Inhibition of histone methylation arrests ongoing graft-versus-host disease in mice by selectively inducing apoptosis of alloreactive effector T cells

Blood

Volumn 119, Issue 5, 2012, Pages 1274-1282

  He, Shan ^a   Wang, Jina ^a,b   Kato, Koji ^a   Xie, Fang ^a   Varambally, Sooryanarayana ^a   Mineishi, Shin ^a   Kuick, Rork ^c   Mochizuki, Kazuhiro ^a   Liu, Yongnian ^a   Nieves, Evelyn ^a   Mani, Ram Shankar ^a   Chinnaiyan, Arul M ^a   Marquez, Victor E ^d   Zhang, Yi ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b FUDAN UNIVERSITY   (China)

^c UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 DEAZANEPLANOCIN A; ALLOANTIGEN; BIM PROTEIN; HISTONE H3; HISTONE METHYLTRANSFERASE; INTERLEUKIN 2; INTERLEUKIN 7; LYSINE; TRANSCRIPTION FACTOR EZH2;

ACUTE GRAFT VERSUS HOST DISEASE; ALLOGENIC BONE MARROW TRANSPLANTATION; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; GENE REPRESSION; HEMATOPOIESIS; HISTONE METHYLATION; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 84863012446     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-06-364422     Document Type: Article

References (49)

1. Wu CJ, Ritz J. Induction of tumor immunity following allogeneic stem cell transplantation. Adv Immunol. 2006;90:133-173. (Pubitemid 43765800)
2. Ferrara JL, Levine JE, Reddy P, Holler E. Graft-versus-host disease. Lancet. 2009;373(9674):1550-1561.
3. Goker H, Haznedaroglu IC, Chao NJ. Acute graft-vs-host disease: pathobiology and management. Exp Hematol. 2001;29(3):259-277. (Pubitemid 32223460)
4. Blazar BR, Murphy WJ. Bone marrow transplantation and approaches to avoid graft-versus-host disease (GVHD). Philos Trans R Soc Lond B Biol Sci. 2005;360(1461):1747-1767. (Pubitemid 43997823)
5. Cuddapah S, Barski A, Zhao K. Epigenomics of T cell activation, differentiation, and memory. Curr Opin Immunol. 2010;22(3):341-347.
6. Wilson CB, Rowell E, Sekimata M. Epigenetic control of T-helper-cell differentiation. Nat Rev Immunol. 2009;9(2):91-105.
7. Hublitz P, Albert M, Peters AH. Mechanisms of transcriptional repression by histone lysine methylation. Int J Dev Biol. 2009;53(2-3):335-354.
8. Wu JI, Lessard J, Crabtree GR. Understanding the words of chromatin regulation. Cell. 2009;136(2):200-206.
9. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693-705. (Pubitemid 46273577)
10. Kelly TK, De Carvalho DD, Jones PA. Epigenetic modifications as therapeutic targets. Nat Biotechnol. 2010;28(10):1069-1078.
11. Araki K, Turner AP, Shaffer VO, et al. mTOR regulates memory CD8 T-cell differentiation. Nature. 2009;460(7251):108-112.
12. Wei G, Wei L, Zhu J, et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity. 2009;30(1):155-167.
13. Choi J, Ritchey J, Prior JL, et al. In vivo administration of hypomethylating agents mitigate graft-versus-host disease without sacrificing graft-versus-leukemia. Blood. 2010;116(1):129-139.
14. Sanchez-Abarca LI, Gutierrez-Cosio S, Santamaria C, et al. Immunomodulatory effect of 5-azacytidine (5-azaC): potential role in the transplantation setting. Blood. 2010;115(1):107-121.
15. Leng C, Gries M, Ziegler J, et al. Reduction of graft-versus-host disease by histone deacetylase inhibitor suberonylanilide hydroxamic acid is associated with modulation of inflammatory cytokine milieu and involves inhibition of STAT1. Exp Hematol. 2006;34(6):776-787. (Pubitemid 43737091)
16. Li N, Zhao D, Kirschbaum M, et al. HDAC inhibitor reduces cytokine storm and facilitates induction of chimerism that reverses lupus in anti-CD3 conditioning regimen. Proc Natl Acad Sci U S A. 2008;105(12):4796-4801. (Pubitemid 351753826)
17. 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 U S A. 2004;101(11):3921-3926. (Pubitemid 38381078)
18. 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.
19. 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. (Pubitemid 46686474)
20. Glazer RI, Hartman KD, Knode MC, et al. 3-Deazaneplanocin: a new and potent inhibitor of S-adenosylhomocysteine hydrolase and its effects on human promyelocytic leukemia cell line HL-60. Biochem Biophys Res Commun. 1986;135(2):688-694. (Pubitemid 16049461)
21. De Clercq E, Cools M, Balzarini J, et al. Broad-spectrum antiviral activities of neplanocin A, 3-deazaneplanocin A, and their 5′-nor derivatives. Antimicrob Agents Chemother. 1989;33(8):1291-1297. (Pubitemid 19191974)
22. Fiskus W, Wang Y, Sreekumar A, et al. Combined epigenetic therapy with the histone methyltransferase EZH2 inhibitor 3-deazaneplanocin A and the histone deacetylase inhibitor panobinostat against human AML cells. Blood. 2009;114(13):2733-2743.
23. Cao R, Wang L, Wang H, et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science. 2002;298(5595):1039-1043. (Pubitemid 35247314)
24. Kato K, Cui S, Kuick R, et al. Identification of stem cell transcriptional programs normally expressed in embryonic and neural stem cells in alloreactive CD8(+) T cells mediating graft-versus-host disease. Biol Blood Marrow Transplant. 2010;16(6):751-771.
25. Zhang Y, Joe G, Hexner E, Zhu J, Emerson SG. Host-reactive CD8+ memory stem cells in graft-versus-host disease. Nat Med. 2005;11(12):1299-1305. (Pubitemid 41752910)
26. Zakrzewski JL, Kochman AA, Lu SX, et al. Adoptive transfer of T-cell precursors enhances T-cell reconstitution after allogeneic hematopoietic stem cell transplantation. Nat Med. 2006;12(9):1039-1047. (Pubitemid 44353385)
27. Cooke KR, Kobzik L, Martin TR, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation, I: the roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-3239. (Pubitemid 26357409)
28. Anderson BE, McNiff JM, Jain D, Blazar BR, Shlomchik WD, Shlomchik MJ. Distinct roles for donor- and host-derived antigen-presenting cells and costimulatory molecules in murine chronic graft-versus-host disease: requirements depend on target organ. Blood. 2005;105(5):2227-2234. (Pubitemid 40731817)
29. Zhang Y, Sandy AR, Wang J, et al. Notch signaling is a critical regulator of allogeneic CD4+ T cell responses mediating graft-versus-host disease. Blood. 2011;117(1):299-308.
30. 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. (Pubitemid 32060253)
31. Duriez PJ, Shah GM. Cleavage of poly(ADP-ribose) polymerase: a sensitive parameter to study cell death. Biochem Cell Biol. 1997;75(4):337-349. (Pubitemid 127733184)
32. Bouillet P, O'Reilly LA. CD95, BIM and T cell homeostasis. Nat Rev Immunol. 2009;9(7):514-519.
33. Pearce EL, Mullen AC, Martins GA, et al. Control of effector CD8+ T cell function by the transcription factor Eomesodermin. Science. 2003;302(5647):1041- 1043. (Pubitemid 37386196)
34. Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell. 2000;100(6):655-669.
35. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006;20(9):1123-1136.
36. Fujii S, Ito K, Ito Y, Ochiai A. Enhancer of zeste homologue 2 (EZH2) down-regulates RUNX3 by increasing histone H3 methylation. J Biol Chem. 2008;283(25):17324-17332.
37. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011;469(7330):343-349.
38. Gattinoni L, Klebanoff CA, Palmer DC, et al. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J Clin Invest. 2005;115(6):1616-1626. (Pubitemid 40814670)
39. Aractingi S, Chosidow O. Cutaneous graft-versus-host disease. Arch Dermatol. 1998;134(5):602-612. (Pubitemid 28222313)
40. Yamashita K, Choi U, Woltz PC, et al. Severe chronic graft-versus-host disease is characterized by a preponderance of CD4(+) effector memory cells relative to central memory cells. Blood. 2004;103(10):3986-3988. (Pubitemid 38596324)
41. Ellis L, Atadja PW, Johnstone RW. Epigenetics in cancer: targeting chromatin modifications. Mol Cancer Ther. 2009;8(6):1409-1420.
42. Crea F, Hurt EM, Mathews LA, et al. Pharmacologic disruption of Polycomb Repressive Complex 2 inhibits tumorigenicity and tumor progression in prostate cancer. Mol Cancer. 2011;10:40.
43. Rao M, Chinnasamy N, Hong JA, et al. Inhibition of histone lysine methylation enhances cancer-testis antigen expression in lung cancer cells: implications for adoptive immunotherapy of cancer. Cancer Res. 2011;71(12):4192-4204.
44. 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. Jul 2008;118(7):2562-2573. (Pubitemid 351949783)
45. Suva ML, Riggi N, Janiszewska M, et al. EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res. 2009;69(24):9211-9218.
46. van den Brink MR, Burakoff SJ. Cytolytic pathways in haematopoietic stem-cell transplantation. Nat Rev Immunol. 2002;2(4):273-281. (Pubitemid 37323227)
47. 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.
48. 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.
49. Snoeck R, Andrei G, Neyts J, et al. Inhibitory activity of S-adenosylhomocysteine hydrolase inhibitors against human cytomegalovirus replication. Antiviral Res. 1993;21(3):197-216. (Pubitemid 23188003)