Double-negative T resident memory cells of the lung react to influenza virus infection via CD11c hi dendritic cells

Mucosal Immunology

Volumn 9, Issue 4, 2016, Pages 999-1014

  Neyt, K ^a,b   GeurtsvanKessel, C H ^c   Lambrecht, B N ^a,b,c  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

^c ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD103 ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR3; FAS LIGAND; GLYCOPROTEIN P 15095; HERMES ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; VIRUS NUCLEOPROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ANTIGEN SPECIFICITY; ARTICLE; BIOACCUMULATION; CELL DIFFERENTIATION; CELL KINETICS; CELL SELECTION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE SEVERITY; FLOW CYTOMETRY; IMMUNE RESPONSE; INFLUENZA; LUNG INFECTION; LUNG PARENCHYMA; MEMORY T LYMPHOCYTE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL MOTION; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; INFLUENZA A VIRUS (H1N1); INFLUENZA A VIRUS (H3N2); LUNG; LYMPHOCYTE ACTIVATION; METABOLISM; MUCOSAL IMMUNITY; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD11C; ANTIGENS, VIRAL; CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; DENDRITIC CELLS; IMMUNITY, MUCOSAL; IMMUNOLOGIC MEMORY; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; LUNG; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NATURAL KILLER T-CELLS; ORTHOMYXOVIRIDAE INFECTIONS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS;

EID: 84975853326     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2015.91     Document Type: Article

References (73)

1. Brandes, M., Klauschen, F., Kuchen, S. & Germain, R.N. A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154, 197-212 (2013).
2. Lambrecht, B.N. & Hammad, H. Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Ann. Rev. Immunol. 30, 243-270 (2012).
3. Galkina, E., Thatte, J., Dabak, V., Williams, M.B., Ley, K. & Braciale, T.J. Preferential migration of effector CD8+ T cells into the interstitium of the normal lung. J. Clin. Invest. 115, 3473-3483 (2005).
4. Yoo, J.K., Fish, E.N. & Braciale, T.J. LAPCs promote follicular helperc Tcell differentiation of Ag-primedCD4+ Tcells during respiratory virus infection. J. Exp. Med. 209, 1853-1867 (2012).
5. Hufford, M.M., Kim, T.S., Sun, J. & Braciale, T.J. Antiviral CD8+ T cell effector activities in situ are regulated by target cell type. J. Exp. Med. 208, 167-180 (2011).
6. Topham, D.J., Tripp, R.A. & Doherty, P.C. CD8+ Tcells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159, 5197-5200 (1997).
7. Johnson, S. et al. Selected Toll-like receptor ligands and viruses promote helper-independent cytotoxic T cell priming by upregulating CD40L on dendritic cells. Immunity 30, 218-227 (2009).
8. Sun, J., Dodd, H., Moser, E.K., Sharma, R. & Braciale, T.J. CD4+ T cell help and innate-derived IL-27 induce Blimp-1-dependent IL-10 production by antiviral CTLs. Nat. Immunol 12, 327-334 (2011).
9. Belz, G.T., Wodarz, D., Diaz, G., Nowak, M.A. & Doherty, P.C. Compromised influenza virus-specific CD8(+)-T-cell memory in CD4(+)-T-cell-deficient mice. J. Virol 76, 12388-12393 (2002).
10. Lee, B.O. et al. CD4 T cell-independent antibody response promotes resolution of primary influenza infection and helps to prevent reinfection. J. Immunol. 175, 5827-5838 (2005).
11. Brown, D.M., Lee, S., Garcia-Hernandez Mde, L. & Swain, S.L. Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J. Virol. 86, 6792-6803 (2012).
12. Scherle, P.A., Palladino, G. & Gerhard, W. Mice can recover from pulmonary influenza virus infection in the absence of class I-restricted cytotoxic T cells. J. Immunol. 148, 212-217 (1992).
13. Brown, D.M., Dilzer, A.M., Meents, D.L. & Swain, S.L. CD4 Tcell-mediated protection from lethal influenza: perforin and antibody-mediated mechanisms give a one-Two punch. J. Immunol. 177, 2888-2898 (2006).
14. Joshi, N.S. et al. Inflammation directs memory precursor and short-lived effector CD8(+) Tcell fates via the graded expression of T-bet transcription factor. Immunity 27, 281-295 (2007).
15. Turner, D.L. et al. Lung niches for the generation and maintenance of tissue-resident memory T cells. Mucosal Immunol. 7, 501-510 (2014).
16. Teijaro, J.R., Turner, D., Pham, Q., Wherry, E.J., Lefrancois, L. & Farber, D.L. Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J. Immunol. 187, 5510-5514 (2011).
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 193, 981-986 (2001).
18. Hogan, R.J. et al. Long-Term maintenance of virus-specific effector memory CD8+ T cells in the lung airways depends on proliferation. J. Immunol. 169, 4976-4981 (2002).
19. Liang, S., Mozdzanowska, K., Palladino, G. & Gerhard, W. Heterosubtypic immunity to influenza type A virus in mice. Effector mechanisms and their longevity. J. Immunol 152, 1653-1661 (1994).
20. Wilkinson, P. et al. An open-ended plea for the development of a global database of HIV vaccine responses. Curr. Opin. HIV AIDS 7, 10-16 (2012).
21. McKinstry, K.K. et al. Memory CD4+ T cells protect against influenza through multiple synergizing mechanisms. J. Clin. Invest 122, 2847-2856 (2012).
22. Wu, T. et al. Lung-residentmemory CD8 Tcells (TRM) are indispensable for optimal cross-protection against pulmonary virus infection. J. Leukoc. Biol 95, 215-224 (2014).
23. DAcquisto, F. & Crompton, T. CD3+CD4-CD8-(double negative) Tcells: saviours or villains of the immune response? Biochem. Pharmacol. 82, 333-340 (2011).
24. Abraham, E., Freitas, A.A. & Coutinho, A.A. Purification and characterization of intraparenchymal lung lymphocytes. J. Immunol. 144, 2117-2122 (1990).
25. Ibraghimov, A.R. & Lynch, R.G. T cell specialization at environmental interfaces: T cells from the lung and the female genital tract of lpr and gld mice differ from their splenic and lymph node counterparts. Eur. J. Immunol. 24, 1848-1852 (1994).
26. Kawakami, K., Teruya, K., Tohyama, M., Kudeken, N., Yonamine, Y. & Saito, A. Mac1 discriminates unusual CD4-CD8-double-negative T cells bearing alpha beta antigen receptor from conventional ones with either CD4 or CD8 in murine lung. Immunol. Lett 46, 143-152 (1995).
27. Takamoto, M., Kusama, Y., Takatsu, K., Nariuchi, H. & Sugane, K. Occurrence of interleukin-5 production by CD4-CD8-(double-negative) Tcells in lungs of both normal and congenitally athymic nude mice infected with Toxocara canis. Immunology 85, 285-291 (1995).
28. Watanabe, N. et al. Th1 and Th2 subsets equally undergo Fas-dependent and-independent activation-induced cell death. Eur. J. Immunol 27, 1858-1864 (1997).
29. Oreshkova, T. et al. Beta(2) integrin deficiency yields unconventional double-negative Tcells distinct from mature classical natural killer Tcells in mice. Immunology 128, 271-286 (2009).
30. Cowley, S.C., Meierovics, A.I., Frelinger, J.A., Iwakura, Y. & Elkins, K.L. Lung CD4-CD8-double-negative T cells are prominent producers of IL-17A and IFN-gamma during primary respiratory murine infection with Francisella tularensis live vaccine strain. J. Immunol 184, 5791-5801 (2010).
31. Rajasekar, R. & Augustin, A. Selection of pulmonary CD4-, CD8-, alpha beta+ Tcells expressing V beta 8Tcell receptors. Am. J. Respir. Cell Mol. Biol. 10, 79-84 (1994).
32. Augustin, A., Kubo, R.T. & Sim, G.K. Resident pulmonary lymphocytes expressing the gamma/delta T-cell receptor. Nature 340, 239-241 (1989).
33. Godfrey, D.I., Stankovic, S. & Baxter, A.G. Raising the NKTcell family. Nat. Immunol. 11, 197-206 (2010).
34. Godfrey, D.I., MacDonald, H.R., Kronenberg, M., Smyth, M.J. & Van Kaer, L. NKT cells: whats in a name?. Nat. Rev. Immunol 4, 231-237 (2004).
35. Ford, M.S., Zhang, Z.X., Chen, W. & Zhang, L. Double-negative T regulatory cells can develop outside the thymus and do not mature from CD8+ T cell precursors. J. Immunol 177, 2803-2809 (2006).
36. Kadena, T. et al. TCR alpha beta+ CD4-CD8-T cells differentiate extrathymically in an lck-independent manner and participate in early response against Listeria monocytogenes infection through interferongamma production. Immunology 91, 511-519 (1997).
37. Mohamood, A.S. et al. Fas-mediated apoptosis regulates the composition of peripheral alphabeta Tcell repertoire by constitutively purging out double negative T cells. PLoS One 3, e3465 (2008).
38. Mehal, W.Z. & Crispe, I.N. TCR ligation on CD8+ T cells creates doublenegative cells in vivo. J. Immunol. 161, 1686-1693 (1998).
39. Naito, T., Tanaka, H., Naoe, Y. & Taniuchi, I. Transcriptional control of T-cell development. Int. Immunol 23, 661-668 (2011).
40. Kedzierska, K., Turner, S.J. & Doherty, P.C. Conserved T cell receptor usage in primary and recall responses to an immunodominant influenza virus nucleoprotein epitope. Proc. Natl Acad. Sci. USA 101, 4942-4947 (2004).
41. Lantz, O. & Bendelac, A. An invariant Tcell receptor alpha chain is used by a unique subset of major histocompatibility complex class I-specific CD4+ and CD4-8-T cells in mice and humans. J. Exp. Med 180, 1097-1106 (1994).
42. Kawano, T. et al. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science 278, 1626-1629 (1997).
43. Wherry, E.J. et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol 4, 225-234 (2003).
44. Mueller, S.N., Gebhardt, T., Carbone, F.R. & Heath, W.R. Memory T cell subsets, migration patterns, and tissue residence. Annu. Rev. Immunol 31, 137-161 (2013).
45. Grebe, K.M., Yewdell, J.W. & Bennink, J.R. Heterosubtypic immunity to influenza A virus: where do we stand? Microbes Infect 10, 1024-1029 (2008).
46. Kreijtz, J.H. et al. Primary influenza A virus infection induces crossprotective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine 25, 612-620 (2007).
47. Plantinga, M. et al. Conventional and monocyte-derived CD11b+ dendritic cells initiate and maintain T helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38, 322-335 (2013).
48. GeurtsvanKessel, C.H. et al. Clearance of influenza virus from the lung depends on migratory langerin+CD11b-but not plasmacytoid dendritic cells. J. Exp. Med 205, 1621-1634 (2008).
49. Kim, T.S., Gorski, S.A., Hahn, S., Murphy, K.M. & Braciale, T.J. Distinct dendritic cell subsets dictate the fate decision between effector and memory CD8(+) T cell differentiation by a CD24-dependent mechanism. Immunity 40, 400-413 (2014).
50. Kim, T.S., Hufford, M.M., Sun, J., Fu, Y.X. & Braciale, T.J. Antigen persistence and the control of local T cell memory by migrant respiratory dendritic cells after acute virus infection. J. Exp. Med. 207, 1161-1172 (2010).
51. Gao, J.F. et al. Regulation of antigen-expressing dendritic cells by double negative regulatory T cells. Eur. J. Immunol 41, 2699-2708 (2011).
52. Chang, J.C., Zhang, L., Distler, S.G., Ziang, G. & Kaplan, A.M. Characterization and function of CD3+ CD4-CD8-TcR-Alpha beta bearing cells infiltrating the lung during the immune response. Reg. Immunol. 4, 25-33 (1992).
53. Rossjohn, J., Pellicci, D.G., Patel, O., Gapin, L. & Godfrey, D.I. Recognition of CD1d-restricted antigens by natural killer Tcells. Nat. Rev. Immunol. 12, 845-857 (2012).
54. Liao, C.M., Zimmer, M.I. & Wang, C.R. The functions of type I and type II natural killer Tcells in inflammatory bowel diseases. Inflamm. Bowel Dis. 19, 1330-1338 (2013).
55. Priatel, J.J., Utting, O. & Teh, H.S. TCR/self-Antigen interactions drive double-negative T cell peripheral expansion and differentiation into suppressor cells. J. Immunol 167, 6188-6194 (2001).
56. Hayes, S.M., Li, L. & Love, P.E. TCR signal strength influences alphabeta/gammadelta lineage fate. Immunity 22, 583-593 (2005).
57. Paget, C. & Trottein, F. Role of type 1 natural killer T cells in pulmonary immunity. Mucosal Immunol 6, 1054-1067 (2013).
58. Edholm, E.S., Grayfer, L. & Robert, J. Evolution of nonclassical MHC-dependent invariant T cells. Cell. Mol. Life Sci. 71, 4763-4780 (2014).
59. Le Bourhis, L., Guerri, L., Dusseaux, M., Martin, E., Soudais, C. & Lantz, O. Mucosal-Associated invariant T cells: unconventional development and function. Trends Immunol 32, 212-218 (2011).
60. Hedrich, C.M. et al. cAMP-responsive element modulator alpha (CREMalpha) trans-represses the transmembrane glycoprotein CD8 and contributes to the generation of CD3+CD4-CD8-T cells in health and disease. J. Biol. Chem. 288, 31880-31887 (2013).
61. Hedrich, C.M. et al. cAMP responsive element modulator (CREM) alpha mediates chromatin remodeling of CD8 during the generation of CD3+ CD4-CD8-T cells. J. Biol. Chem 289, 2361-2370 (2014).
62. Anderson, K.G. et al. Cutting edge: intravascular staining redefines lung CD8 T cell responses. J. Immunol 189, 2702-2706 (2012).
63. Antonelli, L.R. et al. Disparate immunoregulatory potentials for doublenegative (CD4-CD8-) alpha beta and gamma delta T cells from human patients with cutaneous leishmaniasis. Infect. Immun. 74, 6317-6323 (2006).
64. Pinheiro, M.B. et al. CD4-CD8-Alphabeta and gammadelta T cells display inflammatory and regulatory potentials during human tuberculosis. PLoS One 7, e50923 (2012).
65. Martin, E. et al. Stepwise development of MAITcells in mouse and human. PLoS Biol. 7, e54 (2009).
66. Le Bourhis, L. et al. Antimicrobial activity of mucosal-Associated invariant T cells. Nat. Immunol 11, 701-708 (2010).
67. Ross, T.L. et al. Role of CD4+, CD8+ and double negative T-cells in the protection of SCID/beige mice against respiratory challenge with Rhodococcus equi. Can. J. Vet. Res. 60, 186-192 (1996).
68. Zhang, Z.X., Yang, L., Young, K.J., DuTemple, B. & Zhang, L. Identification of a previously unknown antigen-specific regulatory T cell and its mechanism of suppression. Nat. Med 6, 782-789 (2000).
69. Hillhouse, E.E. & Lesage, S. A comprehensive review of the phenotype and function of antigen-specific immunoregulatory double negative T cells. J. Autoimmun. 40, 58-65 (2013).
70. Liang, Q. et al. Double Negative (DN) [CD3(+)CD4(-)CD8(-)] T cells correlate with disease progression during HIV infection. Immunol. Invest 42, 431-437 (2013).
71. Miao, J. et al. Percentages of CD4+CD161+ and CD4-CD8-CD161+ TCells in the synovial fluid are correlated with disease activity in rheumatoid arthritis. Mediators Inflamm. 2015, 563713 (2015).
72. Alunno, A. et al. IL-17-producing CD4-CD8-T cells are expanded in the peripheral blood, infiltrate salivary glands and are resistant to corticosteroids in patients with primary Sjogrens syndrome. Ann. Rheum. Dis 72, 286-292 (2013).
73. Alunno, A. et al. CD4(-)CD8(-) T-cells in primary Sjogrens syndrome: Association with the extent of glandular involvement. J. Autoimmun. 51, 38-43 (2014).