Dynamics of influenza-induced lung-resident memory T cells underlie waning heterosubtypic immunity

Science Immunology

Volumn 2, Issue 7, 2017, Pages

  Slütter, Bram ^a,b   Braeckel Budimir, Natalija Van ^a   Abboud, Georges ^c   Varga, Steven M ^a,d   Salek Ardakani, Shahram ^c   Harty, John T ^a,d  

^a UNIVERSITY OF IOWA   (United States)

^b LEIDEN UNIVERSITY   (Netherlands)

^c UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 85023759326     PISSN: None     EISSN: 24709468     Source Type: Journal    
DOI: 10.1126/sciimmunol.aag2031     Document Type: Article

References (35)

1. S. L. Epstein, G. E. Price, Cross-protective immunity to influenza A viruses. Expert Rev. Vaccines 9, 1325–1341 (2010).
2. + T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung. J. Clin. Invest. 121, 2254–2263 (2011).
3. A. J. McMichael, F. M. Gotch, G. R. Noble, P. A. S. Beare, Cytotoxic T-cell immunity to influenza. N. Engl. J. Med. 309, 13–17 (1983).
4. S. Sridhar, S. Begom, A. Bermingham, K. Hoschler, W. Adamson, W. Carman, T. Bean, W. Barclay, J. J. Deeks, A. Lalvani, Cellular immune correlates of protection against symptomatic pandemic influenza. Nat. Med. 19, 1305–1312 (2013).
5. + T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166, 1813–1822 (2001).
6. + T cells are critical for protection against influenza A virus. Immunity 39, 939–948 (2013).
7. T. Wu, Y. Hu, Y.-T. Lee, K. R. Bouchard, A. Benechet, K. Khanna, L. S. Cauley, Lung-resident memory CD8 T cells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection. J. Leukocyte Biol. 95, 215–224 (2014).
8. S. R. McMaster, J. J. Wilson, H. Wang, J. E. Kohlmeier, Airway-resident memory CD8 T cells provide antigen-specific protection against respiratory virus challenge through rapid IFN-g production. J. Immunol. 195, 203–209 (2015).
9. + T cells during infection with influenza virus due to selective expression of IFITM3. Nat. Immunol. 14, 238–245 (2013).
10. + tissue-resident memory T cells of skin. Nat. Immunol. 14, 1294–1301 (2013).
11. L. K. Mackay, A. T. Stock, J. Z. Ma, C. M. Jones, S. J. Kent, S. N. Mueller, W. R. Heath, F. R. Carbone, T. Gebhardt, Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc. Natl. Acad. Sci. U.S.A. 109, 7037–7042 (2012).
12. T. Gebhardt, L. M. Wakim, L. Eidsmo, P. C. Reading, W. R. Heath, F. R. Carbone, Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524–530 (2009).
13. L. K. Mackay, E. Wynne-Jones, D. Freestone, D. G. Pellicci, L. A. Mielke, D. M. Newman, A. Braun, F. Masson, A. Kallies, G. T. Belz, F. R. Carbone, T-box transcription factors combine with the cytokines TGF-b and IL-15 to control tissue-resident memory T cell fate. Immunity 43, 1101–1111 (2015).
14. + T cells into the interstitium of the normal lung. J. Clin. Invest. 115, 3473–3483 (2005).
15. J. R. Teijaro, D. Turner, Q. Pham, E. J. Wherry, L. Lefrançois, D. L. Farber, Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J. Immunol. 187, 5510–5514 (2011).
16. K. L. Legge, T. J. Braciale, Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity 18, 265–277 (2003).
17. J. McGill, K. L. Legge, 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 (2009).
18. L. G. Ledgerwood, G. Lal, N. Zhang, A. Garin, S. J. Esses, F. Ginhoux, M. Merad, H. Peche, S. A. Lira, Y. Ding, Y. Yang, X. He, E. H. Schuchman, M. L. Allende, J. C. Ochando, J. S. Bromberg, The sphingosine 1-phosphate receptor 1 causes tissue retention by inhibiting the entry of peripheral tissue T lymphocytes into afferent lymphatics. Nat. Immunol. 9, 42–53 (2008).
19. + T cells in the lung airways depends on proliferation. J. Immunol. 169, 4976–4981 (2002).
20. + T cells in the lung airways. J. Immunol. 178, 4721–4725 (2007).
21. + T cells. Nature 477, 216–219 (2011).
22. + T cells. Nat. Immunol. 14, 509–513 (2013).
23. Y.-T. Lee, J. E. Suarez-Ramirez, T. Wu, J. M. Redman, K. Bouchard, G. A. Hadley, L. S. Cauley, Environmental and antigen receptor-derived signals support sustained surveillance of the lungs by pathogen-specific cytotoxic T lymphocytes. J. Virol. 85, 4085–4094 (2011).
24. D. J. Zammit, D. L. Turner, K. D. Klonowski, L. Lefrançois, L. S. Cauley, Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24, 439–449 (2006).
25. + T cells. Nat. Immunol. 14, 1285–1293 (2013).
26. L. A. Monticelli, G. F. Sonnenberg, M. C. Abt, T. Alenghat, C. G. K. Ziegler, T. A. Doering, J. M. Angelosanto, B. J. Laidlaw, C. Y. Yang, T. Sathaliyawala, M. Kubota, D. Turner, J. M. Diamond, A. W. Goldrath, D. L. Farber, R. G. Collman, E. John Wherry, D. Artis, Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12, 1045–1054 (2011).
27. R. Le Goffic, M. Imran Arshad, M. Rauch, A. L’Helgoualc’h, B. Delmas, C. Piquet-Pellorce, M. Samson, Infection with influenza virus induces IL-33 in murine lungs. Am. J. Respir. Cell Mol. Biol. 45, 1125–1132 (2011).
28. M. P. DeBerge, K. H. Ely, R. I. Enelow, Soluble, but not transmembrane, TNF-a is required during influenza infection to limit the magnitude of immune responses and the extent of immunopathology. J. Immunol. 192, 5839–5851 (2014).
29. L. K. Mackay, M. Minnich, N. A. M. Kragten, Y. Liao, B. Nota, C. Seillet, A. Zaid, K. Man, S. Preston, D. Freestone, A. Braun, E. Wynne-Jones, F. M. Behr, R. Stark, D. G. Pellicci, D. I. Godfrey, G. T. Belz, M. Pellegrini, T. Gebhardt, M. Busslinger, W. Shi, F. R. Carbone, R. A. W. van Lier, A. Kallies, K. P. J. M. van Gisbergen, Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes. Science 352, 459–463 (2016).
30. F. Sallusto, D. Lenig, R. Forster, M. Lipp, A. Lanzavecchia, Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708–712 (1999).
31. + T cell responses. J. Immunol. 196, 4253–4262 (2016).
32. A. A. Sultan, V. Thathy, U. Frevert, K. J. H. Robson, A. Crisanti, V. Nussenzweig, R. S. Nussenzweig, R. Ménard, TRAP is necessary for gliding motility and infectivity of plasmodium sporozoites. Cell 90, 511–522 (1997).
33. K. D. Klonowski, K. J. Williams, A. L. Marzo, D. A. Blair, E. G. Lingenheld, L. Lefrançois, Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 20, 551–562 (2004).
34. + T cells are generated after lymphocytic choriomeningitis virus and influenza virus infections. J. Immunol. 185, 2182–2190 (2010).
35. V. Decman, B. J. Laidlaw, L. J. Dimenna, S. Abdulla, K. Mozdzanowska, J. Erikson, H. C. Ertl, E. J. Wherry, Cell-intrinsic defects in the proliferative response of antiviral memory CD8 T cells in aged mice upon secondary infection. J. Immunol. 184, 5151–5159 (2010).