Polycomb repressive complex’s evolutionary conserved function: the role of EZH2 status and cellular background

Clinical Epigenetics

Volumn 8, Issue 1, 2016, Pages

  Gall Trošelj, Koraljka ^a   Novak Kujundzic, Renata ^a   Ugarkovic, Djurdjica ^a  

^a RUDER BO KOVI INSTITUTE   (Croatia)

Author keywords

Cancer; Evolution; EZH2; H3K27me3; Mutation; Polycomb repressive complexes 1 4

Indexed keywords

HISTONE H3; ISOPROTEIN; MESSENGER RNA; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG; EZH2 PROTEIN, HUMAN; HISTONE; POLYCOMB REPRESSIVE COMPLEX 2;

AMINO ACID SEQUENCE; CELLS; EPIGENETICS; GENE MUTATION; GERMLINE MUTATION; HISTONE METHYLATION; HUMAN; MOLECULAR EVOLUTION; MOLECULARLY TARGETED THERAPY; MUTATIONAL ANALYSIS; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SOMATIC MUTATION; SYNDROME; WEAVER SYNDROME; GENETIC EPIGENESIS; GENETICS; METABOLISM; MUTATION;

ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; MUTATION; NEOPLASMS; POLYCOMB REPRESSIVE COMPLEX 2;

EID: 84973879207     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-016-0226-1     Document Type: Review

References (69)

1. Sims RJ, Reinberg D. Is there a code embedded in proteins that is based on post translational modifications? Nat Rev Mol Cell Biol. 2008;9:815.
2. Sarma K, Margueron R, Ivanov A, Pirrotta V, Reinberg D. Ezh2 requires PHF1 to efficiently catalyze H3 lysine 27 trimethylation in vivo. Mol Cell Biol. 2008;28:2718.
3. Prezioso C, Orlando V. Polycomb proteins in mammalian cell differentiation and plasticity. FEBS Lett. 2011;585:2067.
4. Grossniklaus U, Paro R. Transcriptional silencing by Polycomb-Group proteins. Cold Spring Harb Perspect Biol. 2014;6:a019331.
5. Lewis EB. A gene complex controlling segmentation in Drosophila. Nature. 1978;276:565.
6. Whitcomb SJ, Basu A, Allis CD, Bernstein E. Polycomb group proteins: An evolutionary perspective. Trends Genet. 2007;23:494.
7. Shaver S, Casas-Mollano JA, Cerny RL, Cerutti H. Origin of the polycomb repressive complex 2 and gene silencing by an E(z) homolog in the unicellular alga Chlamydomonas. Epigenetics. 2010;5:301.
8. Dumesic PA, Homer CM, Moresco JJ, Pack LR, Shanle EK, Coyle SM, et al. Product binding enforces the genomic specificity of a yeast polycomb repressive complex. Cell. 2015;160:204.
9. Tschiersch B, Hofmann A, Krauss V, Dorn R, Korge G, Reuter G. The protein encoded by the Drosophila position-effect variegation suppressor gene Su(var)3-9 combines domains of antagonistic regulators of homeotic gene complexes. EMBO J. 1994;13:3822.
10. Strome S, Kelly WG, Ercan S, Lieb JD. Regulation of the X chromosomes in C. elegans. Cold Spring Harb Perspect Biol. 2014;6:a018366.
11. Baulcombe DC, Dean C. Epigenetic regulation in plant responses to the environment. Cold Spring Harb Perspect Biol. 2014;6:a019471.
12. Deb G, Singh AK, Gupta S. EZH2: not EZHY (easy) to deal. Mol Cancer Res. 2014;12:639.
13. Kuzmichev A, Jenuwein T, Tempst P, Reinberg D. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell. 2004;14:183.
14. Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, Kirmizis A, et al. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci U S A. 2005;102:1859.
15. Landeira D, Sauer S, Poot R, Dvorkina M, Mazzarella L, Jørgensen HF, et al. Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA Polymerase II to developmental regulators. Nat Cell Biol. 2010;12:618.
16. Pasini D, Malatesta M, Jung HR, Walfridsson J, Willer A, Olsson L, et al. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 2010;38:4958.
17. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011;469:343.
18. Kim H, Kang K, Kim J. AEBP2 as a potential targeting protein for Polycomb Repression Complex PRC2. Nucleic Acids Res. 2009;37:2940.
19. Li G, Margueron R, Ku M, Chambon P, Bernstein BE, Reinberg D. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 2010;24:368.
20. Song J-J, Garlick JD, Kingston RE. Structural basis of histone H4 recognition by p55. Genes Dev. 2008;22:1313.
21. Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ, et al. Role of the polycomb protein EED in the propagation of repressive histone marks. Nature. 2009;461:762.
22. Brockdorff N, Turner B. Dosage compensation in mammals. Cold Spring Harb Perspect Biol. 2015;7:a019406.
23. Swiezewski S, Liu F, Magusin A, Dean C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature. 2009;462:799.
24. Chen WM, Huang MD, Sun DP, Kong R, Xu TP, Xia R, et al. Long intergenic non-coding RNA 00152 promotes tumor cell cycle progression by binding to EZH2 and repressing p15 and p21 in gastric cancer. Oncotarget. 2016. doi:10.18632/oncotarget.6949.
25. Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon YH, Sung ZR, et al. Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development. 2004;131:5263.
26. Weaver DD, Graham CB, Thomas IT, Smith DW. A new overgrowth syndrome with accelerated skeletal maturation, unusual facies, and camptodactyly. J Pediatr. 1974;84:547.
27. Tatton-Brown K, Murray A, Hanks S, Douglas J, Armstrong R, Banka S, et al. Weaver syndrome and EZH2 mutations: Clarifying the clinical phenotype. Am J Med Genet A. 2013;161A:2972.
28. Hobert O, Jallal B, Ullrich A. Interaction of Vav with ENX-1, a putative transcriptional regulator of homeobox gene expression. Mol Cell Biol. 1996;16:3066.
29. 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.
30. 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.
31. Hodis E, Watson IR, Kryukov GV, Arold ST, Imielinski M, Theurillat JP, et al. A landscape of driver mutations in melanoma. Cell. 2012;150:251.
32. McCabe MT, Graves AP, Ganji G, Diaz E, Halsey WS, Jiang Y, et al. Mutation of A677 in histone methyltransferase EZH2 in human B-cell lymphoma promotes hypertrimethylation of histone H3 on lysine 27 (H3K27). Proc Natl Acad Sci U S A. 2012;109:2989.
33. Majer CR, Jin L, Scott MP, Knutson SK, Kuntz KW, Keilhack H, et al. A687V EZH2 is a gain-of-function mutation found in lymphoma patients. FEBS Lett. 2012;586:3448.
34. 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 U S A. 2010;107:20980.
35. Fujikawa D, Nakagawa S, Hori M, Kurokawa N, Soejima A, Nakano K, et al: Polycomb-dependent epigenetic landscape in adult T-cell leukemia. Blood. 2016, doi:10.1182/blood-2015-08-662593.
36. Tsang DP, Wu WK, Kang W, Lee YY, Wu F, Yu Z, et al: Yin Yang 1-mediated epigenetic silencing of tumour-suppressive microRNAs activates nuclear factor-κB in hepatocellular carcinoma. J Pathol. 2016, doi:10.1002/path.4688.
37. Pan X, Papasani M, Hao Y, Calamito M, Wei F, Quinn Iii WJ, et al. YY1 controls Igκ repertoire and B cell development, and localizes with condensin on the Igκ locus. EMBO J. 2013;32:1168.
38. Zhang Q, Padi SK, Tindall DJ, Guo B. Polycomb protein EZH2 suppresses apoptosis by silencing the proapoptotic miR-31. Cell Death Dis. 2014;5:e1486.
39. Popovic R, Martinez-Garcia E, Giannopoulou EG, Zhang Q, Zhang Q, Ezponda T, et al. Histone methyltransferase MMSET/NSD2 alters EZH2 binding and reprograms the myeloma epigenome through global and focal changes in H3K36 and H3K27 methylation. PLoS Genet. 2014;10:e1004566.
40. Agarwal P, Alzrigat M, Párraga AA, Enroth S, Singh U, Ungerstedt J, et al. Genome-wide profiling of histone H3 lysine 27 and lysine 4 trimethylation in multiple myeloma reveals the importance of Polycomb gene targeting and highlights EZH2 as a potential therapeutic target. Oncotarget. 2016. doi:10.18632/oncotarget.6843.
41. Hernando H, Gelato KA, Lesche R, Beckmann G, Koehr S, Otto S, et al. EZH2 inhibition blocks multiple myeloma cell growth through upregulation of epithelial tumor suppressor genes. Mol Cancer Ther. 2016;15:287.
42. 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.
43. Mochizuki-Kashio M, Aoyama K, Sashida G, Oshima M, Tomioka T, Muto T, et al. Ezh2 loss in hematopoietic stem cells predisposes mice to develop heterogeneous malignancies in an Ezh1-dependent manner. Blood. 2015;126:1172.
44. Wassef M, Rodilla V, Teissandier A, Zeitouni B, Gruel N, Sadacca B, et al: Impaired PRC2 activity promotes transcriptional instability and favors breast tumorigenesis. Genes Dev. 2015 (in press, doi: 10.1101/gad.269522.115).
45. Coyle D, Friedmacher F, Puri P. The association between Hirschsprung’s disease and multiple endocrine neoplasia type 2a: a systematic review. Pediatr Surg Int. 2014;30:751.
46. Grzenda A, Lomberk G, Svingen P, Mathison A, Calvo E, Iovanna J, et al. Functional characterization of EZH2β reveals the increased complexity of EZH2 isoforms involved in the regulation of mammalian gene expression. Epigenetics Chromatin. 2013;6:3.
47. Wojtuszkiewicz A, Assaraf YG, Maas MJ, Kaspers GJ, Jansen G, Cloos J. Pre-mRNA splicing in cancer: the relevance in oncogenesis, treatment and drug resistance. Expert Opin Drug Metab Toxicol. 2015;11:673.
48. Novak Kujundžić R, Grbeša I, Ivkić M, Krušlin B, Konjevoda P, Gall Trošelj K. Possible prognostic value of BORIS transcript variants ratio in laryngeal squamous cell carcinomas - a pilot study. Pathol Oncol Res. 2014;20:687.
49. Lee ST, Li Z, Wu Z, Aau M, Guan P, Karuturi RK, et al. Context-specific regulation of NF-κB target gene expression by EZH2 in breast cancers. Mol Cell. 2011;43:798.
50. Yan M, Zhang Y, He B, Xiang J, Wang ZF, Zheng FM, et al. IKKα restoration via EZH2 suppression induces nasopharyngeal carcinoma differentiation. Nat Commun. 2014;5:3661.
51. Xin Y, Lu Q, Li Q. IKK1 control of epidermal differentiation is modulated by notch signaling. Am J Pathol. 2011;178:1568.
52. Kim KH, Kim W, Howard TP, Vazquez F, Tsherniak A, Wu JN, et al. SWI/SNF-mutant cancers depend on catalytic and non-catalytic activity of EZH2. Nat Med. 2015;21:1491.
53. Wei Y, Chen YH, Li LY, Lang J, Yeh SP, Shi B, et al. CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nat Cell Biol. 2011;13:87.
54. Riquelme E, Behrens C, Lin HY, Simon G, Papadimitrakopoulou V, Izzo J, et al. Modulation of EZH2 expression by MEK-ERK or PI3K-AKT signaling in lung cancer is dictated by different KRAS oncogene mutations. Cancer Res. 2016;76:675.
55. Kim E, Kim M, Woo DH, Shin Y, Shin J, Chang N, et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell. 2013;23:839.
56. Serresi M, Gargiulo G, Proost N, Siteur B, Cesaroni M, Koppens M, et al. Polycomb Repressive Complex 2 is a barrier to KRAS-driven inflammation and Epithelial-Mesenchymal transition in non-small-cell lung cancer. Cancer Cell. 2016;29:17.
57. Oshima M, Hasegawa N, Mochizuki-Kashio M, Muto T, Miyagi S, Koide S, et al. Ezh2 regulates the Lin28/let-7 pathway to restrict activation of fetal gene signature in adult hematopoietic stem cells. Exp Hematol. 2016. doi:10.1016/j.exphem.2015.12.009.
58. Beachy SH, Onozawa M, Chung YJ, Slape C, Bilke S, Francis P, et al. Enforced expression of Lin28b leads to impaired T-cell development, release of inflammatory cytokines, and peripheral T-cell lymphoma. Blood. 2012;120:1048.
59. Zhao E, Maj T, Kryczek I, Li W, Wu K, Zhao L, et al. Cancer mediates effector T cell dysfunction by targeting microRNAs and EZH2 via glycolysis restriction. Nat Immunol. 2016;17:95.
60. Holm K, Grabau D, Lövgren K, Aradottir S, Gruvberger-Saal S, Howlin J, et al. Global H3K27 trimethylation and EZH2 abundance in breast tumor subtypes. Mol Oncol. 2012;6:494.
61. Palma G, Frasci G, Chirico A, Esposito E, Siani C, Saturnino C, et al. Triple negative breast cancer: looking for the missing link between biology and treatments. Oncotarget. 2015;6:26560.
62. Bae WK, Yoo KH, Lee JS, Kim Y, Chung IJ, Park MH, et al. The methyltransferase EZH2 is not required for mammary cancer development, although high EZH2 and low H3K27me3 correlate with poor prognosis of ER-positive breast cancers. Mol Carcinog. 2015;54:1172.
63. Wei Y, Xia W, Zhang Z, Liu J, Wang H, Adsay NV, et al. Loss of trimethylation at lysine 27 of histone H3 is a predictor of poor outcome in breast, ovarian, and pancreatic cancers. Mol Carcinog. 2008;47:701e706.
64. Chen X, Song N, Matsumoto K, Nanashima A, Nagayasu T, Hayashi T, et al. High expression of trimethylated histone H3 at lysine 27 predicts better prognosis in non-small cell lung cancer. Int J Oncol. 2013;43:1467.
65. Yang YA, Yu J. EZH2, an epigenetic driver of prostate cancer. Protein Cell. 2013;4:331.
66. Shakhova O. Neural crest stem cells in melanoma development. Curr Opin Oncol. 2014;26:215.
67. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, Haukaas SA, et al. 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.
68. Zingg D, Debbache J, Schaefer SM, Tuncer E, Frommel SC, Cheng PL, et al. The epigenetic modifier EZH2 controls melanoma growth and metastasis through silencing of distinct tumour suppressors. Nat Commun. 2015;6:6051.
69. Morera L, Lübbert M, Jung M. Targeting histone methyltransferases and demethylases in clinical trials for cancer therapy. Clin Epig, Review Series "Epigenetic drugs- from chemistry via biology to medicine and back" (in press).