The chromatin-modifying enzyme Ezh2 is critical for the maintenance of regulatory T cell identity after activation

Immunity

Volumn 42, Issue 2, 2015, Pages 227-238

  DuPage, Michel ^a   Chopra, Gaurav ^a   Quiros, Jason ^a   Rosenthal, Wendy L ^a   Morar, Malika M ^a   Holohan, Dan ^a   Zhang, Ruan ^c   Turka, Laurence ^c   Marson, Alexander ^a,b   Bluestone, Jeffrey A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTOME; EZH2 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; POLYCOMB REPRESSIVE COMPLEX 2;

ADULT; ANIMAL CELL; ARTICLE; AUTOIMMUNITY; CELL LINEAGE; CONTROLLED STUDY; ENZYME INDUCTION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CD8+ T LYMPHOCYTE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CYTOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; PROMOTER REGION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD28; AUTOIMMUNITY; CD8-POSITIVE T-LYMPHOCYTES; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; HEPARIN-BINDING EGF-LIKE GROWTH FACTOR; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; T-LYMPHOCYTES, REGULATORY;

EID: 84922999148     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2015.01.007     Document Type: Article

References (48)

1. Agarwal S., Rao A. Modulation of chromatin structure regulates cytokine gene expression during Tcell differentiation. Immunity 1998, 9:765-775.
2. Ansel K.M., Lee D.U., Rao A. An epigenetic view of helper Tcell differentiation. Nat. Immunol. 2003, 4:616-623.
3. Arvey A., van der Veeken J., Samstein R.M., Feng Y., Stamatoyannopoulos J.A., Rudensky A.Y. Inflammation-induced repression of chromatin bound by the transcription factor Foxp3 in regulatory Tcells. Nat. Immunol. 2014, 15:580-587.
4. Bailey-Bucktrout S.L., Martinez-Llordella M., Zhou X., Anthony B., Rosenthal W., Luche H., Fehling H.J., Bluestone J.A. Self-antigen-driven activation induces instability of regulatory Tcells during an inflammatory autoimmune response. Immunity 2013, 39:949-962.
5. Bettelli E., Pagany M., Weiner H.L., Linington C., Sobel R.A., Kuchroo V.K. Myelin oligodendrocyte glycoprotein-specific Tcell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J.Exp. Med. 2003, 197:1073-1081.
6. Bird J.J., Brown D.R., Mullen A.C., Moskowitz N.H., Mahowald M.A., Sider J.R., Gajewski T.F., Wang C.R., Reiner S.L. Helper Tcell differentiation is controlled by the cell cycle. Immunity 1998, 9:229-237.
7. Campbell D.J., Koch M.A. Phenotypical and functional specialization of FOXP3+ regulatory Tcells. Nat. Rev. Immunol. 2011, 11:119-130.
8. Chang S., Aune T.M. Dynamic changes in histone-methylation 'marks' across the locus encoding interferon-gamma during the differentiation of T helper type 2 cells. Nat. Immunol. 2007, 8:723-731.
9. Darrasse-Jèze G., Deroubaix S., Mouquet H., Victora G.D., Eisenreich T., Yao K.H., Masilamani R.F., Dustin M.L., Rudensky A., Liu K., Nussenzweig M.C. Feedback control of regulatory Tcell homeostasis by dendritic cells invivo. J.Exp. Med. 2009, 206:1853-1862.
10. Fisson S., Darrasse-Jèze G., Litvinova E., Septier F., Klatzmann D., Liblau R., Salomon B.L. Continuous activation of autoreactive CD4+ CD25+ regulatory Tcells in the steady state. J.Exp. Med. 2003, 198:737-746.
11. Gavin M.A., Rasmussen J.P., Fontenot J.D., Vasta V., Manganiello V.C., Beavo J.A., Rudensky A.Y. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 2007, 445:771-775.
12. Grogan J.L., Mohrs M., Harmon B., Lacy D.A., Sedat J.W., Locksley R.M. Early transcription and silencing of cytokine genes underlie polarization of T helper cell subsets. Immunity 2001, 14:205-215.
13. Hill J.A., Feuerer M., Tash K., Haxhinasto S., Perez J., Melamed R., Mathis D., Benoist C. Foxp3 transcription-factor-dependent and -independent regulation of the regulatory Tcell transcriptional signature. Immunity 2007, 27:786-800.
14. Jacob E., Hod-Dvorai R., Schif-Zuck S., Avni O. Unconventional association of the polycomb group proteins with cytokine genes in differentiated T helper cells. J.Biol. Chem. 2008, 283:13471-13481.
15. Keerthivasan S., Aghajani K., Dose M., Molinero L., Khan M.W., Venkateswaran V., Weber C., Emmanuel A.O., Sun T., Bentrem D.J., et al. beta-Catenin promotes colitis and colon cancer through imprinting of proinflammatory properties in Tcells. Sci Transl Med 2014, 6:225ra228.
16. Kim J.M., Rasmussen J.P., Rudensky A.Y. Regulatory Tcells prevent catastrophic autoimmunity throughout the lifespan of mice. Nat. Immunol. 2007, 8:191-197.
17. Koyanagi M., Baguet A., Martens J., Margueron R., Jenuwein T., Bix M. EZH2 and histone 3 trimethyl lysine 27 associated with Il4 and Il13 gene silencing in Th1 cells. J.Biol. Chem. 2005, 280:31470-31477.
18. Lenschow D.J., Herold K.C., Rhee L., Patel B., Koons A., Qin H.Y., Fuchs E., Singh B., Thompson C.B., Bluestone J.A. CD28/B7 regulation of Th1 and Th2 subsets in the development of autoimmune diabetes. Immunity 1996, 5:285-293.
19. Mandal M., Powers S.E., Maienschein-Cline M., Bartom E.T., Hamel K.M., Kee B.L., Dinner A.R., Clark M.R. Epigenetic repression of the Igk locus by STAT5-mediated recruitment of the histone methyltransferase Ezh2. Nat. Immunol. 2011, 12:1212-1220.
20. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
21. Marson A., Kretschmer K., Frampton G.M., Jacobsen E.S., Polansky J.K., MacIsaac K.D., Levine S.S., Fraenkel E., von Boehmer H., Young R.A. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 2007, 445:931-935.
22. Martínez-Llordella M., Esensten J.H., Bailey-Bucktrout S.L., Lipsky R.H., Marini A., Chen J., Mughal M., Mattson M.P., Taub D.D., Bluestone J.A. CD28-inducible transcription factor DEC1 is required for efficient autoreactive CD4+ Tcell response. J.Exp. Med. 2013, 210:1603-1619.
23. Miyao T., Floess S., Setoguchi R., Luche H., Fehling H.J., Waldmann H., Huehn J., Hori S. Plasticity of Foxp3(+) Tcells reflects promiscuous Foxp3 expression in conventional Tcells but not reprogramming of regulatory Tcells. Immunity 2012, 36:262-275.
24. Morikawa H., Ohkura N., Vandenbon A., Itoh M., Nagao-Sato S., Kawaji H., Lassmann T., Carninci P., Hayashizaki Y., Forrest A.R., et al. Differential roles of epigenetic changes and Foxp3 expression in regulatory Tcell-specific transcriptional regulation. Proc. Natl. Acad. Sci. USA 2014, 111:5289-5294. FANTOM Consortium.
25. Ohkura N., Hamaguchi M., Morikawa H., Sugimura K., Tanaka A., Ito Y., Osaki M., Tanaka Y., Yamashita R., Nakano N., et al. T cell receptor stimulation-induced epigenetic changes and Foxp3 expression are independent and complementary events required for Treg cell development. Immunity 2012, 37:785-799.
26. + regulatory Tcells. Nat. Immunol. 2013, 14:959-965.
27. Raaphorst F.M., Otte A.P., van Kemenade F.J., Blokzijl T., Fieret E., Hamer K.M., Satijn D.P.E., Meijer C.J.L.M. Distinct BMI-1 and EZH2 expression patterns in thymocytes and mature Tcells suggest a role for Polycomb genes in human Tcell differentiation. J.Immunol. 2001, 166:5925-5934.
28. Rosenblum M.D., Gratz I.K., Paw J.S., Lee K., Marshak-Rothstein A., Abbas A.K. Response to self antigen imprints regulatory memory in tissues. Nature 2011, 480:538-542.
29. Rubtsov Y.P., Rasmussen J.P., Chi E.Y., Fontenot J., Castelli L., Ye X., Treuting P., Siewe L., Roers A., Henderson W.R., et al. Regulatory Tcell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008, 28:546-558.
30. Salomon B., Lenschow D.J., Rhee L., Ashourian N., Singh B., Sharpe A., Bluestone J.A. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory Tcells that control autoimmune diabetes. Immunity 2000, 12:431-440.
31. Samstein R.M., Arvey A., Josefowicz S.Z., Peng X., Reynolds A., Sandstrom R., Neph S., Sabo P., Kim J.M., Liao W., et al. Foxp3 exploits a pre-existent enhancer landscape for regulatory Tcell lineage specification. Cell 2012, 151:153-166.
32. Smigiel K.S., Richards E., Srivastava S., Thomas K.R., Dudda J.C., Klonowski K.D., Campbell D.J. CCR7 provides localized access to IL-2 and defines homeostatically distinct regulatory Tcell subsets. J.Exp. Med. 2014, 211:121-136.
33. Spivakov M., Fisher A.G. Epigenetic signatures of stem-cell identity. Nat. Rev. Genet. 2007, 8:263-271.
34. Su I.-H., Basavaraj A., Krutchinsky A.N., Hobert O., Ullrich A., Chait B.T., Tarakhovsky A. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 2003, 4:124-131.
35. Su I.-H., Dobenecker M.-W., Dickinson E., Oser M., Basavaraj A., Marqueron R., Viale A., Reinberg D., Wülfing C., Tarakhovsky A. Polycomb group protein ezh2 controls actin polymerization and cell signaling. Cell 2005, 121:425-436.
36. Tai X., Cowan M., Feigenbaum L., Singer A. CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory Tcell differentiation independently of interleukin 2. Nat. Immunol. 2005, 6:152-162.
37. Tang Q., Henriksen K.J., Boden E.K., Tooley A.J., Ye J., Subudhi S.K., Zheng X.X., Strom T.B., Bluestone J.A. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory Tcells. J.Immunol. 2003, 171:3348-3352.
38. Tumes D.J., Onodera A., Suzuki A., Shinoda K., Endo Y., Iwamura C., Hosokawa H., Koseki H., Tokoyoda K., Suzuki Y., et al. The polycomb protein Ezh2 regulates differentiation and plasticity of CD4(+) T helper type 1 and type 2 cells. Immunity 2013, 39:819-832.
39. Wei G., Wei L., Zhu J., Zang C., Hu-Li J., Yao Z., Cui K., Kanno Y., Roh T.-Y., Watford W.T., et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ Tcells. Immunity 2009, 30:155-167.
40. Weiss J.M., Bilate A.M., Gobert M., Ding Y., Curotto de Lafaille M.A., Parkhurst C.N., Xiong H., Dolpady J., Frey A.B., Ruocco M.G., et al. Neuropilin 1 is expressed on thymus-derived natural regulatory Tcells, but not mucosa-generated induced Foxp3+ T reg cells. J. Exp. Med. 2012, 209:1723-1742. S1721.
41. Wilson C.B., Rowell E., Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat. Rev. Immunol. 2009, 9:91-105.
42. Xiong Y., Khanna S., Grzenda A.L., Sarmento O.F., Svingen P.A., Lomberk G.A., Urrutia R.A., Faubion W.A. Polycomb antagonizes p300/CREB-binding protein-associated factor to silence FOXP3 in a Kruppel-like factor-dependent manner. J.Biol. Chem. 2012, 287:34372-34385.
43. Xu K., Wu Z.J., Groner A.C., He H.H., Cai C., Lis R.T., Wu X., Stack E.C., Loda M., Liu T., et al. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent. Science 2012, 338:1465-1469.
44. Yadav M., Louvet C., Davini D., Gardner J.M., Martinez-Llordella M., Bailey-Bucktrout S., Anthony B.A., Sverdrup F.M., Head R., Kuster D.J., et al. Neuropilin-1 distinguishes natural and inducible regulatory Tcells among regulatory Tcell subsets invivo. J. Exp. Med. 2012, 209:1713-1722. S1711-1719.
45. Zhang R., Huynh A., Whitcher G., Chang J., Maltzman J.S., Turka L.A. An obligate cell-intrinsic function for CD28 in Tregs. J.Clin. Invest. 2013, 123:580-593.
46. Zhang Y., Kinkel S., Maksimovic J., Bandala-Sanchez E., Tanzer M.C., Naselli G., Zhang J.G., Zhan Y., Lew A.M., Silke J., et al. The polycomb repressive complex 2 governs life and death of peripheral Tcells. Blood 2014, 124:737-749.
47. Zhou X., Jeker L.T., Fife B.T., Zhu S., Anderson M.S., McManus M.T., Bluestone J.A. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J.Exp. Med. 2008, 205:1983-1991.
48. Zhou X., Bailey-Bucktrout S.L., Jeker L.T., Penaranda C., Martínez-Llordella M., Ashby M., Nakayama M., Rosenthal W., Bluestone J.A. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory Tcells invivo. Nat. Immunol. 2009, 10:1000-1007.