Polycomb genes, miRNA, and their deregulation in B-cell malignancies

Blood

Volumn 125, Issue 8, 2015, Pages 1217-1225

  Wang, Gang Greg ^a   Konze, Kyle D ^b   Tao, Jianguo ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BMI1 PROTEIN; MICRORNA; POLYCOMB GROUP PROTEIN; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN; PROTEIN CBX7; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG;

B CELL LYMPHOMA; B LYMPHOCYTE; B LYMPHOCYTE DIFFERENTIATION; CARCINOGENESIS; CELL MATURATION; CHROMOSOME TRANSLOCATION; EPIGENETICS; GAIN OF FUNCTION MUTATION; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; HUMAN; MALIGNANT TRANSFORMATION; NONHUMAN; ONCOGENE C MYC; PRIORITY JOURNAL; REVIEW; SOMATIC MUTATION; CELL DIFFERENTIATION; CELL TRANSFORMATION; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; PATHOLOGY; PHYSIOLOGY;

B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LYMPHOMA, B-CELL; MICRORNAS; POLYCOMB-GROUP PROTEINS;

EID: 84923351501     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-10-606822     Document Type: Review

References (100)

1. Chi P, Allis CD, Wang GG. Covalent histone modifications-miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer. 2010;10(7):457-469.
2. Arrowsmith CH, Bountra C, Fish PV, Lee K, Schapira M. Epigenetic protein families: a new frontier for drug discovery. Nat Rev Drug Discov. 2012;11(5):384-400.
3. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, Part I: Covalent histone modifications. Trends Mol Med. 2007;13(9): 363-372.
4. Morin RD, Johnson NA, Severson TM, et al. Somatic mutations altering EZH2 (Tyr641) in follicular and diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. 2010;42(2): 181-185.
5. Morin RD, Mendez-Lago M, Mungall AJ, et al. Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature. 2011; 476(7360):298-303.
6. Okosun J, Bödör C, Wang J, et al. Integrated genomic analysis identifies recurrent mutations and evolution patterns driving the initiation and progression of follicular lymphoma. Nat Genet. 2014;46(2):176-181.
7. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011; 469(7330):343-349.
8. Di Croce L, Helin K. Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol. 2013;20(10):1147-1155.
9. Cai L, Rothbart SB, Lu R, et al. An H3K36 methylation-engaging Tudor motif of polycomblike proteins mediates PRC2 complex targeting. Mol Cell. 2013;49(3):571-582.
10. Tavares L, Dimitrova E, Oxley D, et al. RYBPPRC1 complexes mediate H2A ubiquitylation at polycomb target sites independently of PRC2 and H3K27me3. Cell. 2012;148(4):664-678.
11. Leeb M, Pasini D, Novatchkova M, Jaritz M, Helin K, Wutz A. Polycomb complexes act redundantly to repress genomic repeats and genes. Genes Dev. 2010;24(3):265-276.
12. Cooper S, Dienstbier M, Hassan R, et al. Targeting polycomb to pericentric heterochromatin in embryonic stem cells reveals a role for H2AK119u1 in PRC2 recruitment. Cell Reports. 2014;7(5):1456-1470.
13. Blackledge NP, Farcas AM, Kondo T, et al. Variant PRC1 complex-dependent H2A ubiquitylation drives PRC2 recruitment and polycomb domain formation. Cell. 2014;157(6): 1445-1459.
14. Kalb R, Latwiel S, Baymaz HI, et al. Histone H2A monoubiquitination promotes histone H3 methylation in Polycomb repression. Nat Struct Mol Biol. 2014;21(6):569-571.
15. Cao Q, Wang X, Zhao M, et al. The central role of EED in the orchestration of polycomb group complexes. Nat Commun. 2014;5:3127.
16. Bracken AP, Helin K. Polycomb group proteins: navigators of lineage pathways led astray in cancer. Nat Rev Cancer. 2009;9(11):773-784.
17. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell. 2007; 128(4):735-745.
18. van Lohuizen M, Verbeek S, Scheijen B, Wientjens E, van der Gulden H, Berns A. Identification of cooperating oncogenes in E mu-myc transgenic mice by provirus tagging. Cell. 1991;65(5):737-752.
19. Sneeringer CJ, Scott MP, Kuntz KW, 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(49):20980-20985.
20. Yap DB, Chu J, Berg T, et al. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood. 2011;117(8):2451-2459.
21. Klein U, Dalla-Favera R. Germinal centres: role in B-cell physiology and malignancy. Nat Rev Immunol. 2008;8(1):22-33.
22. Wang GG, Allis CD, Chi P. Chromatin remodeling and cancer, Part II: ATP-dependent chromatin remodeling. Trends Mol Med. 2007; 13(9):373-380.
23. Schmidt A, Küppers R. Role of microRNAs in B cell leukemias and lymphomas. Curr Mol Med. 2014;14(5):580-597.
24. Raaphorst FM, van Kemenade FJ, Fieret E, et al. Cutting edge: polycomb gene expression patterns reflect distinct B cell differentiation stages in human germinal centers. J Immunol. 2000;164(1):1-4.
25. Raaphorst FM, Otte AP, van Kemenade FJ, et al. Distinct BMI-1 and EZH2 expression patterns in thymocytes and mature T cells suggest a role for Polycomb genes in human T cell differentiation. J Immunol. 2001;166(10): 5925-5934.
26. van Galen JC, Dukers DF, Giroth C, et al. Distinct expression patterns of polycomb oncoproteins and their binding partners during the germinal center reaction. Eur J Immunol. 2004;34(7):1870-1881.
27. van Kemenade FJ, Raaphorst FM, Blokzijl T, et al. Coexpression of BMI-1 and EZH2 polycomb-group proteins is associated with cycling cells and degree of malignancy in B-cell non-Hodgkin lymphoma. Blood. 2001;97(12): 3896-3901.
28. Visser HP, Gunster MJ, Kluin-Nelemans HC, et al. The Polycomb group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol. 2001; 112(4):950-958.
29. Oguro H, Yuan J, Ichikawa H, et al. Poised lineage specification in multipotential hematopoietic stem and progenitor cells by the polycomb protein Bmi1. Cell Stem Cell. 2010; 6(3):279-286.
30. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Mycinduced apoptosis via INK4a/ARF. Genes Dev. 1999;13(20):2678-2690.
31. Yamashita M, Kuwahara M, Suzuki A, et al. Bmi1 regulates memory CD4 T cell survival via repression of the Noxa gene. J Exp Med. 2008; 205(5):1109-1120.
32. Jagani Z, Wiederschain D, Loo A, et al. The Polycomb group protein Bmi-1 is essential for the growth of multiple myeloma cells. Cancer Res. 2010;70(13):5528-5538.
33. Abd Al Kader L, Oka T, Takata K, et al. In aggressive variants of non-Hodgkin lymphomas, Ezh2 is strongly expressed and polycomb repressive complex PRC1.4 dominates over PRC1.2. Virchows Arch. 2013;463(5):697-711.
34. van Galen JC, Muris JJ, Oudejans JJ, et al. Expression of the polycomb-group gene BMI1 is related to an unfavourable prognosis in primary nodal DLBCL. J Clin Pathol. 2007;60(2): 167-172.
35. Rouhigharabaei L, Ferreiro JF, Put N, et al. BMI1, the polycomb-group gene, is recurrently targeted by genomic rearrangements in progressive B-cell leukemia/lymphoma. Genes Chromosomes Cancer. 2013;52(10):928-944.
36. Glinsky GV, Berezovska O, Glinskii AB. Microarray analysis identifies a death-fromcancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest. 2005;115(6):1503-1521.
37. Lessard J, Sauvageau G. Bmi-1 determines the proliferative capacity of normal and leukaemic stem cells. Nature. 2003;423(6937):255-260.
38. Park IK, Qian D, Kiel M, et al. Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature. 2003; 423(6937):302-305.
39. Scott CL, Gil J, Hernando E, et al. Role of the chromobox protein CBX7 in lymphomagenesis. Proc Natl Acad Sci USA. 2007;104(13): 5389-5394.
40. Wang SS, Menashe I, Cerhan JR, et al. Variations in chromosomes 9 and 6p21.3 with risk of non-Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev. 2011;20(1):42-49.
41. Sánchez-Beato M, Sánchez E, González-Carreró J, et al. Variability in the expression of polycomb proteins in different normal and tumoral tissues. A pilot study using tissue microarrays. Mod Pathol. 2006;19(5):684-694.
42. Calés C, Román-Trufero M, Pavón L, et al. Inactivation of the polycomb group protein Ring1B unveils an antiproliferative role in hematopoietic cell expansion and cooperation with tumorigenesis associated with Ink4a deletion. Mol Cell Biol. 2008;28(3):1018-1028.
43. Shih AH, Abdel-Wahab O, Patel JP, Levine RL. The role of mutations in epigenetic regulators in myeloid malignancies. Nat Rev Cancer. 2012; 12(9):599-612.
44. Simon C, Chagraoui J, Krosl J, et al. A key role for EZH2 and associated genes in mouse and human adult T-cell acute leukemia. Genes Dev. 2012;26(7):651-656.
45. Ntziachristos P, Tsirigos A, Van Vlierberghe P, et al. Genetic inactivation of the polycomb repressive complex 2 in T cell acute lymphoblastic leukemia. Nat Med. 2012;18(2): 298-301.
46. 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.
47. Caganova M, Carrisi C, Varano G, et al. Germinal center dysregulation by histone methyltransferase EZH2 promotes lymphomagenesis. J Clin Invest. 2013;123(12): 5009-5022.
48. Martín-Pérez D, Sánchez E, Maestre L, et al. Deregulated expression of the polycomb-group protein SUZ12 target genes characterizes mantle cell lymphoma. Am J Pathol. 2010; 177(2):930-942.
49. Bödör C, Grossmann V, Popov N, et al. EZH2 mutations are frequent and represent an early event in follicular lymphoma. Blood. 2013; 122(18):3165-3168.
50. Swalm BM, Knutson SK, Warholic NM, et al. Reaction coupling between wild-type and disease-associated mutant EZH2. ACS Chem Biol. 2014;9(11):2459-2464.
51. Barski A, Cuddapah S, Cui K, et al. Highresolution profiling of histone methylations in the human genome. Cell. 2007;129(4):823-837.
52. Majer CR, Jin L, Scott MP, et al. A687V EZH2 is a gain-of-function mutation found in lymphoma patients. FEBS Lett. 2012;586(19):3448-3451.
53. McCabe MT, Graves AP, Ganji G, 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 USA. 2012;109(8): 2989-2994.
54. Ott HM, Graves AP, Pappalardi MB, et al. A687V EZH2 Is a Driver of Histone H3 Lysine 27 (H3K27) Hypertrimethylation. Mol Cancer Ther. 2014;13(12):3062-3073.
55. Sahasrabuddhe AA, Chen X, Chung F, Velusamy T, Lim MS, Elenitoba-Johnson KS. Oncogenic Y641 mutations in EZH2 prevent Jak2/b-TrCP-mediated degradation [published online ahead of print January 27, 2014]. Oncogene.
56. Béguelin W, Popovic R, Teater M, et al. EZH2 is required for germinal center formation and somatic EZH2 mutations promote lymphoid transformation. Cancer Cell. 2013;23(5): 677-692.
57. Velichutina I, Shaknovich R, Geng H, et al. EZH2-mediated epigenetic silencing in germinal center B cells contributes to proliferation and lymphomagenesis. Blood. 2010;116(24): 5247-5255.
58. Berg T, Thoene S, Yap D, et al. A transgenic mouse model demonstrating the oncogenic role of mutations in the polycomb-group gene EZH2 in lymphomagenesis. Blood. 2014;123(25): 3914-3924.
59. Lee SC, Phipson B, Hyland CD, et al. Polycomb repressive complex 2 (PRC2) suppresses Emmyc lymphoma. Blood. 2013;122(15): 2654-2663.
60. van der Vlag J, Otte AP. Transcriptional repression mediated by the human polycombgroup protein EED involves histone deacetylation. Nat Genet. 1999;23(4):474-478.
61. 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.
62. Ohm JE, McGarvey KM, Yu X, et al. A stem celllike chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet. 2007;39(2): 237-242.
63. Schlesinger Y, Straussman R, Keshet I, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet. 2007;39(2): 232-236.
64. Vir é E, Brenner C, Deplus R, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature. 2006;439(7078): 871-874.
65. Martín-Subero JI, Kreuz M, Bibikova M, et al; Molecular Mechanisms in Malignant Lymphomas Network Project of the Deutsche Krebshilfe. New insights into the biology and origin of mature aggressive B-cell lymphomas by combined epigenomic, genomic, and transcriptional profiling. Blood. 2009;113(11):2488-2497.
66. Mullighan CG, Zhang J, Kasper LH, et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature. 2011; 471(7337):235-239.
67. Sander S, Bullinger L, Klapproth K, et al. MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood. 2008; 112(10):4202-4212.
68. Varambally S, Cao Q, Mani RS, et al. Genomic loss of microRNA-101 leads to overexpression of histone methyltransferase EZH2 in cancer. Science. 2008;322(5908):1695-1699.
69. Cao Q, Mani RS, Ateeq B, et al. Coordinated regulation of polycomb group complexes through microRNAs in cancer. Cancer Cell. 2011;20(2): 187-199.
70. Shimono Y, Zabala M, Cho RW, et al. Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell. 2009;138(3):592-603.
71. Wellner U, Schubert J, Burk UC, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 2009;11(12):1487-1495.
72. Marson A, Levine SS, Cole MF, et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell. 2008;134(3):521-533.
73. Yamagishi M, Nakano K, Miyake A, et al. Polycomb-mediated loss of miR-31 activates NIK-dependent NF-kB pathway in adult T cell leukemia and other cancers. Cancer Cell. 2012; 21(1):121-135.
74. Cui J, Cheng Y, Zhang P, et al. Down regulation of miR200c promotes radiation-induced thymic lymphoma by targeting BMI1. J Cell Biochem. 2014;115(6):1033-1042.
75. Zhang X, Zhao X, Fiskus W, 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(4):506-523.
76. Zhang X, Chen X, Lin J, et al. Myc represses miR-15a/miR-16-1 expression through recruitment of HDAC3 in mantle cell and other non-Hodgkin B-cell lymphomas. Oncogene. 2012;31(24):3002-3008.
77. Zhao X, Lwin T, Zhang X, et al. Disruption of the MYC-miRNA-EZH2 loop to suppress aggressive B-cell lymphoma survival and clonogenicity. Leukemia. 2013;27(12):2341-2350.
78. Tao J, Zhao X, Tao J. c-MYC-miRNA circuitry: a central regulator of aggressive B-cell malignancies. Cell Cycle. 2014;13(2):191-198.
79. Chang TC, Yu D, Lee YS, et al. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat Genet. 2008;40(1):43-50.
80. Wang L, Zhang X, Jia LT, et al. c-Myc-mediated epigenetic silencing of MicroRNA-101 contributes to dysregulation of multiple pathways in hepatocellular carcinoma. Hepatology. 2014; 59(5):1850-1863.
81. Cimmino A, Calin GA, Fabbri M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci USA. 2005;102(39): 13944-13949.
82. Zhao JJ, Lin J, Lwin T, et al. microRNA expression profile and identification of miR-29 as a prognostic marker and pathogenetic factor by targeting CDK6 in mantle cell lymphoma. Blood. 2010;115(13):2630-2639.
83. Santanam U, Zanesi N, Efanov A, et al. Chronic lymphocytic leukemia modeled in mouse by targeted miR-29 expression. Proc Natl Acad Sci USA. 2010;107(27):12210-12215.
84. Lwin T, Zhao X, Cheng F, et al. A microenvironment-mediated c-Myc/miR-548m/ HDAC6 amplification loop in non-Hodgkin B cell lymphomas. J Clin Invest. 2013;123(11): 4612-4626.
85. Ferreira AC, Robaina MC, Rezende LM, Severino P, Klumb CE. Histone deacetylase inhibitor prevents cell growth in Burkitt's lymphoma by regulating PI3K/Akt pathways and leads to upregulation of miR-143, miR-145, and miR-101. Ann Hematol. 2014;93(6):983-993.
86. Kreso A, van Galen P, Pedley NM, et al. Selfrenewal as a therapeutic target in human colorectal cancer. Nat Med. 2014;20(1):29-36.
87. 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.
88. 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.
89. 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.
90. Konze KD, Ma A, Li F, et al. An orally bioavailable chemical probe of the Lysine Methyltransferases EZH2 and EZH1. ACS Chem Biol. 2013;8(6):1324-1334.
91. Knutson SK, Warholic NM, Wigle TJ, et al. Durable tumor regression in genetically altered malignant rhabdoid tumors by inhibition of methyltransferase EZH2. Proc Natl Acad Sci USA. 2013;110(19): 7922-7927.
92. Garapaty-Rao S, Nasveschuk C, Gagnon A, et al. Identification of EZH2 and EZH1 small molecule inhibitors with selective impact on diffuse large B cell lymphoma cell growth. Chem Biol. 2013;20(11):1329-1339.
93. Bradley WD, Arora S, Busby J, et al. EZH2 Inhibitor Efficacy in Non-Hodgkin's Lymphoma Does Not Require Suppression of H3K27 Monomethylation. Chem Biol. 2014;21(11): 1463-1475.
94. Knutson SK, Kawano S, Minoshima Y, et al. Selective inhibition of EZH2 by EPZ-6438 leads to potent antitumor activity in EZH2-mutant non-Hodgkin lymphoma. Mol Cancer Ther. 2014;13(4):842-854.
95. Xu B, On DM, Ma A, et al. Selective inhibition of EZH2 and EZH1 enzymatic activity by a small molecule suppresses MLL-rearranged leukemia [published online ahead of print November 13, 2014]. Blood. 2015;125(2): 346-357.
96. Daigle SR, Olhava EJ, Therkelsen CA, et al. Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell. 2011;20(1):53-65.
97. Kim E, Kim M, Woo DH, et al. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer Cell. 2013; 23(6):839-852.
98. Xu K, Wu ZJ, Groner AC, et al. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent. Science. 2012; 338(6113):1465-1469.
99. Popovic R, Martinez-Garcia E, Giannopoulou EG, 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(9): e1004566.
100. Neff T, Sinha AU, Kluk MJ, et al. Polycomb repressive complex 2 is required for MLL-AF9 leukemia. Proc Natl Acad Sci USA. 2012; 109(13):5028-5033.