronically infected cell lines, and induction of HIV expression. Curr. Protoc. Immunol. (2005) Chapter 12, Unit 12 3
82. Voevodin A., Samilchuk E., and Dashti S. A survey for 32 nucleotide deletion in the CCR-5 chemokine receptor gene (deltaccr-5) conferring resistance to human immunodeficiency virus type 1 in different ethnic groups and in chimpanzees. J. Med. Virol. 55 2 (1998) 147-151
83. Wain L.V., Bailes E., Bibollet-Ruche F., Decker J.M., Keele B.F., Van Heuverswyn F., Li Y., Takehisa J., Ngole E.M., Shaw G.M., Peeters M., Hahn B.H., and Sharp P.M. Adaptation of HIV-1 to its human host. Mol. Biol. Evol. 24 8 (2007) 1853-1860
84. Wakasugi H., Bertoglio J., Tursz T., and Fradelizi D. IL 2 receptor induction on human T lymphocytes: role for IL 2 and monocytes. J. Immunol. 135 1 (1985) 321-327
85. Walter N.A., Stebbing J., and Messier W. The potential significance of adaptive evolution and dimerization in chimpanzee intercellular cell adhesion molecules (ICAMs). J. Theor. Biol. 232 3 (2005) 339-346
86. Watanabe M., Ringler D.J., Fultz P.N., MacKey J.J., Boyson J.E., Levine C.G., and Letvin N.L. A chimpanzee-passaged human immunodeficiency virus isolate is cytopathic for chimpanzee cells but does not induce disease. J. Virol. 65 6 (1991) 3344-3348
87. Wei X., Decker J.M., Liu H., Zhang Z., Arani R.B., Kilby J.M., Saag M.S., Wu X., Shaw G.M., and Kappes J.C. Emergence of resistant human immunodeficiency virus type 1 in patients receiving fusion inhibitor (T-20) monotherapy. Antimicrob. Agents Chemother. 46 6 (2002) 1896-1905
88. Wooding S., Stone A.C., Dunn D.M., Mummidi S., Jorde L.B., Weiss R.K., Ahuja S., and Bamshad M.J. Contrasting effects of natural selection on human and chimpanzee CC chemokine receptor 5. Am. J. Hum. Genet. 76 2 (2005) 291-301
89. Wu L., Paxton W.A., Kassam N., Ruffing N., Rottman J.B., Sullivan N., Choe H., Sodroski J., Newman W., Koup R.A., and Mackay C.R. CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J. Exp. Med. 185 9 (1997) 1681-1691
90. Zacharova V., Zachar V., and Goustin A.S. Sequence of chemokine receptor gene CCR5 in chimpanzees, a natural HIV type 1 host. AIDS Res. Hum. Retroviruses. 13 13 (1997) 1159-1161