Differential tropism and replication kinetics of human immunodeficiency virus type 1 isolates in thymocytes: Coreceptor expression allows viral entry, but productive infection of distinct subsets is determined at the postentry level

Journal of Virology

Volumn 72, Issue 12, 1998, Pages 9441-9452

  Pedroza Martins, Livia ^a   Gurney, Kevin B ^a   Torbett, Bruce E ^b   Uittenbogaart, Christel H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD1 ANTIGEN; CD69 ANTIGEN; CHEMOKINE RECEPTOR; RECEPTOR ANTIBODY; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 2; RECOMBINANT INTERLEUKIN 4; RECOMBINANT INTERLEUKIN 7; VIRUS DNA;

ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOPATHOGENIC EFFECT; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; KINETICS; PRIORITY JOURNAL; PROVIRUS; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; VIRUS INFECTIVITY; VIRUS REPLICATION;

EID: 0031794424     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.12.9441-9452.1998     Document Type: Article

References (83)

1. Adachi, A., H. E. Gendelman, S. Koenig, T. Folks, R. Willey, A. Rabson, and M. A. Martin. 1986. Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
2. Aldrovandi, G. M., G. Feuer, L. Gao, B. Jamieson, M. Kristeva, I. S. Y. Chen, and J. A. Zack. 1993. The SCID-hu mouse as a model for HIV-1 infection. Nature 363:732-736.
3. Alkhatib, G., C. Combardiere, C. C. Broder, Y. Feng, P. E. Kennedy, P. M. Murphy, and E. A. Berger. 1996. CC CKR5: a RANTES, MIP-1α, MIP-1β receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272: 1955-1958.
4. Bazan, H. A., G. Alkhatib, C. C. Broder, and E. A. Berger. 1998. Patterns of CCR5, CXCR4, and CCR3 usage by envelope glycoproteins from human immunodeficiency virus type 1 primary isolates. J. Virol. 72:4485-4491.
5. Bjorndal, A., H. Deng, M. Jansson, J. R. Fiore, C. Colognesi, A. Karlsson, J. Albert, G. Scarlatti, D. R. Littman, and E. M. Fenyo. 1997. Coreceptor usage of primary human immunodeficiency virus type 1 isolates varies according to biological phenotype. J. Virol. 71:7478-7487.
6. Bleul, C. C., L. Wu, J. A. Hoxie, T. A. Springer, and C. R. Mackay. 1997. The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc. Natl. Acad. Sci. USA 94:1925-1930.
7. Blue, M., H. Levine, J. F. Daley, K. R. Branton, and S. F. Schlossman. 1989. Expression of CD1 and class I MHC antigens by human thymocytes. J. Immunol. 142:2714-2720.
8. Calabro, M. L., C. Zanotto, F. Calderazzo, C. Crivellaro, A. Del Mistro, A. De Rossi, and L. Chieco-Bianchi. 1995. HIV-1 infection of the thymus: evidence for a cytopathic and thymotropic viral variant in vivo. AIDS Res. Hum. Retroviruses 11:11-19.
9. + T cells. Science 276:273-276.
10. Chassagne, J., P. Verrelle, C. Dionet, F. Clavel, F. Barre-Sinoussi, J. C. Chermann, L. Montagnier, J. C. Gluckmann, and D. Klatzmann. 1986. A monoclonal antibody against LAV gag precursor: use for viral protein analysis and antigenic expression in infected cells. J. Immunol. 136:1442-1445.
11. Clerici, M., and G. M. Shearer. 1994. The Th1-Th2 hypothesis of HIV infection: new insights. Immunol. Today 15:575-581.
12. Connor, R. I., K. E. Sheridan, D. Ceradini, S. Choe, and N. R. Landau. 1997. Change in coreceptor use correlates with disease progression in HIV-1-infected individuals. J. Exp. Med. 185:621-628.
13. Deng, H., R. Liu, W. Ellmeier, S. Choe, D. Unutmaz, M. Burkhart, P. DiMarzio, S. Marmon, R. E. Sutton, C. M. Hill, C. B. Davis, S. C. Peiper, T. J. Schall, D. Littman, and N. R. Landau. 1996. Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661-666.
14. Doranz, B. J., J. Rucker, Y. Yi, R. J. Smyth, M. Samson, S. C. Peiper, M. Parmentier, R. G. Collman, and R. W. Doms. 1996. 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 85:1149-1158.
15. + cells is mediated by the chemokine receptor CC-CKR5. Nature 381:667-672.
16. Endres, M. J., P. R. Clapham, M. Marsh, M. Ahuja, J. Davis Turner, A. McKnight, J. F. Thomas, B. Stoebenau-Haggarty, S. Choe, P. J. Vance, T. N. C. 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.
17. Feng, Y., C. C. Broder, P. E. Kennedy, and E. A. Berger. 1996. HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872-877.
18. Gaulton, G. N., J. V. Scobie, and M. Rosenzweig. 1997. HIV-1 and the thymus. AIDS 11:403-414.
19. Godiska, R., D. Chantry, C. J. Raport, S. Sozzani, P. Allavena, D. Leviten, A. Mantovani, and P. W. Gray. 1997. Human macrophage-derived chemokine (MDC), a novel chemoattractant for monocytes, monocyte-derived dendritic cells, and natural killer cells. J. Exp. Med. 185:1595-1604.
20. Hays, E. F., C. H. Uittenbogaart, L. W. Vollger, J. Brewer, and J. A. Zack. 1992. In vitro studies of HIV-1 expression in thymocytes from infants and children. AIDS 6:265-272.
21. He, J., Y. Chen, M. Farzan, H. Choe, A. Ohagen, S. Gartner, J. Busciglio, X. Yang, W. Hofmann, W. Newman, C. R. Mackay, J. Sodrovski, and D. Gabuzda. 1997. CCR3 and CCR5 are co-receptors for HIV-1 infection of microglia. Nature 385:645-649.
22. He, W., Y. Zhang, Y. Deng, and D. Kabelitz. 1995. Induction of TCR-γδ expression on triple-negative (CD3-CD4-CD8-) human thymocytes. J. Immunol. 154:3726-3731.
23. Heath, H., S. Qin, P. Rao, L. Wu, G. LaRosa, N. Kassam, P. D. Ponath, and C. R. Mackay. 1997. Chemokine receptor usage by eosinophils. The importance of CCR3 demonstrated using an antagonistic monoclonal antibody. J. Clin. Investig. 99:178-184.
24. Hieshima, K., T. Imai, M. Baba, K. Shoudai, K. Ishizuka, T. Nakagawa, J. Tsuruta, M. Takeya, Y. Sakaki, K. Takatsuki, R. Miura, G. Opdenakker, J. Van Damme, O. Yoshie, and H. Nomiyama. 1997. A novel human CC chemokine PARC that is most homologous to macrophage-inflammatory protein-1a/LD78a and chemotactic for T lymphocytes, but not for monocytes. J. Immunol. 159:1140-1149.
25. Huang, Y., W. A. Paxton, S. M. Wolinsky, A. U. Neumann, L. Zhang, T. He, S. Kang, D. Ceradini, Z. Jin, K. Yazdanbakhsh, K. Kunstman, D. Erickson, E. Dragon, N. R. Landau, J. Phair, D. D. Ho, and R. A. Koup. 1996. The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat. Med. 2:1240-1243.
26. Hyjek, E., H. W. Lischner, T. Hyslop, J. Bartkowiak, M. Kubin, G. Trinchieri, and D. Kozbor. 1995. Cytokine patterns during progression to AIDS in children with perinatal HIV infection. J. Immunol. 155:4060-4071.
27. Jamieson, B. D., S. Pang, G. M. Aldrovandi, J. Zha, and J. A. Zack. 1995. In vivo pathogenic properties of two clonal human immunodeficiency virus type 1 isolates. J. Virol. 69:6259-6264.
28. + cell depletion in human immunodeficiency virus type 1-infected SCID-hu mice suggests direct viral killing of thymocytes in vivo. J. Virol. 71:8245-8253.
29. Joshi, V. V., J. M. Oleske, S. Saad, C. Gadol, E. Connor, R. Bobila, and A. B. Minnefor. 1986. Thymus biopsy in children with acquired immunodeficiency syndrome. Arch. Pathol. Lab. Med. 110:837-842.
30. Kitchen, S. G., C. H. Uittenbogaart, and J. A. Zack. 1997. Mechanism of human immunodeficiency virus type 1 localization in CD4-negative thymocytes: differentiation from a CD4-positive precursor allows productive infection. J. Virol. 71:5713-5722.
31. Kitchen, S. G., and J. A. Zack. 1997. CXCR4 expression during lymphopoiesis: implications for human immunodeficiency virus type 1 infection of the thymus. J. Virol. 71:6928-6934.
32. 1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J. Virol. 72:3161-3168.
33. Koyanagi, Y., S. Miles, R. T. Mitsuyasu, J. E. Merill, 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.
34. Kozak, S. L., E. J. Platt, N. Madani, Ferro, Jr., 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.
35. Lawn, R. M., A. Efstratiadus, C. O'Connell, and T. Maniatis. 1980. The nucleotide sequence of the human β-globin gene. Cell 21:647-651.
36. Liao, F., G. Alkhatib, K. W. C. 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.
37. Liu, R., W. A. Paxton, S. Choe, D. Ceradini, S. R. Martin, R. Horuk, M. E. MacDonald, H. Stuhlmann, R. A. Koup, and N. R. Landau. 1996. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86:367-377.
38. Loetscher, P., M. Seitz, M. Baggliolini, and B. Moser. 1996. Interleukin-2 regulates CC chemokine receptor expression and chemotactic responsiveness in T lymphocytes. J. Exp. Med. 184:569-577.
39. Mackall, C. L., T. A. Fleisher, M. R. Brown, M. P. Andrich, C. C. Chen, I. M. Feuerstein, M. E. Horowitz, I. T. Magrath, A. T. Shad, S. M. Steinberg, L. H. Wexler, and R. E. Gress. 1995. Age, thymopoiesis, and CD4+ T-lymphocyte regeneration after intensive chemotherapy. N. Engl. J. Med. 332:143-149.
40. + T cells in vitro. J. Immunol. 152:330-342.
41. 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 monoclonal antibody to a coreceptor (CXCR4) is both cell type and virus strain dependent. J. Virol. 71:1692-1696.
42. Misrahi, M., J. Teglas, N. N'Go, M. Burgard, M. Mayaux, C. Rouzioux, J. Delfraissy, and S. Blanche. 1998. CCR5 chemokine receptor variant in HIV-1 mother-to-child transmission and disease progression in children. JAMA 279:277-280.
43. Moore, N. C., J. Girdlestone, G. Anderson, J. J. T. Owen, and E. J. Jenkinson. 1995. Stimulation of thymocytes before and after positive selection results in the induction of different NF-κB/Rel protein complexes. J. Immunol. 155:4653-4660.
44. Moriuchi, H., M. Moriuchi, and A. S. Fauci. 1997. Cloning and analysis of the promoter region of CCR5, a coreceptor for HIV-1 entry. J. Immunol. 159:5441-5449.
45. Moriuchi, M., H. Moriuchi, W. Turner, and A. S. Fauci. 1997. Cloning and analysis of the promoter region of CXCR4, a coreceptor for HIV-1 entry. J. Immunology 159:4322-4329.
46. Napolitano, M., A. Zingoni, G. Bernardini, G. Spinetti, A. Nista, C. T. Starlazzi, M. Rocchi, and A. Santoni. 1996. Molecular cloning of TER-1, a chemokine receptor-like gene expressed by lymphoid tissues. J. Immunol. 157:2759-2763.
47. Papiernik, M., Y. Brossard, N. Milliez, J. Roume, C. Brechot, F. Barin, A. Goudeau, J.-F. Bach, C. Griscelli, R. Henrion, and R. Vazeux. 1992. Thymic abnormalities in fetuses aborted from human immunodeficiency virus type 1 seropositive women. Pediatrics 89:297-301.
48. + T lymphocytes by HIV-1. J. Exp. Med. 187:1139-1144.
49. Power, C. A., A. Meyer, K. Nemeth, K. B. Bacon, A. J. Hoogewerf, A. E. Proudfoot, and T. N. C. Wells. 1995. Molecular cloning and functional expression of a novel CC chemokine receptor cDNA from a human basophilic cell line. J. Biol. Chem. 270:19495-19500.
50. Prevot, S., J. Audouin, J. Andre-Bougaran, R. Griffais, A. Le Tourneau, J. G. Fournier, and J. Diebold. 1992. Thymic pseudotumorous enlargement due to follicular hyperplasia in a human immunodeficiency virus sero-positive patient. Am. J. Clin. Pathol. 97:420-425.
51. Raport, C. J., J. Goslings, V. L. Schweickart, P. W. Gray, and I. F. Charo. 1996. Molecular cloning and functional characterization of a novel human CC chemokine receptor (CCR5) for RANTES, MIP-1β and MIP-1α. J. Biol. Chem. 271:17161-17166.
52. Res, P., B. Blom, T. Hori, K. Weijer, and H. Spits. 1997. Downregulation of CD1 marks acquisition of functional maturation of human thymocytes and defines a control point in late stages of human T cell development. J. Exp. Med. 185:141-151.
53. Rosenzweig, M., D. P. Clark, and G. N. Gaulton. 1993. Selective thymocyte depletion in neonatal HIV-1 thymic infection. AIDS 7:1601-1605.
54. Rucker, J., A. L. Edinger, M. Sharron, M. Samson, B. Lee, J. F. Berson, Y. Yi, B. Margulies, R. G. Collman, B. J. Doranz, M. Parmentier, and R. W. Doms. 1997. Utilization of chemokine receptors, orphan receptors, and herpesvirus-encoded receptors by diverse human and simian immunodeficiency viruses. J. Virol. 71:8999-9007.
55. Samson, M., F. Libert, B. J. Doranz, J. Rucker, C. Liesnard, C. Farber, S. Saragosti, C. Lapoumeroulie, J. Cognaux, C. Forceille, G. Muyldermans, C. Verhofstede, G. Burtonboy, M. Georges, T. Imai, S. Rana, Y. Yi, R. J. Smyth, R. G. Collman, R. W. Doms, G. Vassart, and M. Parmentier. 1996. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR5 chemokine receptor gene. Nature 382:722-725.
56. Scarlatti G., E. Tresoldi, A. Bjorndal, R. Frederiksson, C. Colognesi, H. K. Deng, M. S. Malnati, A. Plebani, A. G. Siccardi, D. R. Littman, E. M. Fenyo, and P. Lusso. 1997. In vivo evolution of HIV-1 co-receptor usage and sensitivity to chemokine-mediated suppression. Nat. Med. 3:1259-1265.
57. Schmid, I., W. J. Krall, C. H. Uittenbogaart, J. Braun, and J. V. Giorgi. 1992. Dead cell discrimination with 7-amino-actinomycin D in combination with dual color immunofluorescence in single laser flow cytometry. Cytometry 13: 204-208.
58. Schmid, I., C. H. Uittenbogaart, and J. V. Giorgi. 1991. A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry 12:279-285.
59. Schmid, I., C. H. Uittenbogaart, B. Keld, and J. V. Giorgi. 1994. A rapid method for measuring apoptosis and dual-color immunofluorescence by single laser flow cytometry. J. Immunol. Methods 170:145-157.
60. 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.
61. Smith M. W., M. Dean, M. Carrington, C. Winkler, G. A. Huttley, D. A. Lomb, J. J. Goedert, T. R. O'Brien, L. P. Jacobson, R. Kaslow, S. Buchbinder, E. Vittinghoff, D. Vlahov, K. Hoots, and M. W. Hilgartner. 1997. Contrasting genetic influence of CCR2 and CCR5 variants on HIV-1 infection and disease progression. Science 277:959-965.
62. Sozzani S., S. Ghezzi, G. Iannolo, W. Luini, A. Borsatti, N. Polentarutti, A. Sica, M. Locati, C. Mackay, T. N. C. Wells, P. Biswas, E. Vicennzi, G. Poli, and A. Mantovani. 1998. Interleukin 10 increases CCR5 expression and HIV infection in human monocytes. J. Exp. Med. 187:439-444.
63. Spina, C. A., J. C. Guatelli, and D. D. Richman. 1995. Establishment of a stable, inducible form of human immunodeficiency virus type 1 DNA in quiescent CD4 lymphocytes in vitro. J. Virol. 69:2977-2988.
64. Stanley, S. K., J. M. McCune, H. Kaneshima, J. S. Justement, M. Sullivan, E. Boone, M. Baseler, J. Adelsberger, M. Bonyhadi, J. Orenstein, C. H. Fox, and A. S. Fauci. 1993. Human immunodeficiency virus infection of the human thymus and disruption of the thymic microenvironment in the SCID-hu mouse. J. Exp. Med. 178:1151-1163.
65. Stevenson, M., T. L. Stanwick, M. P. Dempsey, and C. A. Lamonica. 1990. HIV-1 replication is controlled at the level of T cell activation and proviral integration. EMBO J. 9:1551-1560.
66. Tedder, T. F., L. C. Clement, and M. D. Cooper. 1985. Human lymphocyte differentiation antigens HB-10 and HB-11. I. Ontogeny of antigen expression. J. Immunol. 134:2983-2988.
67. bright human thymocytes. J. Immunol. 141:2557-2563.
68. Tiffany, H. L., L. L. Lautens, J. Gao, J. Pease, M. Locati, C. Combadiere, W. Modi, T. I. Bonner, and P. M. Murphy. 1997. Identification of CCR8: a human monocyte and thymus receptor for the CC chemokine I-309. J. Exp. Med. 186:165-170.
69. Ueno, Y., T. Boone, and C. H. Uittenbogaart. 1989. Selective stimulation of human thymocyte subpopulations by recombinant IL-4 and IL-3. Cell. Immunol. 118:382-393.
70. Ueno, Y., E. Hays, L. Hultin, and C. H. Uittenbogaart. 1989. Human thymocytes do not respond to interleukin-2 after removal of mature "bright" CD5 positive cells. Cell. Immunol. 124:239-251.
71. Uittenbogaart, C. H., D. J. Anisman, B. D. Jamieson, S. Kitchen, I. Schmid, J. A. Zack, and E. F. Hays. 1996. Differential tropism of HIV-1 isolates for distinct thymocyte subsets in vitro. AIDS 10:F9-F16.
72. Uittenbogaart, C. H., D. J. Anisman, J. A. Zack, A. Economides, I. Schmid, and E. F. Hays. 1995. Effects of cytokines on HIV-1 production by thymocytes. Thymus 23:155-175.
73. Uittenbogaart, C. H., S. Higashitani, I. Schmid, L. W. Vollger, T. Boone, and L. T. Clement. 1990. Interleukin-4 induces expression of the CD45RA antigen on human thymocyte subpopulations. Int. Immunol. 2:1179-1187.
74. Uittenbogaart, C. H., et al. Unpublished data.
75. Valentin, H., M.-T. Nugeyre, F. Vuillier, L. Boumsell, M. Schmid, F. Barre-Sinoussi, and R. A. Pereira. 1994. Two subpopulations of human triple-negative thymic cells are susceptible to infection by human immunodeficiency virus type 1 in vitro. J. Virol. 68:3041-3050.
76. Vandekerckhove, B. A. E., A. Barcena, D. Schols, S. Mohan-Peterson, H. Spits, and M. Roncarolo. 1994. In vivo cytokine expression in the thymus. J. Immunol. 152:1738-1743.
77. + thymocytes and identification of thymic emigrants. J. Immunol. 155:1862-1872.
78. Vicari, A. P., D. J. Figueroa, J. A. Hedrick, J. S. Foster, K. P. Singh, S. Menon, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, K. B. Bacon, and A. Zlotnik. 1997. TECK: a novel CC chemokine specifically expressed by thymic dendritic cells and potentially involved in T cell development. Immunity 7: 291-301.
79. Vollger, L. W., and C. H. Uittenbogaart. 1993. Interleukin-7 promotes the generation of phenotypically mature CD45RA positive human thymocytes in-vitro. Cytokine 5:157-168.
80. Wu, L., G. LaRosa, N. Kassam, C. J. Gordon, H. Heath, N. Ruffing, N. 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.
81. Wu, L., W. A. Paxton, N. Kassam, N. Ruffing, J. B. Rottman, N. Sullivan, H. Choe, J. Sodrovski, W. Newman, R. A. Koup, and C. R. Mackay. 1997. CCR5 levels and expression pattern correlate with infectability by macrophage-tropic HIV-1, in vitro. J. Exp. Med. 185:1681-1691.
82. Zack, J. A., S. J. Arrigo, S. R. Weitman, A. S. Go, A. Haislip, and I. S. Y. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61:213-222.
83. Zack, J. A., A. M. Haislip, P. Krogstad, and I. S. Y. Chen. 1992. Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J. Virol. 66:1717-1725.