CD27 is a thymic determinant of the balance between interferon-γ- and interleukin 17-producing γδ T cell subsets

Nature Immunology

Volumn 10, Issue 4, 2009, Pages 427-436

  Ribot, Julie C ^a,b   deBarros, Ana ^a,b   Pang, Dick John ^c   Neves, Joana F ^c,d   Peperzak, Victor ^e   Roberts, Scott J ^f   Girardi, Michael ^f   Borst, Jannie ^e   Hayday, Adrian C ^g   Pennington, Daniel J ^c   Silva Santos, Bruno ^a,b  

^a UNIVERSITY OF LISBON   (Portugal)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY OF COIMBRA   (Portugal)

^e NETHERLANDS CANCER INSTITUTE   (Netherlands)

^f YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD27 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; LYMPHOTOXIN BETA RECEPTOR; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; EMBRYO; IMMUNE RESPONSE; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE SUBPOPULATION; THYMUS;

ANIMALS; ANTIGENS, CD27; ANTIGENS, CD70; CELLS, CULTURED; INTERFERON-GAMMA; INTERLEUKIN-17; LYMPHOID PROGENITOR CELLS; LYMPHOTOXIN BETA RECEPTOR; MALARIA, CEREBRAL; MICE; MICE, INBRED C57BL; PLASMODIUM BERGHEI; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; THYMUS GLAND;

EID: 62849124659     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.1717     Document Type: Article

References (50)

1. Hayday, A.C. & Pennington, D.J. Key factors in the organized chaos of early T cell development. Nat. Immunol. 8, 137-144 (2007).
2. Bhandoola, A., von Boehmer, H., Petrie, H.T. & Zuniga-Pflucker, J.C. Commitment and developmental potential of extrathymic and intrathymic T cell precursors: Plenty to choose from. Immunity 26, 678-689 (2007).
3. Laky, K., Fleischacker, C. & Fowlkes, B.J. TCR and Notch signaling in CD4 and CD8 T-cell development. Immunol. Rev. 209, 274-283 (2006).
4. Roark, C.L., Simonian, P.L., Fontenot, A.P., Born, W.K. & O'Brien, R.L. γδ T cells: An important source of IL-17. Curr. Opin. Immunol. 20, 353-357 (2008).
5. Vermijlen, D. et al. Distinct cytokine-driven responses of activated blood γδ T cells: Insights into unconventional T cell pleiotropy. J. Immunol. 178, 4304-4314 (2007).
6. + T helper cells. Cell 126, 1121-1133 (2006).
7. T cells. J. Exp. Med. 205 1381-1393 (2008).
8. Lockhart, E., Green, A.M. & Flynn, J.L. IL-17 production is dominated by γδ T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177, 4662-4669 (2006).
9. + γδ T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178, 4466-4472 (2007).
10. Umemura, M. et al. IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178, 3786-3796 (2007).
11. Zhang, F., Meng, G. & Strober, W. Interactions among the transcription factors Runx1, RORγt and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nat. Immunol. 9, 1297-1306 (2008).
12. Yang, Y., Xu, J., Niu, Y., Bromberg, J.S. & Ding, Y. T-bet and Eomesodermin play critical roles in directing T cell differentiation to Th1 versus Th17. J. Immunol. 181, 8700-8710 (2008).
13. Amsen, D. et al. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117, 515-526 (2004).
14. Jensen, K.D. et al. Thymic selection determines γδ T cell effector fate: Antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon γ. Immunity 29, 90-100 (2008).
15. Born, W.K., Reardon, C.L. & O'Brien, R.L. The function of γδ T cells in innate immunity. Curr. Opin. Immunol. 18, 31-38 (2006).
16. + cells. Nat. Immunol. 4, 991-998 (2003).
17. Silva-Santos, B., Pennington, D.J. & Hayday, A.C. Lymphotoxin-mediated regulation of γδ cell-differentiation by αβ T cell progenitors. Science 307, 925-928 (2005).
18. Pennington, D.J. et al. Early events in the thymus affect the balance of effector and regulatory T cells. Nature 444, 1073-1077 (2006).
19. Borst, J., Hendriks, J. & Xiao, Y. CD27 and CD70 in T cell and B cell activation. Curr. Opin. Immunol. 17, 275-281 (2005).
20. Gao, Y. et al. γδ T cells provide an early source of interferon γ in tumor immunity. J. Exp. Med. 198, 433-442 (2003).
21. Roark, C.L. et al. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing γδ T cells. J. Immunol. 179, 5576-5583 (2007).
22. Romani, L. et al. Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451 211-215 (2008).
23. + γδ T cells as fetal thymus-derived naturally occurring IL-17 producers. J. Immunol. 181, 5940-5947 (2008).
24. + regulatory T cells in inflamed synoviai. J. Exp. Med. 201, 1793-1803 (2005).
25. Vossen, M.T. et al. CD27 defines phenotypically and functionally different human NK cell subsets. J. Immunol. 180, 3739-3745 (2008).
26. Kisielow, J., Kopf, M. & Karjalainen, K. SCART scavenger receptors identify a novel subset of adult γδ T cells. J. Immunol. 181 1710-1716 (2008).
27. Ho, M., Webster, H.K., Tongtawe, P., Pattanapanyasat,, K. & Weidanz, W.P. Increased γδ T cells in acute Plasmodium falciparum malaria. Immunol. Lett. 25, 139-141 (1990).
28. Yanez, D.M., Batchelder, J., van der Heyde, H.C., Manning, D.D. & Weidanz, W.P. γδ T-cell function in pathogenesis of cerebral malaria in mice infected with Plasmodium berghei AN KA. Infect. Immun. 67, 446-448 (1999).
29. Ramsburg, E., Tigelaar, R., Craft, J. & Hayday, A. Age-dependent requirement for γδ T cells in the primary but not secondary protective immune response against an intestinal parasite. J. Exp. Med. 198, 1403-1414 (2003).
30. D'Ombrain, M.C., Hansen, D.S., Simpson, K.M. & Schofield, L. γδ T cells expressing NK receptors predominate over NK cells and conventional T cells in the innate IFN-γ response to Plasmodium falciparum malaria. Eur. J. Immunol. 37, 1864-1873 (2007).
31. Pamplona, A. et al. Heme oxygenase-1 and carbon monoxide suppress the pathogenesis of experimental cerebral malaria. Nat. Med. 13 703-710 (2007).
32. H17 and regulatory T cells. Nature 441, 235-238 (2006).
33. Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M. & Stockinger, B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 179-189 (2006).
34. H17 lineage. Nature 441, 231-234 (2006).
35. + cells. Science 305, 248-251 (2004).
36. Ciofani, M., Knowles, G.C., Wiest, D.L., von Boehmer, H. & Zuniga-Pflucker, J.C. Stage-specific and differential notch dependency at the αβ and γδ T lineage bifurcation. Immunity 25, 105-116 (2006).
37. Taghon, T., Yui, M.A., Pant, R., Diamond, R.A. & Rothenberg, E.V. Developmental and molecular characterization of emerging β- and γδ-selected pre-T cells in the adult mouse thymus. Immunity 24, 53-64 (2006).
38. Hendriks, J. et al. CD27 is required for generation and long-term maintenance of T cell immunity. Nat. Immunol. 1, 433-440 (2000).
39. + T cell without effector differentiation. Proc. Natl. Acad. Sci. USA 103, 19454-19459 (2006).
40. neg iNKT cell population involved in airway neutrophilia. J. Exp. Med. 204, 995-1001 (2007).
41. Michel, M.L. et al. Critical role of ROR-γt in a new thymic pathway leading to IL-17-producing invariant NKT cell differentiation. Proc. Natl. Acad. Sci. USA 105, 19845-19850 (2008).
42. Lee, Y.K. et al. Late developmental plasticity in the T helper 17 lineage. Immunity 30, 92-107 (2009).
43. Weaver, C.T., Harrington, L.E., Mangan, P.R., Gavrieli, M. & Murphy, K.M. Th17: An effector CD4 T cell lineage with regulatory T cell ties. Immunity 24, 677-688 (2006).
44. Bendelac, A., Savage, P.B. & Teyton, L. The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (2007).
45. Zuany-Amorim, C. et al. Requirement for γδ T cells in allergic airway inflammation. Science 280, 1265-1267 (1998).
46. Ivanov, I.I. et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4, 337-349 (2008).
47. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
48. Hendriks, J., Xiao, Y. & Borst, J. CD27 promotes survival of activated T cells and complements CD28 in generation and establishment of the effector T cell pool. J. Exp. Med. 198, 1369-1380 (2003).
49. Nolte, M.A. et al. Immune activation modulates hematopoiesis through interactions between CD27 and CD70. Nat. Immunol. 6, 412-418 (2005).
50. Tesselaar, K. et al. Expression of the murine CD27 ligand CD70 in vitro and in vivo. J. Immunol. 170, 33-40 (2003).