Lung-resident CD4+ T cells are sufficient for IL-4R-dependent recall immunity to Nippostrongylus brasiliensis infection

Mucosal Immunology

Volumn 7, Issue 2, 2014, Pages 239-248

  Thawer, S G ^a,c   Horsnell, W G C ^a,c   Darby, M ^a   Hoving, J C ^a   Dewals, B ^a,d   Cutler, A J ^a,d   Lang, D ^b   Brombacher, F ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c Faculty of Veterinary Medicine   (Belgium)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FINGOLIMOD; INTERLEUKIN 4 RECEPTOR ALPHA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL EXPANSION; CONTROLLED STUDY; IMMUNITY; LYMPH NODE; LYMPHOCYTE MIGRATION; LYMPHOCYTOPENIA; LYMPHOID TISSUE; MOUSE; NIPPOSTRONGYLUS BRASILIENSIS; NIPPOSTRONGYLUS BRASILIENSIS INFECTION; NONHUMAN; PRIORITY JOURNAL; RECALL IMMUNITY; REINFECTION; SECONDARY INFECTION; STROMA CELL; STRONGYLE INFECTION; TERTIARY LYMPHOID STRUCTURE; TH2 CELL;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; DISEASE MODELS, ANIMAL; GENE EXPRESSION; IMMUNOLOGIC MEMORY; INTERLEUKIN-4 RECEPTOR ALPHA SUBUNIT; LUNG; LYMPH NODES; MICE; MICE, KNOCKOUT; NIPPOSTRONGYLUS; STRONGYLIDA INFECTIONS;

EID: 84887293841     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2013.40     Document Type: Article

References (41)

1. Hotez, P.J., Brindley, P.J., Bethony, J.M., King, C.H., Pearce, E.J. & Jacobson, J. Helminth infections: The great neglected tropical diseases. J. Clin. Invest. 118, 1311-1321 (2008).
2. Horsnell, W.G.C. et al. Delayed goblet cell hyperplasia, acetylcholine receptor expression, and worm expulsion in SMC-specific IL-4Ralphadeficient mice. PLoS pathog. 3, e1 (2007).
3. Kopf, M., Le Gros, G., Bachmann, M., Lamers, M.C., Bluethmann, H. & Kohler, G. Disruption of the murine IL-4 gene blocks Th2 cytokine responses. Nature 362, 245-248 (1993).
4. Brombacher, F. The role of interleukin-13 in infectious diseases and allergy. BioEssays. 22, 646-656 (2000).
5. Anthony, R.M., Rutitzky, L.I., Urban, J.F. Jr. & Stadecker, M.J. Protective immune mechanisms in helminth infection. Nat. Rev. Immunol. 7, 975-987 (2007).
6. Urban, J.F. Jr., Noben-Trauth,N., Schopf, L.,Madden, K.B. & Finkelman, F.D. Cutting edge: IL-4 receptor expression by non-bone marrow-derived cells is required to expel gastrointestinal nematode parasites. J. Immunol. 167, 6078-6081 (2001).
7. Horsnell, W.G.C. et al. IL-4Ra-responsive smooth muscle cells contribute to initiation of TH2 immunity and pulmonary pathology in Nippostrongylus brasiliensis infections. Mucosal. Immunol. 4, 83-92 (2011).
8. Harvie, M., Camberis, M., Tang, S.-C., Delahunt, B., Paul,W. & LeGros, G. The lung is an important site for priming CD4 T-cell-mediated protective immunity against gastrointestinal helminth parasites. Infect. Immun. 78, 3753-3762 (2010).
9. Anthony, R.M. et al. Memory TH2 cells induce alternatively activated macrophages to mediate protection against nematode parasites. Nat. Med. 12, 955-960 (2007).
10. Sallusto, F., Geginat, J. & Lanzavecchia, A. Central memory and effector memory Tcell subsets: Function, generation, and maintenance. Annu. Rev. Immunol. 22, 745-763 (2004).
11. Katona, I.M., Urban, J.F. Jr.& Finkelman, F. The role of L3T4+ and LYT-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J. Immunol. 140, 3206-3211 (1988).
12. Connor, L.M. et al. A key role for lung-resident memory lymphocytes in protective immune responses after BCG vaccination. Eur. J. Immunol. 40, 2482-2492 (2010).
13. Harris, N.L.,Watt, V., Ronchese, F. & Le Gros, G. Differential Tcell function and fate in lymph node and nonlymphoid tissues. J. Exp. Med. 195, 317-326 (2002).
14. Hogan, B.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, 0-5 (2001).
15. Teijaro, J.R., Turner, D., Pham, Q., Wherry, E.J., Lefranc'ois, 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).
16. Zaph, C., Rook, K.A., Goldschmidt, M., Mohrs, M., Scott, P. & Artis, D. Persistence and function of central and effector memory CD4+ T cells following infection with a gastrointestinal helminth. J. Immunol. 177, 511-518 (2006).
17. Van Panhuys, N., Perret, R., Prout, M., Ronchese, F. & Le Gros, G. Effector lymphoid tissue and its crucial role in protective immunity. Trends Immunol. 26, 242-247 (2005).
18. Chiba, K., Matsuyuki, H., Maeda, Y. & Sugahara, K. Role of sphingosine 1-phosphate receptor type 1 in lymphocyte egress from secondary lymphoid tissues and thymus. Cell. Mol. Immunol. 3, 11-19 (2006).
19. Hofmann, M., Brinkmann, V. & Zerwes, H.-G. FTY720 preferentially depletes naive T cells from peripheral and lymphoid organs. Int. Immunopharmacol. 6, 1902-1910 (2006).
20. Mearns, H. et al. Interleukin-4-promoted T helper 2 responses enhance Nippostrongylus brasiliensis-induced pulmonary pathology. Infect. Immun. 76, 5535-5542 (2008).
21. Lohning, M. et al. T1/ST2 is preferentially expressed on murine Th2 cells, independent of interleukin 4, interleukin 5, and interleukin 10, and important for Th2 effector function. Proc. Natl. Acad. Sci. USA 95, 6930-6935 (1998).
22. Sullivan, B.M. et al. Genetic analysis of basophil function in vivo. Nat. Immunol. 12, 527-535 (2011).
23. Browning, J.L. Inhibition of the lymphotoxin pathway as a therapy for autoimmune disease. Immunol. Rev. 223, 202-220 (2008).
24. Fava, R.A. et al. A role for the lymphotoxin/LIGHT axis in the pathogenesis of murine collagen-induced arthritis. J Immunol. 171, 115-126 (2003).
25. Van de Pavert, S.A. & Mebius, R.E. New insights into the development of lymphoid tissues. Nat. Rev. Immunol. 10, 664-674 (2010).
26. Fava, R. et al. Lymphotoxin-beta receptor blockade reduces CXCL13 in lacrimal glands and improves corneal integrity in the NOD model of sjogren's syndrome. Arthritis Res. & Ther. 13, R182 (2011).
27. Hasnain, S.Z. et al. Muc5ac: A critical componentmediating the rejection of enteric nematodes. J. Exp. Med. 208, 893-900 (2011).
28. Barner, M., Mohrs, M., Brombacher, F. & Kopf, M. Differences between IL-4R alpha-deficient and IL-4-deficient mice reveal a role for IL-13 in the regulation of Th2 responses. Curr. Biol. 8, 669-672 (1998).
29. Herbert, D.R. et al. Alternative macrophage activation is essential for survival during schistosomiasis and downmodulates T helper 1 responses and immunopathology. Immunity 20, 623-635 (2004).
30. Chapman, T.J., Lambert, K. & Topham, D.J. Rapid reactivation of extralymphoid CD4 T cells during secondary infection. PloS One 6, e20493 (2011).
31. Masopust, D., Vezys, V., Marzo, A.L. & Lefranc'ois, L. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291, 2413-2417 (2001).
32. Moyron-Quiroz, J.E. et al. Persistence and responsiveness of immunologic memory in the absence of secondary lymphoid organs. Immunity 25, 643-654 (2006).
33. Hogan, R.J. et al. Activated antigen-specific CD8+ T cells persist in the lungs following recovery from respiratory virus infections. J. Immunol. 166, 1813-1822 (2001).
34. Kaveh, D.A., Bachy, V.S., Hewinson, R.G. & Hogarth, P.J. Systemic BCG immunization induces persistent lung mucosal multifunctional CD4 T(EM) cells which expand following virulent mycobacterial challenge. PloS One 6, e21566 (2011).
35. 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).
36. Moyron-Quiroz, J.E. et al. Role of inducible bronchus associated lymphoid tissue (iBALT) in respiratory immunity. Nat. Med. 10, 927-934 (2004).
37. Randall, T.D. Bronchus-associated lymphoid tissue (BALT) structure and function. Adv. Immunol. 107, 187-241 (2010).
38. Hofmann, J., Greter,M., Du Pasquier, L. & Becher, B. B-cells need a proper house, whereas T-cells are happy in a cave; the dependence of lymphocytes on secondary lymphoid tissues during evolution. Trends Immunol. 31, 144-153 (2010).
39. 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 319, 198-202 (2008).
40. Constant, S.L. et al. Resident lung antigen-presenting cells have the capacity to promote Th2 T cell differentiation in situ. J. Clin. Invest. 110, 1441-1448 (2002).
41. Dewals, B. et al. IL-4Ralpha responsiveness of non-CD4 T cells contributes to resistance in Schistosoma mansoni infection in pan-T cell-specific IL-4Ralpha-deficient mice. Am. J. Pathol. 175, 706-716 (2009).