OTX2 sustains a bivalent-like state of OTX2-bound promoters in medulloblastoma by maintaining their H3K27me3 levels

Acta Neuropathologica

Volumn 125, Issue 3, 2013, Pages 385-394

  Bunt, Jens ^a   Hasselt, Nancy A ^a   Zwijnenburg, Danny A ^a   Koster, Jan ^a   Versteeg, Rogier ^a   Kool, Marcel ^a,b  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

Chromatin immunoprecipitation; H3K27me3; Histone modification; Medulloblastoma; OTX2

Indexed keywords

HISTONE DEMETHYLASE; HISTONE H3 LYSINE 27 DEMETHYLASE; PROTEIN JARID2; PROTEIN KDM6A; PROTEIN KDM6B; PROTEIN KDM7A; TRANSCRIPTION FACTOR OTX2; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EED GENE; EZH2 GENE; GENE EXPRESSION REGULATION; GENE SILENCING; HISTONE METHYLATION; MEDULLOBLASTOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RBBP4 GENE; SUZ12 GENE; TUMOR GENE; UPREGULATION;

CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; HUMANS; MEDULLOBLASTOMA; METHYLATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OTX TRANSCRIPTION FACTORS; POLYCOMB-GROUP PROTEINS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER;

EID: 84878846494     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-012-1069-2     Document Type: Article

References (33)

1. Adamson DC, Shi Q, Wortham M, Northcott PA, Di C, Duncan CG, Li J, McLendon RE, Bigner DD, Taylor MD, Yan H (2010) OTX2 is critical for the maintenance and progression of Shh-independent medulloblastomas. Cancer Res 70(1):181-191. doi: 10.1158/0008-5472.CAN-09-2331
2. Asp P, Blum R, Vethantham V, Parisi F, Micsinai M, Cheng J, Bowman C, Kluger Y, Dynlacht BD (2011) Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci USA 108(22):E149-E158. doi: 10.1073/pnas.1102223108
3. Bai R, Siu IM, Tyler BM, Staedtke V, Gallia GL, Riggins GJ (2010) Evaluation of retinoic acid therapy for OTX2-positive medulloblastomas. Neuro-oncology 12(7):655-663. doi: 10.1093/neuonc/nop062
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 (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125(2):315-326. doi: 10.1016/j.cell.2006.02.041
5. Bigner SH, Friedman HS, Vogelstein B, Oakes WJ, Bigner DD (1990) Amplification of the c-myc gene in human medulloblastoma cell lines and xenografts. Cancer Res 50(8):2347-2350
6. Boon K, Eberhart CG, Riggins GJ (2005) Genomic amplification of orthodenticle homologue 2 in medulloblastomas. Cancer Res 65(3):703-707 pii:65/3/703
7. Bunt J, de Haas TG, Hasselt NE, Zwijnenburg DA, Koster J, Versteeg R, Kool M (2010) Regulation of cell cycle genes and induction of senescence by overexpression of OTX2 in medulloblastoma cell lines. Mol Cancer Res 8(10):1344-1357. doi: 10.1158/1541-7786.MCR-09-0546
8. Bunt J, Hasselt NE, Zwijnenburg DA, Hamdi M, Koster J, Versteeg R, Kool M (2011) OTX2 directly activates cell cycle genes and inhibits differentiation in medulloblastoma cells. Int J Cancer. doi: 10.1002/ijc.26474
9. Bunt J, Hasselt NE, Zwijnenburg DA, Koster J, Versteeg R, Kool M (2011) Joint Binding of OTX2 and MYC in promotor regions is associated with high gene expression in medulloblastoma. PLoS ONE 6(10):e26058. doi: 10.1371/journal.pone. 0026058
10. de Haas T, Oussoren E, Grajkowska W, Perek-Polnik M, Popovic M, Zadravec-Zaletel L, Perera M, Corte G, Wirths O, van Sluis P, Pietsch T, Troost D, Baas F, Versteeg R, Kool M (2006) OTX1 and OTX2 expression correlates with the clinicopathologic classification of medulloblastomas. J Neuropathol Exp Neurol 65(2):176-186. doi: 10.1097/01.jnen.0000199576.70923.8a
11. Di C, Liao S, Adamson DC, Parrett TJ, Broderick DK, Shi Q, Lengauer C, Cummins JM, Velculescu VE, Fults DW, McLendon RE, Bigner DD, Yan H (2005) Identification of OTX2 as a medulloblastoma oncogene whose product can be targeted by all-trans retinoic acid. Cancer Res 65(3):919-924. doi: 65/3/919
12. Ehrbrecht A, Muller U, Wolter M, Hoischen A, Koch A, Radlwimmer B, Actor B, Mincheva A, Pietsch T, Lichter P, Reifenberger G, Weber RG (2006) Comprehensive genomic analysis of desmoplastic medulloblastomas: identification of novel amplified genes and separate evaluation of the different histological components. J Pathol 208(4):554-563. doi: 10.1002/path.1925
13. Gibson P, Tong Y, Robinson G, Thompson MC, Currle DS, Eden C, Kranenburg TA, Hogg T, Poppleton H, Martin J, Finkelstein D, Pounds S, Weiss A, Patay Z, Scoggins M, Ogg R, Pei Y, Yang ZJ, Brun S, Lee Y, Zindy F, Lindsey JC, Taketo MM, Boop FA, Sanford RA, Gajjar A, Clifford SC, Roussel MF, McKinnon PJ, Gutmann DH, Ellison DW, Wechsler-Reya R, Gilbertson RJ (2010) Subtypes of medulloblastoma have distinct developmental origins. Nature 468(7327):1095-1099. doi: 10.1038/nature09587
14. Hui AB, Takano H, Lo KW, Kuo WL, Lam CN, Tong CY, Chang Q, Gray JW, Ng HK (2005) Identification of a novel homozygous deletion region at 6q23.1 in medulloblastomas using high-resolution array comparative genomic hybridization analysis. Clinical Cancer Res off J Am Assoc Cancer Res 11(13):4707-4716. doi: 10.1158/1078-0432.CCR-05-0128
15. Jones DT, Jager N, Kool M, Zichner T, Hutter B, Sultan M, Cho YJ, Pugh TJ, Hovestadt V, Stutz AM, Rausch T, Warnatz HJ, Ryzhova M, Bender S, Sturm D, Pleier S, Cin H, Pfaff E, Sieber L, Wittmann A, Remke M, Witt H, Hutter S, Tzaridis T, Weischenfeldt J, Raeder B, Avci M, Amstislavskiy V, Zapatka M, Weber UD, Wang Q, Lasitschka B, Bartholomae CC, Schmidt M, von Kalle C, Ast V, Lawerenz C, Eils J, Kabbe R, Benes V, van Sluis P, Koster J, Volckmann R, Shih D, Betts MJ, Russell RB, Coco S, Tonini GP, Schuller U, Hans V, Graf N, Kim YJ, Monoranu C, Roggendorf W, Unterberg A, Herold-Mende C, Milde T, Kulozik AE, von Deimling A, Witt O, Maass E, Rossler J, Ebinger M, Schuhmann MU, Fruhwald MC, Hasselblatt M, Jabado N, Rutkowski S, von Bueren AO, Williamson D, Clifford SC, McCabe MG, Collins VP, Wolf S, Wiemann S, Lehrach H, Brors B, Scheurlen W, Felsberg J, Reifenberger G, Northcott PA, Taylor MD, Meyerson M, Pomeroy SL, Yaspo ML, Korbel JO, Korshunov A, Eils R, Pfister SM, Lichter P (2012) Dissecting the genomic complexity underlying medulloblastoma. Nature 488(7409):100-105. doi: 10.1038/nature11284
16. Kool M, Korshunov A, Remke M, Jones DT, Schlanstein M, Northcott PA, Cho YJ, Koster J, Schouten-van Meeteren A, van Vuurden D, Clifford SC, Pietsch T, von Bueren AO, Rutkowski S, McCabe M, Collins VP, Backlund ML, Haberler C, Bourdeaut F, Delattre O, Doz F, Ellison DW, Gilbertson RJ, Pomeroy SL, Taylor MD, Lichter P, Pfister SM (2012) Molecular subgroups of medulloblastoma: an international meta-analysis of transcriptome, genetic aberrations, and clinical data of WNT, SHH, Group 3, and Group 4 medulloblastomas. Acta Neuropathol 123(4):473-484. doi: 10.1007/s00401-012-0958-8
17. Kool M, Koster J, Bunt J, Hasselt NE, Lakeman A, van Sluis P, Troost D, Meeteren NS, Caron HN, Cloos J, Mrsic A, Ylstra B, Grajkowska W, Hartmann W, Pietsch T, Ellison D, Clifford SC, Versteeg R (2008) Integrated genomics identifies five medulloblastoma subtypes with distinct genetic profiles, pathway signatures and clinicopathological features. PLoS ONE 3(8):e3088. doi: 10.1371/journal.pone.0003088
18. Lo KC, Rossi MR, Burkhardt T, Pomeroy SL, Cowell JK (2007) Overlay analysis of the oligonucleotide array gene expression profiles and copy number abnormalities as determined by array comparative genomic hybridization in medulloblastomas. Genes Chromosom Cancer 46(1):53-66. doi: 10.1002/gcc.20388
19. McCabe MG, Ichimura K, Liu L, Plant K, Backlund LM, Pearson DM, Collins VP (2006) High-resolution array-based comparative genomic hybridization of medulloblastomas and supratentorial primitive neuroectodermal tumors. J Neuropathol Exp Neurol 65(6):549-561
20. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Iii AD, Diaz E, Lafrance LV, Mellinger M, Duquenne C, Tian X, Kruger RG, McHugh CF, Brandt M, Miller WH, Dhanak D, Verma SK, Tummino PJ, Creasy CL (2012) EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. Nature. doi: 10.1038/nature11606
21. Mendrzyk F, Radlwimmer B, Joos S, Kokocinski F, Benner A, Stange DE, Neben K, Fiegler H, Carter NP, Reifenberger G, Korshunov A, Lichter P (2005) Genomic and protein expression profiling identifies CDK6 as novel independent prognostic marker in medulloblastoma. J Clin Oncol 23(34):8853-8862. doi: 10.1200/JCO.2005.02.8589
22. Northcott PA, Nakahara Y, Wu X, Feuk L, Ellison DW, Croul S, Mack S, Kongkham PN, Peacock J, Dubuc A, Ra YS, Zilberberg K, McLeod J, Scherer SW, Sunil Rao J, Eberhart CG, Grajkowska W, Gillespie Y, Lach B, Grundy R, Pollack IF, Hamilton RL, Van Meter T, Carlotti CG, Boop F, Bigner D, Gilbertson RJ, Rutka JT, Taylor MD (2009) Multiple recurrent genetic events converge on control of histone lysine methylation in medulloblastoma. Nat Genet 41(4):465-472. doi: 10.1038/ng.336
23. Palhan VB, Chen S, Peng GH, Tjernberg A, Gamper AM, Fan Y, Chait BT, La Spada AR, Roeder RG (2005) Polyglutamine-expanded ataxin-7 inhibits STAGA histone acetyltransferase activity to produce retinal degeneration. Proc Natl Acad Sci USA 102(24):8472-8477. doi: 10.1073/pnas.0503505102
24. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, Gallia GL, Jallo GI, Binder ZA, Nikolsky Y, Hartigan J, Smith DR, Gerhard DS, Fults DW, VandenBerg S, Berger MS, Marie SK, Shinjo SM, Clara C, Phillips PC, Minturn JE, Biegel JA, Judkins AR, Resnick AC, Storm PB, Curran T, He Y, Rasheed BA, Friedman HS, Keir ST, McLendon R, Northcott PA, Taylor MD, Burger PC, Riggins GJ, Karchin R, Parmigiani G, Bigner DD, Yan H, Papadopoulos N, Vogelstein B, Kinzler KW, Velculescu VE (2011) The genetic landscape of the childhood cancer medulloblastoma. Science 331(6016):435-439. doi: 10.1126/science.1198056
25. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, Carneiro MO, Carter SL, Cibulskis K, Erlich RL, Greulich H, Lawrence MS, Lennon NJ, McKenna A, Meldrim J, Ramos AH, Ross MG, Russ C, Shefler E, Sivachenko A, Sogoloff B, Stojanov P, Tamayo P, Mesirov JP, Amani V, Teider N, Sengupta S, Francois JP, Northcott PA, Taylor MD, Yu F, Crabtree GR, Kautzman AG, Gabriel SB, Getz G, Jager N, Jones DT, Lichter P, Pfister SM, Roberts TM, Meyerson M, Pomeroy SL, Cho YJ (2012) Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488(7409):106-110. doi: 10.1038/nature11329
26. Ren B, Robert F, Wyrick JJ, Aparicio O, Jennings EG, Simon I, Zeitlinger J, Schreiber J, Hannett N, Kanin E, Volkert TL, Wilson CJ, Bell SP, Young RA (2000) Genome-wide location and function of DNA binding proteins. Science 290(5500):2306-2309. doi: 10.1126/science.290.5500.2306
27. Robinson G, Parker M, Kranenburg TA, Lu C, Chen X, Ding L, Phoenix TN, Hedlund E, Wei L, Zhu X, Chalhoub N, Baker SJ, Huether R, Kriwacki R, Curley N, Thiruvenkatam R, Wang J, Wu G, Rusch M, Hong X, Becksfort J, Gupta P, Ma J, Easton J, Vadodaria B, Onar-Thomas A, Lin T, Li S, Pounds S, Paugh S, Zhao D, Kawauchi D, Roussel MF, Finkelstein D, Ellison DW, Lau CC, Bouffet E, Hassall T, Gururangan S, Cohn R, Fulton RS, Fulton LL, Dooling DJ, Ochoa K, Gajjar A, Mardis ER, Wilson RK, Downing JR, Zhang J, Gilbertson RJ (2012) Novel mutations target distinct subgroups of medulloblastoma. Nature. doi: 10.1038/nature11213
28. Roth RB, Hevezi P, Lee J, Willhite D, Lechner SM, Foster AC, Zlotnik A (2006) Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics 7(2):67-80. doi: 10.1007/s10048-006-0032-6
29. Rugg-Gunn PJ (2012) Epigenetic features of the mouse trophoblast. Reprod Biomed Online. doi: 10.1016/j.rbmo.2012.01.012
30. Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, Sturn A, Snuffin M, Rezantsev A, Popov D, Ryltsov A, Kostukovich E, Borisovsky I, Liu Z, Vinsavich A, Trush V, Quackenbush J (2003) TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34(2):374-378
31. Tan J, Yang X, Zhuang L, Jiang X, Chen W, Lee PL, Karuturi RK, Tan PB, Liu ET, Yu Q (2007) Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells. Genes Dev 21(9):1050-1063. doi: 10.1101/gad.1524107
32. Taylor MD, Northcott PA, Korshunov A, Remke M, Cho YJ, Clifford SC, Eberhart CG, Parsons DW, Rutkowski S, Gajjar A, Ellison DW, Lichter P, Gilbertson RJ, Pomeroy SL, Kool M, Pfister SM (2012) Molecular subgroups of medulloblastoma: the current consensus. Acta Neuropathol 123(4):465-472. doi: 10.1007/s00401-011-0922-z
33. Young MD, Willson TA, Wakefield MJ, Trounson E, Hilton DJ, Blewitt ME, Oshlack A, Majewski IJ (2011) ChIP-seq analysis reveals distinct H3K27me3 profiles that correlate with transcriptional activity. Nucleic Acids Res 39(17):7415-7427. doi: 10.1093/nar/gkr416