TLR9 contributes to the recognition of EBV by primary monocytes and plasmacytoid dendritic cells

Journal of Immunology

Volumn 185, Issue 6, 2010, Pages 3620-3631

  Fiola, Stéphanie ^a,b,c   Gosselin, David ^b,c   Takada, Kenzo ^d   Gosselin, Jean ^a,b,c  

^a LAVAL UNIVERSITY   (Canada)

^b Université Laval   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

^d HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; CHLOROQUINE; CPG OLIGODEOXYNUCLEOTIDE; INTERLEUKIN 10; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 9; VIRUS DNA;

ANTIVIRAL RESISTANCE; ARTICLE; CELL ACTIVATION; CELL MATURATION; CONFOCAL MICROSCOPY; CYTOKINE RELEASE; ENDOSOME; EPSTEIN BARR VIRUS; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MONOCYTE; PERIPHERAL BLOOD MONONUCLEAR CELL; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; VIRUS PARTICLE; VIRUS PURIFICATION; VIRUS REACTIVATION;

CELL COMMUNICATION; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; EPSTEIN-BARR VIRUS INFECTIONS; GENE EXPRESSION REGULATION; HERPESVIRUS 4, HUMAN; HUMANS; INFLAMMATION MEDIATORS; MONOCYTES; PROTEIN TRANSPORT; TOLL-LIKE RECEPTOR 9; UP-REGULATION;

EID: 78149462940     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903736     Document Type: Article

References (58)

1. Larochelle, B., L. Flamand, P. Gourde, D. Beauchamp, and J. Gosselin. 1998. Epstein-Barr virus infects and induces apoptosis in human neutrophils. Blood 92: 291-299.
2. Savard, M., C. Bélanger, M. Tardif, P. Gourde, L. Flamand, and J. Gosselin. 2000. Infection of primary human monocytes by Epstein-Barr virus. J. Virol. 74: 2612-2619.
3. Xiong, A., R. H. Clarke-Katzenberg, G. Valenzuela, K. M. Izumi, and M. T. Millan. 2004. Epstein-Barr virus latent membrane protein 1 activates nuclear factor-kappa B in human endothelial cells and inhibits apoptosis. Transplantation 78: 41-49.
4. Shimakage, M., M. Kimura, S. Yanoma, M. Ibe, S. Yokota, G. Tsujino, T. Kozuka, T. Dezawa, S. Tamura, A. Ohshima, et al. 1999. Expression of latent and replicative-infection genes of Epstein-Barr virus in macrophage. Arch. Virol. 144: 157-166.
5. van Gorp, J., K. C. Jacobse, R. Broekhuizen, J. Alers, J. G. van den Tweel, and R. A. de Weger. 1994. Encoded latent membrane protein 1 of Epstein-Barr virus on follicular dendritic cells in residual germinal centres in Hodgkin's disease. J. Clin. Pathol. 47: 29-32.
6. Savard, M., and J. Gosselin. 2006. Epstein-Barr virus immunossuppression of innate immunity mediated by phagocytes. Virus Res. 119: 134-145.
7. Aravalli, R. N., S. Hu, T. N. Rowen, J. M. Palmquist, and J. R. Lokensgard. 2005. Cutting edge: TLR2-mediated proinflammatory cytokine and chemokine production by microglial cells in response to herpes simplex virus. J. Immunol. 175: 4189-4193.
8. Compton, T., E. A. Kurt-Jones, K. W. Boehme, J. Belko, E. Latz, D. T. Golenbock, and R. W. Finberg. 2003. Human cytomegalovirus activates inflammatory cytokine responses via CD14 and Toll-like receptor 2. J. Virol. 77: 4588-4596.
9. Kurt-Jones, E. A., M. Chan, S. Zhou, J. Wang, G. Reed, R. Bronson, M. M. Arnold, D. M. Knipe, and R. W. Finberg. 2004. Herpes simplex virus 1 interaction with Toll-like receptor 2 contributes to lethal encephalitis. Proc. Natl. Acad. Sci. USA 101: 1315-1320.
10. Wang, J. P., E. A. Kurt-Jones, O. S. Shin, M. D. Manchak, M. J. Levin, and R. W. Finberg. 2005. Varicella-zoster virus activates inflammatory cytokines in human monocytes and macrophages via Toll-like receptor 2. J. Virol. 79: 12658-12666.
11. Gaudreault, E., S. Fiola, M. Olivier, and J. Gosselin. 2007. Epstein-Barr virus induces MCP-1 secretion by human monocytes via TLR2. J. Virol. 81: 8016-8024.
12. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
13. Lund, J., A. Sato, S. Akira, R. Medzhitov, and A. Iwasaki. 2003. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 198: 513-520.
14. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303: 1529-1531.
15. Krug, A., G. D. Luker, W. Barchet, D. A. Leib, S. Akira, and M. Colonna. 2004. Herpes simplex virus type 1 activates murine natural interferon-producing cells through toll-like receptor 9. Blood 103: 1433-1437.
16. Tabeta, K., P. Georgel, E. Janssen, X. Du, K. Hoebe, K. Crozat, S. Mudd, L. Shamel, S. Sovath, J. Goode, et al. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 101: 3516-3521.
17. Varani, S., M. Cederarv, S. Feld, C. Tammik, G. Frascaroli, M. P. Landini, and C. Söderberg-Nauclér. 2007. Human cytomegalovirus differentially controls B cell and T cell responses through effects on plasmacytoid dendritic cells. J. Immunol. 179: 7767-7776.
18. Lim, W. H., S. Kireta, G. R. Russ, and P. T. Coates. 2007. Human plasmacytoid dendritic cells regulate immune responses to Epstein-Barr virus (EBV) infection and delay EBV-related mortality in humanized NOD-SCID mice. Blood 109: 1043-1050.
19. Guerreiro-Cacais, A. O., L. Li, D. Donati, M. T. Bejarano, A. Morgan, M. G. Masucci, L. Hutt-Fletcher, and V. Levitsky. 2004. Capacity of Epstein-Barr virus to infect monocytes and inhibit their development into dendritic cells is affected by the cell type supporting virus replication. J. Gen. Virol. 85: 2767-2778.
20. Knol, A. C., G. Quéreux, M. C. Pandolfino, A. Khammari, and B. Dreno. 2005. Presence of Epstein-Barr virus in Langerhans cells of CTCL lesions. J. Invest. Dermatol. 124: 280-282.
21. Lindhout, E., A. Lakeman, M. L. Mevissen, and C. de Groot. 1994. Functionally active Epstein-Barr virus-transformed follicular dendritic cell-like cell lines. J. Exp. Med. 179: 1173-1184.
22. Schlitt, A., S. Blankenberg, K. Weise, B. C. Gärtner, T. Mehrer, D. Peetz, J. Meyer, H. Darius, and H. J. Rupprecht. 2005. Herpesvirus DNA (Epstein-Barr virus, herpes simplex virus, cytomegalovirus) in circulating monocytes of patients with coronary artery disease. Acta Cardiol. 60: 605-610.
23. Walling, D. M., A. J. Ray, J. E. Nichols, C. M. Flaitz, and C. M. Nichols. 2007. Epstein-Barr virus infection of Langerhans cell precursors as a mechanism of oral epithelial entry, persistence, and reactivation. J. Virol. 81: 7249-7268.
24. Li, L., D. Liu, L. Hutt-Fletcher, A. Morgan, M. G. Masucci, and V. Levitsky. 2002. Epstein-Barr virus inhibits the development of dendritic cells by promoting apoptosis of their monocyte precursors in the presence of granulocyte macrophage-colony-stimulating factor and interleukin-4. Blood 99: 3725-3734.
25. Bickham, K., K. Goodman, C. Paludan, S. Nikiforow, M. L. Tsang, R. M. Steinman, and C. Münz. 2003. Dendritic cells initiate immune control of epstein-barr virus transformation of B lymphocytes in vitro. J. Exp. Med. 198: 1653-1663.
26. Subklewe, M., C. Paludan, M. L. Tsang, K. Mahnke, R. M. Steinman, and C. Münz. 2001. Dendritic cells cross-present latency gene products from Epstein-Barr virus-transformed B cells and expand tumor-reactive CD8(+) killer T cells. J. Exp. Med. 193: 405-411.
27. Tugizov, S., R. Herrera, P. Veluppillai, J. Greenspan, D. Greenspan, and J. M. Palefsky. 2007. Epstein-Barr virus (EBV)-infected monocytes facilitate dissemination of EBV within the oral mucosal epithelium. J. Virol. 81: 5484-5496.
28. Gosselin, J., M. Savard, M. Tardif, L. Flamand, and P. Borgeat. 2001. Epstein-Barr virus primes human polymorphonuclear leucocytes for the biosynthesis of leukotriene B4. Clin. Exp. Immunol. 126: 494-502.
29. Hutt-Fletcher, L., and S. M. Turk. 2001. Virus isolation. In Epstein-Barr virus protocols. J. B. Wilson, and G. H. W. May, eds. Humana Press, Totowa, NJ, p. 119-123.
30. Maruo, S., L. Yang, and K. Takada. 2001. Roles of Epstein-Barr virus glycoproteins gp350 and gp25 in the infection of human epithelial cells. J. Gen. Virol. 82: 2373-2383.
31. Wilson, J. B., and M. E. Drotar. 2001. Considerations in generating transgenic mice: DNA, RNA and protein extractions fromtissues - rapid and effective blotting. In Epstein-Barr virus protocols. J. B. Wilson, and G. H. W. May, eds. Humana Press, Totowa, NJ, p. 361-377.
32. Barrat, F. J., T. Meeker, J. Gregorio, J. H. Chan, S. Uematsu, S. Akira, B. Chang, O. Duramad, and R. L. Coffman. 2005. Nucleic acids of mammalian origin can act as endogenous ligands for Toll-like receptors and may promote systemic lupus erythematosus. J. Exp. Med. 202: 1131-1139.
33. Krug, A., S. Rothenfusser, V. Hornung, B. Jahrsdörfer, S. Blackwell, Z. K. Ballas, S. Endres, A. M. Krieg, and G. Hartmann. 2001. Identification of CpG oligonucleotide sequences with high induction of IFN-alpha/beta in plasmacytoid dendritic cells. Eur. J. Immunol. 31: 2154-2163.
34. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdörfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168: 4531-4537.
35. Martin, H. J., J. M. Lee, D. Walls, and S. D. Hayward. 2007. Manipulation of the toll-like receptor 7 signaling pathway by Epstein-Barr virus. J. Virol. 81: 9748-9758.
36. Latz, E., A. Schoenemeyer, A. Visintin, K. A. Fitzgerald, B. G. Monks, C. F. Knetter, E. Lien, N. J. Nilsen, T. Espevik, and D. T. Golenbock. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5: 190-198.
37. Fukuda, M. 1991. Lysosomal membrane glycoproteins. Structure, biosynthesis, and intracellular trafficking. J. Biol. Chem. 266: 21327-21330.
38. Pols, M. S., and J. Klumperman. 2008. Trafficking and function of the tetraspanin CD63. Exp. Cell Res. 315: 1584-1592.
39. Agren, J., C. Thiemermann, S. J. Foster, J. E. Wang, and A. O. Aasen. 2006. Cytokine responses to CpG DNA in human leukocytes. Scand. J. Immunol. 64: 61-68.
40. Gursel, M., D. Verthelyi, and D. M. Klinman. 2002. CpG oligodeoxynucleotides induce human monocytes to mature into functional dendritic cells. Eur. J. Immunol. 32: 2617-2622.
41. Paludan, C., D. Schmid, M. Landthaler, M. Vockerodt, D. Kube, T. Tuschl, and C. Münz. 2005. Endogenous MHC class II processing of a viral nuclear antigen after autophagy. Science 307: 593-596.
42. McKenna, K., A. S. Beignon, and N. Bhardwaj. 2005. Plasmacytoid dendritic cells: linking innate and adaptive immunity. J. Virol. 79: 17-27.
43. Monteleone, I., A. M. Platt, E. Jaensson, W. W. Agace, and A. M. Mowat. 2008. IL-10-dependent partial refractoriness to Toll-like receptor stimulation modulates gut mucosal dendritic cell function. Eur. J. Immunol. 38: 1533-1547.
44. Tallóczy, Z., J. Martinez, D. Joset, Y. Ray, A. Gácser, S. Toussi, N. Mizushima, J. D. Nosanchuk, J. Nosanchuk, H. Goldstein, et al. 2008. Methamphetamine inhibits antigen processing, presentation, and phagocytosis. PLoS Pathog. 4: e28.
45. Peng, W. M., C. F. Yu, J. P. Allam, J. Oldenburg, T. Bieber, J. Hoch, A. M. Eis-Hübinger, and N. Novak. 2007. Inhibitory oligodeoxynucleotides downregulate herpes simplex virus-induced plasmacytoid dendritic cell type I interferon production and modulate cell function. Hum. Immunol. 68: 879-887.
46. Sato, A., M. M. Linehan, and A. Iwasaki. 2006. Dual recognition of herpes simplex viruses by TLR2 and TLR9 in dendritic cells. Proc. Natl. Acad. Sci. USA 103: 17343-17348.
47. Sørensen, L. N., L. S. Reinert, L. Malmgaard, C. Bartholdy, A. R. Thomsen, and S. R. Paludan. 2008. TLR2 and TLR9 synergistically control herpes simplex virus infection in the brain. J. Immunol. 181: 8604-8612.
48. Barbalat, R., L. Lau, R. M. Locksley, and G. M. Barton. 2009. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 10: 1200-1207.
49. Zucchini, N., G. Bessou, S. Traub, S. H. Robbins, S. Uematsu, S. Akira, L. Alexopoulou, and M. Dalod. 2008. Cutting edge: Overlapping functions of TLR7 and TLR9 for innate defense against a herpesvirus infection. J. Immunol. 180: 5799-5803.
50. Gilliet, M., W. Cao, and Y. J. Liu. 2008. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat. Rev. Immunol. 8: 594-606.
51. Quan, T. E., R. M. Roman, B. J. Rudenga, V. M. Holers, and J. Craft. 2010. Epstein-Barr virus promotes interferon-alpha production by plasmacytoid dendritic cells. Arthritis Rheum. 62: 1693-1701.
52. Luganini, A., P. Caposio, S. Landolfo, and G. Gribaudo. 2008. Phosphorothioate-modified oligodeoxynucleotides inhibit human cytomegalovirus replication by blocking virus entry. Antimicrob. Agents Chemother. 52: 1111-1120.
53. Schlaepfer, E., A. Audigé, B. von Beust, V. Manolova, M. Weber, H. Joller, M. F. Bachmann, T. M. Kundig, and R. F. Speck. 2004. CpG oligodeoxynucleotides block human immunodeficiency virus type 1 replication in human lymphoid tissue infected ex vivo. J. Virol. 78: 12344-12354.
54. Guggemoos, S., D. Hangel, S. Hamm, A. Heit, S. Bauer, and H. Adler. 2008. TLR9 contributes to antiviral immunity during gammaherpesvirus infection. J. Immunol. 180: 438-443.
55. Samanta, M., D. Iwakiri, T. Kanda, T. Imaizumi, and K. Takada. 2006. EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J. 25: 4207-4214.
56. Lünemann, J. D., T. Kamradt, R. Martin, and C. Münz. 2007. Epstein-barr virus: environmental trigger of multiple sclerosis? J. Virol. 81: 6777-6784.
57. Toussirot, E., and J. Roudier. 2007. Pathophysiological links between rheumatoid arthritis and the Epstein-Barr virus: an update. Joint Bone Spine 74: 418-426.
58. Costenbader, K. H., and E. W. Karlson. 2006. Epstein-Barr virus and rheumatoid arthritis: is there a link? Arthritis Res. Ther. 8: 204.