Plasmacytoid dendritic cells enhance mortality during lethal influenza infections by eliminating virus-specific CD8 T cells

Journal of Immunology

Volumn 184, Issue 8, 2010, Pages 4440-4446

  Langlois, Ryan A ^a,b   Legge, Kevin L ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FAS LIGAND; CD8 ANTIGEN; CD8ALPHA ANTIGEN; FAS ANTIGEN; FASL PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; INFLUENZA; INFLUENZA VIRUS A; MORTALITY; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; PROTEIN INTERACTION; ADOPTIVE TRANSFER; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL MOTION; DENDRITIC CELL; DRUG ANTAGONISM; IMMUNOLOGY; IMMUNOPHENOTYPING; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H2N2; LYMPH NODE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; METABOLISM; METHODOLOGY; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; TRANSPLANTATION; VIROLOGY;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD8; ANTIGENS, CD95; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DENDRITIC CELLS; DOWN-REGULATION; FAS LIGAND PROTEIN; IMMUNOPHENOTYPING; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H2N2 SUBTYPE; LYMPH NODES; LYMPHOCYTE ACTIVATION; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED BALB C; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS;

EID: 77952753345     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902984     Document Type: Article

References (38)

1. Eichelberger, M., W. Allan, M. Zijlstra, R. Jaenisch, and P. C. Doherty. 1991. Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J. Exp. Med. 174: 875-880.
2. Topham, D. J., R. A. Tripp, and P. C. Doherty. 1997. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159: 5197-5200.
3. Graham, M. B., and T. J. Braciale. 1997. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J. Exp. Med. 186: 2063-2068.
4. Kim, T. S., and T. J. Braciale. 2009. Respiratory dendritic cell subsets differ in their capacity to support the induction of virus-specific cytotoxic CD8+ T cell responses. PLoS One 4: e4204.
5. GeurtsvanKessel, C. H., M. A. Willart, L. S. van Rijt, F. Muskens, M. Kool, C. Baas, K. Thielemans, C. Bennett, B. E. Clausen, H. C. Hoogsteden, et al. 2008. Clearance of influenza virus from the lung depends on migratory langerin +CD11b- but not plasmacytoid dendritic cells. J. Exp. Med. 205: 1621-1634.
6. Legge, K. L., and T. J. Braciale. 2003. Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18: 265-277.
7. Belz, G. T., C. M. Smith, L. Kleinert, P. Reading, A. Brooks, K. Shortman, F. R. Carbone, and W. R. Heath. 2004. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl. Acad. Sci. USA 101: 8670-8675.
8. Brincks, E. L., A. Katewa, T. A. Kucaba, T. S. Griffith, and K. L. Legge. 2008. CD8 T cells utilize TRAIL to control influenza virus infection. J. Immunol. 181: 4918-4925.
9. Legge, K. L., and T. J. Braciale. 2005. Lymph node dendritic cells control CD8+ T cell responses through regulated FasL expression. Immunity 23: 649-659.
10. Maldonado-López, R., T. De Smedt, P. Michel, J. Godfroid, B. Pajak, C. Heirman, K. Thielemans, O. Leo, J. Urbain, and M. Moser. 1999. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J. Exp. Med. 189: 587-592.
11. Maldonado-López, R., T. De Smedt, B. Pajak, C. Heirman, K. Thielemans, O. Leo, J. Urbain, C. R. Maliszewski, and M. Moser. 1999. Role of CD8alpha+ and CD8alpha- dendritic cells in the induction of primary immune responses in vivo. J. Leukoc. Biol. 66: 242-246.
12. Henri, S., D. Vremec, A. Kamath, J. Waithman, S. Williams, C. Benoist, K. Burnham, S. Saeland, E. Handman, and K. Shortman. 2001. The dendritic cell populations of mouse lymph nodes. J. Immunol. 167: 741-748. (Pubitemid 32660827)
13. Yoneyama, H., K. Matsuno, Y. Zhang, T. Nishiwaki, M. Kitabatake, S. Ueha, S. Narumi, S. Morikawa, T. Ezaki, B. Lu, et al. 2004. Evidence for recruitment of plasmacytoid dendritic cell precursors to inflamed lymph nodes through high endothelial venules. Int. Immunol. 16: 915-928.
14. Krug, A., R. Uppaluri, F. Facchetti, B. G. Dorner, K. C. Sheehan, R. D. Schreiber, M. Cella, and M. Colonna. 2002. IFN-producing cells respond to CXCR3 ligands in the presence of CXCL12 and secrete inflammatory chemokines upon activation. J. Immunol. 169: 6079-6083. (Pubitemid 36903450)
15. Belz, G. T., S. Bedoui, F. Kupresanin, F. R. Carbone, and W. R. Heath. 2007. Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat. Immunol. 8: 1060-1066.
16. Wolf, A. I., D. Buehler, S. E. Hensley, L. L. Cavanagh, E. J. Wherry, P. Kastner, S. Chan, and W. Weninger. 2009. Plasmacytoid dendritic cells are dispensable during primary influenza virus infection. J. Immunol. 182: 871-879.
17. Fonteneau, J. F., M. Gilliet, M. Larsson, I. Dasilva, C. Münz, Y. J. Liu, and N. Bhardwaj. 2003. Activation of influenza virus-specific CD4+ and CD8+ T cells: a new role for plasmacytoid dendritic cells in adaptive immunity. Blood 101: 3520-3526.
18. Di Pucchio, T., B. Chatterjee, A. Smed-Sörensen, S. Clayton, A. Palazzo, M. Montes, Y. Xue, I. Mellman, J. Banchereau, and J. E. Connolly. 2008. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nat. Immunol. 9: 551-557.
19. Matsue, H., K. Matsue, M. Walters, K. Okumura, H. Yagita, and A. Takashima. 1999. Induction of antigen-specific immunosuppression by CD95L cDNA-transfected 'killer' dendritic cells. Nat. Med. 5: 930-937.
20. Süss, G., and K. Shortman. 1996. A subclass of dendritic cells kills CD4 T cells via Fas/Fas-ligand-induced apoptosis. J. Exp. Med. 183: 1789-1796.
21. Wolfe, T., C. Asseman, A. Hughes, H. Matsue, A. Takashima, and M. G. von Herrath. 2002. Reduction of antiviral CD8 lymphocytes in vivo with dendritic cells expressing Fas ligand-increased survival of viral (lymphocytic choriomeningitis virus) central nervous system infection. J. Immunol. 169: 4867-4872.
22. Kim, S. H., N. Bianco, R. Menon, E. R. Lechman, W. J. Shufesky, A. E. Morelli, and P. D. Robbins. 2006. Exosomes derived from genetically modified DC expressing FasL are anti-inflammatory and immunosuppressive. Mol. Ther. 13: 289-300.
23. de Jong, M. D., C. P. Simmons, T. T. Thanh, V. M. Hien, G. J. Smith, T. N. Chau, D. M. Hoang, N. V. Chau, T. H. Khanh, V. C. Dong, et al. 2006. Fatal outcome of human influenza A (H5N1) is associated with high viral load and hypercytokinemia. Nat. Med. 12: 1203-1207.
24. Tumpey, T. M., X. Lu, T. Morken, S. R. Zaki, and J. M. Katz. 2000. Depletion of lymphocytes and diminished cytokine production in mice infected with a highly virulent influenza A (H5N1) virus isolated from humans. J. Virol. 74: 6105-6116.
25. Perrone, L. A., J. K. Plowden, A. García-Sastre, J. M. Katz, and T. M. Tumpey. 2008. H5N1 and 1918 pandemic influenza virus infection results in early and excessive infiltration of macrophages and neutrophils in the lungs of mice. PLoS Pathog. 4: e1000115.
26. Baskin, C. R., H. Bielefeldt-Ohmann, T. M. Tumpey, P. J. Sabourin, J. P. Long, A. García-Sastre, A. E. Tolnay, R. Albrecht, J. A. Pyles, P. H. Olson, et al. 2009. Early and sustained innate immune response defines pathology and death in nonhuman primates infected by highly pathogenic influenza virus. Proc. Natl. Acad. Sci. USA 106: 3455-3460.
27. Dudley, E., F. Hornung, L. Zheng, D. Scherer, D. Ballard, and M. Lenardo. 1999. NF-kappaB regulates Fas/APO-1/CD95- and TCR- mediated apoptosis of T lymphocytes. Eur. J. Immunol. 29: 878-886.
28. Carey, G. B., D. Donjerković, C. M. Mueller, S. Liu, J. A. Hinshaw, L. Tonnetti, W. Davidson, and D. W. Scott. 2000. B-cell receptor and Fas-mediated signals for life and death. Immunol. Rev. 176: 105-115.
29. Lu, B., L. Wang, D. Medan, D. Toledo, C. Huang, F. Chen, X. Shi, and Y. Rojanasakul. 2002. Regulation of Fas (CD95)-induced apoptosis by nuclear factor-kappaB and tumor necrosis factor-alpha in macrophages. Am. J. Physiol. Cell Physiol. 283: C831-C838.
30. Schram, B. R., and T. L. Rothstein. 2003. NF-kappa B is required for surface Ig-induced Fas resistance in B cells. J. Immunol. 170: 3118-3124.
31. Chun, D. H., K. C. Jung, W. S. Park, I. S. Lee, W. J. Choi, C. J. Kim, S. H. Park, and Y. Bae. 2000. Costimulatory effect of Fas in mouse T lymphocytes. Mol. Cells 10: 642-646.
32. Maksimow, M., T. S. Söderström, S. Jalkanen, J. E. Eriksson, and A. Hänninen. 2006. Fas costimulation of naive CD4 T cells is controlled by NF-kappaB signaling and caspase activity. J. Leukoc. Biol. 79: 369-377.
33. Maksimow, M., M. Santanen, S. Jalkanen, and A. Hänninen. 2003. Responding naive T cells differ in their sensitivity to Fas engagement: early death of many T cells is compensated by costimulation of surviving T cells. Blood 101: 4022-4028.
34. Siegel, R. M., F. K. Chan, H. J. Chun, and M. J. Lenardo. 2000. The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nat. Immunol. 1: 469-474.
35. Buonocore, S., N. O. Haddou, F. Moore, S. Florquin, F. Paulart, C. Heirman, K. Thielemans, M. Goldman, and V. Flamand. 2008. Neutrophil-dependent tumor rejection and priming of tumoricidal CD8+ T cell response induced by dendritic cells overexpressing CD95L. J. Leukoc. Biol. 84: 713-720.
36. Kusuhara, M., K. Matsue, D. Edelbaum, J. Loftus, A. Takashima, and H. Matsue. 2002. Killing of naive T cells by CD95L-transfected dendritic cells (DC): in vivo study using killer DC-DC hybrids and CD4(+) T cells from DO11.10 mice. Eur. J. Immunol. 32: 1035-1043.
37. Sanmiguel, J. C., F. Olaru, J. Li, E. Mohr, and L. E. Jensen. 2009. Interleukin-1 regulates keratinocyte expression of T cell targeting chemokines through interleukin-1 receptor associated kinase-1 (IRAK1) dependent and independent pathways. Cell. Signal. 21: 685-694.
38. Barchet,W., A. Blasius, M. Cella, and M. Colonna. 2005. Plasmacytoid dendritic cells: in search of their niche in immune responses. Immunol. Res. 32: 75-83.