Fluorochrome-based definition of naturally occurring Foxp3+ regulatory T cells of intra- and extrathymic origin

European Journal of Immunology

Volumn 44, Issue 12, 2014, Pages 3632-3645

  Petzold, Cathleen ^a   Steinbronn, Nadine ^b   Gereke, Marcus ^c,d   Strasser, Ruth H ^b   Sparwasser, Tim ^e   Bruder, Dunja ^c,d   Geffers, Robert ^c   Schallenberg, Sonja ^a   Kretschmer, Karsten ^a,f  

^a CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d OTTO VON GUERICKE UNIVERSITY   (Germany)

^e INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^f GERMAN CENTER FOR DIABETES RESEARCH DZD   (Germany)

Author keywords

Fluorochrome reporter; Foxp3; Regulatory T cells; T cell development

Indexed keywords

CD4 ANTIGEN; FLUOROCHROME; GREEN FLUORESCENT PROTEIN; NEUROPILIN 1; RED FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; PHOTOPROTEIN;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; LYMPHOID TISSUE; MOLECULAR GENETICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; STEADY STATE; ANIMAL; BAGG ALBINO MOUSE; CYTOLOGY; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; NONOBESE DIABETIC MOUSE; THYMUS;

ANIMALS; FORKHEAD TRANSCRIPTION FACTORS; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; MICE, KNOCKOUT; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 84923553839     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201444750     Document Type: Article

References (44)

1. Fontenot, J. D., Dooley, J. L., Farr, A. G. and Rudensky, A. Y., Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 2005. 202: 901-906.
2. Fontenot, J. D., Rasmussen, J. P., Williams, L. M., Dooley, J. L., Farr, A. G. and Rudensky, A. Y., Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005. 22: 329-341.
3. Liston, A., Nutsch, K. M., Farr, A. G., Lund, J. M., Rasmussen, J. P., Koni, P. A. and Rudensky, A. Y., Differentiation of regulatory Foxp3+ T cells in the thymic cortex. Proc. Natl. Acad. Sci. USA 2008. 105: 11903-11908.
4. Schallenberg, S., Petzold, C., Tsai, P-Y., Sparwasser, T. and Kretschmer, K., Vagaries of fluorochrome reporter gene expression in Foxp3+ regulatory T cells. PLoS ONE 2012. 7: e41971.
5. Wan, Y. Y. and Flavell, R. A., Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 2005. 102: 5126-5131.
6. Wirnsberger, G., Mair, F. and Klein, L., Regulatory T cell differentiation of thymocytes does not require a dedicated antigen-presenting cell but is under T cell-intrinsic developmental control. Proc. Natl. Acad. Sci. USA 2009. 106: 10278-10283.
7. Klein, L. and Jovanovic, K., Regulatory T cell lineage commitment in the thymus. Semin.Immunol. 2011. 23: 401-409.
8. Curotto de Lafaille, M. A., Lino, A. C., Kutchukhidze, N. and Lafaille, J. J., CD25-T cells generate CD25+Foxp3+ regulatory T cells by peripheral expansion. J. Immunol. 2004. 173: 7259-7268.
9. Knoechel, B., Lohr, J., Kahn, E., Bluestone, J. A. and Abbas, A. K., Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen. J. Exp. Med. 2005. 202: 1375-1386.
10. Coombes, J. L., Siddiqui, K. R., Arancibia-Carcamo, C. V., Hall, J., Sun, C. M., Belkaid, Y. and Powrie, F., A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 2007. 204: 1757-1764.
11. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M. C. and von Boehmer, H., Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 2005. 6: 1219-1227.
12. Kretschmer, K., Heng, T. S. and von Boehmer, H., De novo production of antigen-specific suppressor cells in vivo. Nat. Protoc. 2006. 1: 653-661.
13. Mucida, D., Kutchukhidze, N., Erazo, A., Russo, M., Lafaille, J. J. and Curotto de Lafaille, M. A., Oral tolerance in the absence of naturally occurring Tregs. J. Clin. Invest. 2005. 115: 1923-1933.
14. Petzold, C., Riewaldt, J., Koenig, T., Schallenberg, S. and Kretschmer, K., Dendritic cell-targeted pancreatic beta-cell antigen leads to conversion of self-reactive CD4+ T cells into regulatory T cells and promotes immunotolerance in NOD mice. Rev. Diabet. Stud. 2010. 7: 47-61.
15. Polansky, J. K., Kretschmer, K., Freyer, J., Floess, S., Garbe, A., Baron, U., Olek, S. et al., DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 2008. 38: 1654-1663.
16. Verginis, P., McLaughlin, K. A., Wucherpfennig, K. W., von Boehmer, H. and Apostolou, I., Induction of antigen-specific regulatory T cells in wildtype mice: visualization and targets of suppression. Proc. Natl. Acad. Sci. USA 2008. 105: 3479-3484.
17. Schallenberg, S., Tsai, P. Y., Riewaldt, J. and Kretschmer, K., Identification of an immediate Foxp3-precursor to Foxp3+ regulatory T cells in peripheral lymphoid organs of nonmanipulated mice. J. Exp. Med. 2010. 207: 1393-1407.
18. Feuerer, M., Hill, J. A., Kretschmer, K., von Boehmer, H., Mathis, D. and Benoist, C., Genomic definition of multiple ex vivo regulatory T cell subphenotypes. Proc. Natl. Acad. Sci. USA 2010. 107: 5919-5924.
19. Haribhai, D., Lin, W., Relland, L. M., Truong, N., Williams, C. B. and Chatila, T. A., Regulatory T cells dynamically control the primary immune response to foreign antigen. J. Immunol. 2007. 178: 2961-2972.
20. Feuerer, M., Shen, Y., Littman, D. R., Benoist, C. and Mathis, D., How punctual ablation of regulatory T cells unleashes an autoimmune lesion within the pancreatic islets. Immunity 2009. 31: 654-664.
21. Lahl, K., Loddenkemper, C., Drouin, C., Freyer, J., Arnason, J., Eberl, G., Hamann, A. et al., Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J. Exp. Med. 2007. 204: 57-63.
22. Zhou, X., Jeker, L. T., Fife, B. T., Zhu, S., Anderson, M. S., McManus, M. T. and Bluestone, J. A., Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 2008. 205: 1983-1991.
23. Srinivas, S., Watanabe, T., Lin, C.-S., William, C., Tanabe, Y., Jessell, T. and Costantini, F., Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 2001. 1: 4.
24. Lio, C. W. and Hsieh, C. S., A two-step process for thymic regulatory T cell development. Immunity 2008. 28: 100-111.
25. Klein, L., Khazaie, K. and von Boehmer, H., In vivo dynamics of antigenspecific regulatory T cells not predicted from behavior in vitro. Proc. Natl. Acad. Sci. USA 2003. 100: 8886-8891.
26. Chen, W., Jin, W., Hardegen, N., Lei, K.-J., Li, L., Marinos, N., McGrady, G. et al., Conversion of Peripheral CD4+CD25-naive T cells to CD4+CD25+ regulatory T cells by TGF-{beta} induction of transcription factor Foxp3. J. Exp. Med. 2003. 198: 1875-1886.
27. Nolting, J., Daniel, C., Reuter, S., Stuelten, C., Li, P., Sucov, H., Kim, B-G. et al., Retinoic acid can enhance conversion of naive into regulatory T cells independently of secreted cytokines. J. Exp. Med. 2009. 206: 2131-2139.
28. Benson, M. J., Pino-Lagos, K., Rosemblatt, M. and Noelle, R. J., All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 2007. 204: 1765-1774.
29. Nishio, J., Feuerer, M., Wong, J., Mathis, D. and Benoist, C., Anti-CD3 therapy permits regulatory T cells to surmount T cell receptor-specified peripheral niche constraints. J. Exp. Med. 2010. 207: 1879-1889.
30. Hill, J. A., Feuerer, M., Tash, K., Haxhinasto, S., Perez, J., Melamed, R., Mathis, D. et al., Foxp3 transcription-factor-dependent and-independent regulation of the regulatory T cell transcriptional signature. Immunity 2007. 27: 786-800.
31. Yadav, M., Louvet, C., Davini, D., Gardner, J. M., Martinez-Llordella, M., Bailey-Bucktrout, S., Anthony, B. A. et al., Neuropilin-1 distinguishes natural and inducible regulatory T cells among regulatory T cell subsets in vivo. J. Exp. Med. 2012. 209: 1713-1722.
32. Weiss, J. M., Bilate, A. M., Gobert, M., Ding, Y., Curotto de Lafaille, M. A., Parkhurst, C. N., Xiong, H. et al., Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosagenerated induced Foxp3+ T reg cells. J. Exp. Med. 2012. 209: 1723-1742.
33. Sugimoto, N., Oida, T., Hirota, K., Nakamura, K., Nomura, T., Uchiyama, T. and Sakaguchi, S., Foxp3-dependent and-independentmolecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis. Int. Immunol. 2006. 18: 1197-1209.
34. Thornton, A. M., Korty, P. E., Tran, D. Q., Wohlfert, E. A., Murray, P. E., Belkaid, Y. and Shevach, E. M., Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells. J. Immunol. 2010. 184: 3433-3441.
35. Gottschalk, R. A., Corse, E. and Allison, J. P., Expression of Helios in peripherally induced Foxp3+ regulatory T cells. J. Immunol. 2012. 188: 976-980.
36. Verhagen, J. and Wraith, D. C., Comment on "expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells". J. Immunol. 2010. 185: 7129.
37. Petzold, C., Riewaldt, J., Watts, D., Sparwasser, T., Schallenberg, S. and Kretschmer, K., Foxp3+ regulatory T cells in mouse models of type 1 diabetes. J. Diabetes Res. 2013. 2013: 10:940710.
38. Curotto de Lafaille, M. A. and Lafaille, J. J., Natural and adaptive Foxp3+ regulatory T cells:more of the same or a division of labor? Immunity 2009. 30: 626-635.
39. Cebula, A., Seweryn, M., Rempala, G. A., Pabla, S. S., McIndoe, R. A., Denning, T. L., Bry, L. et al., Thymus-derived regulatory T cells contribute to tolerance to commensal microbiota. Nature 2013. 497: 258-262.
40. Zheng, Y., Josefowicz, S., Chaudhry, A., Peng, X. P., Forbush, K. and Rudensky, A. Y., Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 2010. 463: 808-812.
41. Josefowicz, S. Z., Niec, R. E., Kim, H. Y., Treuting, P., Chinen, T., Zheng, Y., Umetsu, D. T. et al., Extrathymically generated regulatory T cells control mucosal TH2 inflammation. Nature 2012. 482: 395-399.
42. Bettini, M. L., Pan, F., Bettini, M., Finkelstein, D., Rehg, J. E., Floess, S., Bell, B. D. et al., Loss of epigenetic modification driven by the Foxp3 transcription factor leads to regulatory T cell insufficiency. Immunity 2012. 36: 717-730.
43. Darce, J., Rudra, D., Li, L., Nishio, J., Cipolletta, D., Rudensky, A. Y., Mathis, D. et al., An N-terminal mutation of the Foxp3 transcription factor alleviates arthritis but exacerbates diabetes. Immunity 2012. 36: 731-741.
44. Guy-Grand, D., Griscelli, C. and Vassalli, P., The mouse gut T lymphocyte, a novel type of T cell. Nature, origin, and traffic in mice in normal and graft-versus-host conditions. J. Exp. Med. 1978. 148: 1661-1677.