Stat3 programs Th17-specific regulatory T cells to control GN

Journal of the American Society of Nephrology

Volumn 25, Issue 6, 2014, Pages 1291-1302

  Kluger, Malte A ^a   Luig, Michael ^a   Wegscheid, Claudia ^a   Goerke, Boeren ^a   Paust, Hans Joachim ^a   Brix, Silke R ^a   Yan, Isabell ^a   Mittrücker, Hans Willi ^a   Hagl, Beate ^b   Renner, Ellen D ^b   Tiegs, Gisa ^a   Wiech, Thorsten ^a   Stahl, Rolf A K ^a   Panzer, Ulf ^a   Steinmetz, Oliver M ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHEMOKINE RECEPTOR CCR6; STAT3 PROTEIN; TRANSCRIPTION FACTOR FOXP3; CCR6 PROTEIN, HUMAN; CCR6 PROTEIN, MOUSE; STAT3 PROTEIN, HUMAN; STAT3 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE COMPLEX NEPHRITIS; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; KIDNEY BIOPSY; LYMPHOCYTE PROLIFERATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH17 CELL; ACUPUNCTURE; ANCA ASSOCIATED VASCULITIS; ANIMAL; C57BL MOUSE; CELL MOTION; CYTOLOGY; DISEASE MODEL; GENETICS; GLOMERULONEPHRITIS; IMMUNOLOGY; KIDNEY; KNOCKOUT MOUSE; METABOLISM; MIGRAINE; PAIN; PATHOLOGY; SPLEEN;

ACUPUNCTURE; MIGRAINE; PAIN;

ANIMALS; ANTI-NEUTROPHIL CYTOPLASMIC ANTIBODY-ASSOCIATED VASCULITIS; CELL MOVEMENT; DISEASE MODELS, ANIMAL; GLOMERULONEPHRITIS; HUMANS; KIDNEY; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, CCR6; SPLEEN; STAT3 TRANSCRIPTION FACTOR; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84906078630     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2013080904     Document Type: Article

References (48)

1. Mosmann TR, Coffman RL: Heterogeneity of cytokine secretion patterns and functions of helper T cells. Adv Immunol 46: 111-147, 1989
2. Mosmann TR, Coffman RL: TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annu Rev Immunol 7: 145-173, 1989
3. Bluestone JA, Mackay CR, O'Shea JJ, Stockinger B: The functional plasticity of T cell subsets. Nat Rev Immunol 9: 811-816, 2009
4. Zhu J, Yamane H, Paul WE: Differentiation of effector CD4 T cell populations (∗). Annu Rev Immunol 28: 445-489, 2010
5. Hemdan NY, Birkenmeier G, Wichmann G, Abu El-Saad AM, Krieger T, Conrad K, Sack U: Interleukin-17-producing T helper cells in autoimmunity. Autoimmun Rev 9: 785-792, 2010
6. Jäger A, Kuchroo VK: Effector and regulatory T-cell subsets in autoimmunity and tissue inflammation. Scand J Immunol 72: 173-184, 2010
7. Oestreich KJ, Weinmann AS: Transcriptional mechanisms that regulate T helper 1 cell differentiation. Curr Opin Immunol 24: 191-195, 2012
8. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH: A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655-669, 2000
9. Zheng W, Flavell RA: The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89: 587-596, 1997
10. Kaplan MH, Schindler U, Smiley ST, Grusby MJ: Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4: 313-319, 1996
11. Yang XO, Pappu BP, Nurieva R, Akimzhanov A, Kang HS, Chung Y, Ma L, Shah B, Panopoulos AD, Schluns KS, Watowich SS, Tian Q, Jetten AM, Dong C: T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 28: 29-39, 2008
12. Yang XO, Panopoulos AD, Nurieva R, Chang SH, Wang D, Watowich SS, Dong C: STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J Biol Chem282: 9358-9363, 2007
13. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, Cua DJ, Littman DR: The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133, 2006
14. Vignali DA, Collison LW,Workman CJ: Howregulatory T cellswork. Nat Rev Immunol 8: 523-532, 2008
15. Ohkura N, Kitagawa Y, Sakaguchi S: Development andmaintenance of regulatory T cells. Immunity 38: 414-423, 2013
16. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA, Wilkinson JE, Galas D, Ziegler SF, Ramsdell F: Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 27: 68-73, 2001
17. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, Kelly TE, Saulsbury FT, Chance PF, Ochs HD: The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 27: 20-21, 2001
18. Feuerer M, Hill JA, Mathis D, Benoist C: Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nat Immunol 10: 689-695, 2009
19. 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. Nat Immunol 10: 595-602, 2009
20. Zheng Y, Chaudhry A, Kas A, deRoos P, Kim JM, Chu TT, Corcoran L, Treuting P, Klein U, Rudensky AY: Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 458: 351-356, 2009
21. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, Kas A, Rudensky AY: CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326: 986-991, 2009
22. Ghoreschi K, Laurence A, Yang XP, Hirahara K, O'Shea JJ: T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol 32: 395-401, 2011
23. Turner JE, Paust HJ, Steinmetz OM, Panzer U: The Th17 immune response in renal inflammation. Kidney Int 77: 1070-1075, 2010
24. Paust HJ, Turner JE, Steinmetz OM, Peters A, Heymann F, Hölscher C, WolfG, Kurts C,MittrückerHW, Stahl RA, Panzer U: The IL-23/Th17 axis contributes to renal injury in experimental glomerulonephritis. J Am Soc Nephrol 20: 969-979, 2009
25. Steinmetz OM, Summers SA, Gan PY, Semple T, Holdsworth SR, Kitching AR: The Th17-defining transcription factor RORgt promotes glomerulonephritis. J Am Soc Nephrol 22: 472-483, 2011
26. Summers SA, Steinmetz OM, LiM, Kausman JY, Semple T, Edgtton KL, Borza DB, Braley H, Holdsworth SR, Kitching AR: Th1 and Th17 cells induce proliferative glomerulonephritis. J Am Soc Nephrol 20: 2518-2524, 2009
27. Kitching AR, Holdsworth SR: The emergence of TH17 cells as effectors of renal injury. J Am Soc Nephrol 22: 235-238, 2011
28. Ooi JD, Snelgrove SL, Engel DR, Hochheiser K, Ludwig-Portugall I, Nozaki Y, O'Sullivan KM, Hickey MJ, Holdsworth SR, Kurts C, Kitching AR: Endogenous foxp3(+) T-regulatory cells suppress anti-glomerular basement membrane nephritis. Kidney Int 79: 977-986, 2011
29. Ostmann A, Paust HJ, Panzer U, Wegscheid C, Kapffer S, Huber S, Flavell RA, Erhardt A, Tiegs G: Regulatory T cell-derived IL-10 ameliorates crescentic GN. J Am Soc Nephrol 24: 930-942, 2013
30. Gan PY, Steinmetz OM, Tan DS, O'Sullivan KM, Ooi JD, Iwakura Y, Kitching AR, Holdsworth SR: Th17 cells promote autoimmune antimyeloperoxidase glomerulonephritis. J Am Soc Nephrol 21: 925-931, 2010
31. Ooi JD, Phoon RK, Holdsworth SR, Kitching AR: IL-23, not IL-12, directs autoimmunity to theGoodpasture antigen.J Am Soc Nephrol 20: 980-989, 2009
32. Couser WG: Basic and translational concepts of immune-mediated glomerular diseases. J Am Soc Nephrol 23: 381-399, 2012
33. Assmann KJ, Tangelder MM, Lange WP, Schrijver G, Koene RA: Anti-GBM nephritis in the mouse: severe proteinuria in the heterologous phase. Virchows Arch A Pathol Anat Histopathol 406: 285-299, 1985
34. Turner JE, Paust HJ, Steinmetz OM, Peters A, Riedel JH, Erhardt A, Wegscheid C, Velden J, Fehr S, Mittrücker HW, Tiegs G, Stahl RA, Panzer U: CCR6 recruits regulatory T cells and Th17 cells to the kidney in glomerulonephritis. J Am Soc Nephrol 21: 974-985, 2010
35. Schimke LF, Sawalle-Belohradsky J, Roesler J, Wollenberg A, Rack A, BorteM, RieberN, Cremer R,Maass E,Dopfer R, Reichenbach J,Wahn V, Hoenig M, Jansson AF, Roesen-Wolff A, Schaub B, Seger R, Hill HR, Ochs HD, Torgerson TR, Belohradsky BH, Renner ED: Diagnostic approach to the hyper-IgE syndromes: Immunologic and clinical key findings to differentiate hyper-IgE syndromes from atopic dermatitis. J Allergy Clin Immunol 126: 611-617 e611, 2010
36. Minegishi Y, SaitoM, Tsuchiya S, Tsuge I, Takada H, Hara T, Kawamura N, Ariga T, Pasic S, Stojkovic O, Metin A, Karasuyama H: Dominantnegativemutations in the DNA-binding domain of STAT3 cause hyper-IgE syndrome. Nature 448: 1058-1062, 2007
37. Holland SM, DeLeo FR, Elloumi HZ, Hsu AP, Uzel G, Brodsky N, Freeman AF, Demidowich A, Davis J, Turner ML, Anderson VL, Darnell DN, Welch PA, Kuhns DB, Frucht DM, Malech HL, Gallin JI, Kobayashi SD,Whitney AR, Voyich JM,Musser JM,Woellner C, Schäffer AA, Puck JM,Grimbacher B: STAT3mutations in the hyper-IgE syndrome.NEngl J Med 357: 1608-1619, 2007
38. Pandiyan P, Conti HR, Zheng L, Peterson AC, Mathern DR, Hernández-Santos N, Edgerton M, Gaffen SL, Lenardo MJ: CD4(+)CD25(+)Foxp3 (+) regulatory T cells promote Th17 cells in vitro and enhance host resistance in mouse Candida albicans Th17 cell infection model. Immunity 34: 422-434, 2011
39. Li S, Holdsworth SR, Tipping PG: Antibody independent crescentic glomerulonephritis inmu chain deficientmice. Kidney Int 51: 672-678, 1997
40. Steinmetz OM, Stahl RA, Panzer U: Chemokines and B cells in renal inflammation and allograft rejection. Front Biosci (Schol Ed) 1: 13-22, 2009
41. Chaudhry A, Samstein RM, Treuting P, Liang Y, PilsMC, Heinrich JM, Jack RS, Wunderlich FT, Brüning JC, Müller W, Rudensky AY: Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cellmediated inflammation. Immunity 34: 566-578, 2011
42. Akira S: Roles of STAT3 defined by tissue-specific gene targeting. Oncogene 19: 2607-2611, 2000
43. Rubtsov YP, Rasmussen JP,Chi EY, Fontenot J, Castelli L, Ye X, Treuting P, Siewe L, Roers A, Henderson WR Jr, Muller W, Rudensky AY: Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28: 546-558, 2008
44. Panzer U, Steinmetz OM, Paust HJ, Meyer-Schwesinger C, Peters A, Turner JE, Zahner G, Heymann F, Kurts C, Hopfer H, Helmchen U, Haag F, Schneider A, Stahl RA: Chemokine receptor CXCR3 mediates T cell recruitment and tissue injury in nephrotoxic nephritis inmice. J AmSoc Nephrol 18: 2071-2084, 2007
45. Turner JE, Paust HJ, Steinmetz OM, Peters A, Meyer-Schwesinger C, Heymann F, Helmchen U, Fehr S, Horuk R, Wenzel U, Kurts C, Mittrücker HW, Stahl RA, Panzer U: CCR5 deficiency aggravates crescentic glomerulonephritis in mice. J Immunol 181: 6546-6556, 2008
46. Hopfer H, Holzer J, Hünemörder S, Paust HJ, Sachs M, Meyer-Schwesinger C, Turner JE, Panzer U,MittrückerHW: Characterization of the renal CD4+ T-cell response in experimental autoimmune glomerulonephritis. Kidney Int 82: 60-71, 2012
47. Kluger MA, Zahner G, Paust HJ, Schaper M, Magnus T, Panzer U, Stahl RA: Leukocyte-derived MMP9 is crucial for the recruitment of proinflammatory macrophages in experimental glomerulonephritis. Kidney Int 83: 865-877, 2013
48. Hirota K, Turner JE, Villa M, Duarte JH, Demengeot J, Steinmetz OM, Stockinger B: Plasticity of Th17 cells in Peyer's patches is responsible for the induction of T cell-dependent IgA responses. Nat Immunol 14: 372-379, 2013