A rare subset of skin-tropic regulatory T cells expressing Il10/Gzmb inhibits the cutaneous immune response

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ikebuchi, Ryoyo ^a,b,c   Teraguchi, Shunsuke ^d   Vandenbon, Alexis ^d   Honda, Tetsuya ^a   Shand, Francis H W ^e   Nakanishi, Yasutaka ^a   Watanabe, Takeshi ^f   Tomura, Michio ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b OSAKA OHTANI UNIVERSITY   (Japan)

^c JAPAN SOCIETY FOR THE PROMOTION OF SCIENCE   (Japan)

^d OSAKA UNIVERSITY   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f Kitano Hospital   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CCR5 PROTEIN, HUMAN; CHEMOKINE RECEPTOR CCR5; GRANZYME; GZMB PROTEIN, HUMAN; IL10 PROTEIN, HUMAN; INTERLEUKIN 10; LEUKOSIALIN; UN1 SIALOGLYCOPROTEIN, HUMAN;

ANIMAL; CONTACT DERMATITIS; DISEASE MODEL; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; REGULATORY T LYMPHOCYTE; SINGLE CELL ANALYSIS; SKIN;

ANIMALS; DERMATITIS, CONTACT; DISEASE MODELS, ANIMAL; GRANZYMES; HUMANS; INTERLEUKIN-10; LEUKOSIALIN; MICE; RECEPTORS, CCR5; SINGLE-CELL ANALYSIS; SKIN; T-LYMPHOCYTES, REGULATORY;

EID: 84992028354     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep35002     Document Type: Article

References (42)

1. Tomura, M. et al. Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice. J. Clin. Invest. 120, 883-893 (2010).
2. Rosenblum, M. D. et al. Response to self antigen imprints regulatory memory in tissues. Nature 480, 538-42 (2011).
3. Chattopadhyay, P. K., Gierahn, T. M., Roederer, M., Love, J. C. Single-cell technologies for monitoring immune systems. Nat. Immunol. 15, 128-135 (2014).
4. Meacham, C. E., Morrison, S. J. Tumour heterogeneity and cancer cell plasticity. Nature 501, 328-337 (2013).
5. Guo, G. et al. Mapping cellular hierarchy by single-cell analysis of the cell surface repertoire. Cell Stem Cell 13, 492-505 (2013).
6. Ramos, C. A. et al. Evidence for diversity in transcriptional profiles of single hematopoietic stem cells. PLoS Genet. 2, e159 (2006).
7. Arsenio, J. et al. Early specification of CD8+ T lymphocyte fates during adaptive immunity revealed by single-cell gene-expression analyses. Nat. Immunol. 15, 365-372 (2014).
8. Flatz, L., Roychoudhuri, R. Single-cell gene-expression profiling reveals qualitatively distinct CD8 T cells elicited by different genebased vaccines. Proc. Natl. Acad. Sci. USA 108, 5724-5729 (2011).
9. Kondo, S., Mckenzie, R. C., Sauder, D. N. Interleukin-10 inhibits the elicitation phase of allergic contact hypersensitivity. J. Invest. Dermatol. 103, 811-814 (1994).
10. Tomura, M. et al. Tracking and quantification of dendritic cell migration and antigen trafficking between the skin and lymph nodes. Sci. Rep. 4, 1-11 (2014).
11. Tsutsui, H., Karasawa, S., Shimizu, H., Nukina, N., Miyawaki, A. Semi-rational engineering of a coral fluorescent protein into an efficient highlighter. EMBO Rep. 6, 233-238 (2005).
12. Komatsu, N. et al. Heterogeneity of natural Foxp3+ T cells: a committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity. Proc. Natl. Acad. Sci. USA 106, 1903-1908 (2009).
13. Shevach, E. M. Mechanisms of Foxp3+ T regulatory cell-mediated suppression. Immunity 30, 636-645 (2009).
14. Cao, X. et al. Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27, 635-646 (2007).
15. Zhao, D.-M., Thornton, A. M., DiPaolo, R. J., Shevach, E. M. Activated CD4+ CD25+ T cells selectively kill B lymphocytes. Blood 107, 3925-3932 (2006).
16. Boissonnas, A. et al. Foxp3+ T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes. Immunity 32, 266-278 (2010).
17. Tran, D. Q. TGF-: the sword. the wand., the shield of FOXP3+ regulatory T cells. J. Mol. Cell Biol. 4, 29-37 (2012).
18. Maurice, D., Hooper, J., Lang, G., Weston, K. c-Myb regulates lineage choice in developing thymocytes via its target gene Gata3. EMBO J. 26, 3629-3640 (2007).
19. Huber, M., Lohoff, M. IRF4 at the crossroads of effector T-cell fate decision. Eur. J. Immunol. 44, 1886-1895 (2014).
20. Dong, S. et al. Multiparameter single-cell profiling of human CD4+ FOXP3+ regulatory T-cell populations in homeostatic conditions and during graft-versus-host disease. Blood 122, 1802-1812 (2013).
21. Koch, M. A. et al. T-bet+ Treg cells undergo abortive Th1 cell differentiation due to impaired expression of IL-12 receptor 2. Immunity 37, 501-510 (2012).
22. Nakayama, S., Takahashi, H., Kanno, Y., O'Shea, J. J. Helper T cell diversity and plasticity. Curr. Opin. Immunol. 24, 297-302 (2012).
23. Fulton, R. B., Meyerholz, D. K., Varga, S. M. Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J. Immunol. 185, 2382-2392 (2010).
24. Islam, S. A., Luster, A. D. T cell homing to epithelial barriers in allergic disease. Nat. Med. 18, 705-15 (2012).
25. Iellem, A. et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+ ) CD25(+ ) regulatory T cells. J. Exp. Med. 194, 847-53 (2001).
26. Tomura, M. et al. Contrasting quiescent G0 phase with mitotic cell cycling in the mouse immune system. PLoS One 8, e73801 (2013).
27. Loebbermann, J. et al. Regulatory T cells expressing granzyme B play a critical role in controlling lung inflammation during acute viral infection. Mucosal Immunol. 5, 161-72 (2012).
28. Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L., Powrie, F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190, 995-1004 (1999).
29. Glimcher, L. H., Townsend, M. J., Sullivan, B. M., Lord, G. M. Recent developments in the transcriptional regulation of cytolytic effector cells. Nat. Rev. Immunol. 4, 900-911 (2004).
30. Lazarevic, V., Glimcher, L. H. T-bet in disease. Nat. Immunol. 12, 597-606 (2011).
31. Koch, M. A. et al. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10, 595-602 (2009).
32. Tubo, N. J. et al. Single naive CD4+ T cells from a diverse repertoire produce different effector cell types during infection. Cell 153, 785-796 (2013).
33. Prakash, M. D. et al. Granzyme B promotes cytotoxic lymphocyte transmigration via basement membrane remodeling. Immunity 41, 960-972 (2014).
34. Campbell, D. J., Koch, M. A. Phenotypical and functional specialization of FOXP3+ regulatory T cells. Nat. Rev. Immunol. 11, 119-130 (2011).
35. Goebeler, M. et al. Differential and sequential expression of multiple chemokines during elicitation of allergic contact hypersensitivity. Am. J. Pathol. 158, 431-440 (2001).
36. Mitsui, G. et al. Effect of a topical steroid on gene expressions for chemokines in mice with contact hypersensitivity. Int. Immunopharmacol. 4, 57-69 (2004).
37. Yurchenko, E. et al. CCR5-dependent homing of naturally occurring CD4+ regulatory T cells to sites of Leishmania major infection favors pathogen persistence. J. Exp. Med. 203, 2451-2460 (2006).
38. Hall, A. O. H. et al. The cytokines interleukin 27 and interferon-promote distinct Treg cell populations required to limit infectioninduced pathology. Immunity 37, 511-523 (2012).
39. Matsumoto, M. et al. CD43 collaborates with P-selectin glycoprotein ligand-1 to mediate E-selectin-dependent T cell migration into inflamed skin. J. Immunol. 178, 2499-2506 (2007).
40. Islam, S. A. et al. Mouse CCL8, a CCR8 agonist, promotes atopic dermatitis by recruiting IL-5+ TH2 cells. Nat. Immunol. 12, 167-177 (2011).
41. Tomura, M., Itoh, K., Kanagawa, O., Alerts, E. Naive CD4+ T lymphocytes circulate through lymphoid organs to interact with endogenous antigens and upregulate their function. J. Immunol. 184, 4646-4653 (2010).
42. Tomura, M. et al. Monitoring cellular movement in vivo with photoconvertible fluorescence protein 'Kaede' transgenic mice. Proc. Natl. Acad. Sci. USA 105, 10871-10876 (2008).