Inhibition of CD3/CD28-mediated activation of the MEK/ERK signaling pathway represses replication of X4 but not R5 human immunodeficiency virus type 1 in peripheral blood CD4+ T lymphocytes

Journal of Virology

Volumn 74, Issue 6, 2000, Pages 2558-2566

  Popik, Waldemar ^a,b   Pitha, Paula M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; MITOGEN ACTIVATED PROTEIN KINASE;

ANTIGEN EXPRESSION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; NORMAL HUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; T LYMPHOCYTE; VIRUS CELL INTERACTION; VIRUS INHIBITION; VIRUS REPLICATION;

ANTIGENS, CD28; ANTIGENS, CD3; ANTIGENS, CD4; BIOLOGICAL TRANSPORT; BUTADIENES; CD4-POSITIVE T-LYMPHOCYTES; CELL NUCLEUS; CELLS, CULTURED; DNA, VIRAL; DOWN-REGULATION; ENZYME ACTIVATION; ENZYME INHIBITORS; HIV-1; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NITRILES; PROVIRUSES; RECEPTORS, CXCR4; TRANSCRIPTION, GENETIC; VIRUS INTEGRATION; VIRUS REPLICATION;

EID: 0034005659     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.6.2558-2566.2000     Document Type: Article

References (43)

1. Atchison, R. E., J. Gosling, F. S. Monteclaro, C. Franci, L. Digilio, I. F. Charo, and M. A. Goldsmith. 1996. Multiple extracellular elements of CCR5 and HIV-1 entry: dissociation from response to chemokines. Science 274; 1924-1926.
2. 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.
3. Briant, L., V. Robert-Hebmann, V. Sivan, A. Brunet, J. Pouyssegur, and C. Devaux. 1998. Involvement of extracellular signal-regulated kinase module in HIV-mediated CD4 signals controlling activation of nuclear factor-κB and AP-1 transcription factors. J. Immunol. 160:1875-1885.
4. Bukrinskaya, A. G., A. Ghorpade, N. K. Heinzinger, T. E. Smithgall, R. E. Lewis, and M. Stevenson. 1996. Phosphorylation-dependent human immunodeficiency virus type 1 infection and nuclear targeting of viral DNA. Proc. Natl. Acad. Sci. USA 93:367-371.
5. Cantrell, D. 1996. T cell antigen receptor signal transduction pathways Annu. Rev. Immunol. 14:259-274.
6. Chackerian, B., E. M. Long, P. A. Luciw, and J. Overbaugh. 1997. Human immunodeficiency virus type 1 coreceptors participate in postentry stages in the virus replication cycle and function in simian immunodeficiency virus infection. J. Virol. 71:3932-3939.
7. Chun, T.-W., L. Stuyver, S. B. Mizell, A. L. Ehler, J. A. Mican, M. Baseler, A. L. Lloyd, M. A. Nowak, and A. S. Fauci. 1997. Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc. Natl. Acad. Sci. USA 94:13193-13197.
8. Cicala, C., J. Arthos, M. Ruiz, M. Vaccarezza, A. Rubbert, A. Riva, K. Wildt, O. Cohen, and A. S. Fauci. 1999. Induction of phosphorylation and intracellular association of CC chemokine receptor 5 and focal adhesion kinase in primary human CD4+ T cells by macrophage-tropic HIV envelope. J. Immunol. 163:420-426.
9. 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.
10. Davis, C. B., I. Dikic, D. Unutmaz, C. M. Hill, J. Arthos, M. A. Siani, D. A. Thompson, J. Schlessinger, and D. R. Littman. 1997. Signal transduction due to HIV-1 envelope interactions with chemokine receptors CXCR4 or CCR5. J. Exp. Med. 186:1793-1798.
11. Donzella, G. A., D. Schols, S. W. Lin, J. A. Este, K. A. Nagashima, P. J. Maddon, G. P. Allaway, T. P. Sakmar, G. Henson, E. De Clercq, and J. P. Moore. 1998. AMD3100, a small molecule inhibitor of HIV-1 entry via the CXCR4 co-receptor. Nat. Med. 4:72-77.
12. Doranz, B. J., M. J. Orsini, J. D. Turner, T. L. Hoffman, J. F. Berson, J. A. Hoxie, S. C. Peiper, L. F. Brass, and R. W. Doms. 1999. Identification of CXCR4 domains that support coreceptor and chemokine receptor functions. J. Virol. 73:2752-2761.
13. Fais, S., C. Lapenta, S. M. Santini, M. Spada, S. Parlato, M. Logozzi, P. Rizza, and F. Belardelli. 1999. Human immunodeficiency virus type 1 strains R5 and X4 induce different pathogenic effects in hu-PBL-SCID mice, depending on the state of activation/differentiation of human target cells at the time of primary infection. J. Virol. 73:6453-6459.
14. Farzan, M., H. Choe, K. A. Martin, Y. Sun, M. Sidelko, C. R. Mackay, N. P. Gerard, J. Sodroski, and C. Gerard. 1997. HIV-1 entry and macrophage inflammatory protein-1-β-mediated signaling are independent functions of the chemokine receptor CCR5. J. Biol. Chem. 272:6854-6857.
15. Favata, M. F., K. Y. Horiuchi, E. J. Manos, A. J. Daulerio, D. A. Stradley, W. S. Feeser, D. E. Van Dyk, W. J. Pitts, R. A. Earl, F. Hobbs, R. A. Copeland, R. L. Magolda, P. A. Scherle, and J. M. Trzaskos. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chern. 273:18623-18632.
16. Genot, E., S. Cleverley, S. Henning, and D. Cantrell. 1996. Multiple p21ras effector pathways regulate nuclear factor of activated T cells. EMBO J. 15:3923-3933.
17. Hall, S. R., B. M. Heffernan, N. T. Thompson, and W. C. Rowan. 1999. CD4+ CD45RA+ and CD4+ CD45RO+ T cells differ in their TCR-associated signaling responses. Eur. J. Immunol. 29:2098-2106.
18. Jacque, J.-M., A. Mann, H. Enslen, N. Sharova, B. Brichacek, R. J. Davis, and M. Stevenson. 1998. Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase. EMBO J. 17:2607-2618.
19. Kerkhoff, E., R. Houben, S. Loffler, J. Troppmair, J. E. Lee, and U. R. Rapp. 1998. Regulation of c-myc expression by Ras/Raf signalling. Oncogene 16: 211-216.
20. Kinoshita, S., B. K. Chen, H. Kaneshima, and G. P. Nolan. 1998. Host control of HIV-1 parasitism in T cells by the nuclear factor of activated T cells. Cell 95:595-604.
21. 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.
22. Lee, B., M. Sharron, L. J. Montaner, D. Weissman, and R. W. Doms. 1999. Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages. Proc. Natl. Acad. Sci. USA 96:5215-5220.
23. Misse, D., M. Cerutti, N. Noraz, P. Jourdan, J. Favero, G. Devauchelle, H. Yssel, N. Taylor, and F. Veas. 1999. A CD4-independent interaction of human immunodeficiency virus-1 gp120 with CXCR4 induces their cointernalization, cell signaling, and T-cell chemotaxis. Blood 93:2454-2462.
24. Penn, M. L., J.-C. Grivel, B. Schramm, M. A. Goldsmith, and L. Margolis. 1999. CXCR4 utilization is sufficient to trigger CD4+ T cell depletion in HIV-1-infected human lymphoid tissue. Proc. Natl. Acad. Sci. USA 96:663-668.
25. Popik, W., J. E. Hesselgesser, and P. M. Pitha. 1998. Binding of human immunodeficiency virus type 1 to CD4 and CXCR4 receptors differentially regulates expression of inflammatory genes and activates the MEK/ERK signaling pathway. J. Virol. 72:6406-6413.
26. Popik, W., and P. M. Pitha. 1998. Early activation of mitogen-activated protein kinase kinase, extracellular signal-regulated kinase, p38 mitogen-activated protein kinase, and c-Jun N-terminal kinase in response to binding of simian immunodeficiency virus to Jurkat T cells expressing CCR5 receptor. Virology 252:210-217.
27. Riley, J. L., B. L. Levine, N. Craighead, T. Francomano, D. Kim, R. G. Carroll, and C. H. June. 1998. Naïve and memory CD4 T cells differ in their susceptibilities to human immunodeficiency virus type 1 infection following CD28 costimulation: implications for transmission and pathogenesis. J. Virol. 72:8273-8280.
28. Roederer, M., P. A. Raju, D. K. Mitra, L. A. Herzenberg, and L. A. Herzenberg. 1997. HIV does not replicate in naive CD4 T cells stimulated with CD3/CD28. J Clin. Investig. 99:1555-1564.
29. Scarlatti, G., E. Tresoldi, A. Bjorndal, R. Fredriksson, 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.
30. Schmidtmayerova, H., M. Alfano, G. Nuovo, and M. Bukrinsky. 1998. Human immunodeficiency virus type 1 T-lymphotropic strains enter macrophages via a CD4-and CXCR4-mediated pathway: replication is restricted at a postentry level. J. Virol. 72:4633-4642.
31. Schuitemaker, H., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. Y. de Goede, R. P. van Steenwijk, J. M. A. Lange, J. K. M. Eeftink Schattenkerk, F. Miedema, and M. Tersmette. 1992. 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 virus population. J. Virol. 66:1354-1360.
32. Spina, C. A., H. E. Prince, and D. D. Richman. 1997. Preferential replication of HIV-1 in the CD45RO memory cell subset of primary CD4 lymphocytes in vitro. J. Clin. Investeg. 99:1774-1785.
33. 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.
34. Sun, Y., and E. A. Clark. 1999. Expression of the c-myc proto-oncogene is essential for HIV-1 infection in activated T cells. J. Exp. Med. 189:1391-1397.
35. Sun, Y., L. M. Pinchuk, M. B. Agy, and E. A. Clark. 1997. Nuclear import of HIV-1 DNA in resting CD4+ T cells requires a cyclosporin A-sensitive pathway. J. Immunol. 158:512-517.
36. Varmus, H., and R. Swanstrom. 1985. Replication of retroviruses, p. 369. In R. Weiss, N. Teich, H. Varmus, and J. Coffin (ed.), RNA tumor viruses. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
37. + T lymphocytes: R5 but not X4 viruses replicate in the absence of T-cell receptor restimulation. J. Virol. 73:7515-7523.
38. Weissman, D., R. L. Rabin, J. Arthos, A. Rubbert, M. Dybul, R. Swofford, S. Venkatesan, J. M. Farber, and A. S. Fauci. 1997. Macrophage-tropic HIV and SIV envelope proteins induce a signal through the CCR5 chemokine receptor. Nature 389:981-985.
39. Yang, X., and D. Gabuzda. 1998. Mitogen-activated protein kinase phosphorylates and regulates the HIV-1 Vif protein. J. Biol. Chem. 273:29879-29887.
40. Yang, X., and D. Gabuzda. 1999. Regulation of human immunodeficiency virus type 1 infectivity by the ERK mitogen-activated protein kinase signaling pathway. J. Virol. 73:3460-3466.
41. Zack, J., 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.
42. Zhu, T., H. Mo, N. Wang, D. S. Nam, Y. Cao, R. A. Koup, and D. D. Ho. 1993. Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science 261:1179-1181.
43. Zybarth, G., N. Reiling, H. Schmidtmayerova, B. Sherry, and M. Bukrinsky. 1999. Activation-induced resistance of human macrophages to HIV-1 infection in vitro. J. Immunol. 162:400-406.