STAT3 is important for follicular regulatory T cell differentiation

PLoS ONE

Volumn 11, Issue 5, 2016, Pages

  Wu, Hao ^a   Xie, Markus M ^a   Liu, Hong ^a   Dent, Alexander L ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

STAT3 PROTEIN; STAT3 PROTEIN, MOUSE;

ANIMAL; ANTIBODY PRODUCTION; B LYMPHOCYTE; CELL DIFFERENTIATION; GERMINAL CENTER; HELPER CELL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MOUSE; REGULATORY T LYMPHOCYTE; SHEEP;

ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CELL DIFFERENTIATION; GERMINAL CENTER; LYMPHOCYTE ACTIVATION; MICE; SHEEP; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

EID: 85020743755     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0155040     Document Type: Article

References (38)

1. Breitfeld D, Ohl L, Kremmer E, Ellwart J, Sallusto F, Lipp M, et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. The Journal of Experimental Medicine. 2000; 192(11):1545–52. Epub 2000/12/06. PMID: 11104797; PubMed Central PMCID: PMC2193094.
2. Schaerli P, Willimann K, Lang AB, Lipp M, Loetscher P, Moser B. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. The Journal of Experimental Medicine. 2000; 192(11):1553–62. Epub 2000/12/06. PMID: 11104798; PubMed Central PMCID: PMC2193097.
3. Zhu J, Paul WE. Peripheral CD4+ T-cell differentiation regulated by networks of cytokines and transcription factors. Immunological reviews. 2010; 238(1):247–62. Epub 2010/10/26. doi: 10.1111/j.1600-065X.2010.00951.x PMID: 20969597; PubMed Central PMCID: PMC2975272.
4. Nakayamada S, Poholek AC, Lu KT, Takahashi H, Kato M, Iwata S, et al. Type I IFN induces binding of STAT1 to Bcl6: divergent roles of STAT family transcription factors in the T follicular helper cell genetic program. J Immunol. 2014; 192(5):2156–66. Epub 2014/02/04. doi: 10.4049/jimmunol.1300675 PMID: 24489092; PubMed Central PMCID: PMC3967131.
5. Choi YS, Eto D, Yang JA, Lao C, Crotty S. Cutting Edge: STAT1 Is Required for IL-6-Mediated Bcl6 Induction for Early Follicular Helper Cell Differentiation. J Immunol. 2013. Epub 2013/03/01. doi: 10. 4049/jimmunol.1203032 PMID: 23447690.
6. Ray JP, Marshall HD, Laidlaw BJ, Staron MM, Kaech SM, Craft J. Transcription factor STAT3 and type I interferons are corepressive insulators for differentiation of follicular helper and T helper 1 cells. Immunity. 2014; 40(3):367–77. Epub 2014/03/19. doi: 10.1016/j.immuni.2014.02.005 PMID: 24631156; PubMed Central PMCID: PMC3992517.
7. Nakayamada S, Kanno Y, Takahashi H, Jankovic D, Lu KT, Johnson TA, et al. Early Th1 Cell Differentiation Is Marked by a Tfh Cell-like Transition. Immunity. 2011; 35(6):919–31. Epub 2011/12/27. doi: 10. 1016/j.immuni.2011.11.012 PMID: 22195747; PubMed Central PMCID: PMC3244883.
8. Nurieva RI, Chung Y, Martinez GJ, Yang XO, Tanaka S, Matskevitch TD, et al. Bcl6 mediates the development of T follicular helper cells. Science. 2009; 325(5943):1001–5. Epub 2009/07/25. doi: 10.1126/ science.1176676 PMID: 19628815; PubMed Central PMCID: PMC2857334.
9. Vinuesa CG, Cook MC, Angelucci C, Athanasopoulos V, Rui L, Hill KM, et al. A RING-type ubiquitin ligase family member required to repress follicular helper T cells and autoimmunity. Nature. 2005; 435 (7041):452–8. Epub 2005/05/27. doi: 10.1038/nature03555 PMID: 15917799.
10. Linterman MA, Rigby RJ, Wong RK, Yu D, Brink R, Cannons JL, et al. Follicular helper T cells are required for systemic autoimmunity. The Journal of Experimental Medicine. 2009; 206(3):561–76. Epub 2009/02/18. doi: 10.1084/jem.20081886 PMID: 19221396; PubMed Central PMCID: PMC2699132.
11. Odegard JM, Marks BR, DiPlacido LD, Poholek AC, Kono DH, Dong C, et al. ICOS-dependent extrafollicular helper T cells elicit IgG production via IL-21 in systemic autoimmunity. The Journal of Experimental Medicine. 2008; 205(12):2873–86. Epub 2008/11/05. doi: 10.1084/jem.20080840 PMID: 18981236; PubMed Central PMCID: PMC2585848.
12. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003; 299(5609):1057–61. Epub 2003/01/11. doi: 10.1126/science.1079490 PMID: 12522256.
13. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nature Immunology. 2003; 4(4):330–6. Epub 2003/03/04. doi: 10.1038/ni904 PMID: 12612578.
14. Koch MA, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, Campbell DJ. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nature Immunology. 2009; 10(6):595–602. Epub 2009/05/05. doi: 10.1038/ni.1731 PMID: 19412181; PubMed Central PMCID: PMC2712126.
15. Zheng Y, Chaudhry A, Kas A, deRoos P, Kim JM, Chu TT, et al. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature. 2009; 458(7236):351–6. Epub 2009/02/03. doi: 10.1038/nature07674 PMID: 19182775; PubMed Central PMCID: PMC2864791.
16. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, Kas A, et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science. 2009; 326(5955):986–91. Epub 2009/10/03. doi: 10.1126/science.1172702 PMID: 19797626.
17. Kluger MA, Luig M, Wegscheid C, Goerke B, Paust HJ, Brix SR, et al. Stat3 programs Th17-specific regulatory T cells to control GN. Journal of the American Society of Nephrology: JASN. 2014; 25 (6):1291–302. Epub 2014/02/11. doi: 10.1681/ASN.2013080904 PMID: 24511136; PubMed Central PMCID: PMC4033381.
18. Kluger MA, Melderis S, Nosko A, Goerke B, Luig M, Meyer MC, et al. Treg17 cells are programmed by Stat3 to suppress Th17 responses in systemic lupus. Kidney International. 2015. Epub 2015/10/16. doi: 10.1038/ki.2015.296 PMID: 26466322.
19. Chung Y, Tanaka S, Chu F, Nurieva RI, Martinez GJ, Rawal S, et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nature Medicine. 2011; 17(8):983–8. Epub 2011/07/26. doi: 10.1038/nm.2426 PMID: 21785430; PubMed Central PMCID: PMC3151340.
20. Linterman MA, Pierson W, Lee SK, Kallies A, Kawamoto S, Rayner TF, et al. Foxp3+ follicular regulatory T cells control the germinal center response. Nature Medicine. 2011; 17(8):975–82. Epub 2011/07/ 26. doi: 10.1038/nm.2425 PMID: 21785433; PubMed Central PMCID: PMC3182542.
21. Wollenberg I, Agua-Doce A, Hernandez A, Almeida C, Oliveira VG, Faro J, et al. Regulation of the germinal center reaction by Foxp3+ follicular regulatory T cells. J Immunol. 2011; 187(9):4553–60. Epub 2011/10/11. doi: 10.4049/jimmunol.1101328 PMID: 21984700.
22. Ding Y, Li J, Yang P, Luo B, Wu Q, Zajac AJ, 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. 2014; 66(9):2601–12. Epub 2014/06/10. doi: 10.1002/art.38735 PMID: 24909430; PubMed Central PMCID: PMC4146687.
23. Lu KT, Kanno Y, Cannons JL, Handon R, Bible P, Elkahloun AG, et al. Functional and Epigenetic Studies Reveal Multistep Differentiation and Plasticity of In Vitro-Generated and In Vivo-Derived Follicular T Helper Cells. Immunity. 2011. Epub 2011/10/25. doi: 10.1016/j.immuni.2011.07.015 PMID: 22018472.
24. Kato LM, Kawamoto S, Maruya M, Fagarasan S. Gut TFH and IgA: key players for regulation of bacterial communities and immune homeostasis. Immunology and Cell Biology. 2014; 92(1):49–56. Epub 2013/10/09. doi: 10.1038/icb.2013.54 PMID: 24100385.
25. Hirota K, Turner JE, Villa M, Duarte JH, Demengeot J, Steinmetz OM, et al. Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nature Immunology. 2013; 14(4):372–9. Epub 2013/03/12. doi: 10.1038/ni.2552 PMID: 23475182; PubMed Central PMCID: PMC3672955.
26. Wu H, Xu LL, Teuscher P, Liu H, Kaplan MH, Dent AL. An Inhibitory Role for the Transcription Factor Stat3 in Controlling IL-4 and Bcl6 Expression in Follicular Helper T Cells. J Immunol. 2015; 195 (5):2080–9. Epub 2015/07/19. doi: 10.4049/jimmunol.1500335 PMID: 26188063; PubMed Central PMCID: PMC4546859.
27. Baumjohann D, Preite S, Reboldi A, Ronchi F, Ansel KM, Lanzavecchia A, et al. Persistent antigen and germinal center B cells sustain T follicular helper cell responses and phenotype. Immunity. 2013; 38 (3):596–605. Epub 2013/03/19. doi: 10.1016/j.immuni.2012.11.020 PMID: 23499493.
28. Wu H, Chen Y, Liu H, Xu LL, Teuscher P, Wang S, et al. Follicular regulatory T cells repress cytokine production by follicular helper T cells and optimize IgG responses in mice. European Journal of Immunology. 2016. Epub 2016/02/19. doi: 10.1002/eji.201546094 PMID: 26887860.
29. Tsuji M, Komatsu N, Kawamoto S, Suzuki K, Kanagawa O, Honjo T, et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science. 2009; 323(5920):1488–92. Epub 2009/03/17. doi: 10.1126/science.1169152 PMID: 19286559.
30. Chaudhry A, Rudensky AY. Control of inflammation by integration of environmental cues by regulatory T cells. The Journal of Clinical Investigation. 2013; 123(3):939–44. Epub 2013/03/05. doi: 10.1172/ JCI57175 PMID: 23454755; PubMed Central PMCID: PMC3582113.
31. Ramiscal RR, Vinuesa CG. T-cell subsets in the germinal center. Immunological Reviews. 2013; 252 (1):146–55. Epub 2013/02/15. doi: 10.1111/imr.12031 PMID: 23405902.
32. Asao H, Okuyama C, Kumaki S, Ishii N, Tsuchiya S, Foster D, et al. Cutting edge: the common gamma-chain is an indispensable subunit of the IL-21 receptor complex. J Immunol. 2001; 167(1):1–5. Epub 2001/06/22. PMID: 11418623.
33. Takeda K, Kaisho T, Yoshida N, Takeda J, Kishimoto T, Akira S. Stat3 activation is responsible for IL-6dependent T cell proliferation through preventing apoptosis: generation and characterization of T cell-specific Stat3-deficient mice. J Immunol. 1998; 161(9):4652–60. Epub 1998/10/30. PMID: 9794394.
34. Raz R, Lee CK, Cannizzaro LA, d'Eustachio P, Levy DE. Essential role of STAT3 for embryonic stem cell pluripotency. Proceedings of the National Academy of Sciences of the United States of America. 1999; 96(6):2846–51. Epub 1999/03/17. PMID: 10077599; PubMed Central PMCID: PMC15857.
35. Reliene R, Schiestl RH. Differences in animal housing facilities and diet may affect study outcomes-a plea for inclusion of such information in publications. DNA Repair. 2006; 5(6):651–3. Epub 2006/04/04. doi: 10.1016/j.dnarep.2006.02.001 PMID: 16581314.
36. Park SR, Seo GY, Choi AJ, Stavnezer J, Kim PH. Analysis of transforming growth factor-beta1-induced Ig germ-line gamma2b transcription and its implication for IgA isotype switching. European Journal of Immunology. 2005; 35(3):946–56. Epub 2005/02/03. doi: 10.1002/eji.200425848 PMID: 15688346.
37. Hollister K, Chen Y, Wang S, Wu H, Mondal A, Clegg N, et al. The role of follicular helper T cells and the germinal center in HIV-1 gp120 DNA prime and gp120 protein boost vaccination. Human Vaccines & Immunotherapeutics. 2014; 10(7):1985–92. Epub 2014/11/27. doi: 10.4161/hv.28659 PMID: 25424808; PubMed Central PMCID: PMC4186047.
38. Kawamoto S, Maruya M, Kato LM, Suda W, Atarashi K, Doi Y, et al. Foxp3(+) T cells regulate immunoglobulin a selection and facilitate diversification of bacterial species responsible for immune homeostasis. Immunity. 2014; 41(1):152–65. Epub 2014/07/16. doi: 10.1016/j.immuni.2014.05.016 PMID: 25017466.