IRF3 deficiency impacts granzyme B expression and maintenance of memory T cell function in response to viral infection

Microbes and Infection

Volumn 17, Issue 6, 2015, Pages 426-439

  Moore, Tyler C ^a   Vogel, Alexander J ^a   Petro, Thomas M ^b,c   Brown, Deborah M ^a,b  

^a UNIVERSITY OF NEBRASKA   (United States)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cytokines; Influenza A virus; Interferon regulatory factor 3; T cell memory; T cells; Theiler's murine encephalomyelitis virus

Indexed keywords

BETA INTERFERON; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GRANZYME B; INTERFERON REGULATORY FACTOR 3; INTERLEUKIN 12; INTERLEUKIN 15; INTERLEUKIN 17; INTERLEUKIN 6; PEPTIDE; GRANZYME; IRF3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; IMMUNE RESPONSE; INFLUENZA A VIRUS; INNATE IMMUNITY; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THEILER'S MURINE ENCEPHALOMYELITIS VIRUS; VIRUS INFECTION; ANIMAL; DEFICIENCY; IMMUNOLOGY; METABOLISM; T LYMPHOCYTE; THEILOVIRUS;

ANIMALS; GRANZYMES; INTERFERON REGULATORY FACTOR-3; MICE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THEILOVIRUS;

EID: 84942986329     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2015.03.001     Document Type: Article

References (51)

1. Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol 2001;1:135-45.
2. West AP, Shadel GS, Ghosh S. Mitochondria in innate immune responses. Nat Rev Immunol 2011;11:389-402.
3. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, et al. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 2003;4:491-6.
4. Oshiumi H, Matsumoto M, Funami K, Akazawa T, Seya T. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-beta induction. Nat Immunol 2003;4:161-7.
5. Feng X, Heyden NV, Ratner L. Alpha interferon inhibits human T-cell leukemia virus type 1 assembly by preventing Gag interaction with rafts. J Virol 2003;77:13389-95.
6. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc R Soc Lond B Biol Sci 1957;147:258-67.
7. Nilsen TW, Maroney PA, Baglioni C. Synthesis of (2'-5')oligoadenylate and activation of an endoribonuclease in interferon-treated HeLa cells infected with reovirus. J Virol 1982;42:1039-45.
8. Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, Burkard TR, et al. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol 2011;12:624-30.
9. Thomis DC, Samuel CE. Mechanism of interferon action: autoregulation of RNA-dependent P1/eIF-2 alpha protein kinase (PKR) expression in transfected mammalian cells. Proc Natl Acad Sci U S A 1992;89:10837-41.
10. Kohlmeier JE, Cookenham T, Roberts AD, Miller SC, Woodland DL. Type I interferons regulate cytolytic activity of memory CD8(+) T cells in the lung airways during respiratory virus challenge. Immunity 2010;33:96-105.
11. Marshall HD, Prince AL, Berg LJ, Welsh RM. IFN-alpha beta and self-MHC divert CD8 T cells into a distinct differentiation pathway characterized by rapid acquisition of effector functions. J Immunol 2010;185:1419-28.
12. Moore TC, Petro TM. IRF3 and ERK MAP-kinases control nitric oxide production from macrophages in response to poly-I: C. FEBS Lett 2013;587:3014-20.
13. Ryzhakov G, Lai CC, Blazek K, To KW, Hussell T, Udalova I. IL-17 boosts proinflammatory outcome of antiviral response in human cells. J Immunol 2011;187:5357-62.
14. Sweeney SE, Kimbler TB, Firestein GS. Synoviocyte innate immune responses: II. Pivotal role of IFN regulatory factor 3. J Immunol 2010;184:7162-8.
15. Dahlberg A, Auble MR, Petro TM. Reduced expression of IL-12 p35 by SJL/J macrophages responding to Theiler's virus infection is associated with constitutive activation of IRF-3. Virology 2006;353:422-32.
16. Ebihara T, Azuma M, Oshiumi H, Kasamatsu J, Iwabuchi K, Matsumoto K, et al. Identification of a polyI: C-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation. J Exp Med 2010;207:2675-87.
17. Soudja SM, Ruiz AL, Marie JC, Lauvau G. Inflammatory monocytes activate memory CD8(+) T and innate NK lymphocytes independent of cognate antigen during microbial pathogen invasion. Immunity 2012;37:549-62.
18. MacLeod MK, McKee AS, David A, Wang J, Mason R, Kappler JW, et al. Vaccine adjuvants aluminum and monophosphoryl lipid A provide distinct signals to generate protective cytotoxic memory CD8 T cells. Proc Natl Acad Sci U S A 2011;108:7914-9.
19. Starbeck-Miller GR, Xue HH, Harty JT. IL-12 and type I interferon prolong the division of activated CD8 T cells by maintaining highaffinity IL-2 signaling in vivo. J Exp Med 2014;211:105-20.
20. Pipkin ME, Sacks JA, Cruz-Guilloty F, Lichtenheld MG, Bevan MJ, Rao A. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 2010;32:79-90.
21. Ysebrant de Lendonck L, Tonon S, Nguyen M, Vandevenne P, Welsby I, Martinet V, et al. Interferon regulatory factor 3 controls interleukin-17 expression in CD8 T lymphocytes. Proc Natl Acad Sci U S A 2013;110:E3189-97.
22. Lipton HL, Melvold R. Genetic analysis of susceptibility to Theiler's virus-induced demyelinating disease in mice. J Immunol 1984;132:1821-5.
23. Moore TC, Bush KL, Cody L, Brown DM, Petro TM. Interleukin-6 control of early Theiler's murine encephalomyelitis virus replication in macrophages occurs in conjunction with STAT1 activation and nitric oxide production. J Virol 2012;86:10841-51.
24. Palma JP, Lee HG, Mohindru M, Kang BS, Dal Canto M, Miller SD, et al. Enhanced susceptibility to Theiler's virus-induced demyelinating disease in perforin-deficient mice. J Neuroimmunol 2001;116:125-35.
25. Rodriguez M, Zoecklein LJ, Howe CL, Pavelko KD, Gamez JD, Nakane S, et al. Gamma interferon is critical for neuronal viral clearance and protection in a susceptible mouse strain following early intracranial Theiler's murine encephalomyelitis virus infection. J Virol 2003;77:12252-65.
26. Rossi CP, McAllister A, Tanguy M, Kagi D, Brahic M. Theiler's virus infection of perforin-deficient mice. J Virol 1998;72:4515-9.
27. Sanders CJ, Doherty PC, Thomas PG. Respiratory epithelial cells in innate immunity to influenza virus infection. Cell Tissue Res 2011;343:13-21.
28. Bender BS, Small Jr PA. Influenza: pathogenesis and host defense. Semin Respir Infect 1992;7:38-45.
29. Powell TJ, Brown DM, Hollenbaugh JA, Charbonneau T, Kemp RA, Swain SL, et al. CD8+ T cells responding to influenza infection reach and persist at higher numbers than CD4+ T cells independently of precursor frequency. Clin Immunol 2004;113:89-100.
30. Brown DM, Dilzer AM, Meents DL, Swain SL. CD4 T cell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-two punch. J Immunol 2006;177:2888-98.
31. Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL. Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol 2012;86:6792-803.
32. Kohlmeier JE, Woodland DL. Immunity to respiratory viruses. Annu Rev Immunol 2009;27:61-82.
33. Swain SL, Agrewala JN, Brown DM, Jelley-Gibbs DM, Golech S, Huston G, et al. CD4 memory: generation and Multi-faceted roles for CD4 T Cells in protective immunity to influenza. Immunol Rev 2006;211:8-22.
34. Sato M, Suemori H, Hata N, Asagiri M, Ogasawara K, Nakao K, et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000;13:539-48.
35. Hou W, Kang HS, Kim BS. Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J Exp Med 2009;206:313-28.
36. Mohindru M, Kang B, Kim BS. Initial capsid-specific CD4(+) T cell responses protect against Theiler's murine encephalomyelitisvirusinduced demyelinating disease. Eur J Immunol 2006;36:2106-15.
37. Ahmadzadeh M, Farber DL. Functional plasticity of an antigen-specific memory CD4 T cell population. Proc Natl Acad Sci U S A 2002;99: 11802-7.
38. Lipton HL, Kumar AS, Trottier M. Theiler's virus persistence in the central nervous system of mice is associated with continuous viral replication and a difference in outcome of infection of infiltrating macrophages versus oligodendrocytes. Virus Res 2005;111:214-23.
39. Lipton HL, Dal Canto MC. Chronic neurologic disease in Theiler's virus infection of SJL/J mice. J Neurol Sci 1976;30:201-7.
40. Lyman MA, Myoung J, Mohindru M, Kim BS. Quantitative, not qualitative, differences in CD8(+) T cell responses to Theiler's murine encephalomyelitis virus between resistant C57BL/6 and susceptible SJL/J mice. Eur J Immunol 2004;34:2730-9.
41. Joetham A, Okamoto M, TakedaK, Schedel M, OhnishiH, DakhamaA, et al. CD8 regulates T regulatory cell production of IL-6 and maintains their suppressive phenotype in allergic lung disease. J Immunol 2011;186:113-20.
42. Mullen AC, High FA, Hutchins AS, Lee HW, Villarino AV, Livingston DM, et al. Role of T-bet in commitment of TH1 cells before IL-12-dependent selection. Science 2001;292:1907-10.
43. Goriely S, Molle C, Nguyen M, Albarani V, Haddou NO, Lin R, et al. Interferon regulatory factor 3 is involved in Toll-like receptor 4 (TLR4)-and TLR3-induced IL-12p35 gene activation. Blood 2006;107:1078-84.
44. Moore TC, Cody L, Kumm PM, Brown DM, Petro TM. IRF3 helps control acute TMEV infection through IL-6 expression but contributes to acute hippocampus damage following TMEV infection. Virus Res 2013;178:226-33.
45. Le Goffic R, Pothlichet J, Vitour D, Fujita T, Meurs E, Chignard M, et al. Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J Immunol 2007;178:3368-72.
46. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, Matsui K, et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity 2005;23:19-28.
47. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006;314:997-1001.
48. Andersen J, VanScoy S, Cheng TF, Gomez D, Reich NC. IRF-3-dependent and augmented target genes during viral infection. Genes Immun 2008;9:168-75.
49. Hui KP, Lee SM, Cheung CY, Ng IH, Poon LL, Guan Y, et al. Induction of proinflammatory cytokines in primary human macrophages by influenza A virus (H5N1) is selectively regulated by IFN regulatory factor 3 and p38 MAPK. J Immunol 2009;182:1088-98.
50. Ichinohe T, Lee HK, Ogura Y, Flavell R, Iwasaki A. Inflammasome recognition of influenza virus is essential for adaptive immune responses. J Exp Med 2009;206:79-87.
51. Negishi H, Yanai H, Nakajima A, Koshiba R, Atarashi K, Matsuda A, et al. Cross-interference of RLR and TLR signaling pathways modulates antibacterial T cell responses. Nat Immunol 2012;13:659-66.