c-Rel employs multiple mechanisms to promote the thymic development and peripheral function of regulatory T cells in mice.


Journal

European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201

Informations de publication

Date de publication:
08 2021
Historique:
revised: 12 03 2021
received: 23 07 2020
accepted: 05 05 2021
pubmed: 8 5 2021
medline: 8 10 2021
entrez: 7 5 2021
Statut: ppublish

Résumé

The NF-κB transcription factor c-Rel is a critical regulator of Treg ontogeny, controlling multiple points of the stepwise developmental pathway. Here, we found that the thymic Treg defect in c-Rel-deficient (cRel

Identifiants

pubmed: 33960413
doi: 10.1002/eji.202048900
doi:

Substances chimiques

Proto-Oncogene Proteins c-rel 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2006-2026

Subventions

Organisme : NCI NIH HHS
ID : R01 CA157660
Pays : United States

Informations de copyright

© 2021 Wiley-VCH GmbH.

Références

Brunkow, M. E., Jeffery, E. W., Hjerrild, K. A., Paeper, B., Clark, L. B., Yasayko, S.-A., Wilkinson, J. E. et al., Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 2001. 27: 68-73.
Fontenot, J. D., Gavin, M. A. and Rudensky, A. Y., Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 2003. 4: 330-336.
Sakaguchi, S., Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat. Immunol. 2005. 6: 345-352.
Coutinho, A., Caramalho, I., Seixas, E. and Demengeot, J., Thymic commitment of regulatory T Cells is a pathway of TCR-dependent selection that isolates repertoires undergoing positive or negative selection. In Compans, R. W., Cooper, M. D., Honjo, T., Koprowski, H., Melchers, F., Oldstone, M. B. A., Olsnes, S. et al. (Eds.). CD4+CD25+ Regulatory T Cells: Origin, Function and Therapeutic Potential. Current Topics in Microbiology and Immunology. Springer, Berlin, Heidelberg 2005, pp. 43-71.
Carter, J. D., Calabrese, G. M., Naganuma, M. and Lorenz, U., Deficiency of the Src homology region 2 domain-containing phosphatase 1 (SHP-1) causes enrichment of CD4+CD25+ regulatory T cells. J. Immunol. 2005. 174: 6627-6638.
Lee, H.-M., Bautista, J. L., Scott-Browne, J., Mohan, J. F. and Hsieh, C.-S., A broad range of self-reactivity drives thymic regulatory T cell selection to limit responses to self. Immunity 2012. 37: 475-486.
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-β induction of transcription factor Foxp3. J. Exp. Med. 2003. 198: 1875-1886.
Fu, S., Zhang, N., Yopp, A. C., Chen, D., Mao, M., Chen, D., Zhang, H. et al., TGF-β induces Foxp3+ T-regulatory cells from CD4+ CD25- precursors. Am. J. Transplant. 2004. 4: 1614-1627.
Ito, T., Hanabuchi, S., Wang, Y.-H., Park, W. R., Arima, K., Bover, L., Li, Q. et al., Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 2008. 28: 870-880.
Cretney, E., Xin, A., Shi, W., Minnich, M., Masson, F., Miasari, M., Belz, G. T. et al., The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat. Immunol. 2011. 12: 304-311.
Liston, A. and Gray, D. H. D., Homeostatic control of regulatory T cell diversity. Nat. Rev. Immunol. 2014. 14: 154-165.
Cretney, E., Kallies, A. and Nutt, S. L., Differentiation and function of Foxp3+ effector regulatory T cells. Trends Immunol. 2013. 34: 74-80.
Dias, S., D'Amico, A., Cretney, E., Liao, Y., Tellier, J., Bruggeman, C., Almeida, F. F. et al., Effector regulatory T cell differentiation and immune homeostasis depend on the transcription factor Myb. Immunity 2017. 46: 78-91.
Hori, S., Nomura, T. and Sakaguchi, S., Control of regulatory T cell development by the transcription factor Foxp3. Science 2003. 299: 1057-1061.
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.
Gavin, M. A., Rasmussen, J. P., Fontenot, J. D., Vasta, V., Manganiello, V. C., Beavo, J. A. and Rudensky, A. Y., Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007. 445: 771-775.
Ohkura, N., Kitagawa, Y. and Sakaguchi, S., Development and maintenance of regulatory T cells. Immunity 2013. 38: 414-423.
Samstein, R. M., Arvey, A., Josefowicz, S. Z., Peng, X., Reynolds, A., Sandstrom, R., Neph, S. et al., Foxp3 exploits a pre-existent enhancer landscape for regulatory T cell lineage specification. Cell 2012. 151: 153-166.
Luo, C. T. and Li, M. O., Transcriptional control of regulatory T cell development and function. Trends Immunol. 2013. 34: 531-539.
Schuster, M., Plaza-Sirvent, C., Matthies, A.-M., Heise, U., Jeron, A., Bruder, D., Visekruna, A. et al., c-REL and IκBNS govern common and independent steps of regulatory T cell development from novel CD122-expressing pre-precursors. J. Immunol. 2017. 199: 920-930.
Lio, C.-W. J. and Hsieh, C.-S., A two-step process for thymic regulatory T cell development. Immunity 2008. 28: 100-111.
Marshall, D., Sinclair, C., Tung, S. and Seddon, B., Differential requirement for IL-2 and IL-15 during bifurcated development of thymic regulatory T cells. J. Immunol. 2014. 193: 5525-5533.
Fu, W., Ergun, A., Lu, T., Hill, J. A., Haxhinasto, S., Fassett, M. S., Gazit, R. et al., A multiply redundant genetic switch ‘locks in’ the transcriptional signature of regulatory T cells. Nat. Immunol. 2012. 13: 972-980.
Chung, Y., Tanaka, S., Chu, F., Nurieva, R. I., Martinez, G. J., Rawal, S., Wang, Y.-H. et al., Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat. Med. 2011. 17: 983-988.
Koch, M. A., Tucker-Heard, G. a. s., Perdue, N. R., Killebrew, J. R., Urdahl, K. B. and Campbell, D. J., The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 2009. 10: 595-602.
Wohlfert, E. A., Grainger, J. R., Bouladoux, N., Konkel, J. E., Oldenhove, G., Ribeiro, C. H., Hall, J. A. et al., GATA3 controls Foxp3+ regulatory T cell fate during inflammation in mice. J. Clin. Invest. 2011. 121: 4503-4515.
Zheng, Y., Chaudhry, A., Kas, A., deRoos, P., Kim, J. M., Chu, T.-T., Corcoran, L. et al., Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control TH2 responses. Nature 2009. 458: 351-356.
Tartar, D. M., VanMorlan, A. M., Wan, X., Guloglu, F. B., Jain, R., Haymaker, C. L., Ellis, J. S. et al., FoxP3+RORγt+ T helper intermediates display suppressive function against autoimmune diabetes. J. Immunol. 2010. 184: 3377-3385.
Yu, F., Sharma, S., Edwards, J., Feigenbaum, L. and Zhu, J., Dynamic expression of transcription factors T-bet and GATA-3 by regulatory T cells maintains immunotolerance. Nat. Immunol. 2015. 16: 197-206.
Gerondakis, S., Fulford, T. S., Messina, N. L. and Grumont, R. J., NF-κB control of T cell development. Nat. Immunol. 2014. 15: 15-25.
Gückel, E., Frey, S., Zaiss, M. M., Schett, G., Ghosh, S. and Voll, R. E., Cell-intrinsic NF-κB activation is critical for the development of natural regulatory T cells in mice. PLoS One 2011. 6: e20003.
Gerondakis, S. and Siebenlist, U., Roles of the NF-κB pathway in lymphocyte development and function. Cold Spring Harb. Perspect. Biol. 2010. 2: a000182-a000182.
Isomura, I., Palmer, S., Grumont, R. J., Bunting, K., Hoyne, G., Wilkinson, N., Banerjee, A. et al., c-Rel is required for the development of thymic Foxp3+ CD4 regulatory T cells. J. Exp. Med. 2009. 206: 3001-3014.
Deenick, E. K., Elford, A. R., Pellegrini, M., Hall, H., Mak, T. W. and Ohashi, P. S., c-Rel but not NF-κB1 is important for T regulatory cell development. Eur. J. Immunol. 2010. 40: 677-681.
Ruan, Q., Kameswaran, V., Tone, Y., Li, L., Liou, H.-C., Greene, M. I., Tone, M. et al., Development of Foxp3(+) regulatory T cells is driven by the c-rel enhanceosome. Immunity 2009. 31: 932-940.
Visekruna, A., Huber, M., Hellhund, A., Bothur, E., Reinhard, K., Bollig, N., Schmidt, N. et al., c-Rel is crucial for the induction of Foxp3+ regulatory CD4+ T cells but not TH17 cells. Eur. J. Immunol. 2010. 40: 671-676.
Grigoriadis, G., Vasanthakumar, A., Banerjee, A., Grumont, R., Overall, S., Gleeson, P., Shannon, F. et al., c-Rel controls multiple discrete steps in the thymic development of Foxp3(+) CD4 regulatory T cells. PLoS One 2011. 6: e26851.
Oh, H., Grinberg-Bleyer, Y., Liao, W., Maloney, D., Wang, P., Wu, Z., Wang, J. et al., An NF-κB transcription-factor-dependent lineage-specific transcriptional program promotes regulatory T cell identity and function. Immunity 2018. 47: 450-465.
Messina, N., Fulford, T., O'Reilly, L., Loh, W. X., Motyer, J. M., Ellis, D., McLean, C. et al., The NF-κB transcription factor RelA is required for the tolerogenic function of Foxp3(+) regulatory T cells. J. Autoimmun. 2016. 70: 52-62.
Schmidt-Supprian, M., Tian, J., Grant, E. P., Pasparakis, M., Maehr, R., Ovaa, H., Ploegh, H. L. et al., Differential dependence of CD4+CD25+ regulatory and natural killer-like T cells on signals leading to NF-κB activation. Proc. Natl. Acad. Sci. 2004. 101: 4566-4571.
Chang, J.-H., Xiao, Y., Hu, H., Jin, J., Yu, J., Zhou, X., Wu, X. et al., Ubc13 maintains the suppressive function of regulatory T cells and prevents their conversion into effector-like T cells. Nat. Immunol. 2012. 13: 481-490.
Muto, G., Kotani, H., Kondo, T., Morita, R., Tsuruta, S., Kobayashi, T., Luche, H. et al., TRAF6 Is essential for maintenance of regulatory T cells that suppress Th2 type autoimmunity. PLoS One 2013. 8: e74639.
Chang, J.-H., Hu, H. and Sun, S.-C., Survival and maintenance of regulatory T cells require the kinase TAK1. Cellr. Mol. Immun. 2015. 12: 572-579.
Long, M., Park, S.-G., Strickland, I., Hayden, M. S. and Ghosh, S., Nuclear factor-κB modulates regulatory T cell development by directly regulating expression of Foxp3 transcription factor. Immunity 2009. 31: 921-931.
Vasanthakumar, A., Liao, Y., Teh, P., Pascutti, M. F., Oja, A. E., Garnham, A. L., Gloury, R. et al., The TNF receptor superfamily-NF-κB axis is critical to maintain effector regulatory T cells in lymphoid and non-lymphoid tissues. Cell Rep. 2017. 20: 2906-2920.
Liston, A., Siggs, O. M. and Goodnow, C. C., Tracing the action of IL-2 in tolerance to islet-specific antigen. Immunol. Cell Biol. 2007. 85: 338-342.
Apostolou, I., Sarukhan, A., Klein, L. and von Boehmer, H., Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 2002. 3: 756-763.
Moran, A. E., Holzapfel, K. L., Xing, Y., Cunningham, N. R., Maltzman, J. S., Punt, J. and Hogquist, K. A., T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 2011. 208: 1279-1289.
Stadinski, B. D., Trenh, P., Smith, R. L., Bautista, B., Huseby, P. G., Li, G., Stern, L. J. et al., A role for differential variable gene pairing in creating T cell receptors specific for unique major histocompatibility ligands. Immunity 2011. 35: 694-704.
Stadinski, B. D., Shekhar, K., Gómez-Touriño, I., Jung, J., Sasaki, K., Sewell, A. K., Peakman, M. et al., Hydrophobic CDR3 residues promote the development of self-reactive T cells. Nat. Immunol. 2016. 17: 946-955.
Wirasinha, R. C., Singh, M., Archer, S. K., Chan, A., Harrison, P. F., Goodnow, C. C. and Daley, S. R., αβ T-cell receptors with a central CDR3 cysteine are enriched in CD8αα intraepithelial lymphocytes and their thymic precursors. Immunol. Cell Biol. 2018. 96: 553-561.
Chao, A. and Jost, L., Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 2012. 93: 2533-2547.
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K. and Ellison, A. M., Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecologicl Monographs 2014. 84: 45-67.
Mahmud, S. A., Manlove, L. S., Schmitz, H. M., Xing, Y., Wang, Y., Owen, D. L., Schenkel, J. M. et al., Costimulation via the tumor-necrosis factor receptor superfamily couples TCR signal strength to the thymic differentiation of regulatory T cells. Nat. Immunol. 2014. 15: 473-481.
Heise, N., De Silva, N. S., Silva, K., Carette, A., Simonetti, G., Pasparakis, M. and Klein, U., Germinal center B cell maintenance and differentiation are controlled by distinct NF-κB transcription factor subunits. J. Exp. Med. 2014. 211: 2103-2118.
Cowan, J. E., McCarthy, N. I. and Anderson, G., CCR7 controls thymus recirculation, but not production and emigration, of Foxp3(+) T cells. Cell Rep. 2016. 14: 1041-1048.
Cowan, J. E., Parnell, S. M., Nakamura, K., Caamano, J. H., Lane, P. J. L., Jenkinson, E. J., Jenkinson, W. E. et al., The thymic medulla is required for Foxp3+ regulatory but not conventional CD4+ thymocyte development. J. Exp. Med. 2013. 210: 675-681.
Thiault, N., Darrigues, J., Adoue, V., Gros, M., Binet, B., Perals, C., Leobon, B. et al., Peripheral regulatory T lymphocytes recirculating to the thymus suppress the development of their precursors. Nat. Immunol. 2015. 16: 628-634.
Burchill, M. A., Yang, J., Vogtenhuber, C., Blazar, B. R. and Farrar, M. A., IL-2 receptor β-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J. Immunol. 2007. 178: 280-290.
Vogel, C. F. A., Kahn, E. M., Leung, P. S. C., Gershwin, M. E., Chang, W. L. W., Wu, D., Haarmann-Stemmann, T. et al., Cross-talk between aryl hydrocarbon receptor and the inflammatory response: a role for NF-κB. J. Biol. Chem. 2014. 289: 1866-1875.
Grumont, R. J. and Gerondakis, S., Rel induces interferon regulatory factor 4 (IRF-4) expression in lymphocytes: modulation of interferon-regulated gene expression by Rel/nuclear factor κB. J. Exp. Med. 2000. 191: 1281.
Hinz, M., Lemke, P., Anagnostopoulos, I., Hacker, C., Krappmann, D., Mathas, S., Dorken, B. et al., Nuclear factor κB-dependent gene expression profiling of hodgkin's disease tumor cells, pathogenetic significance, and link to constitutive signal transducer and activator of transcription 5a activity. J. Exp. Med. 2002. 196: 605-617.
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 mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 2012. 209: 1723-1742.
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.
Maria, A., English, K. A. and Gorham, J. D., Appropriate development of the liver Treg compartment is modulated by the microbiota and requires TGF-β and MyD88. J. Immunol. Res. 2014. 2014: 279736-279736.
Zheng, S. G., Wang, J., Wang, P., Gray, J. D. and Horwitz, D. A., IL-2 is essential for TGF-β to convert naive CD4+CD25− cells to CD25+Foxp3+ regulatory T cells and for expansion of these cells. J. Immunol. 2007. 178: 2018-2027.
Molinero, L. L., Miller, M. L., Evaristo, C. and Alegre, M. L., High TCR stimuli prevent induced regulatory T cell differentiation in a NF-κB-dependent manner. J. Immunol. 2011. 186: 4609-4617.
Schulze-Luehrmann, J. and Ghosh, S., Antigen-receptor signaling to nuclear factor κB. Immunity 2006. 25: 701-715.
Gerondakis, S., Strasser, A., Metcalf, D., Grigoriadis, G., Scheerlinck, J. Y. and Grumont, R. J., Rel-deficient T cells exhibit defects in production of interleukin 3 and granulocyte-macrophage colony-stimulating factor. Proc. Natl. Acad. Sci. 1996. 93: 3405-3409.
Kallies, A., Hasbold, J., Tarlinton, D. M., Dietrich, W., Corcoran, L. M., Hodgkin, P. D. and Nutt, S. L., Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 2004. 200: 967-977.
Vasanthakumar, A., Moro, K., Xin, A., Liao, Y., Gloury, R., Kawamoto, S., Fagarasan, S. et al., The transcriptional regulators IRF4, BATF and IL-33 orchestrate development and maintenance of adipose tissue-resident regulatory T cells. Nat. Immunol. 2015. 16: 276-285.
Shevach, E. M., Foxp3+ T regulatory cells: still many unanswered questions-a perspective after 20 years of study. Front. Immunol. 2018. 9: 1048.
Winstead, C. J., Fraser, J. M. and Khoruts, A., Regulatory CD4+CD25+Foxp3+ T cells selectively inhibit the spontaneous form of lymphopenia-induced proliferation of naive T cells. J. Immunol. 2008. 180: 7305-7317.
Daley, S. R., Hu, D. Y. and Goodnow, C. C., Helios marks strongly autoreactive CD4+ T cells in two major waves of thymic deletion distinguished by induction of PD-1 or NF-κB. J. Exp. Med. 2013. 210: 269-285.
Hu, D. Y., Yap, J. Y., Wirasinha, R. C., Howard, D. R., Goodnow, C. C. and Daley, S. R., A timeline demarcating two waves of clonal deletion and Foxp3 upregulation during thymocyte development. Immunol. Cell Biol. 2016. 94: 357-366.
Breed, E. R., Watanabe, M. and Hogquist, K. A., Measuring thymic clonal deletion at the population level. J. Immunol. 2019. 202: 3226-3233.
Hu, D. Y., Wirasinha, R. C., Goodnow, C. C. and Daley, S. R., IL-2 prevents deletion of developing T-regulatory cells in the thymus. Cell Death Differ 2017. 24: 1007-1016.
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.
Hassler, T., Urmann, E., Teschner, S., Federle, C., Dileepan, T., Schober, K., Jenkins, M. K. et al., Inventories of naive and tolerant mouse CD4 T cell repertoires reveal a hierarchy of deleted and diverted T cell receptors. Proc. Natl. Acad. Sci. USA 2019. 116: 18537-18543.
Stadinski, B. D., Blevins, S. J., Spidale, N. A., Duke, B. R., Huseby, P. G., Stern, L. J. and Huseby, E. S., A temporal thymic selection switch and ligand binding kinetics constrain neonatal Foxp3+ Treg cell development. Nat. Immunol. 2019. 20: 1046-1058.
Cozzo Picca, C., Simons, D. M., Oh, S., Aitken, M., Perng, O. A., Mergenthaler, C., Kropf, E. et al., CD4+CD25+Foxp3+ regulatory T cell formation requires more specific recognition of a self-peptide than thymocyte deletion. Proc. Natl. Acad. Sci. USA 2011. 108: 14890-14895.
Zhan, Y., Gerondakis, S., Coghill, E., Bourges, D., Xu, Y., Brady, J. L. and Lew, A. M., Glucocorticoid-induced TNF receptor expression by T cells is reciprocally regulated by NF-κB and NFAT. J. Immunol. 2008. 181: 5405-5413.
Grigoriadis, G., Zhan, Y., Grumont, R. J., Metcalf, D., Handman, E., Cheers, C. and Gerondakis, S., The Rel subunit of NF-κB-like transcription factors is a positive and negative regulator of macrophage gene expression: distinct roles for Rel in different macrophage populations. EMBO J. 1996. 15: 7099.
Gilmore, T. D. and Gerondakis, S., The c-Rel transcription factor in development and disease. Genes Cancer 2011. 2: 695-711.
Nikolouli, E., Elfaki, Y., Herppich, S., Schelmbauer, C., Delacher, M., Falk, C., Mufazalov, I. A. et al., Recirculating IL-1R2(+) Tregs fine-tune intrathymic Treg development under inflammatory conditions. Cell Mol. Immunol. 2020. 18: 182-193.
Smigiel, K. S., Richards, E., Srivastava, S., Thomas, K. R., Dudda, J. C., Klonowski, K. D. and Campbell, D. J., CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory T cell subsets. J. Exp. Med. 2014. 211: 121-136.
Köntgen, F., Grumont, R. J., Strasser, A., Metcalf, D., Li, R., Tarlinton, D. and Gerondakis, S., Mice lacking the c-rel proto-oncogene exhibit defects in lymphocyte proliferation, humoral immunity, and interleukin-2 expression. Genes Develop. 1995. 9: 1965-1977.
Liou, H. C., Jin, Z., Tumang, J., Andjelic, S., Smith, K. A. and Liou, M. L., c-Rel is crucial for lymphocyte proliferation but dispensable for T cell effector function. Int. Immunol. 1999. 11: 361-371.
Gilmore, T. D., Kalaitzidis, D., Liang, M.-C. and Starczynowski, D. T., The c-Rel transcription factor and B-cell proliferation: a deal with the devil. Oncogene 2004. 23: 2275-2286.
Lorenz, V. N., Schön, M. P. and Seitz, C. S., c-Rel downregulation affects cell cycle progression of human keratinocytes. J. Invest. Dermatol. 2014. 134: 415-422.
Grumont, R. J., Rourke, I. J., O'Reilly, L. A., Strasser, A., Miyake, K., Sha, W. and Gerondakis, S., B lymphocytes differentially use the Rel and nuclear factor κB1 (NF-κB1) transcription factors to regulate cell cycle progression and apoptosis in quiescent and mitogen-activated cells. J. Exp. Med. 1998. 187: 663-674.
Levine, A. G., Arvey, A., Jin, W. and Rudensky, A. Y., Continuous requirement for the TCR in regulatory T cell function. Nat. Immunol. 2014. 15: 1070-1078.
Vahl, J. C., Drees, C., Heger, K., Heink, S., Fischer, J. C., Nedjic, J., Ohkura, N. et al., Continuous T cell receptor signals maintain a functional regulatory T cell pool. Immunity 2014. 41: 722-736.
van Ham, M., Teich, R., Philipsen, L., Niemz, J., Amsberg, N., Wissing, J., Nimtz, M. et al., TCR signalling network organization at the immunological synapses of murine regulatory T cells. Eur. J. Immunol. 2017. 47: 2043-2058.
Li, Z., Ju, X., Silveira, P. A., Abadir, E., Hsu, W.-H., Hart, D. N. J. and Clark, G. J., CD83: activation marker for antigen presenting cells and its therapeutic potential. Front. Immunol. 2019. 10: 1312.
Grinberg-Bleyer, Y., Oh, H., Desrichard, A., Bhatt, D. M., Caron, R., Chan, T. A., Schmid, R. M. et al., NF-κB c-Rel is crucial for the regulatory T cell immune checkpoint in cancer. Cell 2018. 170: 1096-1108.
Rubtsov, Y. P., Rasmussen, J. P., Chi, E. Y., Fontenot, J., Castelli, L., Ye, X., Treuting, P. et al., Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008. 28: 546-558.
Campbell, I. K., Gerondakis, S., O'Donnell, K. and Wicks, I. P., Distinct roles for the NF-κB1 (p50) and c-Rel transcription factors in inflammatory arthritis. J. Clin. Invest. 2000. 105: 1799-1806.
Low, J. T., Hughes, P., Lin, A., Siebenlist, U., Jain, R., Yaprianto, K., Gray, D. H. D. et al., Impact of loss of NF-κB1, NF-κB2 or c-REL on SLE-like autoimmune disease and lymphadenopathy in Faslpr/lpr mutant mice. Immunol Cell Biol 2016. 94: 66-78.
Wan, Y. Y. and Flavell, R. A., Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. 2005. 102: 5126-5131.
Ho, W. Y., Cooke, M. P., Goodnow, C. C. and Davis, M. M., Resting and anergic B cells are defective in CD28-dependent costimulation of naive CD4+ T cells. J. Exp. Med. 1994. 179: 1539-1549.
Akkaraju, S., Ho, W. Y., Leong, D., Canaan, K., Davis, M. M. and Goodnow, C. C., A range of CD4 T cell tolerance: partial inactivation to organ-specific antigen allows nondestructive thyroiditis or insulitis. Immunity 1997. 7: 255-271.
Cossarizza, A., Chang, H.-D., Radbruch, A., Acs, A., Adam, D., Adam-Klages, S., Agace, W. W. et al., Guidelines for the use of flow cytometry and cell sorting in immunological studies (second edition). Eur. J. Immunol. 2019. 49: 1457-1973.
Grumont, R. J. and Gerondakis, S., The subunit composition of NF-κB complexes changes during B-cell development. Cell Growth Differ. 1994. 5: 1321.
Tsyganov, K., Perry, A. J., Archer, S. K. and Powell, D. R., RNAsik: a pipeline for complete and reproducible RNA-seq analysis that runs anywhere with speed and ease. J Open Source Software. 2018. 3: 583.
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P. et al., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 2013. 29: 15-21.
Liao, Y., Smyth, G. K. and Shi, W., featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 2014. 30: 923-930.
Powell, D. R., Degust: interactive RNA-seq analysis 2019.
Shugay, M., Britanova, O. V., Merzlyak, E. M., Turchaninova, M. A., Mamedov, I. Z., Tuganbaev, T. R., Bolotin, D. A. et al., Towards error-free profiling of immune repertoires. Nat Methods 2014. 11: 653-655.
Hill, M. O., Diversity and evenness: a unifying notation and its consequences. Ecology 1973. 54: 427-432.

Auteurs

Thomas S Fulford (TS)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Raelene Grumont (R)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Rushika C Wirasinha (RC)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Darcy Ellis (D)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Adele Barugahare (A)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.
Monash Bioinformatics Platform, School of Biomedical Sciences, Monash University, Melbourne, Australia.

Stephen J Turner (SJ)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.
Department of Microbiology, Monash University, Melbourne, Australia.

Haroon Naeem (H)

Monash Bioinformatics Platform, School of Biomedical Sciences, Monash University, Melbourne, Australia.

David Powell (D)

Monash Bioinformatics Platform, School of Biomedical Sciences, Monash University, Melbourne, Australia.

Paul A Lyons (PA)

Cambridge Institute of Therapeutic Immunology and Infectious Disease, Jeffrey Cheah Biomedical Centre, University of Cambridge, Cambridge, England, UK.
Department of Medicine, University of Cambridge, University of Cambridge School of Clinical Medicine, Cambridge, England, UK.

Kenneth G C Smith (KGC)

Cambridge Institute of Therapeutic Immunology and Infectious Disease, Jeffrey Cheah Biomedical Centre, University of Cambridge, Cambridge, England, UK.
Department of Medicine, University of Cambridge, University of Cambridge School of Clinical Medicine, Cambridge, England, UK.

Sebastian Scheer (S)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Colby Zaph (C)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Ulf Klein (U)

Division of Haematology & Immunology, Leeds Institute of Medical Research at St. James's, University of Leeds, Leeds, LS2 7TF.

Stephen R Daley (SR)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

Steve Gerondakis (S)

Infection and Immunity Program, Monash Biomedicine Discovery Institute and Department of Biochemistry and Molecular Biology, Monash University, Melbourne, Australia.

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