Neisseria gonorrhoeae effectively blocks HIV-1 replication by eliciting a potent TLR9-dependent interferon-α response from plasmacytoid dendritic cells

Cellular Microbiology

Volumn 12, Issue 12, 2010, Pages 1703-1717

  Dobson Belaire, Wendy N ^a   Rebbapragada, Anuradha ^a   Malott, Rebecca J ^a   Yue, Feng Yun ^a   Kovacs, Colin ^b   Kaul, Rupert ^a   Ostrowski, Mario A ^a,c   Gray Owen, Scott D ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b Canadian Immunodeficiency Research Collaborative   (Canada)

^c ST MICHAEL'S HOSPITAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; TOLL LIKE RECEPTOR 9;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; NEISSERIA GONORRHOEAE; NEISSERIACEAE INFECTION; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS REPLICATION;

CELLS, CULTURED; DENDRITIC CELLS; HIV INFECTIONS; HIV-1; HUMANS; INTERFERON-ALPHA; LEUKOCYTES, MONONUCLEAR; NEISSERIA GONORRHOEAE; TOLL-LIKE RECEPTOR 9; VIRUS REPLICATION;

BACTERIA (MICROORGANISMS); HUMAN IMMUNODEFICIENCY VIRUS 1; NEISSERIA GONORRHOEAE;

EID: 78449295245     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01502.x     Document Type: Article

References (58)

1. Achtman, M., Neibert, M., Crowe, B.A., Strittmatter, W., Kusecek, B., Weyse, E., et al. (1988) Purification and characterization of eight class 5 outer membrane protein variants from a clone of Neisseria meningitidis serogroup A. J Exp Med 168: 507-525.
2. Agrawal, T., Vats, V., Wallace, P.K., Singh, A., Salhan, S., and Mittal, A. (2009) Recruitment of myeloid and plasmacytoid dendritic cells in cervical mucosa during Chlamydia trachomatis infection. Clin Microbiol Infect 15: 50-59.
3. Anzala, A.O., Simonsen, J.N., Kimani, J., Ball, T.B., Nagelkerke, N.J., Rutherford, J., et al. (2000) Acute sexually transmitted infections increase human immunodeficiency virus type 1 plasma viremia, increase plasma type 2 cytokines, and decrease CD4 cell counts. J Infect Dis 182: 459-466.
4. Baca-Regen, L., Heinzinger, N., Stevenson, M., and Gendelman, H.E. (1994) Alpha interferon-induced antiretroviral activities: restriction of viral nucleic acid synthesis and progeny virion production in human immunodeficiency virus type 1-infected monocytes. J Virol 68: 7559-7565.
5. Barron, M.A., Blyveis, N., Palmer, B.E., MaWhinney, S., and Wilson, C.C. (2003) Influence of plasma viremia on defects in number and immunophenotype of blood dendritic cell subsets in human immunodeficiency virus 1-infected individuals. J Infect Dis 187: 26-37.
6. Bogdan, C., Mattner, J., and Schleicher, U. (2004) The role of type I interferons in non-viral infections. Immunol Rev 202: 33-48.
7. Chen, A., Boulton, I.C., Pongoski, J., Cochrane, A., and Gray-Owen, S.D. (2003) Induction of HIV-1 LTR-mediated transcription by Neisseria gonorrhoeae. AIDS 17: 625-628.
8. Coccia, E.M., Krust, B., and Hovanessian, A.G. (1994) Specific inhibition of viral protein synthesis in HIV-infected cells in response to interferon treatment. J Biol Chem 269: 23087-23094.
9. Cohen, M.S. (1998) Sexually transmitted diseases enhance HIV transmission: no longer a hypothesis. Lancet 351 (Suppl. 3): 5-7.
10. Cohen, M.S., Hoffman, I.F., Royce, R.A., Kazembe, P., Dyer, J.R., Daly, C.C., et al. (1997) Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet 349: 1868-1873.
11. Ding, J., Rapista, A., Teleshova, N., Mosoyan, G., Jarvis, G.A., Klotman, M.E., et al. (2010) Neisseria gonorrhoeae enhances HIV-1 infection of primary resting CD4+ T cells through TLR2 activation. J Immunol 184: 2814-2824.
12. Donaghy, H., Pozniak, A., Gazzard, B., Qazi, N., Gilmour, J., Gotch, F., et al. (2001) Loss of blood CD11c(+) myeloid and CD11c(-) plasmacytoid dendritic cells in patients with HIV-1 infection correlates with HIV-1 RNA virus load. Blood 98: 2574-2576.
13. Fernie, B.F., Poli, G., and Fauci, A.S. (1991) Alpha interferon suppresses virion but not soluble human immunodeficiency virus antigen production in chronically infected T-lymphocytic cells. J Virol 65: 3968-3971.
14. Finke, J.S., Shodell, M., Shah, K., Siegal, F.P., and Steinman, R.M. (2004) Dendritic cell numbers in the blood of HIV-1 infected patients before and after changes in antiretroviral therapy. J Clin Immunol 24: 647-652.
15. Fleming, D.T., and Wasserheit, J.N. (1999) From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 75: 3-17.
16. Galvin, S.R., and Cohen, M.S. (2004) The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2: 33-42.
17. Ghys, P.D., Fransen, K., Diallo, M.O., Ettiegne-Traore, V., Coulibaly, I.M., Yeboue, K.M., et al. (1997) The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Cote d'Ivoire. AIDS 11: F85-F93.
18. Gursel, I., Gursel, M., Yamada, H., Ishii, K.J., Takeshita, F., and Klinman, D.M. (2003) Repetitive elements in mammalian telomeres suppress bacterial DNA-induced immune activation. J Immunol 171: 1393-1400.
19. Hardy, A.W., Graham, D.R., Shearer, G.M., and Herbeuval, J.P. (2007) HIV turns plasmacytoid dendritic cells (pDC) into TRAIL-expressing killer pDC and down-regulates HIV coreceptors by Toll-like receptor 7-induced IFN-alpha. Proc Natl Acad Sci USA 104: 17453-17458.
20. Ho, D.D., Hartshorn, K.L., Rota, T.R., Andrews, C.A., Kaplan, J.C., Schooley, R.T., et al. (1985) Recombinant human interferon alfa-A suppresses HTLV-III replication in vitro. Lancet 1: 602-604.
21. Izaguirre, A., Barnes, B.J., Amrute, S., Yeow, W.S., Megjugorac, N., Dai, J., et al. (2003) Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J Leukoc Biol 74: 1125-1138.
22. Jarrossay, D., Napolitani, G., Colonna, M., Sallusto, F., and Lanzavecchia, A. (2001) Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur J Immunol 31: 3388-3393.
23. Kadowaki, N., Ho, S., Antonenko, S., Malefyt, R.W., Kastelein, R.A., Bazan, F., et al. (2001) Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J Exp Med 194: 863-869.
24. Kaul, R., Rowland-Jones, S.L., Gillespie, G., Kimani, J., Dong, T., Kiama, P., et al. (2002) Gonococcal cervicitis is associated with reduced systemic CD8+ T cell responses in human immunodeficiency virus type 1-infected and exposed, uninfected sex workers. J Infect Dis 185: 1525-1529.
25. Klotman, M.E., Rapista, A., Teleshova, N., Micsenyi, A., Jarvis, G.A., Lu, W., et al. (2008) Neisseria gonorrhoeae-induced human defensins 5 and 6 increase HIV infectivity: role in enhanced transmission. J Immunol 180: 6176-6185.
26. Koot, M., Wout, A.B., Kootstra, N.A., De Goede, R.E., Tersmette, M., and Schuitemaker, H. (1996) Relation between changes in cellular load, evolution of viral phenotype, and the clonal composition of virus populations in the course of human immunodeficiency virus type 1 infection. J Infect Dis 173: 349-354.
27. Korenromp, E.L., White, R.G., Orroth, K.K., Bakker, R., Kamali, A., Serwadda, D., et al. (2005) Determinants of the impact of sexually transmitted infection treatment on prevention of HIV infection: a synthesis of evidence from the Mwanza, Rakai, and Masaka intervention trials. J Infect Dis 191 (Suppl. 1): S168-S178.
28. Koup, R.A., Ho, D.D., Poli, G., and Fauci, A.S. (2001) Isolation and quantitation of HIV in peripheral blood. Curr Protoc Immunol Chapter 12: Unit 12.2.
29. Kupsch, E.-M., Knepper, B., Kuroki, T., Heuer, I., and Meyer, T.F. (1993) Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J 12: 641-650.
30. Lassen, K., Han, Y., Zhou, Y., Siliciano, J., and Siliciano, R.F. (2004) The multifactorial nature of HIV-1 latency. Trends Mol Med 10: 525-531.
31. Levine, W.C., Pope, V., Bhoomkar, A., Tambe, P., Lewis, J.S., Zaidi, A.A., et al. (1998) Increase in endocervical CD4 lymphocytes among women with nonulcerative sexually transmitted diseases. J Infect Dis 177: 167-174.
32. Liu, X., Mosoian, A., Li-Yun, C.T., Zerhouni-Layachi, B., Snyder, A., Jarvis, G.A., et al. (2006) Gonococcal lipooligosaccharide suppresses HIV infection in human primary macrophages through induction of innate immunity. J Infect Dis 194: 751-759.
33. Lund, J.M., Linehan, M.M., Iijima, N., and Iwasaki, A. (2006) Cutting edge: plasmacytoid dendritic cells provide innate immune protection against mucosal viral infection in situ. J Immunol 177: 7510-7514.
34. Magnusson, M., Tobes, R., Sancho, J., and Pareja, E. (2007) Cutting edge: natural DNA repetitive extragenic sequences from gram-negative pathogens strongly stimulate TLR9. J Immunol 179: 31-35.
35. Martinelli, E., Cicala, C., Van, R.D., Goode, D.J., Macleod, K., Arthos, J., et al. (2007) HIV-1 gp120 inhibits TLR9-mediated activation and IFN-{alpha} secretion in plasmacytoid dendritic cells. Proc Natl Acad Sci USA 104: 3396-3401.
36. Meylan, P.R., Guatelli, J.C., Munis, J.R., Richman, D.D., and Kornbluth, R.S. (1993) Mechanisms for the inhibition of HIV replication by interferons-alpha, -beta, and -gamma in primary human macrophages. Virology 193: 138-148.
37. Mogensen, K.E., Lewerenz, M., Reboul, J., Lutfalla, G., and Uze, G. (1999) The type I interferon receptor: structure, function, and evolution of a family business. J Interferon Cytokine Res 19: 1069-1098.
38. Mogensen, T.H., Paludan, S.R., Kilian, M., and Ostergaard, L. (2006) Live Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis activate the inflammatory response through Toll-like receptors 2, 4, and 9 in species-specific patterns. J Leukoc Biol 80: 267-277.
39. Moniz, R.J., Chan, A.M., and Kelly, K.A. (2009) Identification of dendritic cell subsets responding to genital infection by Chlamydia muridarum. FEMS Immunol Med Microbiol 55: 226-236.
40. Moss, G.B., Overbaugh, J., Welch, M., Reilly, M., Bwayo, J., Plummer, F.A., et al. (1995) Human immunodeficiency virus DNA in urethral secretions in men: association with gonococcal urethritis and CD4 cell depletion. J Infect Dis 172: 1469-1474.
41. Neil, S.J., Zang, T., and Bieniasz, P.D. (2008) Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451: 425-430.
42. Nkengasong, J.N., Kestens, L., Ghys, P.D., Koblavi-Deme, S., Bile, C., Kalou, M., et al. (2001) Human immunodeficiency virus Type 1 (HIV-1) plasma virus load and markers of immune activation among HIV-infected female sex workers with sexually transmitted diseases in Abidjan, Cote d'Ivoire. J Infect Dis 183: 1405-1408.
43. Okumura, A., Lu, G., Pitha-Rowe, I., and Pitha, P.M. (2006) Innate antiviral response targets HIV-1 release by the induction of ubiquitin-like protein ISG15. Proc Natl Acad Sci USA 103: 1440-1445.
44. Rothenfusser, S., Tuma, E., Endres, S., and Hartmann, G. (2002) Plasmacytoid dendritic cells: the key to CpG. Hum Immunol 63: 1111-1119.
45. Salyers, A.A., and Whitt, D.D. (2002) Neisseria species. In Bacterial Pathogenesis, A Molecular Approach. Washington, DC: ASM Press, pp. 437-451.
46. Sato, M., Taniguchi, T., and Tanaka, N. (2001) The interferon system and interferon regulatory factor transcription factors - studies from gene knockout mice. Cytokine Growth Factor Rev 12: 133-142.
47. Sheung, A., Rebbapragada, A., Shin, L.Y., Dobson-Belaire, W., Kimani, J., Ngugi, E., et al. (2008) Mucosal Neisseria gonorrhoeae coinfection during HIV acquisition is associated with enhanced systemic HIV-specific CD8 T-cell responses. AIDS 22: 1729-1737.
48. Shirazi, Y., and Pitha, P.M. (1992) Alpha interferon inhibits early stages of the human immunodeficiency virus type 1 replication cycle. J Virol 66: 1321-1328.
49. Shirazi, Y., and Pitha, P.M. (1998) Interferon downregulates CXCR4 (fusin) gene expression in peripheral blood mononuclear cells. J Hum Virol 1: 69-76.
50. Simard, S., Maurais, E., Gilbert, C., and Tremblay, M.J. (2008) LPS reduces HIV-1 replication in primary human macrophages partly through an endogenous production of type I interferons. Clin Immunol 127: 198-205.
51. Sjolinder, H., Mogensen, T.H., Kilian, M., Jonsson, A.B., and Paludan, S.R. (2008) Important role for Toll-like receptor 9 in host defense against meningococcal sepsis. Infect Immun 76: 5421-5428.
52. Soumelis, V., Scott, I., Gheyas, F., Bouhour, D., Cozon, G., Cotte, L., et al. (2001) Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients. Blood 98: 906-912.
53. Stark, G.R., Kerr, I.M., Williams, B.R., Silverman, R.H., and Schreiber, R.D. (1998) How cells respond to interferons. Annu Rev Biochem 67: 227-264.
54. Taniguchi, T., Ogasawara, K., Takaoka, A., and Tanaka, N. (2001) IRF family of transcription factors as regulators of host defense. Annu Rev Immunol 19: 623-655.
55. UNAIDS (2008) 2008 Report on the Global AIDS Epidemic. Geneva: UNAIDS.
56. World Health Organization (2001) Global Prevalence and Incidence of Selected Curable Sexually Transmitted Infections: Overview and Estimates. Geneva: World Health Organization.
57. Zhang, J., Li, G., Bafica, A., Pantelic, M., Zhang, P., Broxmeyer, H., et al. (2005) Neisseria gonorrhoeae enhances infection of dendritic cells by HIV type 1. J Immunol 174: 7995-8002.
58. Zhou, Y., Zhang, H., Siliciano, J.D., and Siliciano, R.F. (2005) Kinetics of human immunodeficiency virus type 1 decay following entry into resting CD4+ T cells. J Virol 79: 2199-2210.