EZH2 in normal and malignant hematopoiesis

Leukemia

Volumn 28, Issue 1, 2014, Pages 44-49

  Lund, K ^a   Adams, P D ^a   Copland, M ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

cancer stem cell; EZH2; EZH2 inhibitors; hematopoiesis; lymphoma

Indexed keywords

HISTONE DEACETYLASE INHIBITOR; TRANSCRIPTION FACTOR EZH2;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; CANCER CHEMOTHERAPY; CANCER STEM CELL; CELL FATE; ENZYME INHIBITION; EPIGENETICS; GAIN OF FUNCTION MUTATION; GENE REPRESSION; HEMATOLOGIC MALIGNANCY; HEMATOPOIESIS; HUMAN; LARGE CELL LYMPHOMA; LOSS OF FUNCTION MUTATION; MIXED MYELODYSPLASTIC MYELOPROLIFERATIVE DISEASE; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; TRANSCRIPTION REGULATION;

EPIGENESIS, GENETIC; HEMATOLOGIC NEOPLASMS; HEMATOPOIESIS; HUMANS; POINT MUTATION; POLYCOMB REPRESSIVE COMPLEX 2; STEM CELLS;

EID: 84891854229     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.288     Document Type: Review

References (60)

1. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000; 403: 41-45. (Pubitemid 30038513)
2. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P et al. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002; 298: 1039-1043. (Pubitemid 35247314)
3. Zhou J, Bi C, Cheong LL, Mahara S, Liu SC, Tay KG et al. The histone methyltransferase inhibitor, DZNep, up-regulates TXNIP, increases ROS production, and targets leukemia cells in AML. Blood 2011; 118: 2830-2839.
4. Miranda TB, Cortez CC, Yoo CB, Liang G, Abe M, Kelly TK et al. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol Cancer Ther 2009; 8: 1579-1588.
5. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL et al. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 2007; 21: 1050-1063. (Pubitemid 46686474)
6. Fiskus W, Wang Y, Sreekumar A, Buckley KM, Shi H, Jillella 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: 2733-2743.
7. Knutson SK, Wigle TJ, Warholic NM, Sneeringer CJ, Allain CJ, Klaus CR et al. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Nat Chem Biol 2012; 8: 890-896.
8. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature 2012; 492: 108-112.
9. Francis NJ, Kingston RE, Woodcock CL. Chromatin compaction by a polycomb group protein complex. Science 2004; 306: 1574-1577. (Pubitemid 39564957)
10. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439: 871-874. (Pubitemid 43255707)
11. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS et al. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004; 431: 873-878. (Pubitemid 39434086)
12. 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: 1123-1136.
13. Chou RH, Yu YL, Hung MC. The roles of EZH2 in cell lineage commitment. Am J Transl Res 2011; 3: 243-250.
14. de Haan G, Gerrits A. Epigenetic control of hematopoietic stem cell aging-The case of Ezh2. Ann NY Acad Sci 2007; 1106: 233-239. (Pubitemid 47443044)
15. Kamminga LM, Bystrykh LV, de Boer A, Houwer S, Douma J, Weersing E et al. The Polycomb group gene Ezh2 prevents hematopoietic stem cell exhaustion. Blood 2006; 107: 2170-2179. (Pubitemid 43289403)
16. Ezhkova E, Pasolli HA, Parker JS, Stokes N, Su IH, Hannon G et al. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 2009; 136: 1122-1135.
17. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. Embo J 2003; 22: 5323-5335. (Pubitemid 37279943)
18. Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730-737. (Pubitemid 27298715)
19. Dolnik A, Engelmann JC, Scharfenberger-Schmeer M, Mauch J, Kelkenberg-Schade S, Haldemann B et al. Commonly altered genomic regions in acute myeloid leukemia are enriched for somatic mutations involved in chromatin remodeling and splicing. Blood 2012; 120: e83-e92.
20. Khan SN, Jankowska AM, Mahfouz R, Dunbar AJ, Sugimoto Y, Hosono N et al. Multiple mechanisms deregulate EZH2 and histone H3 lysine 27 epigenetic changes in myeloid malignancies. Leukemia 2013; 27: 1301-1309.
21. Thiel AT, Feng Z, Pant DK, Chodosh LA, Hua X. The trithorax protein partner menin acts in tandem with EZH2 to suppress C/EBPalpha and differentiation in MLL-AF9 leukemia. Haematologica 2013; 98: 918-927.
22. Velichutina I, Shaknovich R, Geng H, Johnson NA, Gascoyne RD, Melnick AM et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood 2010; 116: 5247-5255.
23. van Vlerken LE, Kiefer CM, Morehouse C, Li Y, Groves C, Wilson SD et al. EZH2 is required for breast and pancreatic cancer stem cell maintenance and can be used as a functional cancer stem cell reporter. Stem Cells Transl Med 2013; 2: 43-52.
24. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C et al. Epigenetic stem cell signature in cancer. Nat Genet 2007; 39: 157-158. (Pubitemid 46184343)
25. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 2007; 39: 232-236. (Pubitemid 46184355)
26. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet 2007; 39: 237-242. (Pubitemid 46184356)
27. O'Hagan HM, Wang W, Sen S, Destefano Shields C, Lee SS, Zhang YW et al. Oxidative damage targets complexes containing DNA methyltransferases, SIRT1, and polycomb members to promoter CpG Islands. Cancer Cell 2011; 20: 606-619.
28. Kaur M, Cole MD. MYC acts via the PTEN tumor suppressor to elicit autoregulation and genome-wide gene repression by activation of the Ezh2 methyltransferase. Cancer Res 2013; 73: 695-705.
29. Zhang X, Zhao X, Fiskus W, Lin J, Lwin T, Rao R et al. Coordinated silencing of MYC-mediated miR-29 by HDAC3 and EZH2 as a therapeutic target of histone modification in aggressive B-Cell lymphomas. Cancer Cell 2012; 22: 506-523.
30. Varambally S, Cao Q, Mani RS, Shankar S, Wang X, Ateeq B et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 2008; 322: 1695-1699.
31. Guo Y, Ying L, Tian Y, Yang P, Zhu Y, Wang Z et al. miR-144 downregulation increases bladder cancer cell proliferation by targeting EZH2 and regulating Wnt signaling. FEBS J 2013; 280: 4531-4538.
32. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002; 419: 624-629.
33. Kleer CG, Cao Q, Varambally S, Shen RL, Ota L, Tomlins SA et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003; 100: 11606-11611. (Pubitemid 37205983)
34. Ren G, Baritaki S, Marathe H, Feng J, Park S, Beach S et al. Polycomb protein EZH2 regulates tumor invasion via the transcriptional repression of the metastasis suppressor RKIP in breast and prostate cancer. Cancer Res 2012; 72: 3091-3104.
35. Raaphorst FM, van Kemenade FJ, Blokzijl T, Fieret E, Hamer KM, Satijn DP et al. Coexpression of BMI-1 and EZH2 polycomb group genes in Reed-Sternberg cells of Hodgkin's disease. Am J Pathol 2000; 157: 709-715. (Pubitemid 32109362)
36. Visser HP, Gunster MJ, Kluin-Nelemans HC, Manders EM, Raaphorst FM, Meijer CJ et al. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol 2001; 112: 950-958. (Pubitemid 32322920)
37. Morin RD, Johnson NA, Severson TM, Mungall AJ, An J, Goya R et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet 2010; 42: 181-185.
38. Sasaki D, Imaizumi Y, Hasegawa H, Osaka A, Tsukasaki K, Choi YL et al. Overexpression of Enhancer of zeste homolog 2 with trimethylation of lysine 27 on histone H3 in adult T-cell leukemia/lymphoma as a target for epigenetic therapy. Haematologica 2011; 96: 712-719.
39. Sneeringer CJ, Scott MP, Kuntz KW, Knutson SK, Pollock RM, Richon VM et al. Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. Proc Natl Acad Sci USA 2010; 107: 20980-20985.
40. Beguelin W, Popovic R, Teater M, Jiang Y, Bunting KL, Rosen M et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell 2013; 23: 677-692.
41. Grubach L, Juhl-Christensen C, Rethmeier A, Olesen LH, Aggerholm A, Hokland P et al. Gene expression profiling of Polycomb, Hox and Meis genes in patients with acute myeloid leukaemia. Eur J Haematol 2008; 81: 112-122. (Pubitemid 352022720)
42. Xu F, Li X, Wu L, Zhang Q, Yang R, Yang Y et al. Overexpression of the EZH2, RING1 and BMI1 genes is common in myelodysplastic syndromes: relation to adverse epigenetic alteration and poor prognostic scoring. Ann Hematol 2011; 90: 643-653.
43. Herrera-Merchan A, Arranz L, Ligos JM, de Molina A, Dominguez O, Gonzalez S. Ectopic expression of the histone methyltransferase Ezh2 in haematopoietic stem cells causes myeloproliferative disease. Nat Commun 2012; 3: 623.
44. Tanaka S, Miyagi S, Sashida G, Chiba T, Yuan J, Mochizuki-Kashio M et al. Ezh2 augments leukemogenecity by reinforcing differentiation blockage in acute myeloid leukemia. Blood 2012; 120: 1107-1117.
45. Abdel-Wahab O, Adli M, LaFave LM, Gao J, Hricik T, Shih AH et al. ASXL1 mutations promote myeloid transformation through loss of PRC2-mediated gene repression. Cancer Cell 2012; 22: 180-193.
46. Ernst T, Chase AJ, Score J, Hidalgo-Curtis CE, Bryant C, Jones AV et al. Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders. Nat Genet 2010; 42: 722-726.
47. Nikoloski G, Langemeijer SM, Kuiper RP, Knops R, Massop M, Tonnissen ER et al. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat Genet 2010; 42: 665-667.
48. Guglielmelli P, Biamonte F, Score J, Hidalgo-Curtis C, Cervantes F, Maffioli M et al. EZH2 mutational status predicts poor survival in myelofibrosis. Blood 2011; 118: 5227-5234.
49. Ntziachristos P, Tsirigos A, Van Vlierberghe P, Nedjic J, Trimarchi T, Flaherty MS et al. Genetic inactivation of the polycomb repressive complex 2 in T cell acute lymphoblastic leukemia. Nat Med 2012; 18: 298-301.
50. Simon C, Chagraoui J, Krosl J, Gendron P, Wilhelm B, Lemieux S et al. A key role for EZH2 and associated genes in mouse and human adult T-cell acute leukemia. Genes Dev 2012; 26: 651-656.
51. Mochizuki-Kashio M, Mishima Y, Miyagi S, Negishi M, Saraya A, Konuma T et al. Dependency on the polycomb gene Ezh2 distinguishes fetal from adult hematopoietic stem cells. Blood 2011; 118: 6553-6561.
52. Gore SD, Baylin S, Sugar E, Carraway H, Miller CB, Carducci M et al. Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer Res 2006; 66: 6361-6369.
53. He S, Wang J, Kato K, Xie F, Varambally S, Mineishi S 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: 1274-1282.
54. Zhao X, Lwin T, Zhang X, Huang A, Wang J, Marquez VE et al. Disruption of the MYC-miRNA-EZH2 loop to suppress aggressive B-cell lymphoma survival and clonogenicity. Leukemia 2013; 27: 2341-2350.
55. Qi W, Chan H, Teng L, Li L, Chuai S, Zhang R et al. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proc Natl Acad Sci USA 2012; 109(): 21360-21365.
56. Ryan RJ, Nitta M, Borger D, Zukerberg LR, Ferry JA, Harris NL et al. EZH2 codon 641 mutations are common in BCL2-rearranged germinal center B cell lymphomas. PLoS One 2011; 6: e28585.
57. Zhou L, Ruvolo VR, McQueen T, Chen W, Samudio IJ, Conneely O et al. HDAC inhibition by SNDX-275 (Entinostat) restores expression of silenced leukemiaassociated transcription factors Nur77 and Nor1 and of key pro-apoptotic proteins in AML. Leukemia 2013; 27: 1358-1368.
58. Horton SJ, Huntly BJ. Recent advances in acute myeloid leukemia stem cell biology. Haematologica 2012; 97: 966-974.
59. Ozbalak M, Cetiner M, Bekoz H, Atesoglu EB, Ar C, Salihoglu A et al. Azacitidine has limited activity in 'real life' patients with MDS and AML: a single centre experience. Hematol Oncol 2012; 30: 76-81.
60. Craddock C, Quek L, Goardon N, Freeman S, Siddique S, Raghavan M et al. Azacitidine fails to eradicate leukemic stem/progenitor cell populations in patients with acute myeloid leukemia and myelodysplasia. Leukemia 2013; 27: 1028-1036.