Follicular regulatory T cells can be specific for the immunizing antigen and derive from naive T cells

Nature Communications

Volumn 7, Issue , 2016, Pages

  Aloulou, Meryem ^a,b,c   Carr, Edward J ^d   Gador, Mylène ^a,b,c   Bignon, Alexandre ^d   Liblau, Roland S ^a,b,c   Fazilleau, Nicolas ^a,b,c   Linterman, Michelle A ^d  

^a INSERM   (France)

^b CNRS   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d BABRAHAM INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CD4 ANTIGEN; DIPHTHERIA TOXIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR FOXP3; CD274 PROTEIN, MOUSE; PROGRAMMED DEATH 1 LIGAND 1;

ANTIGEN; CELLS AND CELL COMPONENTS; GENE EXPRESSION; IMMUNE SYSTEM; IMMUNIZATION; INFECTIVITY; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; CELL SPECIFICITY; CONTROLLED STUDY; HUMORAL IMMUNITY; IMMUNITY; IMMUNIZATION; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; REGULATORY T LYMPHOCYTE; T FOLLICULAR REGULATORY CELL; ANIMAL; C57BL MOUSE; FEMALE; IMMUNOLOGY; METABOLISM;

ANIMALS; ANTIGENS, CD274; FEMALE; MICE, INBRED C57BL; T-LYMPHOCYTES, REGULATORY;

EID: 84961373922     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10579     Document Type: Article

References (33)

1. Fazilleau, N., Mark, L., McHeyzer-Williams, L. J. & McHeyzer-Williams, M. G. Follicular helper T cells: lineage and location. Immunity 30, 324-335 (2009).
2. Chan, T. D. & Brink, R. Affinity-based selection and the germinal center response. Immunol. Rev. 247, 11-23 (2012).
3. Vinuesa, C. G., Sanz, I. & Cook, M. C. Dysregulation of germinal centres in autoimmune disease. Nat. Rev. Immunol. 9, 845-857 (2009).
4. Vanderleyden, I., Linterman, M. A. & Smith, K. G. Regulatory T cells and control of the germinal centre response. Arthritis Res. Ther. 16, 471 (2014).
5. Lim, H. W., Hillsamer, P. & Kim, C. H. Regulatory T cells can migrate to follicles upon T cell activation and suppress GC-Th cells and GC-Th cell-driven B cell responses. J. Clin. Invest. 114, 1640-1649 (2004).
6. Linterman, M. A. et al. Foxp3(+) follicular regulatory T cells control the germinal center response. Nat. Med. 17, 975-982 (2011).
7. Chung, Y. et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 17, 983-988 (2011).
8. Wollenberg, I. et al. Regulation of the germinal center reaction by foxp3 + follicular regulatory T cells. J. Immunol. 187, 4553-4560 (2011).
9. Miyazaki, M. et al. Id2 and Id3 maintain the regulatory T cell pool to suppress inflammatory disease. Nat. Immunol. 15, 767-776 (2014).
10. Vaeth, M. et al. Follicular regulatory T cells control humoral autoimmunity via NFAT2-regulated CXCR5 expression. J. Exp. Med. 211, 545-561 (2014).
11. Liu, X. et al. Transcription factor achaete-scute homologue 2 initiates follicular T-helper-cell development. Nature 507, 513-518 (2014).
12. Sage, P. T., Paterson, A. M., Lovitch, S. B. & Sharpe, A. H. The coinhibitory receptor ctla-4 controls B cell responses by modulating T follicular helper, T follicular regulatory, and T regulatory cells. Immunity 41, 1026-1039 (2014).
13. Wing, J. B., Ise, W., Kurosaki, T. & Sakaguchi, S. Regulatory T cells control antigen-specific expansion of Tfh cell number and humoral immune responses via the coreceptor CTLA-4. Immunity 41, 1013-1025 (2014).
14. Ding, Y. et al. Interleukin-21 promotes germinal center reaction by skewing the follicular regulatory T cell to follicular helper T cell balance in autoimmune BXD2 mice. Arthritis Rheumatol. 66, 2601-2612 (2014).
15. Fazilleau, N. et al. Lymphoid reservoirs of antigen-specific memory T helper cells. Nat. Immunol. 8, 753-761 (2007).
16. Fazilleau, N., McHeyzer-Williams, L. J., Rosen, H. & McHeyzer-Williams, M. G. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat. Immunol. 10, 375-384 (2009).
17. Jordan, M. S. et al. Thymic selection of CD4 + CD25 + regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2, 301-306 (2001).
18. Walker, L. S., Chodos, A., Eggena, M., Dooms, H. & Abbas, A. K. Antigen-dependent proliferation of CD4 + CD25 + regulatory T cells in vivo. J. Exp. Med. 198, 249-258 (2003).
19. Hsieh, C. S. et al. Recognition of the peripheral self by naturally arising CD25 + CD4 + T cell receptors. Immunity 21, 267-277 (2004).
20. Krishnamoorthy, G. et al. Myelin-specific T cells also recognize neuronal autoantigen in a transgenic mouse model of multiple sclerosis. Nat. Med. 15, 626-632 (2009).
21. Moon, J. J. et al. Naive CD4(+) T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 27, 203-213 (2007).
22. Nelson, R. W. et al. T cell receptor cross-reactivity between similar foreign and self peptides influences naive cell population size and autoimmunity. Immunity 42, 95-107 (2015).
23. Korn, T. et al. IL-6 controls Th17 immunity in vivo by inhibiting the conversion of conventional T cells into Foxp3 + regulatory T cells. Proc. Natl Acad. Sci. USA 105, 18460-18465 (2008).
24. Weiss, J. M. et al. Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3 + T reg cells. J. Exp. Med. 209, 1723-1742 (2012).
25. Yadav, M. et al. Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 209, 1713-1722 (2012).
26. Chakarov, S. & Fazilleau, N. Monocyte-derived dendritic cells promote T follicular helper cell differentiation. EMBO Mol. Med. 6, 590-603 (2014).
27. Lahl, K. & Sparwasser, T. In vivo depletion of FoxP3 + Tregs using the DEREG mouse model. Methods Mol. Biol. 707, 157-172 (2011).
28. Moriyama, S. et al. Sphingosine-1-phosphate receptor 2 is critical for follicular helper T cell retention in germinal centers. J. Exp. Med. 211, 1297-1305 (2014).
29. Francisco, L. M. et al. PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J. Exp. Med. 206, 3015-3029 (2009).
30. Sage, P. T., Francisco, L. M., Carman, C. V. & Sharpe, A. H. The receptor PD-1 controls follicular regulatory T cells in the lymph nodes and blood. Nat. Immunol. 14, 152-161 (2012).
31. Khan, A. R. et al. PD-L1(hi) B cells are critical regulators of humoral immunity. Nat. Commun. 6, 5997 (2015).
32. Rookhuizen, D. C. & DeFranco, A. L. Toll-like receptor 9 signaling acts on multiple elements of the germinal center to enhance antibody responses. Proc. Natl Acad. Sci. USA 111, 3224-3233 (2014).
33. Forster, R. et al. A putative chemokine receptor, BLR1, directs B cell migration to defined lymphoid organs and specific anatomic compartments of the spleen. Cell 87, 1037-1047 (1996).