The polycomb group protein EZH2 is a novel therapeutic target in tongue cancer

Oncotarget

Volumn 4, Issue 12, 2013, Pages 2532-2549

  Li, Zhongwu ^a   Wang, Yanling ^a   Qiu, Jing ^a   Li, Qiang ^a   Yuan, Chunping ^a   Zhang, Wei ^a   Wang, Dongmiao ^a   Ye, Jinhai ^a   Jiang, Hongbin ^a   Yang, Jianrong ^a   Cheng, Jie ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

DZNep; EZH2; Polycomb complex; Tongue squamous cell carcinoma

Indexed keywords

3 DEAZANEPLANOCIN A; FLUOROURACIL; HERMES ANTIGEN; KI 67 ANTIGEN; POLYCOMB GROUP PROTEIN; PROTEIN P16; PROTEIN P21; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR EZH2; UVOMORULIN;

ADULT; AGED; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLOGICAL ACTIVITY; CANCER GRADING; CANCER GROWTH; CANCER INHIBITION; CANCER MODEL; CANCER PATIENT; CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SUBPOPULATION; CERVICAL LYMPH NODE; COLONY FORMATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; OVERALL SURVIVAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SURVIVAL TIME; TONGUE CANCER; TUMOR XENOGRAFT;

ADENOSINE; ANIMALS; APOPTOSIS; CELL LINE, TUMOR; FEMALE; HUMANS; MALE; MICE; MICE, NUDE; MIDDLE AGED; MOLECULAR TARGETED THERAPY; POLYCOMB REPRESSIVE COMPLEX 2; RANDOM ALLOCATION; RNA, SMALL INTERFERING; TONGUE NEOPLASMS; TRANSFECTION; TUMOR CELLS, CULTURED;

EID: 84891921366     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.1503     Document Type: Article

References (53)

1. Ferlay J, Shin HR, Bray F, Forman D, Mathers C and Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. International journal of cancer Journal international du cancer. 2010; 127(12):2893-2917.
2. Argiris A, Karamouzis MV, Raben D and Ferris RL. Head and neck cancer. Lancet. 2008; 371(9625):1695-1709.
3. Scully C and Bagan JV. Recent advances in oral oncology 2008; squamous cell carcinoma imaging, treatment, prognostication and treatment outcomes. Oral oncology. 2009; 45(6):e25-30.
4. Haddad RI and Shin DM. Recent advances in head and neck cancer. The New England journal of medicine. 2008; 359(11):1143-1154.
5. Simon JA and Kingston RE. Mechanisms of polycomb gene silencing: knowns and unknowns. Nature reviews Molecular cell biology. 2009; 10(10):697-708.
6. Margueron R and Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature. 2011; 469(7330):343-349.
7. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA and Chinnaiyan AM. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature. 2002; 419(6907):624-629.
8. Cao W, Ribeiro Rde O, Liu D, Saintigny P, Xia R, Xue Y, Lin R, Mao L and Ren H. EZH2 promotes malignant behaviors via cell cycle dysregulation and its mRNA level associates with prognosis of patient with non-small cell lung cancer. PloS one. 2012; 7(12):e52984.
9. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, Haukaas SA, Salvesen HB, Otte AP and Akslen LA. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. Journal of clinical oncology: official journal of the American Society of Clinical Oncology. 2006; 24(2):268-273.
10. Ferraro A, Mourtzoukou D, Kosmidou V, Avlonitis S, Kontogeorgos G, Zografos G and Pintzas A. EZH2 is regulated by ERK/AKT and targets integrin alpha2 gene to control Epithelial-Mesenchymal Transition and anoikis in colon cancer cells. The international journal of biochemistry&cell biology. 2013; 45(2):243-254.
11. Chase A and Cross NC. Aberrations of EZH2 in cancer. Clinical cancer research: an official journal of the American Association for Cancer Research. 2011; 17(9):2613-2618.
12. Smits M, Nilsson J, Mir SE, van der Stoop PM, Hulleman E, Niers JM, de Witt Hamer PC, Marquez VE, Cloos J, Krichevsky AM, Noske DP, Tannous BA and Wurdinger T. miR-101 is down-regulated in glioblastoma resulting in EZH2-induced proliferation, migration, and angiogenesis. Oncotarget. 2010; 1(8):710-720.
13. Cao Q, Yu J, Dhanasekaran SM, Kim JH, Mani RS, Tomlins SA, Mehra R, Laxman B, Cao X, Yu J, Kleer CG, Varambally S and Chinnaiyan AM. Repression of E-cadherin by the polycomb group protein EZH2 in cancer. Oncogene. 2008; 27(58):7274-7284.
14. Zhong J, Min L, Huang H, Li L, Li D, Li J, Ma Z and Dai L. EZH2 regulates the expression of p16 in the nasopharyngeal cancer cells. Technology in cancer research&treatment. 2013; 12(3):269-274.
15. Crea F, Hurt EM, Mathews LA, Cabarcas SM, Sun L, Marquez VE, Danesi R and Farrar WL. Pharmacologic disruption of Polycomb Repressive Complex 2 inhibits tumorigenicity and tumor progression in prostate cancer. Molecular cancer. 2011; 10:40.
16. Chen Y, Lin MC, Yao H, Wang H, Zhang AQ, Yu J, Hui CK, Lau GK, He ML, Sung J and Kung HF. Lentivirus-mediated RNA interference targeting enhancer of zeste homolog 2 inhibits hepatocellular carcinoma growth through down-regulation of stathmin. Hepatology. 2007; 46(1):200-208.
17. Crea F, Fornaro L, Bocci G, Sun L, Farrar WL, Falcone A and Danesi R. EZH2 inhibition: targeting the crossroad of tumor invasion and angiogenesis. Cancer metastasis reviews. 2012; 31(3-4):753-761.
18. Glazer RI, Hartman KD, Knode MC, Richard MM, Chiang PK, Tseng CK and Marquez VE. 3-Deazaneplanocin: a new and potent inhibitor of S-adenosylhomocysteine hydrolase and its effects on human promyelocytic leukemia cell line HL-60. Biochemical and biophysical research communications. 1986; 135(2):688-694.
19. Fiskus W, Wang Y, Sreekumar A, Buckley KM, Shi H, Jillella A, Ustun C, Rao R, Fernandez P, Chen J, Balusu R, Koul S, Atadja P, Marquez VE and Bhalla KN. 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.
20. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, Karuturi RK, Tan PB, Liu ET and Yu Q. Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes&development. 2007; 21(9):1050-1063.
21. Benoit YD, Witherspoon MS, Laursen KB, Guezguez A, Beausejour M, Beaulieu JF, Lipkin SM and Gudas LJ. Pharmacological inhibition of polycomb repressive complex-2 activity induces apoptosis in human colon cancer stem cells. Experimental cell research. 2013; 319(10):1463-1470.
22. Chiba T, Suzuki E, Negishi M, Saraya A, Miyagi S, Konuma T, Tanaka S, Tada M, Kanai F, Imazeki F, Iwama A and Yokosuka O. 3-Deazaneplanocin A is a promising therapeutic agent for the eradication of tumor-initiating hepatocellular carcinoma cells. International journal of cancer Journal international du cancer. 2012; 130(11):2557-2567.
23. Wang C, Liu X, Chen Z, Huang H, Jin Y, Kolokythas A, Wang A, Dai Y, Wong DT and Zhou X. Polycomb group protein EZH2-mediated E-cadherin repression promotes metastasis of oral tongue squamous cell carcinoma. Molecular carcinogenesis. 2013; 52(3):229-236.
24. Cao W, Feng Z, Cui Z, Zhang C, Sun Z, Mao L and Chen W. Up-regulation of enhancer of zeste homolog 2 is associated positively with cyclin D1 overexpression and poor clinical outcome in head and neck squamous cell carcinoma. Cancer. 2012; 118(11):2858-2871.
25. Kidani K, Osaki M, Tamura T, Yamaga K, Shomori K, Ryoke K and Ito H. High expression of EZH2 is associated with tumor proliferation and prognosis in human oral squamous cell carcinomas. Oral oncology. 2009; 45(1):39-46.
26. Fiskus W, Rao R, Balusu R, Ganguly S, Tao J, Sotomayor E, Mudunuru U, Smith JE, Hembruff SL, Atadja P, Marquez VE and Bhalla K. Superior efficacy of a combined epigenetic therapy against human mantle cell lymphoma cells. Clinical cancer research: an official journal of the American Association for Cancer Research. 2012; 18(22):6227-6238.
27. Bracken AP, Kleine-Kohlbrecher D, Dietrich N, Pasini D, Gargiulo G, Beekman C, Theilgaard-Monch K, Minucci S, Porse BT, Marine JC, Hansen KH and Helin K. The Polycomb group proteins bind throughout the INK4A-ARF locus and are disassociated in senescent cells. Genes&development. 2007; 21(5):525-530.
28. Collado M, Blasco MA and Serrano M. Cellular senescence in cancer and aging. Cell. 2007; 130(2):223-233.
29. Hu S, Yu L, Li Z, Shen Y, Wang J, Cai J, Xiao L and Wang Z. Overexpression of EZH2 contributes to acquired cisplatin resistance in ovarian cancer cells in vitro and in vivo. Cancer biology&therapy. 2010; 10(8):788-795.
30. Aranda V. Cancer epigenetics: Unraveling chromatin checkpoints. Nature medicine. 2013; 19(9):1102.
31. Koh CM, Iwata T, Zheng Q, Bethel C, Yegnasubramanian S and De Marzo AM. Myc enforces overexpression of EZH2 in early prostatic neoplasia via transcriptional and post-transcriptional mechanisms. Oncotarget. 2011; 2(9):669-683.
32. Asangani IA, Harms PW, Dodson L, Pandhi M, Kunju LP, Maher CA, Fullen DR, Johnson TM, Giordano TJ, Palanisamy N and Chinnaiyan AM. Genetic and epigenetic loss of microRNA-31 leads to feed-forward expression of EZH2 in melanoma. Oncotarget. 2012; 3(9):1011-1025.
33. Cao W, Younis RH, Li J, Chen H, Xia R, Mao L, Chen W and Ren H. EZH2 promotes malignant phenotypes and is a predictor of oral cancer development in patients with oral leukoplakia. Cancer prevention research. 2011; 4(11):1816-1824.
34. Choudhury SR, Balasubramanian S, Chew YC, Han B, Marquez VE and Eckert RL. (-)-Epigallocatechin-3-gallate and DZNep reduce polycomb protein level via a proteasome-dependent mechanism in skin cancer cells. Carcinogenesis. 2011; 32(10):1525-1532.
35. Chang CJ and Hung MC. The role of EZH2 in tumour progression. British journal of cancer. 2012; 106(2):243-247.
36. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E and Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. The EMBO journal. 2003; 22(20):5323-5335.
37. Kheradmand Kia S, Solaimani Kartalaei P, Farahbakhshian E, Pourfarzad F, von Lindern M and Verrijzer CP. EZH2-dependent chromatin looping controls INK4a and INK4b, but not ARF, during human progenitor cell differentiation and cellular senescence. Epigenetics&chromatin. 2009; 2(1):16.
38. Collado M and Serrano M. Senescence in tumours: evidence from mice and humans. Nature reviews Cancer. 2010; 10(1):51-57.
39. Tong ZT, Cai MY, Wang XG, Kong LL, Mai SJ, Liu YH, Zhang HB, Liao YJ, Zheng F, Zhu W, Liu TH, Bian XW, Guan XY, Lin MC, Zeng MS, Zeng YX, et al. EZH2 supports nasopharyngeal carcinoma cell aggressiveness by forming a co-repressor complex with HDAC1/HDAC2 and Snail to inhibit E-cadherin. Oncogene. 2012; 31(5):583-594.
40. Liu LK, Jiang XY, Zhou XX, Wang DM, Song XL and Jiang HB. Upregulation of vimentin and aberrant expression of E-cadherin/beta-catenin complex in oral squamous cell carcinomas: correlation with the clinicopathological features and patient outcome. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc. 2010; 23(2):213-224.
41. Beck B and Blanpain C. Unravelling cancer stem cell potential. Nature reviews Cancer. 2013; 13(10):727-738.
42. Chang CJ, Yang JY, Xia W, Chen CT, Xie X, Chao CH, Woodward WA, Hsu JM, Hortobagyi GN and Hung MC. EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-beta-catenin signaling. Cancer cell. 2011; 19(1):86-100.
43. Kim E, Kim M, Woo DH, Shin Y, Shin J, Chang N, Oh YT, Kim H, Rheey J, Nakano I, Lee C, Joo KM, Rich JN, Nam DH and Lee J. Phosphorylation of EZH2 activates STAT3 signaling via STAT3 methylation and promotes tumorigenicity of glioblastoma stem-like cells. Cancer cell. 2013; 23(6):839-852.
44. Ougolkov AV, Bilim VN and Billadeau DD. Regulation of pancreatic tumor cell proliferation and chemoresistance by the histone methyltransferase enhancer of zeste homologue 2. Clinical cancer research: an official journal of the American Association for Cancer Research. 2008; 14(21):6790-6796.
45. Zhang Y, Liu G, Lin C, Liao G and Tang B. Silencing the EZH2 gene by RNA interference reverses the drug resistance of human hepatic multidrug-resistant cancer cells to 5-Fu. Life sciences. 2013; 92(17-19):896-902.
46. Miranda TB, Cortez CC, Yoo CB, Liang G, Abe M, Kelly TK, Marquez VE and Jones PA. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Molecular cancer therapeutics. 2009; 8(6):1579-1588.
47. Sun F, Li J, Yu Q and Chan E. Loading 3-deazaneplanocin A into pegylated unilamellar liposomes by forming transient phenylboronic acid-drug complex and its pharmacokinetic features in Sprague-Dawley rats. European journal of pharmaceutics and biopharmaceutics: official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik eV. 2012; 80(2):323-331.
48. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Della Pietra A, 3rd, Diaz E, LaFrance LV, Mellinger M, Duquenne C, Tian X, Kruger RG, McHugh CF, et al. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. 2012; 492(7427):108-112.
49. Qi W, Chan H, Teng L, Li L, Chuai S, Zhang R, Zeng J, Li M, Fan H, Lin Y, Gu J, Ardayfio O, Zhang JH, Yan X, Fang J, Mi Y, et al. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Proceedings of the National Academy of Sciences of the United States of America. 2012; 109(52):21360-21365.
50. Cha TL, Zhou BP, Xia W, Wu Y, Yang CC, Chen CT, Ping B, Otte AP and Hung MC. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science. 2005; 310(5746):306-310.
51. Lee ST, Li Z, Wu Z, Aau M, Guan P, Karuturi RK, Liou YC and Yu Q. Context-specific regulation of NF-kappaB target gene expression by EZH2 in breast cancers. Molecular cell. 2011; 43(5):798-810.
52. Yamagishi M, Nakano K, Miyake A, Yamochi T, Kagami Y, Tsutsumi A, Matsuda Y, Sato-Otsubo A, Muto S, Utsunomiya A, Yamaguchi K, Uchimaru K, Ogawa S and Watanabe T. Polycomb-mediated loss of miR-31 activates NIK-dependent NF-kappaB pathway in adult T cell leukemia and other cancers. Cancer cell. 2012; 21(1):121-135.
53. Wei Z, Wang Y, Li Z, Yuan C, Zhang W, Wang D, Ye J, Jiang H, Wu Y and Cheng J. Overexpression of Hippo pathway effector TAZ in tongue squamous cell carcinoma: correlation with clinicopathological features and patients' prognosis. Journal of oral pathology&medicine: official publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology. 2013.