TLR2 activation enhances HIV nuclear import and infection through T cell activation-independent and -dependent pathways

Journal of Immunology

Volumn 188, Issue 3, 2012, Pages 992-1001

  Ding, Jian ^a   Chang, Theresa L ^a,b  

^a PUBLIC HEALTH RESEARCH INSTITUTE   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD4 ANTIGEN; CYCLOSPORIN A; I KAPPA B KINASE ALPHA; I KAPPA B KINASE INHIBITOR; INTERLEUKIN 2; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; T LYMPHOCYTE RECEPTOR; TOLL LIKE RECEPTOR 2;

ARTICLE; CD4+ T LYMPHOCYTE; CELL CYCLE PROGRESSION; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOSTIMULATION; NONHUMAN; NUCLEAR IMPORT; PRIORITY JOURNAL; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; VIRUS CELL INTERACTION;

ACTIVE TRANSPORT, CELL NUCLEUS; CELLS, CULTURED; HIV; HIV INFECTIONS; HUMANS; LYMPHOCYTE ACTIVATION; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 2;

EID: 84856569976     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102098     Document Type: Article

References (57)

1. Cohen, M. S., and W. C. Miller. 1998. Sexually transmitted diseases and human immunodeficiency virus infection: cause, effect, or both? Int. J. Infect. Dis. 3: 1-4. (Pubitemid 28531447)
2. Plummer, F. A., J. N. Simonsen, D. W. Cameron, J. O. Ndinya-Achola, J. K. Kreiss, M. N. Gakinya, P. Waiyaki, M. Cheang, P. Piot, A. R. Ronald, et al. 1991. Cofactors in male-female sexual transmission of human immunodeficiency virus type 1. J. Infect. Dis. 163: 233-239.
3. Cameron, D. W., J. N. Simonsen, L. J. D'Costa, A. R. Ronald, G. M. Maitha, M. N. Gakinya, M. Cheang, J. O. Ndinya-Achola, P. Piot, R. C. Brunham, et al. 1989. Female to male transmission of human immunodeficiency virus type 1: risk factors for seroconversion in men. Lancet 2: 403-407. (Pubitemid 19195957)
4. Ghys, P. D., K. Fransen, M. O. Diallo, V. Ettiègne-Traoré, I. M. Coulibaly, K. M. Yeboué, M. L. Kalish, C. Maurice, J. P. Whitaker, A. E. Greenberg, and M. Laga. 1997. The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Côte d'Ivoire. AIDS 11: F85-F93. (Pubitemid 27421168)
5. Prebeck, S., H. Brade, C. J. Kirschning, C. P. da Costa, S. Dürr, H. Wagner, and T. Miethke. 2003. The Gram-negative bacterium Chlamydia trachomatis L2 stimulates tumor necrosis factor secretion by innate immune cells independently of its endotoxin. Microbes Infect. 5: 463-470. (Pubitemid 36570472)
6. Singleton, T. E., P. Massari, and L. M. Wetzler. 2005. Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J. Immunol. 174: 3545-3550. (Pubitemid 40354063)
7. + T cells through TLR2 activation. J. Immunol. 184: 2814-2824.
8. Lee, M. S., and Y. J. Kim. 2007. Signaling pathways downstream of patternrecognition receptors and their cross talk. Annu. Rev. Biochem. 76: 447-480.
9. Palm, N. W., and R. Medzhitov. 2009. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 227: 221-233.
10. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
11. + T cells. Science 286: 1353-1357.
12. + T cells more susceptible to productive infection with X4 and R5 HIV-type 1. J. Immunol. 179: 4357-4366.
13. Blasius, A. L., and B. Beutler. 2010. Intracellular Toll-like receptors. Immunity 32: 305-315.
14. Lee, M. S., and Y. J. Kim. 2007. Signaling pathways downstream of patternrecognition receptors and their cross talk. Annu. Rev. Biochem. 76: 447-480.
15. Li, X., S. Jiang, and R. I. Tapping. 2010. Toll-like receptor signaling in cell proliferation and survival. Cytokine 49: 1-9.
16. Fauci, A. S. 1996. Host factors and the pathogenesis of HIV-induced disease. Nature 384: 529-534. (Pubitemid 26415922)
17. Unutmaz, D. 2001. T cell signaling mechanisms that regulate HIV-1 infection. Immunol. Res. 23: 167-177. (Pubitemid 32575358)
18. Graziosi, C., K. R. Gantt, M. Vaccarezza, J. F. Demarest, M. Daucher, M. S. Saag, G. M. Shaw, T. C. Quinn, O. J. Cohen, C. C. Welbon, et al. 1996. Kinetics of cytokine expression during primary human immunodeficiency virus type 1 infection. Proc. Natl. Acad. Sci. USA 93: 4386-4391. (Pubitemid 26144297)
19. Alfano, M., and G. Poli. 2005. Role of cytokines and chemokines in the regulation of innate immunity and HIV infection. Mol. Immunol. 42: 161-182. (Pubitemid 39361447)
20. Kabelitz, D. 2007. Expression and function of Toll-like receptors in T lymphocytes. Curr. Opin. Immunol. 19: 39-45. (Pubitemid 46084902)
21. Imanishi, T., H. Hara, S. Suzuki, N. Suzuki, S. Akira, and T. Saito. 2007. Cutting edge: TLR2 directly triggers Th1 effector functions. J. Immunol. 178: 6715-6719. (Pubitemid 46847393)
22. Komai-Koma, M., L. Jones, G. S. Ogg, D. Xu, and F. Y. Liew. 2004. TLR2 is expressed on activated T cells as a costimulatory receptor. Proc. Natl. Acad. Sci. USA 101: 3029-3034. (Pubitemid 38327729)
23. Loures, F. V., A. Pina, M. Felonato, and V. L. Calich. 2009. TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J. Immunol. 183: 1279-1290.
24. Nichols, J. R., A. L. Aldrich, M. M. Mariani, D. Vidlak, N. Esen, and T. Kielian. 2009. TLR2 deficiency leads to increased Th17 infiltrates in experimental brain abscesses. J. Immunol. 182: 7119-7130.
25. + regulatory T cells in HIV infection. Microbes Infect. 7: 1063-1065.
26. Kanwar, B., D. Favre, and J. M. McCune. 2010. Th17 and regulatory T cells: implications for AIDS pathogenesis. Curr. Opin. HIV AIDS 5: 151-157.
27. Elhed, A., and D. Unutmaz. 2010. Th17 cells and HIV infection. Curr. Opin. HIV AIDS 5: 146-150.
28. 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. (Pubitemid 27098147)
29. Chen, B. K., K. Saksela, R. Andino, and D. Baltimore. 1994. Distinct modes of human immunodeficiency virus type 1 proviral latency revealed by superinfection of nonproductively infected cell lines with recombinant luciferase-encoding viruses. J. Virol. 68: 654-660. (Pubitemid 24022165)
30. Wersto, R. P., F. J. Chrest, J. F. Leary, C. Morris, M. A. Stetler-Stevenson, and E. Gabrielson. 2001. Doublet discrimination in DNA cell-cycle analysis. Cytometry 46: 296-306. (Pubitemid 33055231)
31. Zack, J. A., S. J. Arrigo, S. R. Weitsman, A. S. Go, A. Haislip, and I. S. Chen. 1990. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 61: 213-222.
32. Zazzi, M., L. Romano, M. Catucci, G. Venturi, A. De Milito, P. Almi, A. Gonnelli, M. Rubino, U. Occhini, and P. E. Valensin. 1997. Evaluation of the presence of 2-LTR HIV-1 unintegrated DNA as a simple molecular predictor of disease progression. J. Med. Virol. 52: 20-25. (Pubitemid 27243549)
33. Cara, A., A. Cereseto, F. Lori, and M. S. Reitz, Jr. 1996. HIV-1 protein expression from synthetic circles of DNA mimicking the extrachromosomal forms of viral DNA. J. Biol. Chem. 271: 5393-5397. (Pubitemid 26083873)
34. + T cells requires a cyclosporin A-sensitive pathway. J. Immunol. 158: 512-517.
35. + regulatory T cell function via innate TLR2 signaling. J. Clin. Invest. 116: 2022-2032.
36. MacLeod, H., and L. M. Wetzler. 2007. T cell activation by TLRs: a role for TLRs in the adaptive immune response. Sci. STKE 2007: pe48.
37. 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. (Pubitemid 28544121)
38. Kinoshita, S., L. 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. (Pubitemid 27148590)
39. Sherry, B., G. Zybarth, M. Alfano, L. Dubrovsky, R. Mitchell, D. Rich, P. Ulrich, R. Bucala, A. Cerami, and M. Bukrinsky. 1998. Role of cyclophilin A in the uptake of HIV-1 by macrophages and T lymphocytes. Proc. Natl. Acad. Sci. USA 95: 1758-1763. (Pubitemid 28103467)
40. Flanagan, W. M., B. Corthésy, R. J. Bram, and G. R. Crabtree. 1991. Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352: 803-807. (Pubitemid 21912434)
41. Korin, Y. D., and J. A. Zack. 1998. Progression to the G1b 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. (Pubitemid 28175559)
42. Krokan, H., E. Wist, and R. H. Krokan. 1981. Aphidicolin inhibits DNA synthesis by DNA polymerase a and isolated nuclei by a similar mechanism. Nucleic Acids Res. 9: 4709-4719. (Pubitemid 12237221)
43. Oliere, S., M. Arguello, T. Mesplede, V. Tumilasci, P. Nakhaei, D. Stojdl, N. Sonenberg, J. Bell, and J. Hiscott. 2008. Vesicular stomatitis virus oncolysis of T lymphocytes requires cell cycle entry and translation initiation. J. Virol. 82: 5735-5749. (Pubitemid 351822249)
44. Barton, G. M., and R. Medzhitov. 2003. Toll-like receptor signaling pathways. Science 300: 1524-1525. (Pubitemid 36682871)
45. Xu, D., M. Komai-Koma, and F. Y. Liew. 2005. Expression and function of Toll-like receptor on T cells. Cell. Immunol. 233: 85-89. (Pubitemid 41074059)
46. Cron, R. Q. 2001. HIV-1, NFAT, and cyclosporin: immunosuppression for the immunosuppressed? DNA Cell Biol. 20: 761-767.
47. Rohr, O., C. Marban, D. Aunis, and E. Schaeffer. 2003. Regulation of HIV-1 gene transcription: from lymphocytes to microglial cells. J. Leukoc. Biol. 74: 736-749. (Pubitemid 38040350)
48. Luban, J., K. L. Bossolt, E. K. Franke, G. V. Kalpana, and S. P. Goff. 1993. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 73: 1067-1078. (Pubitemid 23180482)
49. Krishnan, L., K. A. Matreyek, I. Oztop, K. Lee, C. H. Tipper, X. Li, M. J. Dar, V. N. Kewalramani, and A. Engelman. 2010. The requirement for cellular transportin 3 (TNPO3 or TRN-SR2) during infection maps to human immunodeficiency virus type 1 capsid and not integrase. J. Virol. 84: 397-406.
50. Frantz, B., E. C. Nordby, G. Bren, N. Steffan, C. V. Paya, R. L. Kincaid, M. J. Tocci, S. J. O'Keefe, and E. A. O'Neill. 1994. Calcineurin acts in synergy with PMA to inactivate I κB/MAD3, an inhibitor of NF-kB. EMBO J. 13: 861-870.
51. Oswald-Richter, K., S. M. Grill, M. Leelawong, and D. Unutmaz. 2004. HIV infection of primary human T cells is determined by tunable thresholds of T cell activation. Eur. J. Immunol. 34: 1705-1714. (Pubitemid 39256053)
52. Unutmaz, D., V. N. KewalRamani, S. Marmon, and D. R. Littman. 1999. Cytokine signals are sufficient for HIV-1 infection of resting human T lymphocytes. J. Exp. Med. 189: 1735-1746.
53. + T cells display altered human immunodeficiency virus infection kinetics: implications for the efficacy of antiviral agents. J. Virol. 83: 3374-3378.
54. Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351: 95-105.
55. Bain, J., L. Plater, M. Elliott, N. Shpiro, C. J. Hastie, H. McLauchlan, I. Klevernic, J. S. Arthur, D. R. Alessi, and P. Cohen. 2007. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408: 297-315.
56. Clerk, A., and P. H. Sugden. 1998. The p38-MAPK inhibitor, SB203580, inhibits cardiac stress-activated protein kinases/c-Jun N-terminal kinases (SAPKs/JNKs). FEBS Lett. 426: 93-96. (Pubitemid 28198162)
57. Lewthwaite, J. C., E. R. Bastow, K. J. Lamb, J. Blenis, C. P. Wheeler-Jones, and A. A. Pitsillides. 2006. A specific mechanomodulatory role for p38 MAPK in embryonic joint articular surface cell MEK-ERK pathway regulation. J. Biol. Chem. 281: 11011-11018. (Pubitemid 43855524)