Type I interferons regulate cytolytic activity of memory CD8+ T cells in the lung airways during respiratory virus challenge

Immunity

Volumn 33, Issue 1, 2010, Pages 96-105

  Kohlmeier, Jacob E ^a   Cookenham, Tres ^a   Roberts, Alan D ^a   Miller, Shannon C ^a   Woodland, David L ^a  

^a TRUDEAU INSTITUTE   (United States)

Author keywords

Cellimmuno; Microbio

Indexed keywords

ALPHA INTERFERON RECEPTOR; GRANZYME B; INTERFERON; STAT1 PROTEIN;

AIRWAY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOLYSIS; HOST CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INNATE IMMUNITY; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY VIRUS; SIGNAL TRANSDUCTION; VIRUS INHIBITION; VIRUS REPLICATION;

ANIMALS; ANTIGENS, VIRAL; BONE MARROW TRANSPLANTATION; CD8-POSITIVE T-LYMPHOCYTES; CYTOTOXICITY, IMMUNOLOGIC; GRANZYMES; HUMANS; IMMUNIZATION, SECONDARY; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS; INTERFERON TYPE I; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; RADIATION CHIMERA; RECEPTOR, INTERFERON ALPHA-BETA; RESPIRATORY MUCOSA; RESPIROVIRUS INFECTIONS; SENDAI VIRUS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; VIRUS REPLICATION;

EID: 77954939630     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2010.06.016     Document Type: Article

References (44)

1. Agarwal P., Raghavan A., Nandiwada S.L., Curtsinger J.M., Bohjanen P.R., Mueller D.L., Mescher M.F. Gene regulation and chromatin remodeling by IL-12 and type I IFN in programming for CD8 T cell effector function and memory. J. Immunol. 2009, 183:1695-1704.
2. Borron P.J., Crouch E.C., Lewis J.F., Wright J.R., Possmayer F., Fraher L.J. Recombinant rat surfactant-associated protein D inhibits human T lymphocyte proliferation and IL-2 production. J. Immunol. 1998, 161:4599-4603.
3. Brincks E.L., Katewa A., Kucaba T.A., Griffith T.S., Legge K.L. CD8 T cells utilize TRAIL to control influenza virus infection. J. Immunol. 2008, 181:4918-4925.
4. Chen H.D., Fraire A.E., Joris I., Brehm M.A., Welsh R.M., Selin L.K. Memory CD8+ T cells in heterologous antiviral immunity and immunopathology in the lung. Nat. Immunol. 2001, 2:1067-1076.
5. de Bree G.J., van Leeuwen E.M., Out T.A., Jansen H.M., Jonkers R.E., van Lier R.A. Selective accumulation of differentiated CD8+ T cells specific for respiratory viruses in the human lung. J. Exp. Med. 2005, 202:1433-1442.
6. Devadas S., Das J., Liu C., Zhang L., Roberts A.I., Pan Z., Moore P.A., Das G., Shi Y. Granzyme B is critical for T cell receptor-induced cell death of type 2 helper T cells. Immunity 2006, 25:237-247.
7. Durbin J.E., Hackenmiller R., Simon M.C., Levy D.E. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996, 84:443-450.
8. Ely K.H., Cauley L.S., Roberts A.D., Brennan J.W., Cookenham T., Woodland D.L. Nonspecific recruitment of memory CD8+ T cells to the lung airways during respiratory virus infections. J. Immunol. 2003, 170:1423-1429.
9. Ely K.H., Cookenham T., Roberts A.D., Woodland D.L. Memory T cell populations in the lung airways are maintained by continual recruitment. J. Immunol. 2006, 176:537-543.
10. Fehniger T.A., Cai S.F., Cao X., Bredemeyer A.J., Presti R.M., French A.R., Ley T.J. Acquisition of murine NK cell cytotoxicity requires the translation of a pre-existing pool of granzyme B and perforin mRNAs. Immunity 2007, 26:798-811.
11. Fernandez-Sesma A., Marukian S., Ebersole B.J., Kaminski D., Park M.S., Yuen T., Sealfon S.C., García-Sastre A., Moran T.M. Influenza virus evades innate and adaptive immunity via the NS1 protein. J. Virol. 2006, 80:6295-6304.
12. Gebhardt T., Wakim L.M., Eidsmo L., Reading P.C., Heath W.R., Carbone F.R. Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 2009, 10:524-530.
13. Goodman A.G., Zeng H., Proll S.C., Peng X., Cillóniz C., Carter V.S., Korth M.J., Tumpey T.M., Katze M.G. The alpha/beta interferon receptor provides protection against influenza virus replication but is dispensable for inflammatory response signaling. J. Virol. 2010, 84:2027-2037.
14. Hayden F.G., Fritz R., Lobo M.C., Alvord W., Strober W., Straus S.E. Local and systemic cytokine responses during experimental human influenza A virus infection. Relation to symptom formation and host defense. J. Clin. Invest. 1998, 101:643-649.
15. Heidema J., Rossen J.W., Lukens M.V., Ketel M.S., Scheltens E., Kranendonk M.E., van Maren W.W., van Loon A.M., Otten H.G., Kimpen J.L., van Bleek G.M. Dynamics of human respiratory virus-specific CD8+ T cell responses in blood and airways during episodes of common cold. J. Immunol. 2008, 181:5551-5559.
16. Hogan R.J., Usherwood E.J., Zhong W., Roberts A.A., Dutton R.W., Harmsen A.G., Woodland D.L. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 2001, 166:1813-1822.
17. Hogan R.J., Zhong W., Usherwood E.J., Cookenham T., Roberts A.D., Woodland D.L. Protection from respiratory virus infections can be mediated by antigen-specific CD4(+) T cells that persist in the lungs. J. Exp. Med. 2001, 193:981-986.
18. Hou S., Doherty P.C., Zijlstra M., Jaenisch R., Katz J.M. Delayed clearance of Sendai virus in mice lacking class I MHC-restricted CD8+ T cells. J. Immunol. 1992, 149:1319-1325.
19. Jenkins M.R., Kedzierska K., Doherty P.C., Turner S.J. Heterogeneity of effector phenotype for acute phase and memory influenza A virus-specific CTL. J. Immunol. 2007, 179:64-70.
20. Jenkins M.R., Trapani J.A., Doherty P.C., Turner S.J. Granzyme K expressing cytotoxic T lymphocytes protects against influenza virus in granzyme AB-/- mice. Viral Immunol. 2008, 21:341-346.
21. Johnson B.J., Costelloe E.O., Fitzpatrick D.R., Haanen J.B., Schumacher T.N., Brown L.E., Kelso A. Single-cell perforin and granzyme expression reveals the anatomical localization of effector CD8+ T cells in influenza virus-infected mice. Proc. Natl. Acad. Sci. USA 2003, 100:2657-2662.
22. Juelich T., Sutcliffe E.L., Sutcliffe E., Denton A., He Y., Doherty P.C., Parish C.R., Parish C., Turner S.J., Turner S.J., et al. Interplay between chromatin remodeling and epigenetic changes during lineage-specific commitment to granzyme B expression. J. Immunol. 2009, 183:7063-7072.
23. Kohlmeier J.E., Woodland D.L. Immunity to respiratory viruses. Annu. Rev. Immunol. 2009, 27:61-82.
24. Kohlmeier J.E., Miller S.C., Woodland D.L. Cutting edge: Antigen is not required for the activation and maintenance of virus-specific memory CD8+ T cells in the lung airways. J. Immunol. 2007, 178:4721-4725.
25. Kohlmeier J.E., Miller S.C., Smith J., Lu B., Gerard C., Cookenham T., Roberts A.D., Woodland D.L. The chemokine receptor CCR5 plays a key role in the early memory CD8+ T cell response to respiratory virus infections. Immunity 2008, 29:101-113.
26. Liang S., Mozdzanowska K., Palladino G., Gerhard W. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 1994, 152:1653-1661.
27. Meraz M.A., White J.M., Sheehan K.C., Bach E.A., Rodig S.J., Dighe A.S., Kaplan D.H., Riley J.K., Greenlund A.C., Campbell D., et al. Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 1996, 84:431-442.
28. Mintern J.D., Guillonneau C., Carbone F.R., Doherty P.C., Turner S.J. Cutting edge: Tissue-resident memory CTL down-regulate cytolytic molecule expression following virus clearance. J. Immunol. 2007, 179:7220-7224.
29. Moltedo B., López C.B., Pazos M., Becker M.I., Hermesh T., Moran T.M. Cutting edge: Stealth influenza virus replication precedes the initiation of adaptive immunity. J. Immunol. 2009, 183:3569-3573.
30. Moss P.A., Moots R.J., Rosenberg W.M., Rowland-Jones S.J., Bodmer H.C., McMichael A.J., Bell J.I. Extensive conservation of alpha and beta chains of the human T-cell antigen receptor recognizing HLA-A2 and influenza A matrix peptide. Proc. Natl. Acad. Sci. USA 1991, 88:8987-8990.
31. Nguyen K.B., Cousens L.P., Doughty L.A., Pien G.C., Durbin J.E., Biron C.A. Interferon alpha/beta-mediated inhibition and promotion of interferon gamma: STAT1 resolves a paradox. Nat. Immunol. 2000, 1:70-76.
32. Reading P.C., Whitney P.G., Barr D.P., Wojtasiak M., Mintern J.D., Waithman J., Brooks A.G. IL-18, but not IL-12, regulates NK cell activity following intranasal herpes simplex virus type 1 infection. J. Immunol. 2007, 179:3214-3221.
33. Regner M., Pavlinovic L., Koskinen A., Young N., Trapani J.A., Müllbacher A. Cutting edge: Rapid and efficient in vivo cytotoxicity by cytotoxic T cells is independent of granzymes A and B. J. Immunol. 2009, 183:37-40.
34. Takeda A., Hamano S., Yamanaka A., Hanada T., Ishibashi T., Mak T.W., Yoshimura A., Yoshida H. Cutting edge: Role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment. J. Immunol. 2003, 170:4886-4890.
35. Topham D.J., Tripp R.A., Doherty P.C. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 1997, 159:5197-5200.
36. Topham D.J., Castrucci M.R., Wingo F.S., Belz G.T., Doherty P.C. The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 2001, 167:6983-6990.
37. Tough D.F., Borrow P., Sprent J. Induction of bystander T cell proliferation by viruses and type I interferon in vivo. Science 1996, 272:1947-1950.
38. Touvrey C., Derré L., Devevre E., Corthesy P., Romero P., Rufer N., Speiser D.E. Dominant human CD8 T cell clonotypes persist simultaneously as memory and effector cells in memory phase. J. Immunol. 2009, 182:6718-6726.
39. Turner S.J., Diaz G., Cross R., Doherty P.C. Analysis of clonotype distribution and persistence for an influenza virus-specific CD8+ T cell response. Immunity 2003, 18:549-559.
40. Vallbracht S., Unsöld H., Ehl S. Functional impairment of cytotoxic T cells in the lung airways following respiratory virus infections. Eur. J. Immunol. 2006, 36:1434-1442.
41. Wakim L.M., Waithman J., van Rooijen N., Heath W.R., Carbone F.R. Dendritic cell-induced memory T cell activation in nonlymphoid tissues. Science 2008, 319:198-202.
42. Wang X., Li M., Zheng H., Muster T., Palese P., Beg A.A., García-Sastre A. Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J. Virol. 2000, 74:11566-11573.
43. Woodland D.L., Kohlmeier J.E. Migration, maintenance and recall of memory T cells in peripheral tissues. Nat. Rev. Immunol. 2009, 9:153-161.
44. Wright J.R. Immunoregulatory functions of surfactant proteins. Nat. Rev. Immunol. 2005, 5:58-68.