The histone methyltransferase Ezh2 is a crucial epigenetic regulator of allogeneic T-cell responses mediating graft-versus-host disease

Blood

Volumn 122, Issue 25, 2013, Pages 4119-4128

  He, Shan ^a   Xie, Fang ^a   Liu, Yongnian ^a   Tong, Qing ^a   Mochizuki, Kazuhiro ^a   Lapinski, Philip E ^a   Mani, Ram Shankar ^a   Reddy, Pavan ^a   Mochizuki, Izumi ^a   Chinnaiyan, Arul M ^a   Mineishi, Shin ^b   King, Philip D ^a   Zhang, Yi ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; MINOR HISTOCOMPATIBILITY ANTIGEN; STAT4 PROTEIN; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR T BET; APOPTOSIS REGULATORY PROTEIN; BCL 2 LIKE PROTEIN 11; BCL-2-LIKE PROTEIN 11; EZH2 PROTEIN, MOUSE; MEMBRANE PROTEIN; ONCOPROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; STAT4 PROTEIN, MOUSE; T BOX TRANSCRIPTION FACTOR; T BOX TRANSCRIPTION FACTOR TBX21; T-BOX TRANSCRIPTION FACTOR TBX21;

ALLOGENIC BONE MARROW TRANSPLANTATION; ALLOIMMUNITY; ALLOREACTIVE T CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; EFFECTOR CELL; ENZYME ACTIVITY; EPIGENETICS; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; HISTOCOMPATIBILITY; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; THYMOCYTE; ALLOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW TRANSPLANTATION; ENZYMOLOGY; GENETIC EPIGENESIS; GENETICS; KNOCKOUT MOUSE; METABOLISM; METHYLATION; PATHOLOGY;

ALLOGRAFTS; ANIMALS; APOPTOSIS REGULATORY PROTEINS; BONE MARROW TRANSPLANTATION; EPIGENESIS, GENETIC; GRAFT VS HOST DISEASE; MEMBRANE PROTEINS; METHYLATION; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; POLYCOMB REPRESSIVE COMPLEX 2; PROTO-ONCOGENE PROTEINS; STAT4 TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTES;

EID: 84893482395     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-05-505180     Document Type: Article

References (50)

1. Blazar BR, Murphy WJ, Abedi M. Advances in graft-versus-host disease biology and therapy. Nat Rev Immunol. 2012;12(6):443-458.
2. Ferrara JL, Levine JE, Reddy P, Holler E. Graftversus-host disease. Lancet. 2009;373(9674): 1550-1561.
3. Kolb HJ. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood. 2008;112(12):4371-4383.
4. Wu CJ, Ritz J. Induction of tumor immunity following allogeneic stem cell transplantation. Adv Immunol. 2006;90:133-173.
5. Ho VT, Soiffer RJ. The history and future of T-cell depletion as graft-versus-host disease prophylaxis for allogeneic hematopoietic stem cell transplantation. Blood. 2001;98(12):3192-3204.
6. Shlomchik WD. Graft-versus-host disease. Nat Rev Immunol. 2007;7(5):340-352.
7. van den Brink MR, Burakoff SJ. Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol. 2002;2(4): 273-281.
8. Wilson CB, Rowell E, Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol. 2009;9(2):91-105.
9. He S, Tong Q, Bishop DK, Zhang Y. Histone methyltransferase and histone methylation in inflammatory T-cell responses. Immunotherapy. 2013;5(9):989-1004.
10. He S, Wang J, Kato K, et al. Inhibition of histone methylation arrests ongoing graft-versus-host disease in mice by selectively inducing apoptosis of alloreactive effector T cells. Blood. 2012; 119(5):1274-1282.
11. Miranda TB, Cortez CC, Yoo CB, et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol Cancer Ther. 2009;8(6): 1579-1588.
12. Tan J, Yang X, Zhuang L, et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev. 2007;21(9): 1050-1063.
13. Badeaux AI, Shi Y. Emerging roles for chromatin as a signal integration and storage platform. Nat Rev Mol Cell Biol. 2013;14(4):211-224.
14. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011; 469(7330):343-349.
15. Kamminga LM, Bystrykh LV, de Boer A, et al. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood. 2006; 107(5):2170-2179.
16. Su IH, Dobenecker MW, Dickinson E, et al. Polycomb group protein ezh2 controls actin polymerization and cell signaling. Cell. 2005; 121(3):425-436.
17. Su IH, Basavaraj A, Krutchinsky AN, et al. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat Immunol. 2003;4(2):124-131.
18. Kato K, Cui S, Kuick R, et al. Identification of stem cell transcriptional programs normally expressed in embryonic and neural stem cells in alloreactive CD81 T cells mediating graft-versus-host disease. Biol Blood Marrow Transplant. 2010; 16(6):751-771.
19. Shono Y, Ueha S, Wang Y, et al. Bone marrow graft-versus-host disease: early destruction of hematopoietic niche after MHC-mismatched hematopoietic stem cell transplantation. Blood. 2010;115(26):5401-5411.
20. Na IK, Lu SX, Yim NL, et al. The cytolytic molecules Fas ligand and TRAIL are required for murine thymic graft-versus-host disease. J Clin Invest. 2010;120(1):343-356.
21. Suchin EJ, Langmuir PB, Palmer E, Sayegh MH, Wells AD, Turka LA. Quantifying the frequency of alloreactive T cells in vivo: new answers to an old question. J Immunol. 2001;166(2):973-981.
22. Jameson SC. Maintaining the norm: T-cell homeostasis. Nat Rev Immunol. 2002;2(8): 547-556.
23. Edinger M, Hoffmann P, Ermann J, et al. CD41 CD251 regulatory T cells preserve graft-versustumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9(9):1144-1150.
24. Agarwal P, Raghavan A, Nandiwada SL, et al. Gene regulation and chromatin remodeling by IL-12 and type I IFN in programming for CD8 T cell effector function and memory. J Immunol. 2009; 183(3):1695-1704.
25. Bouillet P, O'Reilly LA. CD95, BIM and T cell homeostasis. Nat Rev Immunol. 2009;9(7): 514-519.
26. Tripathi P, Koss B, Opferman JT, Hildeman DA. Mcl-1 antagonizes Bax/Bak to promote effector CD4(1) and CD8(1) T-cell responses. Cell Death Differ. 2013;20(8):998-1007.
27. 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(19):13471-13481.
28. 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(36): 31470-31477.
29. Burman AC, Banovic T, Kuns RD, et al. IFNgamma differentially controls the development of idiopathic pneumonia syndrome and GVHD of the gastrointestinal tract. Blood. 2007;110(3): 1064-1072.
30. Yi T, Chen Y, Wang L, et al. Reciprocal differentiation and tissue-specific pathogenesis of Th1, Th2, and Th17 cells in graft-versus-host disease. Blood. 2009;114(14):3101-3112.
31. Zhu J, Yamane H, Paul WE. Differentiation of effector CD4 T cell populations (∗). Annu Rev Immunol. 2010;28:445-489.
32. Berger M, Wettstein PJ, Korngold R. T cell subsets involved in lethal graft-versus-host disease directed to immunodominant minor histocompatibility antigens. Transplantation. 1994;57(7):1095-1102.
33. Zhang Y, Joe G, Hexner E, Zhu J, Emerson SG. Alloreactive memory T cells are responsible for the persistence of graft-versus-host disease. J Immunol. 2005;174(5):3051-3058.
34. Choi EY, Christianson GJ, Yoshimura Y, et al. Real-time T-cell profiling identifies H60 as a major minor histocompatibility antigen in murine graftversus-host disease. Blood. 2002;100(13): 4259-4265.
35. De Carvalho DD, Sharma S, You JS, et al. DNA methylation screening identifies driver epigenetic events of cancer cell survival. Cancer Cell. 2012; 21(5):655-667.
36. Choi J, Ritchey J, Prior JL, et al. In vivo administration of hypomethylating agents mitigate graft-versus-host disease without sacrificing graftversus-leukemia. Blood. 2010;116(1):129-139.
37. Sánchez-Abarca LI, Gutierrez-Cosio S, Santamaría C, et al. Immunomodulatory effect of 5-azacytidine (5-azaC): potential role in the transplantation setting. Blood. 2010;115(1): 107-121.
38. Reddy P, Maeda Y, Hotary K, et al. Histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces acute graft-versus-host disease and preserves graft-versus-leukemia effect. Proc Natl Acad Sci USA. 2004;101(11):3921-3926.
39. Choi S, Reddy P. HDAC inhibition and graft versus host disease. Mol Med. 2011;17(5-6): 404-416.
40. Reddy P, Sun Y, Toubai T, et al. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest. 2008;118(7):2562-2573.
41. Coulombe RA Jr, Sharma RP, Huggins JW. Pharmacokinetics of the antiviral agent 3-deazaneplanocin A. Eur J Drug Metab Pharmacokinet. 1995;20(3):197-202.
42. Zhang Y, Sandy AR, Wang J, et al. Notch signaling is a critical regulator of allogeneic CD41 T-cell responses mediating graft-versus-host disease. Blood. 2011;117(1):299-308.
43. Valenzuela JO, Iclozan C, Hossain MS, et al. PKCtheta is required for alloreactivity and GVHD but not for immune responses toward leukemia and infection in mice. J Clin Invest. 2009;119(12): 3774-3786.
44. Mochizuki K, Xie F, He S, et al. Delta-like ligand 4 identifies a previously uncharacterized population of inflammatory dendritic cells that plays important roles in eliciting allogeneic T cell responses in mice. J Immunol. 2013;190(7):3772-3782.
45. Tran IT, Sandy AR, Carulli AJ, et al. Blockade of individual Notch ligands and receptors controls graft-versus-host disease. J Clin Invest. 2013; 123(4):1590-1604.
46. Chao N. Control of GVHD: it's in our DNA! Blood. 2012;119(5):1102-1103.
47. Konze KD, Ma A, Li F, et al. An Orally Bioavailable Chemical Probe of the Lysine Methyltransferases EZH2 and EZH1. ACS Chem Biol. 2013. [Epub ahead of print]
48. McCabe MT, Ott HM, Ganji G, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. 2012; 492(7427):108-112.
49. Knutson SK, Wigle TJ, Warholic NM, et al. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat Chem Biol. 2012;8(11):890-896.
50. Qi W, Chan H, Teng L, et al. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc Natl Acad Sci USA. 2012; 109(52):21360-21365.