Enhancer of Zeste 2 (EZH2) is up-regulated in malignant gliomas and in glioma stem-like cells

Neuropathology and Applied Neurobiology

Volumn 37, Issue 4, 2011, Pages 381-394

  Orzan, F ^a   Pellegatta, S ^a   Poliani, P L ^a   Pisati, F ^a   Caldera, V ^b   Menghi, F ^c   Kapetis, D ^d   Marras, C ^a   Schiffer, D ^b   Finocchiaro, G ^a  

^a UNIVERSITY OF MILANO BICOCCA   (Italy)

^b UNIVERSITY OF BRESCIA   (Italy)

^c Centro Ricerche di Neuro Bio Oncologia   (Italy)

^d GREAT ORMOND STREET HOSPITAL   (United Kingdom)

Author keywords

CD133; EZH2; Glioblastoma; Glioma stem like cells; HDAC; Polycomb

Indexed keywords

TRANSCRIPTION FACTOR EZH2; DNA BINDING PROTEIN; EZH2 PROTEIN, HUMAN; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; TRANSCRIPTION FACTOR; VORINOSTAT;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; GLIOBLASTOMA; GLIOMA CELL; GLIOMA STEM LIKE CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BRAIN TUMOR; CANCER STEM CELL; CELL SEPARATION; CHROMATIN IMMUNOPRECIPITATION; DISEASE COURSE; DNA MICROARRAY; DRUG EFFECT; FLOW CYTOMETRY; GENETICS; GLIOMA; IMMUNOHISTOCHEMISTRY; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CD133; EZH2; GLIOBLASTOMAS; GLIOMA STEM-LIKE CELLS; HDAC; POLYCOMB;

GENE EXPRESSION; GENE EXPRESSION REGULATION; ORGANIC ACIDS; POLYMERASE CHAIN REACTION; PROTEINS; STEM CELLS;

TUMORS;

ANIMALS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL SEPARATION; CHROMATIN IMMUNOPRECIPITATION; DISEASE PROGRESSION; DNA-BINDING PROTEINS; FLOW CYTOMETRY; GLIOMA; HISTONE DEACETYLASE INHIBITORS; HUMANS; HYDROXAMIC ACIDS; IMMUNOHISTOCHEMISTRY; MICE; NEOPLASTIC STEM CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS; UP-REGULATION;

MURINAE;

EID: 79959416877     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/j.1365-2990.2010.01132.x     Document Type: Article

References (34)

1. Valk-Lingbeek ME, Bruggeman SW, van Lohuizen M. Stem cells and cancer; the polycomb connection. Cell 2004; 118: 409-18
2. Simon JA, Lange CA. Roles of the EZH2 histone methyltransferase in cancer epigenetics. Mutat Res 2008; 647: 21-9
3. Vire E, Brenner C, Deplus R, Blanchon L, FragaM, Didelot C, Morey L, Van Eynde A, Bernard D, Vanderwinden JM, Bollen M, Esteller M, Di Croce L, de Launoit Y, Fuks F. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439: 871-4
4. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, Jaenisch R, Wagschal A, Feil R, Schreiber SL, Lander ES. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125: 315
5. Agger K, Cloos PAC, Christensen J, Pasini D, Rose S, Rappsilber J, Issaeva I, Canaani E, Salcini AE, Helin K. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007; 449: 731
6. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, Tempst P, Jones RS, Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002; 298: 1039-43
7. Bruggeman SW, Hulsman D, Tanger E, Buckle T, Blom M, Zevenhoven J, van Tellingen O, van Lohuizen M. Bmi1 controls tumor development in an Ink4a/Arfindependent manner in amouse model for glioma. Cancer Cell 2007; 12: 328-41
8. Tunici P, Bissola L, Lualdi E, Pollo B, Cajola L, Broggi G, Sozzi G, Finocchiaro G. Genetic alterations and in vivo tumorigenicity of neurospheres derived from an adult glioblastoma. Mol Cancer 2004; 3: 25
9. Das S, Srikanth M, Kessler JA. Cancer stem cells and glioma. Nat Clin Pract Neurol 2008; 4: 427-35
10. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, Park JK, Fine HA. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closelymirror the phenotype and genotype of primary tumors than do serumcultured cell lines. Cancer Cell 2006; 9: 391-403
11. Lee J, Son MJ, Woolard K, Donin NM, Li A, Cheng CH, Kotliarova S, Kotliarov Y, Walling J, Ahn S, Kim M, Totonchy M, Cusack T, Ene C, Ma H, Su Q, Zenklusen JC, Zhang W, Maric D, Fine HA. Epigenetic-mediated dysfunction of the bone morphogenetic protein pathway inhibits differentiation of glioblastoma-initiating cells. Cancer Cell 2008; 13: 69-80
12. Nagarajan RP, Costello JF. Epigenetic mechanisms in glioblastoma multiforme. Semin Cancer Biol 2009; 19: 188
13. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-8
14. Cambon AC, Khalyfa A, Cooper NG, Thompson CM. Analysis of probe level patterns in Affymetrix microarray data. BMC Bioinformatics 2007; 8: 146
15. Pellegatta S, Poliani PL, Corno D, Menghi F, Ghielmetti F, Suarez-Merino B, Caldera V, Nava S, Ravanini M, Facchetti F, Bruzzone MG, Finocchiaro G. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res 2006; 66: 10247-52
16. Fiskus W, Pranpat M, Balasis M, Herger B, Rao R, Chinnaiyan A, Atadja P, Bhalla K. Histone deacetylase inhibitors deplete enhancer of zeste 2 and associated polycomb repressive complex 2 proteins in human acute leukemia cells. Mol Cancer Ther 2006; 5: 3096-104
17. van der Vlag J, Otte AP. Transcriptional repression mediated by the human polycomb-group protein EED involves histone deacetylation. Nat Genet 1999; 23: 474-8
18. Eyupoglu IY, Hahnen E, Buslei R, Siebzehnrubl FA, Savaskan NE, Luders M, Trankle C, Wick W, Weller M, Fahlbusch R, Blumcke I. Suberoylanilide hydroxamic acid (SAHA) has potent anti-glioma properties in vitro, ex vivo and in vivo. J Neurochem 2005; 93: 992-9
19. Sher F, Rössler R, Brouwer N, Balasubramaniyan V, Boddeke E, Copray S. Differentiation of neural stem cells into oligodendrocytes: involvement of the polycomb group protein Ezh2. Stem Cells 2008; 26: 2875-83
20. Siebzehnrubl FA, Jeske I, Muller D, Buslei R, Coras R, Hahnen E, Huttner HB, Corbeil D, Kaesbauer J, Appl T, von Horsten S, Blumcke I. Spontaneous in vitro transformation of adult neural precursors into stem-like cancer cells. Brain Pathol 2009; 19: 399-408
21. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008; 40: 499-507
22. An Z, Gluck CB, Choy ML, Kaufman LJ. Suberoylanilide hydroxamic acid limits migration and invasion of glioma cells in two and three dimensional culture. Cancer Lett 2010; 292: 215-27
23. Liby P, Kostrouchova M, Pohludka M, Yilma P, Hrabal P, Sikora J, Brozova E, Kostrouchova M, Rall JE, Kostrouch Z. Elevated and deregulated expression of HDAC3 in human astrocytic glial tumours. Folia Biol (Praha) 2006; 52: 21-33
24. Garrick D, De Gobbi M, Samara V, Rugless M, Holland M, Ayyub H, Lower K, Sloane-Stanley J, Gray N, Koch C, Dunham I, Higgs DR. The role of the polycomb complex in silencing alpha-globin gene expression in nonerythroid cells. Blood 2008; 112: 3889-99
25. Spiller SE, Ravanpay AC, Hahn AW, Olson JM. Suberoylanilide hydroxamic acid is effective in preclinical studies of medulloblastoma. J Neurooncol 2006; 79: 259-70
26. Furchert SE, Lanvers-Kaminsky C, Juurgens H, Jung M, Loidl A, Fruhwald MC. Inhibitors of histone deacetylases as potential therapeutic tools for high-risk embryonal tumors of the nervous system of childhood. Int J Cancer 2007; 120: 1787-94
27. Ugur HC, Ramakrishna N, Bello L, Menon LG, Kim SK, Black PM, Carroll RS. Continuous intracranial administration of suberoylanilide hydroxamic acid (SAHA) inhibits tumor growth in an orthotopic glioma model. J Neurooncol 2007; 83: 267-75
28. Yin D, Ong JM, Hu J, Desmond JC, Kawamata N, Konda BM, Black KL, Koeffler HP. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor: effects on gene expression and growth of glioma cells in vitro and in vivo. Clin Cancer Res 2007; 13: 1045-52
29. Galanis E, Jaeckle KA, Maurer MJ, Reid JM, Ames MM, Hardwick JS, Reilly JF, Loboda A, Nebozhyn M, Fantin VR, Richon VM, Scheithauer B, Giannini C, Flynn PJ, Moore DF, Jr, Zwiebel J, Buckner JC. Phase II Trial of Vorinostat in Recurrent Glioblastoma Multiforme: A North Central Cancer Treatment Group Study. J Clin Oncol 2009
30. Siebzehnrubl FA, Buslei R, Eyupoglu IY, Seufert S, Hahnen E, Blumcke I. Histone deacetylase inhibitors increase neuronal differentiation in adult forebrain precursor cells. Exp Brain Res 2007; 176: 672-8
31. Tabu K, Sasai K, Kimura T, Wang L, Aoyanagi E, Kohsaka S, Tanino M, Nishihara H, Tanaka S. Promoter hypomethylation regulates CD133 expression in human gliomas. Cell Res 2008; 18: 1037-46
32. Zeppernick F, Ahmadi R, Campos B, Dictus C, Helmke BM, Becker N, Lichter P, Unterberg A, Radlwimmer B, Herold-Mende CC. Stem Cell Marker CD133 Affects Clinical Outcome in Glioma Patients. Clin Cancer Res 2008; 14: 123-9
33. SuvaML, Riggi N, Janiszewska M, Radovanovic I, Provero P, Stehle JC, Baumer K, Le Bitoux MA, Marino D, Cironi L, Marquez VE, Clement V, Stamenkovic I. EZH2 is essential for glioblastoma cancer stem cell maintenance. Cancer Res 2009; 69: 9211-18
34. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, Haukaas SA, Salvesen HB, Otte AP, 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. J Clin Oncol 2006; 24: 268-73