A Distinct Lung-Interstitium-Resident Memory CD8+ T Cell Subset Confers Enhanced Protection to Lower Respiratory Tract Infection

Cell Reports

Volumn 16, Issue 7, 2016, Pages 1800-1809

  Gilchuk, Pavlo ^a,b   Hill, Timothy M ^b,e   Guy, Clifford ^c   McMaster, Sean R ^d   Boyd, Kelli L ^b   Rabacal, Whitney A ^b   Lu, Pengcheng ^b   Shyr, Yu ^b   Kohlmeier, Jacob E ^d   Sebzda, Eric ^b   Green, Douglas R ^c   Joyce, Sebastian ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

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

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNITED STATES MILITARY ACADEMY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; VACCINIA VACCINE; CXCR3 PROTEIN, MOUSE; VIRUS ANTIGEN; VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG EFFICACY; IMMUNE RESPONSE; IMMUNOGENICITY; IN VIVO STUDY; LOWER RESPIRATORY TRACT INFECTION; LUNG INTERSTITIUM; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTECTION; VACCINATION; VACCINIA; VACCINIA VIRUS; VIRUS IMMUNITY; AMINO ACID SEQUENCE; ANIMAL; BIOSYNTHESIS; BODY WEIGHT; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; IMMUNOPHENOTYPING; INTRANASAL DRUG ADMINISTRATION; LUNG; MUCOSAL IMMUNITY; PATHOGENICITY; PATHOLOGY; RESPIRATORY TRACT INFECTIONS; TRANSGENIC MOUSE; VIROLOGY; VIRUS LOAD;

ADMINISTRATION, INTRANASAL; AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, VIRAL; BODY WEIGHT; CD8-POSITIVE T-LYMPHOCYTES; GENE EXPRESSION; IMMUNITY, MUCOSAL; IMMUNOLOGIC MEMORY; IMMUNOPHENOTYPING; LUNG; MICE; MICE, TRANSGENIC; RECEPTORS, CXCR3; RESPIRATORY TRACT INFECTIONS; VACCINATION; VACCINIA; VACCINIA VIRUS; VIRAL LOAD; VIRAL VACCINES;

EID: 84997719773     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.07.037     Document Type: Article

References (38)

1. ∗0702-restricted CTL epitopes. Hum. Immunol. 64 (2003), 211–223.
2. Anderson, K.G., Sung, H., Skon, C.N., Lefrancois, L., Deisinger, A., Vezys, V., Masopust, D., Cutting edge: intravascular staining redefines lung CD8 T cell responses. J. Immunol. 189 (2012), 2702–2706.
3. Anderson, K.G., Mayer-Barber, K., Sung, H., Beura, L., James, B.R., Taylor, J.J., Qunaj, L., Griffith, T.S., Vezys, V., Barber, D.L., Masopust, D., Intravascular staining for discrimination of vascular and tissue leukocytes. Nat. Protoc. 9 (2014), 209–222.
4. Ariotti, S., Beltman, J.B., Chodaczek, G., Hoekstra, M.E., van Beek, A.E., Gomez-Eerland, R., Ritsma, L., van Rheenen, J., Marée, A.F., Zal, T., et al. Tissue-resident memory CD8+ T cells continuously patrol skin epithelia to quickly recognize local antigen. Proc. Natl. Acad. Sci. USA 109 (2012), 19739–19744.
5. Barletta, K.E., Cagnina, R.E., Wallace, K.L., Ramos, S.I., Mehrad, B., Linden, J., Leukocyte compartments in the mouse lung: distinguishing between marginated, interstitial, and alveolar cells in response to injury. J. Immunol. Methods 375 (2012), 100–110.
6. + T cells responding to infection. Nat. Immunol. 16 (2015), 406–414.
7. Bivas-Benita, M., Gillard, G.O., Bar, L., White, K.A., Webby, R.J., Hovav, A.H., Letvin, N.L., Airway CD8(+) T cells induced by pulmonary DNA immunization mediate protective anti-viral immunity. Mucosal Immunol. 6 (2013), 156–166.
8. Clark, R.A., Resident memory T cells in human health and disease. Sci. Transl. Med., 7, 2015, 269rv1.
9. Courtney, A.N., Thapa, P., Singh, S., Wishahy, A.M., Zhou, D., Sastry, J., Intranasal but not intravenous delivery of the adjuvant α-galactosylceramide permits repeated stimulation of natural killer T cells in the lung. Eur. J. Immunol. 41 (2011), 3312–3322.
10. Gilchuk, P., Spencer, C.T., Conant, S.B., Hill, T., Gray, J.J., Niu, X., Zheng, M., Erickson, J.J., Boyd, K.L., McAfee, K.J., et al. Discovering naturally processed antigenic determinants that confer protective T cell immunity. J. Clin. Invest. 123 (2013), 1976–1987.
11. Halle, S., Dujardin, H.C., Bakocevic, N., Fleige, H., Danzer, H., Willenzon, S., Suezer, Y., Hämmerling, G., Garbi, N., Sutter, G., et al. Induced bronchus-associated lymphoid tissue serves as a general priming site for T cells and is maintained by dendritic cells. J. Exp. Med. 206 (2009), 2593–2601.
12. Halle, S., Keyser, K.A., Stahl, F.R., Busche, A., Marquardt, A., Zheng, X., Galla, M., Heissmeyer, V., Heller, K., Boelter, J., et al. In vivo killing capacity of cytotoxic T cells is limited and involves dynamic Interactions and T cell cooperativity. Immunity 44 (2016), 233–245.
13. Hasenberg, M., Stegemann-Koniszewski, S., Gunzer, M., Cellular immune reactions in the lung. Immunol. Rev. 251 (2013), 189–214.
14. Hickman, H.D., Reynoso, G.V., Ngudiankama, B.F., Cush, S.S., Gibbs, J., Bennink, J.R., Yewdell, J.W., CXCR3 chemokine receptor enables local CD8(+) T cell migration for the destruction of virus-infected cells. Immunity 42 (2015), 524–537.
15. Jiang, X., Clark, R.A., Liu, L., Wagers, A.J., Fuhlbrigge, R.C., Kupper, T.S., Skin infection generates non-migratory memory CD8+ T(RM) cells providing global skin immunity. Nature 483 (2012), 227–231.
16. Khanna, K.M., Aguila, C.C., Redman, J.M., Suarez-Ramirez, J.E., Lefrançois, L., Cauley, L.S., In situ imaging reveals different responses by naïve and memory CD8 T cells to late antigen presentation by lymph node DC after influenza virus infection. Eur. J. Immunol. 38 (2008), 3304–3315.
17. Kohlmeier, J.E., Cookenham, T., Miller, S.C., Roberts, A.D., Christensen, J.P., Thomsen, A.R., Woodland, D.L., CXCR3 directs antigen-specific effector CD4+ T cell migration to the lung during parainfluenza virus infection. J. Immunol. 183 (2009), 4378–4384.
18. Lelkes, E., Headley, M.B., Thornton, E.E., Looney, M.R., Krummel, M.F., The spatiotemporal cellular dynamics of lung immunity. Trends Immunol. 35 (2014), 379–386.
19. Li, A.V., Moon, J.J., Abraham, W., Suh, H., Elkhader, J., Seidman, M.A., Yen, M., Im, E.J., Foley, M.H., Barouch, D.H., Irvine, D.J., Generation of effector memory T cell-based mucosal and systemic immunity with pulmonary nanoparticle vaccination. Sci. Transl. Med., 5, 2013, 204ra130.
20. Liu, L., Zhong, Q., Tian, T., Dubin, K., Athale, S.K., Kupper, T.S., Epidermal injury and infection during poxvirus immunization is crucial for the generation of highly protective T cell-mediated immunity. Nat. Med. 16 (2010), 224–227.
21. Mackay, L.K., Rahimpour, A., Ma, J.Z., Collins, N., Stock, A.T., Hafon, M.L., Vega-Ramos, J., Lauzurica, P., Mueller, S.N., Stefanovic, T., et al. The developmental pathway for CD103(+)CD8+ tissue-resident memory T cells of skin. Nat. Immunol. 14 (2013), 1294–1301.
22. Manicassamy, B., Manicassamy, S., Belicha-Villanueva, A., Pisanelli, G., Pulendran, B., García-Sastre, A., Analysis of in vivo dynamics of influenza virus infection in mice using a GFP reporter virus. Proc. Natl. Acad. Sci. USA 107 (2010), 11531–11536.
23. McMaster, S.R., Wilson, J.J., Wang, H., Kohlmeier, J.E., Airway-resident memory CD8 T cells provide antigen-specific protection against respiratory virus challenge through rapid IFN-γ production. J. Immunol. 195 (2015), 203–209.
24. Moyron-Quiroz, J.E., Rangel-Moreno, J., Hartson, L., Kusser, K., Tighe, M.P., Klonowski, K.D., Lefrançois, L., Cauley, L.S., Harmsen, A.G., Lund, F.E., Randall, T.D., Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity 25 (2006), 643–654.
25. Norbury, C.C., Malide, D., Gibbs, J.S., Bennink, J.R., Yewdell, J.W., Visualizing priming of virus-specific CD8+ T cells by infected dendritic cells in vivo. Nat. Immunol. 3 (2002), 265–271.
26. Park, C.O., Kupper, T.S., The emerging role of resident memory T cells in protective immunity and inflammatory disease. Nat. Med. 21 (2015), 688–697.
27. Rangel-Moreno, J., Carragher, D.M., de la Luz Garcia-Hernandez, M., Hwang, J.Y., Kusser, K., Hartson, L., Kolls, J.K., Khader, S.A., Randall, T.D., The development of inducible bronchus-associated lymphoid tissue depends on IL-17. Nat. Immunol. 12 (2011), 639–646.
28. Salek-Ardakani, S., Moutaftsi, M., Sette, A., Croft, M., Targeting OX40 promotes lung-resident memory CD8 T cell populations that protect against respiratory poxvirus infection. J. Virol. 85 (2011), 9051–9059.
29. Schenkel, J.M., Masopust, D., Tissue-resident memory T cells. Immunity 41 (2014), 886–897.
30. Schenkel, J.M., Fraser, K.A., Beura, L.K., Pauken, K.E., Vezys, V., Masopust, D., T cell memory. Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science 346 (2014), 98–101.
31. Semmling, V., Lukacs-Kornek, V., Thaiss, C.A., Quast, T., Hochheiser, K., Panzer, U., Rossjohn, J., Perlmutter, P., Cao, J., Godfrey, D.I., et al. Alternative cross-priming through CCL17-CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat. Immunol. 11 (2010), 313–320.
32. Sheridan, B.S., Pham, Q.M., Lee, Y.T., Cauley, L.S., Puddington, L., Lefrançois, L., Oral infection drives a distinct population of intestinal resident memory CD8(+) T cells with enhanced protective function. Immunity 40 (2014), 747–757.
33. Shin, H., Iwasaki, A., A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491 (2012), 463–467.
34. Slütter, B., Pewe, L.L., Kaech, S.M., Harty, J.T., Lung airway-surveilling CXCR3(hi) memory CD8(+) T cells are critical for protection against influenza A virus. Immunity 39 (2013), 939–948.
35. Steinert, E.M., Schenkel, J.M., Fraser, K.A., Beura, L.K., Manlove, L.S., Igyártó, B.Z., Southern, P.J., Masopust, D., Quantifying memory CD8 T cells reveals regionalization of immunosurveillance. Cell 161 (2015), 737–749.
36. Takamura, S., Roberts, A.D., Jelley-Gibbs, D.M., Wittmer, S.T., Kohlmeier, J.E., Woodland, D.L., The route of priming influences the ability of respiratory virus-specific memory CD8+ T cells to be activated by residual antigen. J. Exp. Med. 207 (2010), 1153–1160.
37. Vanderbilt, J.N., Allen, L., Gonzalez, R.F., Tigue, Z., Edmondson, J., Ansaldi, D., Gillespie, A.M., Dobbs, L.G., Directed expression of transgenes to alveolar type I cells in the mouse. Am. J. Respir. Cell Mol. Biol. 39 (2008), 253–262.
38. Wu, T., Hu, Y., Lee, Y.T., Bouchard, K.R., Benechet, A., Khanna, K., Cauley, L.S., Lung-resident memory CD8 T cells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection. J. Leukoc. Biol. 95 (2014), 215–224.