Lung-resident memory CD8 T cells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection

Journal of Leukocyte Biology

Volumn 95, Issue 2, 2014, Pages 215-224

  Wu, Tao ^a   Hu, Yinghong ^a   Lee, Young Tae ^a   Bouchard, Keith R ^a   Benechet, Alexandre ^a   Khanna, Kamal ^a   Cauley, Linda S ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Cellular immunity; Fluorescence microscopy; Immunization; Influenza virus

Indexed keywords

CROSS REACTING ANTIBODY; FINGOLIMOD; INFLUENZA VACCINE; VIRUS ANTIBODY; ALPHA E INTEGRINS; ALPHA INTEGRIN; LEUKOCYTE ANTIGEN; OVALBUMIN; PDCD1 PROTEIN, MOUSE; PROGRAMMED DEATH 1 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CELL SURFACE; CELLULAR DISTRIBUTION; CELLULAR IMMUNITY; CONFOCAL LASER MICROSCOPY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CROSS PROTECTION; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HETEROSUBTYPIC IMMUNITY; HISTOLOGY; IMMUNIZATION; INFLUENZA; INFLUENZA VIRUS; LUNG PARENCHYMA; LUNG RESIDENT MEMORY CD8 T LYMPHOCYTE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRACHEOBRONCHIAL TREE; VIRAL CLEARANCE; VIRUS CULTURE; VIRUS REPLICATION; WEIGHT REDUCTION; ANIMAL; CELL PROLIFERATION; DOG; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLUENZA VIRUS A; LUNG; LYMPHOCYTE ACTIVATION; MDCK CELL; METABOLISM; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; SPECIES DIFFERENCE; TIME; VIROLOGY;

CELLULAR IMMUNITY; FLUORESCENCE MICROSCOPY; IMMUNIZATION; INFLUENZA VIRUS;

ANIMALS; ANTIBODIES, VIRAL; ANTIGENS, CD; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CROSS PROTECTION; DOGS; IMMUNIZATION; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS; INTEGRIN ALPHA CHAINS; LUNG; LYMPHOCYTE ACTIVATION; MADIN DARBY CANINE KIDNEY CELLS; MICE; ORTHOMYXOVIRIDAE INFECTIONS; OVALBUMIN; PROGRAMMED CELL DEATH 1 RECEPTOR; SPECIES SPECIFICITY; TIME FACTORS;

EID: 84893386522     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.0313180     Document Type: Article

References (44)

1. Topham, D. J., Tripp, R. A., Doherty, P. C. (1997) CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159, 5197-5200.
2. Belz, G. T., Xie, W., Altman, J. D., Doherty, P. C. (2000) A previously unrecognized H-2D(b)-restricted peptide prominent in the primary influenza A virus-specific CD8(+) T-cell response is much less apparent following secondary challenge. J. Virol. 74, 3486-3493.
3. Liang, S., Mozdzanowska, K., Palladino, G., Gerhard, W. (1994) Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol. 152, 1653-1661.
4. Nguyen, H. H., Moldoveanu, Z., Novak, M. J., van Ginkel, F. W., Ban, E., Kiyono, H., McGhee, J. R., Mestecky, J. (1999) Heterosubtypic immunity to lethal influenza A virus infection is associated with virus-specific CD8(+) cytotoxic T lymphocyte responses induced in mucosa-associated tissues. Virology 254, 50-60.
5. Kreijtz, J. H., Bodewes, R., van Amerongen, G., Kuiken, T., Fouchier, R. A., Osterhaus, A. D., Rimmelzwaan, G. F. (2007) Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 25, 612-620.
6. Doherty, P. C., Topham, D. J., Tripp, R. A. (1996) Establishment and persistence of virus-specific CD4+ and CD8+ T cell memory. Immunol. Rev. 150, 23-44.
7. Sallusto, F., Lenig, D., Forster, R., Lipp, M., Lanzavecchia, A. (1999) Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708-712.
8. Masopust, D., Vezys, V., Marzo, A. L., Lefrançois, L. (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413-2417.
9. Hogan, R. J., Usherwood, E. J., Zhong, W., Roberts, A. A., Dutton, R. W., Harmsen, A. G., Woodland, D. L. (2001) Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166, 1813-1822.
10. Marshall, D. R., Turner, S. J., Belz, G. T., Wingo, S., Andreansky, S., Sangster, M. Y., Riberdy, J. M., Liu, T., Tan, M., Doherty, P. C. (2001) Measuring the diaspora for virus-specific CD8+ T cells. Proc. Natl. Acad. Sci. USA 98, 6313-6318.
11. Lee, Y. T., Suarez-Ramirez, J. E., Wu, T., Redman, J. M., Bouchard, K., Hadley, G. A., Cauley, L.S. (2011) Environmental and antigen receptorderived signals support sustained surveillance of the lungs by pathogenspecific cytotoxic T lymphocytes. J. Virol. 85, 4085-4094.
12. Cauley, L. S., Lefrançois, L. (2013) Guarding the perimeter: protection of the mucosa by tissue-resident memory T cells. Mucosal Immunol. 6, 14-23.
13. Zammit, D. J., Turner, D. L., Klonowski, K. D., Lefrançois, L., Cauley, L. S. (2006) Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity 24, 439-449.
14. Gebhardt, T., Mackay, L.K. (2012) Local immunity by tissue-resident CD8(+) memory T cells. Front. Immunol. 3, 340.
15. Klonowski, K. D., Williams, K. J., Marzo, A. L., Blair, D. A., Lingenheld, E. G., Lefrançois, L. (2004) Dynamics of blood-borne CD8 memory T cell migration in vivo. Immunity 20, 551-562.
16. Casey, K. A., Fraser, K. A., Schenkel, J. M., Moran, A., Abt, M. C., Beura, L. K., Lucas, P. J., Artis, D., Wherry, E. J., Hogquist, K., Vezys, V., Masopust, D. (2012) Antigen-independent differentiation and maintenance of effector-like resident memory T cells in tissues. J. Immunol. 188, 4866-4875.
17. Wakim, L. M., Woodward-Davis, A., Bevan, M. J. (2010) Memory T cells persisting within the brain after local infection show functional adaptations to their tissue of residence. Proc. Natl. Acad. Sci. USA 107, 17872-17879.
18. Ely, K. H., Cookenham, T., Roberts, A. D., Woodland, D. L. (2006) Memory T cell populations in the lung airways are maintained by continual recruitment. J. Immunol. 176, 537-543.
19. Ely, K. H., Cauley, L. S., Roberts, A. D., Brennan, J. W., Cookenham, T., Woodland, D. L. (2003) Nonspecific recruitment of memory CD8+ T cells to the lung airways during respiratory virus infections. J. Immunol. 170, 1423-1429.
20. Suarez-Ramirez, J. E., Wu, T., Lee, Y. T., Aguila, C. C., Bouchard, K. R., Cauley, L. S. (2011) Division of labor between subsets of lymph node dendritic cells determines the specificity of the CD8 T-cell recall response to influenza infection. Eur. J. Immunol. 41, 2632-2641.
21. Hikono, H., Kohlmeier, J. E., Ely, K. H., Scott, I., Roberts, A. D., Blackman, M. A., Woodland, D. L. (2006) T-cell memory and recall responses to respiratory virus infections. Immunol. Rev. 211, 119-132.
22. Hogquist, K. A., Jameson, S. C., Heath, W. R., Howard, J. L., Bevan, M. J., Carbone, F. R. (1994) T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27.
23. Topham, D. J., Castrucci, M. R., Wingo, F. S., Belz, G. T., Doherty, P. C. (2001) The role of antigen in the localization of naive, acutely activated, and memory CD8(+) T cells to the lung during influenza pneumonia. J. Immunol. 167, 6983-6990.
24. Mintern, J. D., Bedoui, S., Davey, G. M., Moffat, J. M., Doherty, P. C., Turner, S. J. (2009) Transience of MHC class I-restricted antigen presentation after influenza A virus infection. Proc. Natl. Acad. Sci. USA 106, 6724-6729.
25. Daly, K., Nguyen, P., Woodland, D. L., Blackman, M. A. (1995) Immunodominance of major histocompatibility complex class I-restricted influenza virus epitopes can be influenced by the T-cell receptor repertoire. J. Virol. 69, 7416-7422.
26. Flynn, K. J., Belz, G. T., Altman, J. D., Ahmed, R., Woodland, D. L., Doherty, P. C. (1998) Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity 8, 683-691.
27. Huprikar, J., Rabinowitz, S. (1980) A simplified plaque assay for influenza viruses in Madin-Darby kidney (MDCK) cells. J. Virol. Methods 1, 117-120.
28. Perrone, L. A., Ahmad, A., Veguilla, V., Lu, X., Smith, G., Katz, J. M., Pushko, P., Tumpey, T. M. (2009) Intranasal vaccination with 1918 influenza virus-like particles protects mice and ferrets from lethal 1918 and H5N1 influenza virus challenge. J. Virol. 83, 5726-5734.
29. Kitamura, D., Roes, J., Kuhn, R., Rajewsky, K. (1991) A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin μ chain gene. Nature 350, 423-426.
30. Gebhardt, T., Mueller, S. N., Heath, W. R., Carbone, F. R. (2013) Peripheral tissue surveillance and residency by memory T cells. Trends Immunol. 34, 27-32.
31. Barber, D. L., Wherry, E. J., Masopust, D., Zhu, B., Allison, J. P., Sharpe, A. H., Freeman, G. J., Ahmed, R. (2006) Restoring function in exhausted CD8 T cells during chronic viral infection. Nature 439, 682-687.
32. Holt, P. G., Schon-Hegrad, M. A. (1987) Localization of T cells, macrophages and dendritic cells in rat respiratory tract tissue: implications for immune function studies. Immunology 62, 349-356.
33. Yopp, A. C., Ledgerwood, L. G., Ochando, J. C., Bromberg, J. S. (2006) Sphingosine 1-phosphate receptor modulators: a new class of immunosuppressants. Clin. Transplant. 20, 788-795.
34. Ostler, T., Hussell, T., Surh, C. D., Openshaw, P., Ehl, S. (2001) Longterm persistence and reactivation of T cell memory in the lung of mice infected with respiratory syncytial virus. Eur. J. Immunol. 31, 2574-2582.
35. Mackay, L. K., Stock, A. T., Ma, J. Z., Jones, C. M., Kent, S. J., Mueller, S. N., Heath, W. R., Carbone, F. R., Gebhardt, T. (2012) Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation. Proc. Natl. Acad. Sci. USA 109, 7037-7042.
36. Khanna, K. M., Bonneau, R. H., Kinchington, P. R., Hendricks, R. L. (2003) Herpes simplex virus-specific memory CD8+ T cells are selectively activated and retained in latently infected sensory ganglia. Immunity 18, 593-603.
37. Slifka, M. K., Whitton, J. L. (2000) Antigen-specific regulation of T cellmediated cytokine production. Immunity 12, 451-457.
38. Gehring, A. J., Koh, S., Chia, A., Paramasivam, K., Chew, V. S., Ho, Z. Z., Lee, K. H., Maini, M. K., Madhavan, K., Lim, S. G., Bertoletti, A. (2011) Licensing virus-specific T cells to secrete the neutrophil attracting chemokine CXCL-8 during hepatitis B virus infection. PLoS One 6, e23330.
39. Mutnal, M., Hu, S., Little, M., Lokensgard, J. (2011) Memory T cells persisting in the brain following MCMV infection induce long-term microglial activation via interferon-γ. J. Neurovirol. 17, 424-437.
40. Borron, P. J., Crouch, E. C., Lewis, J. F., Wright, J. R., Possmayer, F., Fraher, L. J. (1998) Recombinant rat surfactant-associated protein D inhibits human T lymphocyte proliferation and IL-2 production. J. Immunol. 161, 4599-4603.
41. Le, F. A., Jalil, A., Vergnon, I., Le Maux, C. B., Lazar, V., Bismuth, G., Chouaib, S., Mami-Chouaib, F. (2007) α E β 7 Integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis. J. Exp. Med. 204, 559-570.
42. Hofmann, M., Pircher, H. (2011) E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands. Proc. Natl. Acad. Sci. USA 108, 16741-16746.
43. Gebhardt, T., Wakim, L. M., Eidsmo, L., Reading, P. C., Heath, W. R., Carbone, F. R. (2009) Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524-530.
44. Shin, H., Iwasaki, A. (2012) A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491, 463-467.