The magnitude of the T cell response to a clinically significant dose of influenza virus is regulated by TRAIL

Journal of Immunology

Volumn 187, Issue 9, 2011, Pages 4581-4588

  Brincks, Erik L ^a,b,c   Gurung, Prajwal ^a,b,d   Langlois, Ryan A ^a,b,e   Hemann, Emily A ^a,b   Legge, Kevin L ^a,b   Griffith, Thomas S ^a,b,f  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c TRUDEAU INSTITUTE   (United States)

^d ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MIG PROTEIN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; CYTOTOXICITY; IMMUNOREGULATION; INFLUENZA A (H1N1); INFLUENZA VIRUS A H1N1; LUNG; LYMPHOCYTE COUNT; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MORBIDITY; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; VIRAL CLEARANCE; WILD TYPE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; EPITOPES, T-LYMPHOCYTE; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; LUNG; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; SURVIVAL ANALYSIS; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 80555149840     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002241     Document Type: Article

References (53)

1. Epstein, S. L., C. Y. Lo, J. A. Misplon, and J. R. Bennink. 1998. Mechanism of protective immunity against influenza virus infection in mice without antibodies. J. Immunol. 160: 322-327. (Pubitemid 28116745)
2. Swain, S. L., R. W. Dutton, and D. L. Woodland. 2004. T cell responses to influenza virus infection: effector and memory cells. Viral Immunol. 17: 197-209. (Pubitemid 38880421)
3. Lawrence, C. W., and T. J. Braciale. 2004. Activation, differentiation, and migration of naive virus-specific CD8+ T cells during pulmonary influenza virus infection. J. Immunol. 173: 1209-1218. (Pubitemid 38924298)
4. Lawrence, C. W., R. M. Ream, and T. J. Braciale. 2005. Frequency, specificity, and sites of expansion of CD8+ T cells during primary pulmonary influenza virus infection. J. Immunol. 174: 5332-5340. (Pubitemid 40593171)
5. 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. (Pubitemid 41779486)
6. Doherty, P. C. 1996. Cytotoxic T cell effector and memory function in viral immunity. Curr. Top. Microbiol. Immunol. 206: 1-14. (Pubitemid 26025609)
7. 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. (Pubitemid 127470043)
8. Langlois, R. A., and K. L. Legge. 2010. Plasmacytoid dendritic cells enhance mortality during lethal influenza infections by eliminating virus-specific CD8 T cells. J. Immunol. 184: 4440-4446.
9. Creswell, L. L., M. Rosenbloom, J. L. Cox, T. B. Ferguson, Sr., N. T. Kouchoukos, T. L. Spray, M. K. Pasque, T. B. Ferguson, Jr., T. H. Wareing, and C. B. Huddleston. 1992. Intraaortic balloon counterpulsation: patterns of usage and outcome in cardiac surgery patients. Ann. Thorac. Surg. 54: 11-18, discussion 18-20.
10. Kohlmeier, J. E., T. Cookenham, S. C. Miller, A. D. Roberts, J. P. Christensen, A. R. Thomsen, and D. L. Woodland. 2009. CXCR3 directs antigen-specific effector CD4+ T cell migration to the lung during parainfluenza virus infection. J. Immunol. 183: 4378-4384.
11. Kohlmeier, J. E., S. C. Miller, J. Smith, B. Lu, C. Gerard, T. Cookenham, A. D. Roberts, and D. L. Woodland. 2008. The chemokine receptor CCR5 plays a key role in the early memory CD8+ T cell response to respiratory virus infections. Immunity 29: 101-113.
12. Kohlmeier, J. E., and D. L. Woodland. 2006. Memory T cell recruitment to the lung airways. Curr. Opin. Immunol. 18: 357-362.
13. Galkina, E., J. Thatte, V. Dabak, M. B. Williams, K. Ley, and T. J. Braciale. 2005. Preferential migration of effector CD8+ T cells into the interstitium of the normal lung. J. Clin. Invest. 115: 3473-3483. (Pubitemid 43121835)
14. Fadel, S. A., S. K. Bromley, B. D. Medoff, and A. D. Luster. 2008. CXCR3-deficiency protects influenza-infected CCR5-deficient mice from mortality. Eur. J. Immunol. 38: 3376-3387.
15. Richter, M. V., and D. J. Topham. 2007. The alpha1beta1 integrin and TNF receptor II protect airway CD8+ effector T cells from apoptosis during influenza infection. J. Immunol. 179: 5054-5063.
16. Thatte, J., V. Dabak, M. B. Williams, T. J. Braciale, and K. Ley. 2003. LFA-1 is required for retention of effector CD8 T cells in mouse lungs. Blood 101: 4916-4922. (Pubitemid 36857754)
17. 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.
18. Griffith, T. S., and D. H. Lynch. 1998. TRAIL: a molecule with multiple receptors and control mechanisms. Curr. Opin. Immunol. 10: 559-563. (Pubitemid 28479189)
19. Pitti, R. M., S. A. Marsters, S. Ruppert, C. J. Donahue, A. Moore, and A. Ashkenazi. 1996. Induction of apoptosis by Apo-2 ligand, a new member of the tumor necrosis factor cytokine family. J. Biol. Chem. 271: 12687-12690. (Pubitemid 26175834)
20. Wiley, S. R., K. Schooley, P. J. Smolak, W. S. Din, C. P. Huang, J. K. Nicholl, G. R. Sutherland, T. D. Smith, C. Rauch, C. A. Smith, and R. G. Goodwin. 1995. Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 3: 673-682. (Pubitemid 26091143)
21. Clarke, P., S. M. Meintzer, S. Gibson, C. Widmann, T. P. Garrington, G. L. Johnson, and K. L. Tyler. 2000. Reovirus-induced apoptosis is mediated by TRAIL. J. Virol. 74: 8135-8139. (Pubitemid 30641660)
22. Kotelkin, A., E. A. Prikhod'ko, J. I. Cohen, P. L. Collins, and A. Bukreyev. 2003. Respiratory syncytial virus infection sensitizes cells to apoptosis mediated by tumor necrosis factor-related apoptosis-inducing ligand. J. Virol. 77: 9156-9172. (Pubitemid 37011013)
23. Lund, J. M., L. Alexopoulou, A. Sato, M. Karow, N. C. Adams, N. W. Gale, A. Iwasaki, and R. A. Flavell. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101: 5598-5603. (Pubitemid 38481202)
24. Sedger, L. M., D. M. Shows, R. A. Blanton, J. J. Peschon, R. G. Goodwin, D. Cosman, and S. R. Wiley. 1999. IFN-gamma mediates a novel antiviral activity through dynamic modulation of TRAIL and TRAIL receptor expression. J. Immunol. 163: 920-926. (Pubitemid 29328103)
25. Vidalain, P. O., O. Azocar, B. Lamouille, A. Astier, C. Rabourdin-Combe, and C. Servet-Delprat. 2000. Measles virus induces functional TRAIL production by human dendritic cells. J. Virol. 74: 556-559. (Pubitemid 30002941)
26. Washburn, B., M. A. Weigand, A. Grosse-Wilde, M. Janke, H. Stahl, E. Rieser, M. R. Sprick, V. Schirrmacher, and H. Walczak. 2003. TNF-related apoptosis-inducing ligand mediates tumoricidal activity of human monocytes stimulated by Newcastle disease virus. J. Immunol. 170: 1814-1821. (Pubitemid 36197397)
27. Zeng, J., P. Fournier, and V. Schirrmacher. 2002. Induction of interferon-alpha and tumor necrosis factor-related apoptosis-inducing ligand in human blood mononuclear cells by hemagglutinin-neuraminidase but not F protein of New-castle disease virus. Virology 297: 19-30. (Pubitemid 34734906)
28. Ishikawa, E., M. Nakazawa, M. Yoshinari, and M. Minami. 2005. Role of tumor necrosis factor-related apoptosis-inducing ligand in immune response to influenza virus infection in mice. J. Virol. 79: 7658-7663. (Pubitemid 40756799)
29. Zhou, J., H. K. Law, C. Y. Cheung, I. H. Ng, J. S. Peiris, and Y. L. Lau. 2006. Functional tumor necrosis factor-related apoptosis-inducing ligand production by avian influenza virus-infected macrophages. J. Infect. Dis. 193: 945-953.
30. Herold, S., M. Steinmueller, W. vonWulffen, L. Cakarova, R. Pinto, S. Pleschka, M. Mack, W. A. Kuziel, N. Corazza, T. Brunner, et al. 2008. Lung epithelial apoptosis in influenza virus pneumonia: the role of macrophage-expressed TNF-related apoptosis-inducing ligand. J. Exp. Med. 205: 3065-3077.
31. CDC. 2005. Fact Sheet: Key Facts about Influenza and Influenza Vaccine. Department of Health and Human Services, Washington, DC.
32. Sedger, L. M., M. B. Glaccum, J. C. Schuh, S. T. Kanaly, E. Williamson, N. Kayagaki, T. Yun, P. Smolak, T. Le, R. Goodwin, and B. Gliniak. 2002. Characterization of the in vivo function of TNF-alpha-related apoptosis-inducing ligand, TRAIL/Apo2L, using TRAIL/Apo2L gene-deficient mice. Eur. J. Immunol. 32: 2246-2254. (Pubitemid 34965887)
33. 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. (Pubitemid 36263001)
34. Kilbourne, E. D. 1969. Future influenza vaccines and the use of genetic recombinants. Bull. World Health Organ. 41: 643-645.
35. Reed, L. J., and H. Muench. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27: 493-497.
36. McGill, J., and K. L. Legge. 2009. Cutting edge: contribution of lung-resident T cell proliferation to the overall magnitude of the antigen-specific CD8 T cell response in the lungs following murine influenza virus infection. J. Immunol. 183: 4177-4181.
37. Moskophidis, D., and D. Kioussis. 1998. Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J. Exp. Med. 188: 223-232. (Pubitemid 28357751)
38. Lukacher, A. E., V. L. Braciale, and T. J. Braciale. 1984. In vivo effector function of influenza virus-specific cytotoxic T lymphocyte clones is highly specific. J. Exp. Med. 160: 814-826. (Pubitemid 14074780)
39. Sato, K., S. Hida, H. Takayanagi, T. Yokochi, N. Kayagaki, K. Takeda, H. Yagita, K. Okumura, N. Tanaka, T. Taniguchi, and K. Ogasawara. 2001. Antiviral response by natural killer cells through TRAIL gene induction by IFN-alpha/beta. Eur. J. Immunol. 31: 3138-3146. (Pubitemid 33100505)
40. Zilliox, M. J., G. Parmigiani, and D. E. Griffin. 2006. Gene expression patterns in dendritic cells infected with measles virus compared with other pathogens. Proc. Natl. Acad. Sci. USA 103: 3363-3368. (Pubitemid 43346475)
41. McGill, J., N. Van Rooijen, and K. L. Legge. 2008. Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J. Exp. Med. 205: 1635-1646.
42. McGill, J., N. Van Rooijen, and K. L. Legge. 2010. IL-15 trans-presentation by pulmonary dendritic cells promotes effector CD8 T cell survival during influenza virus infection. J. Exp. Med. 207: 521-534.
43. Lotze, M. T., H. J. Zeh, A. Rubartelli, L. J. Sparvero, A. A. Amoscato, N. R. Washburn, M. E. Devera, X. Liang, M. Tör, and T. Billiar. 2007. The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol. Rev. 220: 60-81. (Pubitemid 350045579)
44. Diehl, G. E., H. H. Yue, K. Hsieh, A. A. Kuang, M. Ho, L. A. Morici, L. L. Lenz, D. Cado, L. W. Riley, and A. Winoto. 2004. TRAIL-R as a negative regulator of innate immune cell responses. Immunity 21: 877-889. (Pubitemid 39626676)
45. Griffith, T. S., S. R. Wiley, M. Z. Kubin, L. M. Sedger, C. R. Maliszewski, and N. A. Fanger. 1999. Monocyte-mediated tumoricidal activity via the tumor necrosis factor-related cytokine, TRAIL. J. Exp. Med. 189: 1343-1354.
46. Fanger, N. A., C. R. Maliszewski, K. Schooley, and T. S. Griffith. 1999. Human dendritic cells mediate cellular apoptosis via tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J. Exp. Med. 190: 1155-1164. (Pubitemid 29496508)
47. Halaas, O., R. Vik, A. Ashkenazi, and T. Espevik. 2000. Lipopolysaccharide induces expression of APO2 ligand/TRAIL in human monocytes and macrophages. Scand. J. Immunol. 51: 244-250. (Pubitemid 30151507)
48. Lünemann, J. D., S. Waiczies, S. Ehrlich, U. Wendling, B. Seeger, T. Kamradt, and F. Zipp. 2002. Death ligand TRAIL induces no apoptosis but inhibits activation of human (auto)antigen-specific T cells. J. Immunol. 168: 4881-4888. (Pubitemid 34495949)
49. Lightfield, K. L., J. Persson, S. W. Brubaker, C. E. Witte, J. von Moltke, E. A. Dunipace, T. Henry, Y. H. Sun, D. Cado, W. F. Dietrich, et al. 2008. Critical function for Naip5 in inflammasome activation by a conserved carboxy-terminal domain of flagellin. Nat. Immunol. 9: 1171-1178.
50. Thomas, P. G., P. Dash, J. R. Aldridge, Jr., A. H. Ellebedy, C. Reynolds, A. J. Funk, W. J. Martin, M. Lamkanfi, R. J. Webby, K. L. Boyd, et al. 2009. The intracellular sensor NLRP3 mediates key innate and healing responses to influenza A virus via the regulation of caspase-1. Immunity 30: 566-575.
51. Allen, I. C., M. A. Scull, C. B. Moore, E. K. Holl, E. McElvania-TeKippe, D. J. Taxman, E. H. Guthrie, R. J. Pickles, and J. P. Ting. 2009. The NLRP3 inflammasome mediates in vivo innate immunity to influenza A virus through recognition of viral RNA. Immunity 30: 556-565.
52. La Gruta, N. L., K. Kedzierska, J. Stambas, and P. C. Doherty. 2007. A question of self-preservation: immunopathology in influenza virus infection. Immunol. Cell Biol. 85: 85-92. (Pubitemid 46398724)
53. Flynn, K. J., G. T. Belz, J. D. Altman, R. Ahmed, D. L. Woodland, and P. C. Doherty. 1998. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8: 683-691. (Pubitemid 28294515)