Permanent occupancy of the human immunodeficiency virus type 1 enhancer by NF-κB is needed for persistent viral replication in monocytes

Journal of Virology

Volumn 70, Issue 5, 1996, Pages 2930-2938

  Jacque J M ^a   Fernandez B ^a   Arenzana Seisdedos, F ^a   Thomas, D ^a   Baleux, F ^a   Virelizier, J L ^a   Bachelerie, F ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; ENHANCER REGION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; VIRUS DNA CELL DNA INTERACTION; VIRUS MUTATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

EID: 0029940011     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.5.2930-2938.1996     Document Type: Article

References (67)

1. Adams, M., L. Sharmeen, J. Kimpton, J. M. Romeo, J. V. Garcia, B. M. Peterlin, M. Groudine, and M. Emerman. 1994. Cellular latency in human immunodeficiency virus-infected individuals with high CD4 levels can be detected by the presence of promoter-proximal transcripts. Proc. Natl. Acad. Sci. USA 91:3862-3866.
2. Alcamí, J., T. Laín De Lera, L. Folgueira, M. A. Pedraza, J. M. Jacqué, F. Bachelerie, A. R. Noriega, R. T. Hay, D. Harrich, R. B. Gaynor, J.-L. Virelizier, and F. Arenzana-Seisdedos. 1995. Absolute dependence on κB responsive elements for initiation and Tat-mediated amplification of HIV transcription in blood CD4 T lymphocytes. EMBO J. 14:1552-1560.
3. Arenzana-Seisdedos, F., J. Thompson, M. Rodriguez, F. Bachelerie, D. Thomas, and R. Hay. 1995. Inducible nuclear expression of newly synthesized IκBα negatively regulates DNA-binding and transcriptional activities of NF-κB. Mol. Cell Biol. 15:2689-2696.
4. Arrigo, S., S. R. Weitsman, J. D. Rosenblatt, and I. S. Y. Chen. 1989. Analysis of rev function on human immunodeficiency virus type 1 replication in lymphoid cells by using a quantitative polymerase chain reaction method. J. Virol. 63:4875-1881.
5. Bachelerie, F., J. Alcami, F. Arenzana-Seisdedos, and J.-L. Virelizier. 1991. HIV enhancer activity perpetuated by NF-kappa B induction on infection of monocytes. Nature (London) 350:709-712.
6. Baeuerle, P. A., and D. Baltimore. 1988 Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-κB transcription factor. Cell 53:211-217.
7. Beg, A. A., T. S. Finco, P. V. Nantermet, and A. S. Baldwin, Jr. 1993 Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα. a mechanism for NF-κB activation. Mol. Cell. Biol. 13:3301-3310
8. Bellas, R. E., N. Hopkins, and Y. Li. 1993. The NF-κB binding site is necessary for efficient replication of simian immunodeficiency virus of macaques in primary macrophages but not in T cells in vitro. J. Virol. 67:2908-2913
9. Berkhout, B., A. Gatignol, A. B. Rabson, and K. T. Jeang. 1990 TAR-independent activation of the HIV-1 LTR: evidence that tat requires specific regions of the promoter. Cell 62:757-767.
10. Brown, K. S., S. Park, T. Kanno, G. Franzoso, and U. Siebenlist. 1993. Mutual regulation of the transcriptional activator NF-κB and its inhibitor. IκBα. Proc. Natl. Acad Sci. USA 90:2532-2536.
11. Cannon, P., S.-H. Kim, C. Ulich, and S. Kim. 1994. Analysis of Tat function in human immunodeficiency virus type 1-infected low-level-expression cell lines U1 and ACH2. J. Virol. 68:1993-1997
12. Chen, B. K., K. Saksela, R. Andino, and D. Baltimore. 1994. Distinct modes of human immunodeficiency virus type 1 proviral latency revealed by super-infection of nonproductively infected cell lines with recombinant luciferase-encoding viruses. J Virol. 68:654-660
13. Chen, Z., J. Haegler, V. J. Palombella, F. Melandri, D. Scherer, D. Ballard, and T. Maniatis. 1995 Signal-induced site-specific phosphorylation targets IκBα to the ubiquitin-proteasome pathway. Genes Dev. 9:1586-1597.
14. Chiao, P. J., S. Miyamoto, and I. M. Verma. 1994. Autoregulation of IκBα activity. Proc Natl Acad. Sci. USA 91:28-32.
15. Demarchi, F., P. D'Agaro, A. Falaschi, and M. Giacca. 1993. In vivo foot-printing analysis of constitutive and inducible protein-DNA interactions at the long terminal repeat of human immunodeficiency virus type 1. J. Virol. 67:7450-7460.
16. Du, W., D. Thanos, and T. Maniatis. 1993. Mechanisms of transcriptional synergism between distinct virus-inducible enhancer elements. Cell 74:887-898.
17. Duan, L., J. W. Oakes, A. Ferraro, O. Bagasra, and R. J. Pomerantz. 1994. Tat and Rev differentially affect restricted replication of human immunodeficiency virus type 1 in various cells. Virology 199:474-478.
18. Folks, T. M., K. A. Clouse, J. Justement, A. Rabson, E. Duh, J. H. Kerhl, and A. S. Fauci. 1989. Tumor necrosis factor alpha induces expression of human immunodeficiency virus in a chronically infected T-cell clone Proc. Natl. Acad. Sci. USA 86:2365-2368.
19. Folks, T. M., J. Justement, A. Kinter, C. A. Dinarello, and A. S. Fauci. 1987. Cytokine induced expression of HIV-1 in a chronically infected promonocytic cell line. Science 238:800-802.
20. Fujita, T., G. P. Nolan, S. Ghosh, and D. Baltimore. 1992. Independent modes of transcriptional activation by the p50 and p65 subunits of NF-κB. Genes Dev. 6:775-782.
21. Gaynor, R. 1992. Cellular transcription factors involved in the regulation of HIV-1 gene expression AIDS 6:347-363.
22. Gendelman, H. E., and P. S. Morahan. 1992 Macrophages in viral infection in the macrophage, p. 189-191. Oxford University Press, Oxford
23. Greenberg, M. E., and E. B. Ziff. 1984. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature (London) 311:433-438
24. Griffin, G. E., K. Leung, T. Folks, S. Kunkels, and G. J. Nabel. 1989. Activation of HIV gene expression during monocyte differentiation by induction of NF-κB. Nature (London) 339:70-73
25. Grilli, M., J.-J. Chiu, and M. J. Lenardo. 1993. NF-κB and rel: participants in a multiform transcriptional regulator system. Int. Rev. Cytol. 143:1-62.
26. Gualberto, A., M. L. Hixon, T. S. Finco, N. D. Perkins, G. J. Nabel, and A. S. Baldwin, Jr. 1995. A proliferative p53-responsive element mediates tumor necrosis factor alpha induction of the human immunodeficiency virus type 1 long terminal repeat. Mol. Cell. Biol. 15:3450-3459.
27. Hamoui, S., J.-P. Benedetto, M. Garret, and J. Bonnet. 1994. Quantitation of mRNA species by RT-PCR on total mRNA population. PCR Methods Appl. 4:160-166.
28. 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.
29. Haskill S., A. A. Beg, S. M. Tompkins, J. S. Morris, A. D. Yurochko, A. Sampson-Johannes, K. Mondal, P. Ralph, and A. S. Baldwin, Jr. 1991. Characterization of an immediate-early gene induced in adherent monocytes that encodes IκB-like activity. Cell 65:1281-1289.
30. Henkel, T., T. Machleidt, I. Alkalay, M. Kronke, Y. Ben-Neriah, and P. A. Baeuerle. 1993. Rapid proteolysis of IκBα is necessary for activation of transcription factor NF-κB. Nature (London) 365:182-185.
31. Ho, D., A. Neuman, 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 (London) 373:123-126.
32. Ho, W.-Z., R. Cherukuri, and S. D. Douglas. 1994. The macrophage and HIV-1, p. 569-588. In B. S. Zwilling and T. K. Eisenstein (ed.), Macrophages-pathogen interactions. Marcel Dekker, Inc., New York.
33. Inoue, J., L. D. Kerr, A. Kakizuka, and I. M. Verma 1992. IκBγ a 70 kd protein identical to the C-terminal half of p110NF-κB: a new member of the IκB family. Cell 68:1109-1120.
34. Le Bail, O., R. Schmidt-Ullrich, and A. Israël 1993. Promoter analysis of the gene encoding the IκBα/MAD-3 inhibitor of NF-κB: positive regulation by members of the rel/NF-κB family. EMBO J. 12:5043-5049.
35. Liou, H. C., G. P. Nolan, S. Gosh, T. Fujita, and D. Baltimore. 1992. The NF-kappa B p50 precursor, p105 contains an internal I kappa B-like inhibitor that preferentially inhibits p50. EMBO J. 11:3003-3009.
36. Liu, J., N. D. Perkins, R. M. Schmid, and G. J. Nabel. 1992. Specific NF-κB subunits act in concert with Tat to stimulate human immunodeficiency virus type I transcription. J. Virol. 66:3883-3887.
37. Luznik, L., G. Kraus, J. Guatelli, D. Richman, and F. Wong-Staal. 1995. Tat-independent replication of human immunodeficiency viruses. J. Clin Invest. 95:328-332.
38. McElhinny, J. A., W. S. MacMorran, G. D. Bren, R. M. Ten, A. Israël, and C. V. Paya. 1995. Regulation of IκBα and p105 in monocytes and macrophages persistently infected with human immunodeficiency virus, J. Virol. 69:1500-1509.
39. Mechti, N., M. Piechaczyck, J.-M. Blanchard, L. Marty, A. Bonnieu, P. Jeanteur, and B. Lebleu. 1986. Transcriptional and post-transcriptional regulation of c-myc expression during the differentiation of murine erythroleukemia Friend cells. Nucleic Acids Res. 14:9653-9666.
40. Mellits, K. H., R. T. Hay, and S. Goodbourn. 1993. Proteolitic degradation of MAD-3 (IκBα) and enhanced processing of the NF-κB precursor p105 are obligatory steps in the activation of NF-κB. Nucleic Acids Res. 21:5059-5066.
41. Meltzer, M. S., and H. E. Gendelman. 1992 Mononuclear phagocytes as targets, tissue reservoirs, and immunoregulatory cells in human immunodeficiency virus disease, p. 239-263 In S W. Russell and S. Gordon (ed.), Macrophages biology and activation. Springer-Verlag, New York.
42. Molinari, M., and J. Milner. 1995. p53 in complex with DNA is resistant to ubiquitin-dependent proteolysis in the presence of HPV-16 E6. Oncogene 10:1849-1854
43. Moses, A. V., C. Ibanez, R. Gaynor, P. Ghazal, and J. A. Nelson. 1994. Differential role of long terminal repeat control elements for the regulation of basal and Tat-mediated transcription of the human immunodeficiency virus in stimulated and unstimulated primary human macrophages J Virol. 68:298-307.
44. Mounts, P., T.-C. Wu, and K. Peden. 1989. Method for cloning single-stranded oligonucleotides in plasmid vector. BioTechniques 7:356-359.
45. Nabel, G. J., and D. Baltimore. 1987. An inducible transcription factor that activates expression of human immunodeficiency virus in T cells. Nature (London) 326:711-713.
46. Palombella, V. J., O. Rando, A. L. Goldberg, and T. Maniatis. 1994. The ubiquitin-proteasome pathway is required for processing the NF-κB1 precursor protein and the activation of NF-κB. Cell 78:773-785.
47. Paya, C., R. Ten, C. Bessia, J. Alcami, R. T. Hay, and J.-L. Virelizier. 1992. NF-κB-dependent induction of the NF-κB p50 subunit gene promoter underlies self-perpetuation of HIV transcription in monocytic cells. Proc. Natl Acad. Sci. USA 89:7826-7830.
48. Perkins, N. D., A. B. Agranoff, E. Pascal, and G. J. Nabel. 1994. An interaction between the DNA-binding domains of RelA (p65) and Sp1 mediates human immunodeficiency virus gene activation. Mol. Cell. Biol. 14:6570-6583.
49. Perkins, N. D., N. Lawrence Edwards, C. S. Duckett, A. B. Agranoff, R. M. Schmid, and G. J. Nabel. 1993. A cooperative interaction between NF-κB and Sp1 is required for HIV-1 enhancer activation. EMBO J. 12:3551-3558
50. Poli, G., A. L. Kinter, and A. S. Fauci. 1994. Interleukin 1 induced expression of the human immunodeficiency virus alone and in synergy with interleukin 6 in chronically infected U1 cells: inhibition of inductive effects by the interleukin 1 receptor antagonist. Proc. Natl. Acad Sci. USA 91:108-112
51. Poli, G., A. Kinter, J. S. Justement, J. H. Kehrl, P. Bressler, S. Stanley, and A. Fauci. 1990. Tumor necrosis factor α functions in an autocrine manner in the induction of human immunodeficiency virus expression. Proc. Natl Acad. Sci USA 87:782-785.
52. Pomerantz, R. J., D. Trono, M. B. Feinberg, and D. Baltimore. 1990 Cells nonproductively infected with HIV-1 exhibit an aberrant pattern of viral RNA expression: a molecular model for latency. Cell 61:1271-1276.
53. Ponte, P., S. Y. Ng, J. Engel, P. Gunning, and L. Kedes. 1984. Evolutionary conservation in the untranslated regions of actin mRNAs: DNA sequence of human beta-actin cDNA. Nucleic Acids Res. 12:1687-1696.
54. Rock, K. L., C. Gramm, L. Rothstein, K. Clark, R. Stein, L. Dick, D. Hwang, and A. L. Goldberg. 1994. Inhibitors of the proteasome block degradation of most cell proteins and the generation of peptides presented on MHC class I molecules Cell 78:761-771.
55. Roff, M., J. Thompson, L. Rothstein, M. S. Rodriguez, J.-M. Jacqué, F. Baleux, F. Arenzana-Seisdedos, and R. T. Hay. Role of IκBα ubiquitination signal induced activation of NF-κB in vivo. J Biol Chem., in press.
56. Roulston, A., P. Beauparlant, N. Rice, and J. Hiscott. 1993. Chronic human immunodeficiency virus type 1 infection stimulates distinct NF-κB/rel DNA binding activities in myelomonoblastic cells. J. Virol. 67:5235-5246.
57. Roulston, A., R. Lin, P. Beauparlant, M. A. Wainberg, and J. Hiscott. 1995. Regulation of human immunodeficiency virus type 1 and cytokine gene expression in myeloid cells by NF-κB/Rel transcription factors. Microbiol. Rev 59:481-505.
58. Schmitz, M. L., and P. A. Baeuerle. 1991. The p65 subunit is responsible for the strong transcription activating potential of NF-κB. EMBO J. 10:3805-3817.
59. Schwartz, O., J.-L. Virelizier, L. Montagnier, and U. Hazan. 1990. A microtransfection method using luciferase gene for the study of HIV LTR activity. Gene 88:197-205.
60. Sun, S.-C., P. A. Ganchi, D. W. Ballard, and W. C. Greene. 1993. NF-κB controls expression of inhibitor IκB-α: evidence for an inducible autorregulatory pathway Science 259:1912-1915
61. Taylor, J. P., R. Pomerantz, O. Bagasra, M. Chowdhury, J. Rappaport, K. Khalili, and S. Amini. 1992. TAR-independent transactivation by Tat in cells derived from the CNS. a novel mechanism of HIV-1 gene regulation. EMBO J. 11:3395-3403.
62. Thompson, J. E., R. J. Phillips, H. Erdjument-Bromage, P. Tempst, and S. Ghosh. 1995 IκB-β regulates the persistent response in a biphasic activation of NF-κB. Cell 80:573-582.
63. Traencker, E. B., S. Wilk, and P. A. Baeuerle. 1994. A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of IκB-α that is still bound to NF-κB. EMBO J. 13:5433-5441.
64. Vlach, J., A. Garcia, J.-M. Jacqué, M. S. Rodriguez, S. Michelson, and J.-L. Virelizier. 1995. Induction of Sp1 phosphorylation and NF-κB-independent HIV promoter domain activity in T lymphocytes stimulated by okadaic acid. Virology 208:753-761.
65. Wei, X., S. K. Ghosh, M. E. Taylor, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoeffer, M. A. Nowak, B. H. Hahn, M. S. Saag, and G. M. Chaw. 1995 Viral dynamics in human immunodeficiency virus type 1 infection. Nature (London) 373:117-122.
66. Wulczyn, F. G., M. Naumann, and C. Scheidereit. 1992. Candidate proto-oncogene bcl-3 encodes a subunit-specific inhibitor of transcription factor NF-kappa B. Nature (London) 358:597-599.
67. Zack, J., S. Arrigo, S. R. Weitsman, A. 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.