High-level replication of human immunodeficiency virus in thymocytes requires NF-κB activation through interaction with thymic epithelial cells

Journal of Virology

Volumn 73, Issue 3, 1999, Pages 2064-2073

  Chêne, Laurent ^a   Nugeyre, Marie Thérèse ^a   Barré Sinoussi, Françoise ^a   Israël, Nicole ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 7; TUMOR NECROSIS FACTOR;

ARTICLE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; LONG TERMINAL REPEAT; NONHUMAN; PRIORITY JOURNAL; THYMOCYTE; VIRUS REPLICATION;

EID: 0345390063     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.3.2064-2073.1999     Document Type: Article

References (69)

1. Akashi, K., M. Kondo, U. von Freeden, U. Jeffry, R. Murray, and I. L. Weissman. 1997. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 89:1033-1041.
2. Autran, B., P. Guiet, M. Raphael, M. Grandadam, H. Agut, D. Candotti, P. Grenot, F. Puech, P. Debré, and J.-Y. Cesbron. 1996. Thymocytes and thymic microenvironment alterations during a systemic HIV infection in a severe combined immunodeficient mouse model. AIDS 10:717-727.
3. Bach, M. K., and J. R. Brashler. 1995. Evidence that granulocyte/macrophage-colony-stimulating factor and interferon-gamma maintain the viability of human peripheral blood monocytes in part by their suppression of IL-10 production. Int. Arch. Allergy Immunol. 107:90-92.
4. Bachelerie, F., M. S. Rodriguez, C. Dargemont, D. Rousset, D. Thomas, J. L. Virelizier, and F. Arenzana-Seisdedos. 1997. Nuclear export signal of IκBα interferes with the Rev-dependent posttranscriptional regulation of human immunodeficiency virus type I. J. Cell Sci. 110:2883-2893.
5. Baldwin, A. S. 1996. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-683.
6. Braun, J., H. Valentin, M. T. Nugeyre, H. Ohayon, P. Gounon, and S. F. Barré-Sinoussi. 1996. Productive and persistent infection of human thymic epithelial cells in vitro with HIV-1. Virology 225:413-418.
7. Burkly, L., C. Hession, L. Ogata, C. Reilly, L. A. Marconi, D. Olson, R. Tizard, R. Gate, and D. Lo. 1995. Expression of relB is required for the development of thymic medulla and dendritic cells. Nature 373:531-536.
8. Chen, B. K., M. B. Feinberg, and D. Baltimore. 1997. The κB sites in the human immunodeficiency virus type 1 long terminal repeat enhance virus replication yet are not absolutely required for viral growth. J. Virol. 71:5495-5504.
9. Chêne, L., et al. Unpublished data.
10. Coffin, J. M. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267:483-489.
11. Duh, E. J., W. J. Maury, T. M. Folks, A. S. Fauci, and A. B. Rabson. 1989. Tumor necrosis factor α activates human immunodeficiency virus type 1 through induction of nuclear factor binding to the NF-κB sites in the long terminal repeat. Proc. Natl. Acad. Sci. USA 86:5974-5978.
12. Feuillard, J., C. Dargemont, V. Ferreira, N. Tarantino, P. Debre, M. Raphael, and M. Korner. 1997. Nuclear Rel-A and C-Rel protein complexes are differentially distributed within human thymocytes. J. Immunol. 158:2585-2591.
13. Fisher, M., I. MacNeil, T. Suda, J. Cupp, K. Shortman, and A. Zlotnik. 1991. Cytokines production by mature and immature thymocytes. J. Immunol. 146:3452-3456.
14. Flory, E., A. Hoffmeyer, U. Smola, U. R. Rapp, and J. T. Bruder. 1996. Raf-1 kinase targets GA-binding protein in transcriptional regulation of the human immunodeficiency virus type 1 promoter. J. Virol. 70:2260-2268.
15. Fujita, T., G. P. Nolan, H. C. Liou, M. L. Scott, and D. Baltimore. 1993. The candidate proto oncogene Bcl-3 encodes a transcriptional coactivator that activates through NF-kappa B p50 homodimers. Genes Dev. 7:1354-1363.
16. Gaynor, R. B. 1995. Regulation of HIV-1 gene expression by the transactivator protein Tat. Curr. Top. Microbiol. Immunol. 193:51-77.
17. Giroir, B. P., T. Brown, and B. Beutler. 1992. Constitutive synthesis of tumor necrosis factor in the thymus. Proc. Natl. Acad. Sci. USA 89:4864-4868.
18. Gringhuis, S. I., L. Deleij, E. W. Verschuren, P. Borger, and E. Vellenga. 1997. Interleukin-7 upregulates the interleukin-2-gene expression in activated human T lymphocytes at the transcriptional level by enhancing the DNA binding activities of both nuclear factor of activated T cells and activator protein-1. Blood 90:2690-2700.
19. Harrich, D., J. Garcia, R. Mitsuyasu, and R. Gaynor. 1990. TAR independent activation of the human immunodeficiency virus in phorbol ester stimulated T lymphocytes. EMBO J. 9:4417-4423.
20. Hazan, U., D. Thomas, J. Alcami, F. Bachelerie, N. Israël, H. Yssel, J.-L. Virelizier, and F. Arenzana-Seisdedos. 1990. Stimulation of a human T-cell clone with anti-CD3 or tumor necrosis factor induces NF-κB translocation but not human immunodeficiency virus 1 enhancer-dependent transcription. Proc. Natl. Acad. Sci. USA 87:7861-7865.
21. Hellerstein, M. K., and J. M. McCune. 1997. T cell turnover in HIV-1 disease. Immunity 7:583-589.
22. Herbelin, A., F. Machavoine, E. Schneider, M. Papiernik, and M. Dy. 1992. IL-7 is requisite for IL-1-induced thymocyte proliferation. Involvement of IL-7 in the synergistic effects of granulocyte-macrophage colony-stimulating factor or tumor necrosis factor with IL-1. J. Immunol. 148:99-105.
23. Herbelin, A., F. Machavoine, A. Vicari, E. Schneider, M. Papiernik, H. Ziltener, C. Penit, and M. Dy. 1994. Endogenous granulocyte-macrophage colony-stimulating factor is involved in IL-1-and IL-7-induced murine thymocyte proliferation. J. Immunol. 153:1973-1981.
24. Hernandez-Caselles, T., M. Martinez-Esparza, D. Sancho, G. Rubio, and P. Aparicio. 1995. Interleukin-7 rescues human activated T lymphocytes from apoptosis induced by glucocorticosteroids and regulates bcl-2 and CD25 expression. Hum. Immunol. 43:181-189.
25. Ho, D. D., A. U. Neumann, A. S. Perelson, W. Chen, J. M. Leonard, and M. Markowitz. 1995. Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373:123-126.
26. Israël, A., O. Yano, F. Logeat, M. Kieran, and P. Kourilsky. 1989. Two purified factors bind to the same sequence in the enhancer of mouse MHC class I genes: one of them is a positive regulator induced upon differentiation of teratocarcinoma cells. Nucleic Acids Res. 17:5245-5257.
27. Israël, A. Personal communication.
28. Israël, N., U. Hazan, J. Alcami, A. Munier, F. Arenzana-Seisdedos, F. Bachelerie, A. Israël, and J. L. Virelizier. 1989. Tumor necrosis factor stimulates transcription of HIV-1 in human T lymphocytes, independently and synergistically with mitogens. J. Immunol. 143:3956-3960.
29. Iversen, P. O., L. B. To, and A. F. Lopez. 1996. Apoptosis of hemopoietic cells by the human granulocyte-macrophage colony-stimulating factor mutant E21R. Proc. Natl. Acad. Sci. USA 93:2785-2789.
30. 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.
31. Kinoshita, S., L. S. Su, M. Amano, L. A. Timmerman, H. Kaneshima, and G. P. Nolan. 1997. The T cell activation factor NF-ATc positively regulates HIV-1 replication and gene expression in T cells. Immunity 6:235-244.
32. Kinoshita, T., T. Yokoda, K. Arai, and A. Miyajima. 1995. Regulation of Bcl-2 expression by oncogenic Ras protein in hematopoetic cells. Oncogene 10:2207-2212.
33. Kitano, K., C. N. Abboud, D. H. Ryan, S. G. Quan, G. C. Baldwin, and D. W. Golde. 1991. Macrophage-active colony-stimulating factors enhance human immunodeficiency virus type 1 infection in bone marrow stem cells. Blood 77:1699-1705.
34. 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.
35. Kopp, E. B., and S. Ghosh. 1995. NF-kappa B and rel proteins in innate immunity. Adv. Immunol. 58:1-27.
36. Le, P. T., S. Lazorick, L. P. Whichard, Y.-C. Yang, S. C. Clark, B. F. Haynes, and K. H. Singer. 1990. Human thymic epithelial cells produce IL-6, granulocyte-monocyte-CSF, and leukemia inhibitory factor. J. Immunol. 145: 3310-3315.
37. Leonard, J., C. Parrott, W. A. Buckler, W. Turner, E. K. Ross, M. A. Martin, and A. B. Rabson. 1989. The NF-kappa B binding sites in the human immunodeficiency virus type 1 long terminal repeat are not required for virus infectivity. J. Virol. 63:4919-4924.
38. Leonard, W. J., E. W. Shores, and P. E. Love. 1995. Role of the common cytokine receptor gamma chain in cytokine signaling and lymphoid development. Immunol. Rev. 148:97-114.
39. Lernbecher, T., U. Muller, and T. Wirth. 1993. Distinct NF-kappa B/Rel transcription factors are responsible for tissue-specific and induciblc gene activation. Nature 365:767-770.
40. Lin, J. X., T. S. Migone, M. Tsang, M. Friedmann, J. A. Weatherbee, L. Zhou, A. Yamauchi, E. T. Bloom. J. Mietz, S. John, and W. J. Leonard. 1995. The role of shared receptor motifs and common Stat proteins in the generation of cytokine pleiotropy and redundancy by 1L-2, IL-4, IL-7. IL-13, and IL-15. Immunity 2:331-339.
41. May, M. J., and S. Ghosh. 1997. Rel/NF-kappa B and I kappa B proteins: an overview. Semin. Cancer Biol. 8:63-73.
42. McCune, J. M. 1997. Thymic function in HIV-1 disease. Semin. Immunol. 9:397-404.
43. Montgomery, R. A., and M. J. Dallman. 1997. Semi-quantitative polymerase chain reaction analysis of cytokine and cytokine receptor gene expression during thymic ontogeny. Cytokine 9:717-726.
44. Murray, R., T. Suda, N. Wrighton, F. Lee, and A. Zlotnik. 1989. IL-7 is a growth and maintenance factor for mature and immature thymocyte subsets. Int. Immunol. 1:526-531.
45. Okazaki, H., M. Ito, T. Sudo, M. Hattori, S. Kano, Y. Katsura, and N. Minato. 1989. IL-7 promoters thymocyte proliferation and maintains immunocompetent thymocytes bearing alpha beta or gamma delta T-cell receptors in vitro: synergism with IL-2. J. Immunol. 143:2917-2922.
46. Osborn, L., S. Kunkel, and G. J. Nabel. 1989. Tumor necrosis factor alpha and interleukin 1 stimulate the human immunodeficiency virus enhancer by activation of the nuclear factor kappa B. Proc. Natl. Acad. Sci. USA 86: 2336-2340.
47. Papiernik, M., Y. Brossard, N. Mulliez, 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. Plum, J., S. M. De, G. Leclercq, B. Verhasselt, and B. Vandekerckhove. 1996. Interleukin-7 is a critical growth factor in early human T-cell development. Blood 88:4239-4245.
49. Rosenzweig, M., D. P. Clark, and G. N. Gaulton. 1993. Selective thymocyte depletion in neonatal HIV-1 thymic infection. AIDS 7:1601-1605.
50. Rothe, M., L. Chêne, M. Nugeyre, F. Barré-Sinoussi, and N. Israël. 1998. Contact with thymic epithelial cells as a prerequisite for cytokines enhanced HIV-1 replication in thymocytes. J. Virol. 72:5852-5861.
51. Sakata, T., S. Iwagami, Y. Tsuruta, H. Teraoka, Y. Tatsumi, Y. Kita, S. Nishikawa, Y. Takai, and H. Fujiwara. 1990. Constitutive expression of IL-7 mRNA and production of IL-7 by a cloned thymic stromal cell line. J. Leukoc. Biol. 48:205-209.
52. Sanchez-Pescador, R., M. Power, P. Barr, K. Steimer, M. Stempien, S. Brown-Shimer, W. Gee, A. Renard, A. Randolph, and J, Levy. 1985. Nucleotide sequence and expression of an AIDS-associated retrovirus (ARV-2). Science 227:484-494.
53. Santee, S. M., and S. L. Owen. 1996. Human tumor necrosis factor receptor p75/80 (CD120b) gene structure and promoter characterization. J. Biol. Chem. 271:21151-21159.
54. Schwartz, O., J. Virelizier, L. Montagnier, and U. Hazan. 1990. A microtransfection method using the luciferase encoding reporter gene for the assay of HIV LTR promoter activity. Gene 88:197-205.
55. Seth, A., D. R. Hodge, D. M. Thompson, L. Robinson, A. Panayiotakis, D. K. Watson, and T. S. Papas. 1993. ETS family proteins activate transcription from HIV-1 long terminal repeat. AIDS Res. Hum. Retroviruses 9:1017-1023.
56. 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.
57. Stein, B., A. S. Baldwin, D. W. Ballard, W. C. Greene, P. Angel, and P. Herrlich. 1993. Cross-coupling of the NF-kappa-B p65 and Fos/Jun transcription factors produces potentiated biological function. EMBO J. 12: 3879-3891.
58. Su, L., H. Kaneshima, M. Bonyhadi, S. Salimi, D. Kraft, L. Rabin, and J. M. McCune. 1995. HIV-1-induced thymocyte depletion is associated with indirect cylopathicity and infection of progenitor cells in vivo. Immunity 2:25-36.
59. Sudo, T., S. Nishikawa, N. Ohno, N. Akiyama, M. Tamakoshi, H. Yoshida, and S. Nishikawa. 1993. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc. Natl. Acad. Sci. USA 90:9125-9129.
60. Tanaka, K. E., W. C. Hatch, Y. Kress, R. Soeiro, T. Calvelli, W. K. Rashbaum, A. Rubinstein, and W. D. Lyman. 1992. HIV-1 infection of human fetal thymocytes. J. Acquired Immune Defic. Syndr. 5:94-101.
61. 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 10:9-16.
62. Valentin, H., M.-T. Nugeyre, F. Vuillier, L. Boumsell, M. Schmid, F. Barré-Sinoussi, and R. 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.
63. Wei, X., S. K. Ghosh, M. E. Taylor, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoefer, M. A. Nowak, B. H. Hahn, M. S. Saag, and G. M. Shaw. 1995. Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373:117-122.
64. Weih, F., D. Carrasco, and R. Bravo. 1994. Constitutive and inducible Rel/ NF-kappa B activities in mouse thymus and spleen. Oncogene 9:3289-3297.
65. Whiteside, S., M. Ernst, O. Lebail, C. Laurent-Winter, N. Rice, and A. Israel. 1995. N-and C-terminal sequences control degradation of MAD3/IκBα in response to inducers of NF-kappa B activity. Mol. Cell. Biol. 15:5339-5345.
66. Whiteside, S. T., and A. Israël. 1997. I kappa B proteins: structure, function and regulation. Semin. Cancer Biol. 8:75-82.
67. Withersward, E. S., R. G. Amado, P. S. Koka, B. D. Jamieson, A. H. Kaplan, I. Chen, and J. A. Zack. 1997. Transient renewal of thymopoiesis in HIV-infected human thymic implants following antiviral therapy. Nat. Med. 3:1102-1109.
68. Wolf, S. S., and A. Cohen. 1992. Expression of cytokines and their receptors by human thymocytes and thymic stromal cells. Immunology 77:362-368.
69. Zuniga-Pflücker, J. C., D. Jiang, and M. J. Lenardo. 1995. Requirement for TNF-α and IL-1α in fetal thymocyte commitment and differentiation. Science 268:1906-1909.