FcγRIIB prevents inflammatory type I IFN production from plasmacytoid dendritic cells during a viral memory response

Journal of Immunology

Volumn 194, Issue 9, 2015, Pages 4240-4250

  Flores, Marcella ^a   Chew, Claude ^a   Tyan, Kevin ^a   Huang, Wu Qing ^a   Salem, Aliasger ^b   Clynes, Raphael ^a  

^a NewYork Presbyterian Hospital   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; FC RECEPTOR IIA; FC RECEPTOR IIB; VIRUS ANTIBODY; FC RECEPTOR; FCGR2B PROTEIN, HUMAN; INTERFERON; TOLL LIKE RECEPTOR 9;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIGEN ANTIBODY COMPLEX; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOSOME; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; INTERNALIZATION; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; SECONDARY INFECTION; SENDAI VIRUS; SENDAI VIRUS INFECTION; SIGNAL TRANSDUCTION; SPLEEN CELL; VIRUS CELL INTERACTION; ANIMAL; BIOSYNTHESIS; DENDRITIC CELL; GENE EXPRESSION; GENETICS; HUMAN; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; METABOLISM; PROTEIN TRANSPORT; RESPIROVIRUS INFECTION; SPLEEN; TRANSGENIC MOUSE; VIRUS INFECTION;

ANIMALS; ANTIBODIES, VIRAL; DENDRITIC CELLS; GENE EXPRESSION; HUMANS; IMMUNOLOGIC MEMORY; INTERFERON TYPE I; MICE; MICE, TRANSGENIC; PROTEIN TRANSPORT; RECEPTORS, IGG; RESPIROVIRUS INFECTIONS; SENDAI VIRUS; SIGNAL TRANSDUCTION; SPLEEN; TOLL-LIKE RECEPTOR 9; VIRUS DISEASES;

EID: 84928484981     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1401296     Document Type: Article

References (45)

1. Swanson, C. L., T. J. Wilson, P. Strauch, M. Colonna, R. Pelanda, and R. M. Torres. 2010. Type I IFN enhances follicular B cell contribution to the T cell-independent antibody response. J. Exp. Med. 207: 1485-1500.
2. Jego, G., A. K. Palucka, J. P. Blanck, C. Chalouni, V. Pascual, and J. Banchereau. 2003. Plasmacytoid dendritic cells induce plasma cell differentiation through type I interferon and interleukin 6. Immunity 19: 225-234.
3. Asselin-Paturel, C., G. Brizard, K. Chemin, A. Boonstra, A. O'Garra, A. Vicari, and G. Trinchieri. 2005. Type I interferon dependence of plasmacytoid dendritic cell activation and migration. J. Exp. Med. 201: 1157-1167.
4. Colonna, M., G. Trinchieri, and Y. J. Liu. 2004. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 5: 1219-1226.
5. Takagi, H., T. Fukaya, K. Eizumi, Y. Sato, K. Sato, A. Shibazaki, H. Otsuka, A. Hijikata, T. Watanabe, O. Ohara, et al. 2011. Plasmacytoid dendritic cells are crucial for the initiation of inflammation and T cell immunity in vivo. Immunity 35: 958-971.
6. Swiecki, M., S. Gilfillan, W. Vermi, Y. Wang, and M. Colonna. 2010. Plasma-cytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8(+) T cell accrual. Immunity 33: 955-966.
7. Cervantes-Barragan, L., K. L. Lewis, S. Firner, V. Thiel, S. Hugues, W. Reith, B. Ludewig, and B. Reizis. 2012. Plasmacytoid dendritic cells control T-cell response to chronic viral infection. Proc. Natl. Acad. Sci. USA 109: 3012-3017.
8. Allman, D., M. Dalod, C. Asselin-Paturel, T. Delale, S. H. Robbins, G. Trinchieri, C. A. Biron, P. Kastner, and S. Chan. 2006. Ikaros is required for plasmacytoid dendritic cell differentiation. Blood 108: 4025-4034.
9. 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.
10. Cervantes-Barragan, L., R. Züst, F. Weber, M. Spiegel, K. S. Lang, S. Akira, V. Thiel, and B. Ludewig. 2007. Control of coronavirus infection through plasmacytoid dendritic-cell-derived type I interferon. Blood 109: 1131-1137.
11. Dalod, M., T. P. Salazar-Mather, L. Malmgaard, C. Lewis, C. Asselin-Paturel, F. Brière, G. Trinchieri, and C. A. Biron. 2002. Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 195: 517-528.
12. Barchet, W., M. Cella, B. Odermatt, C. Asselin-Paturel, M. Colonna, and U. Kalinke. 2002. Virus-induced interferon alpha production by a dendritic cell subset in the absence of feedback signaling in vivo. J. Exp. Med. 195: 507-516.
13. Prakash, A., E. Smith, C. K. Lee, and D. E. Levy. 2005. Tissue-specific positive feedback requirements for production of type I interferon following virus infection. J. Biol. Chem. 280: 18651-18657.
14. Panchanathan, V., G. Chaudhri, and G. Karupiah. 2005. Interferon function is not required for recovery from a secondary poxvirus infection. Proc. Natl. Acad. Sci. USA 102: 12921-12926.
15. Kohlmeier, J. E., T. Cookenham, A. D. Roberts, S. C. Miller, and D. L. Woodland. 2010. Type I interferons regulate cytolytic activity of memory CD8(+) T cells in the lung airways during respiratory virus challenge. Immunity 33: 96-105.
16. Gallagher, K. M., S. Lauder, I. W. Rees, A. M. Gallimore, and A. J. Godkin. 2009. Type I interferon (IFN alpha) acts directly on human memory CD4+ T cells altering their response to antigen. J. Immunol. 183: 2915-2920.
17. Fuertes Marraco, S. A., C. L. Scott, P. Bouillet, A. Ives, S. Masina, D. Vremec, E. S. Jansen, L. A. O'Reilly, P. Schneider, N. Fasel, et al. 2011. Type I interferon drives dendritic cell apoptosis via multiple BH3-only proteins following activation by PolyIC in vivo. PLoS ONE 6: e20189.
18. O'Bryan, J. M., J. A. Potts, H. L. Bonkovsky, A. Mathew, and A. L. Rothman, HALT-C Trial Group. 2011. Extended interferon-alpha therapy accelerates telomere length loss in human peripheral blood T lymphocytes. PLoS ONE 6: e20922.
19. Swiecki, M., Y. Wang, W. Vermi, S. Gilfillan, R. D. Schreiber, and M. Colonna. 2011. Type I interferon negatively controls plasmacytoid dendritic cell numbers in vivo. J. Exp. Med. 208: 2367-2374.
20. Boasso, A., C. M. Royle, S. Doumazos, V. N. Aquino, M. Biasin, L. Piacentini, B. Tavano, D. Fuchs, F. Mazzotta, S. Lo Caputo, et al. 2011. Overactivation of plasmacytoid dendritic cells inhibits antiviral T-cell responses: a model for HIV immunopathogenesis. Blood 118: 5152-5162.
21. McKenzie, S. E., S. M. Taylor, P. Malladi, H. Yuhan, D. L. Cassel, P. Chien, E. Schwartz, A. D. Schreiber, S. Surrey, and M. P. Reilly. 1999. The role of the human Fc receptor Fc gamma RIIA in the immune clearance of platelets: a transgenic mouse model. J. Immunol. 162: 4311-4318.
22. Guiducci, C., G. Ott, J. H. Chan, E. Damon, C. Calacsan, T. Matray, K. D. Lee, R. L. Coffman, and F. J. Barrat. 2006. Properties regulating the nature of the plasmacytoid dendritic cell response to Toll-like receptor 9 activation. J. Exp. Med. 203: 1999-2008.
23. McDonald, J. H., and K. W. Dunn. 2013. Statistical tests for measures of colocalization in biological microscopy. J. Microsc. 252: 295-302.
24. Blasius, A. L., E. Giurisato, M. Cella, R. D. Schreiber, A. S. Shaw, and M. Colonna. 2006. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 177: 3260-3265.
25. Flores, M., D. D. Desai, M. Downie, B. Liang, M. P. Reilly, S. E. McKenzie, and R. Clynes. 2009. Dominant expression of the inhibitory FcgammaRIIB prevents antigen presentation by murine plasmacytoid dendritic cells. J. Immunol. 183: 7129-7139.
26. Sasai, M., M. M. Linehan, and A. Iwasaki. 2010. Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 329: 1530-1534.
27. Henault, J., J. Martinez, J. M. Riggs, J. Tian, P. Mehta, L. Clarke, M. Sasai, E. Latz, M. M. Brinkmann, A. Iwasaki, et al. 2012. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 37: 986-997.
28. Park, B., M. M. Brinkmann, E. Spooner, C. C. Lee, Y. M. Kim, and H. L. Ploegh. 2008. Proteolytic cleavage in an endolysosomal compartment is required for activation of Toll-like receptor 9. Nat. Immunol. 9: 1407-1414.
29. Segura, E., J. Wong, and J. A. Villadangos. 2009. Cutting edge: B220+CCR9- dendritic cells are not plasmacytoid dendritic cells but are precursors of conventional dendritic cells. J. Immunol. 183: 1514-1517.
30. Link, A., F. Zabel, Y. Schnetzler, A. Titz, F. Brombacher, and M. F. Bachmann. 2012. Innate immunity mediates follicular transport of particulate but not soluble protein antigen. J. Immunol. 188: 3724-3733.
31. Phan, T. G., J. A. Green, E. E. Gray, Y. Xu, and J. G. Cyster. 2009. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat. Immunol. 10: 786-793.
32. Phan, T. G., I. Grigorova, T. Okada, and J. G. Cyster. 2007. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat. Immunol. 8: 992-1000.
33. Honke, N., N. Shaabani, G. Cadeddu, U. R. Sorg, D. E. Zhang, M. Trilling, K. Klingel, M. Sauter, R. Kandolf, N. Gailus, et al. 2012. Enforced viral replication activates adaptive immunity and is essential for the control of a cytopathic virus. Nat. Immunol. 13: 51-57.
34. Zuniga, E. I., L. Y. Liou, L. Mack, M. Mendoza, and M. B. Oldstone. 2008. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 4: 374-386.
35. Bergthaler, A., L. Flatz, A. Verschoor, A. N. Hegazy, M. Holdener, K. Fink, B. Eschli, D. Merkler, R. Sommerstein, E. Horvath, et al. 2009. Impaired antibody response causes persistence of prototypic T cell-contained virus. PLoS Biol. 7: e1000080.
36. Båve, U., M. Magnusson, M. L. Eloranta, A. Perers, G. V. Alm, and L. Rönnblom. 2003. Fc gamma RIIa is expressed on natural IFN-alphaproducing cells (plasmacytoid dendritic cells) and is required for the IFNalpha production induced by apoptotic cells combined with lupus IgG. J. Immunol. 171: 3296-3302.
37. Schijf, M. A., M. V. Lukens, D. Kruijsen, N. O. van Uden, J. Garssen, F. E. Coenjaerts, B. Van't Land, and G. M. van Bleek. 2013. Respiratory syncytial virus induced type I IFN production by pDC is regulated by RSV-infected airway epithelial cells, RSV-exposed monocytes and virus specific antibodies. PLoS ONE 8: e81695.
38. Green, D. S., T. Lum, and J. A. Green. 2004. IgG-derived Fc down-regulates virus-induced plasmacytoid dendritic cell (pDC) IFNalpha production. Cytokine 26: 209-216.
39. Buchbinder, S. P., D. V. Mehrotra, A. Duerr, D. W. Fitzgerald, R. Mogg, D. Li, P. B. Gilbert, J. R. Lama, M. Marmor, C. Del Rio, et al Step Study Protocol Team. 2008. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-ofconcept trial. Lancet 372: 1881-1893.
40. + T-cell responses but is attenuated by preexisting Ad5 immunity. Proc. Natl. Acad. Sci. USA 109: E3503-E3512.
41. Ato, M., Y. Takahashi, H. Fujii, S. Hashimoto, T. Kaji, S. Itamura, Y. Horiuchi, Y. Arakawa, M. Tashiro, and T. Takemori. 2013. Influenza A whole virion vaccine induces a rapid reduction of peripheral blood leukocytes via interferon-α-dependent apoptosis. Vaccine 31: 2184-2190.
42. Koyama, S., T. Aoshi, T. Tanimoto, Y. Kumagai, K. Kobiyama, T. Tougan, K. Sakurai, C. Coban, T. Horii, S. Akira, and K. J. Ishii. 2010. Plasmacytoid dendritic cells delineate immunogenicity of influenza vaccine subtypes. Sci. Transl. Med. 2: 25ra24.
43. Takeda, A., C. U. Tuazon, and F. A. Ennis. 1988. Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science 242: 580-583.
44. Fabricius, D., M. Neubauer, B. Mandel, C. Schütz, A. Viardot, A. Vollmer, B. Jahrsdörfer, and K. M. Debatin. 2010. Prostaglandin E2 inhibits IFN-alpha secretion and Th1 costimulation by human plasmacytoid dendritic cells via E-prostanoid 2 and E-prostanoid 4 receptor engagement. J. Immunol. 184: 677-684.
45. Eloranta, M. L., T. Lövgren, D. Finke, L. Mathsson, J. Rönnelid, B. Kastner, G. V. Alm, and L. Rönnblom. 2009. Regulation of the interferon-alpha production induced by RNA-containing immune complexes in plasmacytoid dendritic cells. Arthritis Rheum. 60: 2418-2427.