Chronic myelogenous leukemia-initiating cells require polycomb group protein EZH2

Cancer Discovery

Volumn 6, Issue 11, 2016, Pages 1237-1247

  Xie, Huafeng ^a   Peng, Cong ^a   Huang, Jialiang ^a,b   Li, Bin E ^a   Kim, Woojin ^a   Smith, Elenoe C ^a   Fujiwara, Yuko ^a   Qi, Jun ^c   Cheloni, Giulia ^d,e   Das, Partha P ^a   Nguyen, Minh ^a   Li, Shaoguang ^d   Bradner, James E ^c   Orkin, Stuart H ^a,f  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF FLORENCE   (Italy)

^f HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POLYCOMB GROUP PROTEIN EZH2; POLYCOMB REPRESSIVE COMPLEX 2; UNCLASSIFIED DRUG; BCR ABL PROTEIN; EZH1 PROTEIN, HUMAN; EZH2 PROTEIN, HUMAN; PROTEIN KINASE INHIBITOR; TRANSCRIPTION FACTOR EZH2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW TRANSPLANTATION; CELL CYCLE PROGRESSION; CHRONIC MYELOID LEUKEMIA; CRISPR CAS SYSTEM; DISEASE ERADICATION; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE INACTIVATION; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; LEUKEMIA REMISSION; MOLECULAR CLONING; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CANCER STEM CELL; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; CRISPR-CAS SYSTEMS; DRUG RESISTANCE, NEOPLASM; ENHANCER OF ZESTE HOMOLOG 2 PROTEIN; FUSION PROTEINS, BCR-ABL; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; LEUKEMIA, MYELOGENOUS, CHRONIC, BCR-ABL POSITIVE; MICE; NEOPLASTIC STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 2; PROTEIN KINASE INHIBITORS; SIGNAL TRANSDUCTION;

EID: 84995366767     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-15-1439     Document Type: Article

References (45)

1. Nowell PC, Hungerford DA. Chromosome studies on normal and leukemic human leukocytes. J Natl Cancer Inst 1960; 25: 85-109.
2. Fainstein E, Marcelle C, Rosner A, Canaani E, Gale RP, Dreazen O, et al. A new fused transcript in Philadelphia chromosome positive acute lymphocytic leukaemia. Nature 1987; 330: 386-8.
3. Ulmer A, Tabea Tauer J, Glauche I, Jung R, Suttorp M. TK inhibitor treatment disrupts growth hormone axis: Clinical observations in children with CML and experimental data from a juvenile animal model. Klin Padiatr 2013; 225: 120-6.
4. Price KE, Saleem N, Lee G, Steinberg M. Potential of ponatinib to treat chronic myeloid leukemia and acute lymphoblastic leukemia. Onco Targets Ther 2013; 6: 1111-8.
5. Ahmed W, Van Etten RA. Alternative approaches to eradicating the malignant clone in chronic myeloid leukemia: Tyrosine-kinase inhibitor combinations and beyond. Hematology Am Soc Hematol Educ Program 2013; 2013: 189-200.
6. Druker BJ, Tamura S, Buchdunger E, Ohno S, Segal GM, Fanning S, et al. Effects of a selective inhibitor of the Abl tyrosine kinase on the growth of Bcr-Abl positive cells. Nat Med 1996; 2: 561-6.
7. Cortes JE, Kim DW, Pinilla-Ibarz J, le Coutre P, Paquette R, Chuah C, et al. A phase 2 trial of ponatinib in Philadelphia chromosomepositive leukemias. N Engl J Med 2013; 369: 1783-96.
8. Zabriskie MS, Eide CA, Tantravahi SK, Vellore NA, Estrada J, Nicolini FE, et al. BCR-ABL1 compound mutations combining key kinase domain positions confer clinical resistance to ponatinib in Ph chromosome-positive leukemia. Cancer Cell 2014; 26: 428-42
9. 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: 624-9.
10. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, 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: 11606-11.
11. Sudo T, Utsunomiya T, Mimori K, Nagahara H, Ogawa K, Inoue H, et al. Clinicopathological significance of EZH2 mRNA expression in patients with hepatocellular carcinoma. Br J Cancer 2005; 92: 1754-8.
12. Chase A, Cross NC. Aberrations of EZH2 in cancer. Clin Cancer Res 2011; 17: 2613-8.
13. 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: 709-15.
14. 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: 722-6.
15. 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: 665-7.
16. 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: 5227-34.
17. 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: 651-6.
18. Neff T, Sinha AU, Kluk MJ, Zhu N, Khattab MH, Stein L, et al. Polycomb repressive complex 2 is required for MLL-AF9 leukemia. Proc Natl Acad Sci USA 2012; 109: 5028-33.
19. Wilson BG, Wang X, Shen X, McKenna ES, Lemieux ME, Cho YJ, et al. Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 2010; 18: 316-28.
20. Xie H, Xu J, Hsu JH, Nguyen M, Fujiwara Y, Peng C, et al. Polycomb repressive complex 2 regulates normal hematopoietic stem cell function in a developmental-stage-specific manner. Cell Stem Cell 2014; 14: 68-80.
21. Cramer-Morales K, Nieborowska-Skorska M, Scheibner K, Padget M, Irvine DA, Sliwinski T, et al. Personalized synthetic lethality induced by targeting RAD52 in leukemias identified by gene mutation and expression profile. Blood 2013; 122: 1293-304.
22. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005; 102: 15545-50.
23. Talpaz M, Shah NP, Kantarjian H, Donato N, Nicoll J, Paquette R, et al. Dasatinib in imatinib-resistant Philadelphia chromosomepositive leukemias. N Engl J Med 2006; 354: 2531-41.
24. Hu Y, Swerdlow S, Duffy TM, Weinmann R, Lee FY, Li S. Targeting multiple kinase pathways in leukemic progenitors and stem cells is essential for improved treatment of Ph+ leukemia in mice. Proc Natl Acad Sci USA 2006; 103: 16870-5.
25. Zhang B, Ho YW, Huang Q, Maeda T, Lin A, Lee SU, et al. Altered microenvironmental regulation of leukemic and normal stem cells in chronic myelogenous leukemia. Cancer Cell 2012; 21: 577-92.
26. Xu K, Wu ZJ, Groner AC, He HH, Cai C, Lis RT, et al. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycombindependent. Science 2012; 338: 1465-9.
27. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 2002; 16: 2893-905.
28. Joshi P, Carrington EA, Wang L, Ketel CS, Miller EL, Jones RS, et al. Dominant alleles identify SET domain residues required for histone methyltransferase of Polycomb repressive complex 2. J Biol Chem 2008; 283: 27757-66.
29. 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: 108-12.
30. Xu B, On DM, Ma A, Parton T, Konze KD, Pattenden SG, et al. Selective inhibition of EZH2 and EZH1 enzymatic activity by a small molecule suppresses MLL-rearranged leukemia. Blood 2015; 125: 346-57.
31. Konze KD, Ma A, Li F, Barsyte-Lovejoy D, Parton T, Macnevin CJ, et al. An orally bioavailable chemical probe of the lysine methyltransferases EZH2 and EZH1. ACS Chem Biol 2013; 8: 1324-34.
32. Zhang H, Qi J, Reyes JM, Li L, Rao PK, Li F, et al. Oncogenic deregulation of EZH2 as an opportunity for targeted therapy in lung cancer. Cancer Discov 2016 Jun 16. [Epub ahead of print].
33. Okamura S, Arakawa H, Tanaka T, Nakanishi H, Ng CC, Taya Y, et al. p53DINP1, a p53-inducible gene, regulates p53-dependent apoptosis. Mol Cell 2001; 8: 85-94.
34. Liu J, Weiss HL, Rychahou P, Jackson LN, Evers BM, Gao T. Loss of PHLPP expression in colon cancer: Role in proliferation and tumorigenesis. Oncogene 2009; 28: 994-1004.
35. Moulton T, Crenshaw T, Hao Y, Moosikasuwan J, Lin N, Dembitzer F, et al. Epigenetic lesions at the H19 locus in Wilms’ tumour patients. Nat Genet 1994; 7: 440-7.
36. Guan KL, Jenkins CW, Li Y, Nichols MA, Wu X, O’Keefe CL, et al. Growth suppression by p18, a p16INK4/MTS1-and p14INK4B/ MTS2-related CDK6 inhibitor, correlates with wild-type pRb function. Genes Dev 1994; 8: 2939-52.
37. Shi J, Wang E, Milazzo JP, Wang Z, Kinney JB, Vakoc CR. Discovery of cancer drug targets by CRISPR-Cas9 screening of protein domains. Nat Biotechnol 2015; 33: 661-7.
38. Brinkman EK, Chen T, Amendola M, van Steensel B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res 2014; 42: e168.
39. Prost S, Relouzat F, Spentchian M, Ouzegdouh Y, Saliba J, Massonnet G, et al. Erosion of the chronic myeloid leukaemia stem cell pool by PPARgamma agonists. Nature 2015; 525: 380-3.
40. Abraham SA, Hopcroft LE, Carrick E, Drotar ME, Dunn K, Williamson AJ, et al. Dual targeting of p53 and c-MYC selectively eliminates leukaemic stem cells. Nature 2016; 534: 341-6.
41. 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.
42. Scott MT, KorfiK, Saffrey P, Hopcroft LEM, Kinstrie R, Pellicano F, et al. Epigenetic reprogramming sensitizes CML stem cells to combined EZH2 and tyrosine kinase inhibition. Cancer Discov 2016; 6: 1248-57.
43. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe Y, Jessell TM, et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 2001; 1: 4.
44. Shen X, Liu Y, Hsu YJ, Fujiwara Y, Kim J, Mao X, et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 2008; 32: 491-502.
45. Li S, Ilaria RL Jr, Million RP, Daley GQ, Van Etten RA. The P190, P210, and P230 forms of the BCR/ABL oncogene induce a similar chronic myeloid leukemia-like syndrome in mice but have different lymphoid leukemogenic activity. J Exp Med 1999; 189: 1399-412.