Characterization of the EZH2-MMSET Histone Methyltransferase Regulatory Axis in Cancer

Molecular Cell

Volumn 49, Issue 1, 2013, Pages 80-93

  Asangani, Irfan A ^a   Ateeq, Bushra ^a   Cao, Qi ^a   Dodson, Lois ^a   Pandhi, Mithil ^a   Kunju, Lakshmi P ^a   Mehra, Rohit ^a   Lonigro, Robert J ^a   Siddiqui, Javed ^a   Palanisamy, Nallasivam ^a   Wu, Yi Mi ^a   Cao, Xuhong ^a   Kim, Jung H ^a   Zhao, Meng ^c   Qin, Zhaohui S ^c   Iyer, Mathew K ^a,b   Maher, Christopher A ^a,b   Kumar Sinha, Chandan ^a   Varambally, Sooryanarayana ^a   Chinnaiyan, Arul M ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE METHYLTRANSFERASE;

ARTICLE; CARCINOGENESIS; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MULTIPLE MYELOMA; MULTIPLE MYELOMA SET DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION;

3' UNTRANSLATED REGIONS; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; GENE EXPRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; HUMANS; MALE; MICE; MICE, INBRED BALB C; MICE, NUDE; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM TRANSPLANTATION; POLYCOMB REPRESSIVE COMPLEX 2; PROSTATIC NEOPLASMS; REPRESSOR PROTEINS; RNA INTERFERENCE; TISSUE ARRAY ANALYSIS; TRANSCRIPTIONAL ACTIVATION;

EID: 84872269688     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.10.008     Document Type: Article

References (55)

1. Albert M., Helin K. Histone methyltransferases in cancer. Semin. Cell Dev. Biol. 2010, 21:209-220.
2. Bachmann I.M., Halvorsen O.J., Collett K., Stefansson I.M., Straume O., Haukaas S.A., Salvesen H.B., Otte A.P., Akslen L.A. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J. Clin. Oncol. 2006, 24:268-273.
3. Baylin S.B., Jones P.A. A decade of exploring the cancer epigenome - biological and translational implications. Nat. Rev. Cancer 2011, 11:726-734.
4. Berezovska O.P., Glinskii A.B., Yang Z., Li X.M., Hoffman R.M., Glinsky G.V. Essential role for activation of the Polycomb group (PcG) protein chromatin silencing pathway in metastatic prostate cancer. Cell Cycle 2006, 5:1886-1901.
5. Bracken A.P., Kleine-Kohlbrecher D., Dietrich N., Pasini D., Gargiulo G., Beekman C., Theilgaard-Mönch K., Minucci S., Porse B.T., Marine J.C., et al. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes Dev. 2007, 21:525-530.
6. Brito J.L., Walker B., Jenner M., Dickens N.J., Brown N.J., Ross F.M., Avramidou A., Irving J.A., Gonzalez D., Davies F.E., Morgan G.J. MMSET deregulation affects cell cycle progression and adhesion regulons in t(4;14) myeloma plasma cells. Haematologica 2009, 94:78-86.
7. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
8. Cao Q., Yu J., Dhanasekaran S.M., Kim J.H., Mani R.S., Tomlins S.A., Mehra R., Laxman B., Cao X., Yu J., et al. Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene 2008, 27:7274-7284.
9. Cao Q., Mani R.S., Ateeq B., Dhanasekaran S.M., Asangani I.A., Prensner J.R., Kim J.H., Brenner J.C., Jing X., Cao X., et al. Coordinated regulation of polycomb group complexes through microRNAs in cancer. Cancer Cell 2011, 20:187-199.
10. Chase A., Cross N.C. Aberrations of EZH2 in cancer. Clin. Cancer Res. 2011, 17:2613-2618.
11. Cheng A.S., Lau S.S., Chen Y., Kondo Y., Li M.S., Feng H., Ching A.K., Cheung K.F., Wong H.K., Tong J.H., et al. EZH2-mediated concordant repression of Wnt antagonists promotes β-catenin-dependent hepatocarcinogenesis. Cancer Res. 2011, 71:4028-4039.
12. Chesi M., Nardini E., Lim R.S., Smith K.D., Kuehl W.M., Bergsagel P.L. The t(4;14) translocation in myeloma dysregulates both FGFR3 and a novel gene, MMSET, resulting in IgH/MMSET hybrid transcripts. Blood 1998, 92:3025-3034.
13. Crea F., Paolicchi E., Marquez V.E., Danesi R. Polycomb genes and cancer: time for clinical application?. Crit. Rev. Oncol. Hematol. 2012, 83:184-193.
14. Creasy, C.L., McCabe, M.T., Korenchuk, S., Diaz, E., Ott, H., Thompson, C.S., Ganji, G., Gorman, S.A., LaFrance, L.V., Brandt, M., et al. (2012). A novel selective EZH2 inhibitor exhibits anti-tumor activity in lymphoma with EZH2 activating mutations Paper presented at: American Association for Cancer Research Annual Conference (Chicago, AACR).
15. Ernst T., Chase A.J., Score J., Hidalgo-Curtis C.E., Bryant C., Jones A.V., Waghorn K., Zoi K., Ross F.M., Reiter A., et al. Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders. Nat. Genet. 2010, 42:722-726.
16. Friedman J.M., Liang G., Liu C.C., Wolff E.M., Tsai Y.C., Ye W., Zhou X., Jones P.A. The putative tumor suppressor microRNA-101 modulates the cancer epigenome by repressing the polycomb group protein EZH2. Cancer Res. 2009, 69:2623-2629.
17. Gong Y., Huo L., Liu P., Sneige N., Sun X., Ueno N.T., Lucci A., Buchholz T.A., Valero V., Cristofanilli M. Polycomb group protein EZH2 is frequently expressed in inflammatory breast cancer and is predictive of worse clinical outcome. Cancer 2011, 117:5476-5484.
18. Herrera-Merchan A., Arranz L., Ligos J.M., 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.
19. Hudlebusch H.R., Santoni-Rugiu E., Simon R., Ralfkiær E., Rossing H.H., Johansen J.V., Jørgensen M., Sauter G., Helin K. The histone methyltransferase and putative oncoprotein MMSET is overexpressed in a large variety of human tumors. Clin. Cancer Res. 2011, 17:2919-2933.
20. Jaju R.J., Fidler C., Haas O.A., Strickson A.J., Watkins F., Clark K., Cross N.C., Cheng J.F., Aplan P.D., Kearney L., et al. A novel gene, NSD1, is fused to NUP98 in the t(5;11)(q35;p15.5) in de novo childhood acute myeloid leukemia. Blood 2001, 98:1264-1267.
21. Jiao Y., Shi C., Edil B.H., de Wilde R.F., Klimstra D.S., Maitra A., Schulick R.D., Tang L.H., Wolfgang C.L., Choti M.A., et al. DAXX/ATRX, MEN1, and mTOR pathway genes are frequently altered in pancreatic neuroendocrine tumors. Science 2011, 331:1199-1203.
22. Jones P.A., Baylin S.B. The epigenomics of cancer. Cell 2007, 128:683-692.
23. Kassambara A., Klein B., Moreaux J. MMSET is overexpressed in cancers: link with tumor aggressiveness. Biochem. Biophys. Res. Commun. 2009, 379:840-845.
24. Kleer C.G., Cao Q., Varambally S., Shen R., Ota I., Tomlins S.A., Ghosh D., Sewalt R.G., Otte A.P., Hayes D.F., 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.
25. Kondo Y., Shen L., Cheng A.S., Ahmed S., Boumber Y., Charo C., Yamochi T., Urano T., Furukawa K., Kwabi-Addo B., et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat. Genet. 2008, 40:741-750.
26. Kotake Y., Cao R., Viatour P., Sage J., Zhang Y., Xiong Y. pRB family proteins are required for H3K27 trimethylation and Polycomb repression complexes binding to and silencing p16INK4alpha tumor suppressor gene. Genes Dev. 2007, 21:49-54.
27. Krivtsov A.V., Armstrong S.A. MLL translocations, histone modifications and leukaemia stem-cell development. Nat. Rev. Cancer 2007, 7:823-833.
28. Kuo A.J., Cheung P., Chen K., Zee B.M., Kioi M., Lauring J., Xi Y., Park B.H., Shi X., Garcia B.A., et al. NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming. Mol. Cell 2011, 44:609-620.
29. Lauring J., Abukhdeir A.M., Konishi H., Garay J.P., Gustin J.P., Wang Q., Arceci R.J., Matsui W., Park B.H. The multiple myeloma associated MMSET gene contributes to cellular adhesion, clonogenic growth, and tumorigenicity. Blood 2008, 111:856-864.
30. Lawson D.A., Xin L., Lukacs R.U., Cheng D., Witte O.N. Isolation and functional characterization of murine prostate stem cells. Proc. Natl. Acad. Sci. USA 2007, 104:181-186.
31. Li Y., Trojer P., Xu C.F., Cheung P., Kuo A., Drury W.J., Qiao Q., Neubert T.A., Xu R.M., Gozani O., Reinberg D. The target of the NSD family of histone lysine methyltransferases depends on the nature of the substrate. J. Biol. Chem. 2009, 284:34283-34295.
32. Lu C., Han H.D., Mangala L.S., Ali-Fehmi R., Newton C.S., Ozbun L., Armaiz-Pena G.N., Hu W., Stone R.L., Munkarah A., et al. Regulation of tumor angiogenesis by EZH2. Cancer Cell 2010, 18:185-197.
33. Margueron R., Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011, 469:343-349.
34. Martinez-Garcia E., Popovic R., Min D.J., Sweet S.M., Thomas P.M., Zamdborg L., Heffner A., Will C., Lamy L., Staudt L.M., et al. The MMSET histone methyl transferase switches global histone methylation and alters gene expression in t(4;14) multiple myeloma cells. Blood 2011, 117:211-220.
35. Min J., Zaslavsky A., Fedele G., McLaughlin S.K., Reczek E.E., De Raedt T., Guney I., Strochlic D.E., Macconaill L.E., Beroukhim R., et al. An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-kappaB. Nat. Med. 2010, 16:286-294.
36. Morin R.D., Johnson N.A., Severson T.M., Mungall A.J., An J., Goya R., Paul J.E., Boyle M., Woolcock B.W., Kuchenbauer F., 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.
37. Nguyen A.T., Zhang Y. The diverse functions of Dot1 and H3K79 methylation. Genes Dev. 2011, 25:1345-1358.
38. Nikoloski G., Langemeijer S.M., Kuiper R.P., Knops R., Massop M., Tönnissen E.R., van der Heijden A., Scheele T.N., Vandenberghe P., de Witte T., et al. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat. Genet. 2010, 42:665-667.
39. Ram O., Goren A., Amit I., Shoresh N., Yosef N., Ernst J., Kellis M., Gymrek M., Issner R., Coyne M., et al. Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 2011, 147:1628-1639.
40. Richter G.H., Plehm S., Fasan A., Rössler S., Unland R., Bennani-Baiti I.M., Hotfilder M., Löwel D., von Luettichau I., Mossbrugger I., et al. EZH2 is a mediator of EWS/FLI1 driven tumor growth and metastasis blocking endothelial and neuro-ectodermal differentiation. Proc. Natl. Acad. Sci. USA 2009, 106:5324-5329.
41. Sander S., Bullinger L., Klapproth K., Fiedler K., Kestler H.A., Barth T.F., Möller P., Stilgenbauer S., Pollack J.R., Wirth T. MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood 2008, 112:4202-4212.
42. Santra M., Zhan F., Tian E., Barlogie B., Shaughnessy J. A subset of multiple myeloma harboring the t(4;14)(p16;q32) translocation lacks FGFR3 expression but maintains an IGH/MMSET fusion transcript. Blood 2003, 101:2374-2376.
43. Seligson D.B., Horvath S., Shi T., Yu H., Tze S., Grunstein M., Kurdistani S.K. Global histone modification patterns predict risk of prostate cancer recurrence. Nature 2005, 435:1262-1266.
44. Spannhoff A., Sippl W., Jung M. Cancer treatment of the future: inhibitors of histone methyltransferases. Int. J. Biochem. Cell Biol. 2009, 41:4-11.
45. Stec I., Wright T.J., van Ommen G.J., de Boer P.A., van Haeringen A., Moorman A.F., Altherr M.R., den Dunnen J.T. WHSC1, a 90 kb SET domain-containing gene, expressed in early development and homologous to a Drosophila dysmorphy gene maps in the Wolf-Hirschhorn syndrome critical region and is fused to IgH in t(4;14) multiple myeloma. Hum. Mol. Genet. 1998, 7:1071-1082.
46. Takeshita F., Minakuchi Y., Nagahara S., Honma K., Sasaki H., Hirai K., Teratani T., Namatame N., Yamamoto Y., Hanai K., et al. Efficient delivery of small interfering RNA to bone-metastatic tumors by using atelocollagen in vivo. Proc. Natl. Acad. Sci. USA 2005, 102:12177-12182.
47. Tan J., Yang X., Zhuang L., Jiang X., Chen W., Lee P.L., Karuturi R.K., Tan P.B., Liu E.T., Yu Q. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev. 2007, 21:1050-1063.
48. Varambally S., Dhanasekaran S.M., Zhou M., Barrette T.R., Kumar-Sinha C., Sanda M.G., Ghosh D., Pienta K.J., Sewalt R.G., Otte A.P., et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002, 419:624-629.
49. Varambally S., Cao Q., Mani R.S., Shankar S., Wang X., Ateeq B., Laxman B., Cao X., Jing X., Ramnarayanan K., et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science 2008, 322:1695-1699.
50. Varela I., Tarpey P., Raine K., Huang D., Ong C.K., Stephens P., Davies H., Jones D., Lin M.L., Teague J., et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 2011, 469:539-542.
51. Wagner E.J., Carpenter P.B. Understanding the language of Lys36 methylation at histone H3. Nat. Rev. Mol. Cell Biol. 2012, 13:115-126.
52. Yamada A., Fujii S., Daiko H., Nishimura M., Chiba T., Ochiai A. Aberrant expression of EZH2 is associated with a poor outcome and P53 alteration in squamous cell carcinoma of the esophagus. Int. J. Oncol. 2011, 38:345-353.
53. Yamagishi M., Nakano K., Miyake A., Yamochi T., Kagami Y., Tsutsumi A., Matsuda Y., Sato-Otsubo A., Muto S., Utsunomiya A., et al. Polycomb-mediated loss of miR-31 activates NIK-dependent NF-κB pathway in adult T cell leukemia and other cancers. Cancer Cell 2012, 21:121-135.
54. Yu J., Cao Q., Mehra R., Laxman B., Yu J., Tomlins S.A., Creighton C.J., Dhanasekaran S.M., Shen R., Chen G., et al. Integrative genomics analysis reveals silencing of beta-adrenergic signaling by polycomb in prostate cancer. Cancer Cell 2007, 12:419-431.
55. Zhang J., Ding L., Holmfeldt L., Wu G., Heatley S.L., Payne-Turner D., Easton J., Chen X., Wang J., Rusch M., et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 2012, 481:157-163.