Identification and characterization of latency-associated peptide-expressing γδT cells

Nature Communications

Volumn 6, Issue , 2015, Pages

  Rezende, Rafael M ^a   Da Cunha, Andre P ^a   Kuhn, Chantal ^a   Rubino, Stephen ^a   M'Hamdi, Hanane ^a,b   Gabriely, Galina ^a   Vandeventer, Tyler ^a   Liu, Shirong ^a   Cialic, Ron ^a   Pinheiro Rosa, Natalia ^c   Oliveira, Rafael P ^c   Gaublomme, Jellert T ^d,e   Obholzer, Nikolaus ^a   Kozubek, James ^a   Pochet, Nathalie ^a,f   Faria, Ana M C ^c   Weiner, Howard L ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^d HARVARD UNIVERSITY   (United States)

^e HARVARD UNIVERSITY   (United States)

^f BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; CD27 ANTIGEN; CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR9; GAMMA INTERFERON; LATENCY ASSOCIATED PEPTIDE; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; ATF3 PROTEIN, MOUSE; CYTOKINE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR;

BLOOD; CELLS AND CELL COMPONENTS; DISEASE; GENE EXPRESSION; IMMUNE RESPONSE; PEPTIDE; PHENOTYPE; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DOWN REGULATION; GAMMA DELTA T LYMPHOCYTE; HOST PATHOGEN INTERACTION; IMMUNOREGULATION; INTESTINE FUNCTION; INTESTINE FUNCTION DISORDER; LAMINA PROPRIA; MOUSE; NONHUMAN; PEYER PATCH; PHENOTYPE; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SMALL INTESTINE; THYMUS; UPREGULATION; ADULT; ANIMAL; COLITIS; CONGENIC STRAIN; DISEASE MODEL; FLOW CYTOMETRY; GENETICS; HUMAN; IMMUNOLOGY; IN VITRO STUDY; INTESTINE MUCOSA; MONONUCLEAR CELL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE SUBPOPULATION;

ACTIVATING TRANSCRIPTION FACTOR 3; ADULT; ANIMALS; ANIMALS, CONGENIC; ANTIGEN-PRESENTING CELLS; COLITIS; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IN VITRO TECHNIQUES; INTERFERON-GAMMA; INTESTINAL MUCOSA; LEUKOCYTES, MONONUCLEAR; MICE; PEYER'S PATCHES; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84949490902     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9726     Document Type: Article

References (56)

1. Girardi, M. Immunosurveillance and immunoregulation by gammadelta T cells. J. Invest. Dermatol. 126, 25-31 (2006
2. Vantourout, P. & Hayday, A. Six-of-the-best: unique contributions of gammadelta T cells to immunology. Nat. Rev. Immunol. 13, 88-100 (2013
3. Wesch, D., Peters, C., Oberg, H. H., Pietschmann, K. & Kabelitz, D. Modulation of gammadelta T cell responses by TLR ligands. Cell. Mol. Life Sci. 68, 2357-2370 (2011
4. Ponomarev, E. D. & Dittel, B. N. Gamma delta T cells regulate the extent and duration of inflammation in the central nervous system by a Fas liganddependent mechanism. J. Immunol. 174, 4678-4687 (2005
5. Martin, B., Hirota, K., Cua, D. J., Stockinger, B. & Veldhoen, M. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31, 321-330 (2009
6. Haas, J. D. et al. CCR6 and NK1.1 distinguish between IL-17A and IFNgamma-producing gammadelta effector T cells. Eur. J. Immunol. 39, 3488-3497 (2009
7. Ribot, J. C. et al. CD27 is a thymic determinant of the balance between interferon-gamma- and interleukin 17-producing gammadelta T cell subsets. Nat. Immunol. 10, 427-436 (2009
8. Petermann, F. et al. gammadelta T cells enhance autoimmunity by restraining regulatory T cell responses via an interleukin-23-dependent mechanism. Immunity 33, 351-363 (2010
9. Roark, C. L. et al. Exacerbation of collagen-induced arthritis by oligoclonal, IL-17-producing gamma delta T cells. J. Immunol. 179, 5576-5583 (2007
10. Do, J. S., Visperas, A., Dong, C., Baldwin, 3rd W. M. & Min, B. Cutting edge: Generation of colitogenic Th17 CD4 T cells is enhanced by IL-17 gammadelta T cells. J. Immunol. 186, 4546-4550 (2011
11. Park, K. et al. TCR-mediated ThPOK induction promotes development of mature (CD24-) gammadelta thymocytes. EMBO J. 29, 2329-2341 (2010
12. Inagaki-Ohara, K. et al. Mucosal T cells bearing TCRgammadelta play a protective role in intestinal inflammation. J. Immunol. 173, 1390-1398 (2004
13. Chen, Y., Chou, K., Fuchs, E., Havran, W. L. & Boismenu, R. Protection of the intestinal mucosa by intraepithelial gamma delta T cells. Proc. Natl Acad. Sci. USA 99, 14338-14343 (2002
14. Mielke, L. A. et al. Retinoic acid expression associates with enhanced IL-22 production by gammadelta T cells and innate lymphoid cells and attenuation of intestinal inflammation. J. Exp. Med. 210, 1117-1124 (2013
15. Weiner, H. L., da Cunha, A. P., Quintana, F. & Wu, H. Oral tolerance. Immunol. Rev. 241, 241-259 (2011
16. Mengel, J. et al. Anti-gamma delta T cell antibody blocks the induction and maintenance of oral tolerance to ovalbumin in mice. Immunol. Lett. 48, 97-102 (1995
17. Fujihashi, K. et al. gammadelta T cells regulate mucosally induced tolerance in a dose-dependent fashion. Int. Immunol. 11, 1907-1916 (1999
18. Kang, N. et al. Identification and characterization of Foxp3(+) gammadelta T cells in mouse and human. Immunol. Lett. 125, 105-113 (2009
19. Casetti, R. et al. Cutting edge: TGF-beta1 and IL-15 Induce FOXP3 gammadelta regulatory T cells in the presence of antigen stimulation. J. Immunol. 183, 3574-3577 (2009
20. Rhodes, K. A., Andrew, E. M., Newton, D. J., Tramonti, D. & Carding, S. R. A subset of IL-10-producing gammadelta T cells protect the liver from Listeria-elicited, CD8(+) T cell-mediated injury. Eur. J. Immunol. 38, 2274-2283 (2008
21. Collins, R. A. et al. Gammadelta T cells present antigen to CD4 alphabeta T cells. J. Leukoc. Biol. 63, 707-714 (1998
22. Cheng, L. et al. Mouse gammadelta T cells are capable of expressing MHC class II molecules, and of functioning as antigen-presenting cells. J. Neuroimmunol. 203, 3-11 (2008
23. Brandes, M., Willimann, K. & Moser, B. Professional antigen-presentation function by human gammadelta T Cells. Science 309, 264-268 (2005
24. Hu, C. et al. Antigen-presenting effects of effector memory Vg9Vd2 T cells in rheumatoid arthritis. Cell. Mol. Immunol. 9, 245-254 (2011
25. Ochi, H. et al. Oral CD3-specific antibody suppresses autoimmune encephalomyelitis by inducing CD4+CD25-LAP T cells. Nat. Med. 12, 627-635 (2006
26. Chen, M. L., Yan, B. S., Kozoriz, D. & Weiner, H. L. Novel CD8 Treg suppress EAE by TGF-beta- and IFN-gamma-dependent mechanisms. Eur. J. Immunol. 39, 3423-3435 (2009
27. Tran, D. Q. et al. GARP (LRRC32) is essential for the surface expression of latent TGF-beta on platelets and activated FOXP3 regulatory T cells. Proc. Natl Acad. Sci. USA 106, 13445-13450 (2009
28. Heilig, J. S. & Tonegawa, S. Diversity of murine gamma genes and expression in fetal and adult T lymphocytes. Nature 322, 836-840 (1986
29. Powrie, F. et al. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4 T cells. Immunity 1, 553-562 (1994
30. Dieleman, L. A. et al. Dextran sulfate sodium-induced colitis occurs in severe combined immunodeficient mice. Gastroenterology 107, 1643-1652 (1994
31. Sonnenberg, G. F., Fouser, L. A. & Artis, D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12, 383-390 (2011
32. Coombes, J. L. et al. A functionally specialized population of mucosal CD103 DCs induces Foxp3 regulatory T cells via a TGF-beta and retinoic aciddependent mechanism. J. Exp. Med. 204, 1757-1764 (2007
33. Andersson, J. et al. CD4 FoxP3 regulatory T cells confer infectious tolerance in a TGF-beta-dependent manner. J. Exp. Med. 205, 1975-1981 (2008
34. Oida, T. & Weiner, H. L. TGF-beta induces surface LAP expression on murine CD4 T cells independent of Foxp3 induction. PLoS ONE 5, e15523 (2010
35. Whitmore, M. M. et al. Negative regulation of TLR-signaling pathways by activating transcription factor-3. J. Immunol. 179, 3622-3630 (2007
36. Rosenberger, C. M., Clark, A. E., Treuting, P. M., Johnson, C. D. & Aderem, A. ATF3 regulates MCMV infection in mice by modulating IFN-gamma expression in natural killer cells. Proc. Natl Acad. Sci. USA 105, 2544-2549 (2008
37. Iwata, M. et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity 21, 527-538 (2004
38. Kazen, A. R. & Adams, E. J. Evolution of the V, D, and J gene segments used in the primate gammadelta T-cell receptor reveals a dichotomy of conservation and diversity. Proc. Natl Acad. Sci. USA 108, E332-E340 (2011
39. Hayday, A. C. Gammadelta T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196 (2009
40. Hayday, A. C. [gamma][delta] cells: a right time and a right place for a conserved third way of protection. Annu. Rev. Immunol. 18, 975-1026 (2000
41. Otsuka, A., Hanakawa, S., Miyachi, Y. & Kabashima, K. CD39: a new surface marker of mouse regulatory gammadelta T cells. J. Allergy Clin. Immunol. 131, 1448-1451 (2013
42. Huber, S. A., Graveline, D., Newell, M. K., Born, W. K. & O?Brien, R. L. V gamma 1 T cells suppress and V gamma 4 T cells promote susceptibility to coxsackievirus B3-induced myocarditis in mice. J. Immunol. 165, 4174-4181 (2000
43. Jung, C., Hugot, J. P. & Barreau, F. Peyer?s patches: the immune sensors of the intestine. Int. J. Inflam. 2010, 823710 (2010
44. Chassaing, B., Aitken, J. D., Malleshappa, M. & Vijay-Kumar, M. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104, Unit 15.25 (2014
45. Gorfu, G., Rivera-Nieves, J. & Ley, K. Role of beta7 integrins in intestinal lymphocyte homing and retention. Curr. Mol. Med. 9, 836-850 (2009
46. Hai, T., Wolford, C. C. & Chang, A. Y.-S. ATF3, a hub of the cellular adaptiveresponse network, in the pathogenesis of diseases: is modulation of inflammation a unifying component?. Gene Expr. 15, 1-11 (2010
47. Jensen, K. D. et al. Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity 29, 90-100 (2008
48. Turchinovich, G. & Hayday, A. C. Skint-1 identifies a common molecular mechanism for the development of interferon-gamma-secreting versus interleukin-17-secreting gammadelta T cells. Immunity 35, 59-68 (2011
49. Crawford, S. E. et al. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93, 1159-1170 (1998
50. Schultz-Cherry, S., Lawler, J. & Murphy-Ullrich, J. E. The type 1 repeats of thrombospondin 1 activate latent transforming growth factor-beta. J. Biol. Chem. 269, 26783-26788 (1994
51. Schultz-Cherry, S., Ribeiro, S., Gentry, L. & Murphy-Ullrich, J. E. Thrombospondin 1 binds and activates the small and large forms of latent transforming growth factor-beta in a chemically defined system. J. Biol. Chem. 269, 26775-26782 (1994
52. Li, S. S. et al. T lymphocyte expression of thrombospondin-1 and adhesion to extracellular matrix components. Eur. J. Immunol. 32, 1069-1079 (2002
53. Yang, K. et al. Deficiency of thrombospondin-1 reduces Th17 differentiation and attenuates experimental autoimmune encephalomyelitis. J. Autoimmun. 32, 94-103 (2009
54. Trapnell, C. et al. Differential gene and transcript expression analysis of RNAseq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562-578 (2012
55. Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010
56. Roberts, A., Trapnell, C., Donaghey, J., Rinn, J. L. & Pachter, L. Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol. 12, R22 (2011