Widespread resetting of DNA methylation in glioblastoma-initiating cells suppresses malignant cellular behavior in a lineage-dependent manner

Genes and Development

Volumn 27, Issue 6, 2013, Pages 654-669

  Stricker, Stefan H ^a,b   Feber, Andrew ^a   Engström, Pär G ^c   Carén, Helena ^a   Kurian, Kathreena M ^d   Takashima, Yasuhiro ^e,f   Watts, Colin ^f,g   Way, Michael ^h   Dirks, Peter ⁱ   Bertone, Paul ^c,e,j,k   Smith, Austin ^e,f   Beck, Stephan ^a   Pollard, Steven M ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Samantha Dickson Brain Cancer Unit   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d FRENCHAY HOSPITAL   (United Kingdom)

^e University of Cambridge   (United Kingdom)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h THE FRANCIS CRICK INSTITUTE   (United Kingdom)

ⁱ HOSPITAL FOR SICK CHILDREN   (Canada)

^j Genome Biology Unit   (Germany)

^k EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

more..

Author keywords

DNA methylation; Epigenetics; Glioblastoma; Neural stem cell; Reprogramming

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; POLYCOMB REPRESSIVE COMPLEX 2; SECRETED FRIZZLED RELATED PROTEIN 2; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TES; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CARCINOGENICITY; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOTILITY; CONTROLLED STUDY; DNA METHYLATION; EPIGENETICS; GLIOBLASTOMA; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; XENOTRANSPLANTATION;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL LINEAGE; CELL TRANSFORMATION, NEOPLASTIC; DNA METHYLATION; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOBLASTOMA; HUMANS; MICE; MICE, INBRED NOD; NEURAL STEM CELLS; NUCLEAR REPROGRAMMING; PLURIPOTENT STEM CELLS; TRANSPLANTATION, HETEROLOGOUS;

EID: 84875340771     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.212662.112     Document Type: Article

References (43)

1. Avissar-Whiting M, Koestler DC, Houseman EA, Christensen BC, Kelsey KT, Marsit CJ. 2011. Polycomb group genes are targets of aberrant DNA methylation in renal cell carcinoma. Epigenetics 6: 703-709.
2. Baylin S, Bestor TH. 2002. Altered methylation patterns in cancer cell genomes: Cause or consequence? Cancer Cell 1: 299-305.
3. Bennett LB, Schnabel JL, Kelchen JM, Taylor KH, Guo J, Arthur GL, Papageorgio CN, Shi H, Caldwell CW. 2009. DNA hypermethylation accompanied by transcriptional repression in follicular lymphoma. Genes Chromosomes Cancer 48: 828-841.
4. Boeda B, Briggs DC, Higgins T, Garvalov BK, Fadden AJ, McDonald NQ, Way M. 2007. Tes, a specific Mena interacting partner, breaks the rules for EVH1 binding. Mol Cell 28: 1071-1082.
5. Cancer Genome Atlas Research Network. 2008. Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455: 1061-1068.
6. Carette JE, Pruszak J, Varadarajan M, Blomen VA, Gokhale S, Camargo FD, Wernig M, Jaenisch R, Brummelkamp TR. 2010. Generation of iPSCs from cultured human malignant cells. Blood 115: 4039-4042.
7. Christensen BC, Smith AA, Zheng S, Koestler DC, Houseman EA, Marsit CJ, Wiemels JL, Nelson HH, Karagas MR, Wrensch MR, et al. 2011. DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. J Natl Cancer Inst 103: 143-153.
8. Dvinge H, Bertone P. 2009. HTqPCR: High-throughput analysis and visualization of quantitative real-time PCR data in R. Bioinformatics 25: 3325-3326.
9. Engström PG, Tommei D, Stricker SH, Ender C, Pollard SM, Bertone P. 2012. Digital transcriptome profiling of normal and glioblastoma-derived neural stem cells identifies genes associated with patient survival. Genome Med 4: 76.
10. Fael Al-Mayhani TM, Ball SL, Zhao JW, Fawcett J, Ichimura K, Collins PV, Watts C. 2009. An efficient method for derivation and propagation of glioblastoma cell lines that conserves the molecular profile of their original tumours. J Neurosci Methods 176: 192-199.
11. Falk A, Koch P, Kesavan J, Takashima Y, Ladewig J, Alexander M, Wiskow O, Tailor J, Trotter M, Pollard S, et al. 2012. Capture of neuroepithelial-like stem cells from pluripotent stem cells provides a versatile system for in vitro production of human neurons. PLoS ONE 7: e29597.
12. Feinberg AP, Ohlsson R, Henikoff S. 2006. The epigenetic progenitor origin of human cancer. Nat Rev Genet 7: 21-33.
13. Fourkala E-O, Hauser-Kronberger C, Apostolidou S, Burnell M, Jones A, Grall J, Reitsamer R, Fiegl H, Jacobs I, Menon U, et al. 2010. DNA methylation of polycomb group target genes in cores taken from breast cancer centre and periphery. Breast Cancer Res Treat 120: 345-355.
14. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, DiMeco F, Vescovi A. 2004. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64: 7011-7021.
15. Hanahan D, Weinberg RA. 2000. The hallmarks of cancer. Cell 100: 57-70.
16. Holm TM, Jackson-Grusby L, Brambrink T, Yamada Y, Rideout WM, Jaenisch R. 2005. Global loss of imprinting leads to widespread tumorigenesis in adult mice. Cancer Cell 8: 275-285.
17. Jones PA, Baylin SB. 2007. The epigenomics of cancer. Cell 128: 683-692.
18. Kaji K, Norrby K, Paca A, Mileikovsky M, Mohseni P, Woltjen K. 2009. Virus-free induction of pluripotency and subsequent excision of reprogramming factors. Nature 458: 771-775.
19. Kavanagh E, Joseph B. 2011. The hallmarks of CDKN1C (p57, KIP2) in cancer. Biochim Biophys Acta 1816: 50-56.
20. Kim JB, Zaehres H, Wu G, Gentile L, Ko K, Sebastiano V, Arauzo-Bravo MJ, Ruau D, Han DW, Zenke M, et al. 2008. Pluripotent stem cells induced from adult neural stem cells by reprogramming with two factors. Nature 454: 646-650.
21. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, Donin NM, Pastorino S, Purow BW, Christopher N, Zhang W, et al. 2006. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9: 391-403.
22. Martinez R, Martin-Subero JI, Rohde V, Kirsch M, Alaminos M, Fernandez AF, Ropero S, Schackert G, Esteller M. 2009. A microarray-based DNA methylation study of glioblastoma multiforme. Epigenetics 4: 255-264.
23. Miyoshi N, Ishii H, Nagai K, Hoshino H, Mimori K, Tanaka F, Nagano H, Sekimoto M, Doki Y, Mori M. 2010. Defined factors induce reprogramming of gastrointestinal cancer cells. Proc Natl Acad Sci 107: 40-45.
24. Mueller W, Nutt CL, Ehrich M, Riemenschneider MJ, von Deimling A, van den Boom D, Louis DN. 2007. Downregulation of RUNX3 and TES by hypermethylation in glioblastoma. Oncogene 26: 583-593.
25. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, et al. 2010. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17: 510-522.
26. Pateras IS, Apostolopoulou K, Koutsami M, Evangelou K, Tsantoulis P, Liloglou T, Nikolaidis G, Sigala F, Kittas C, Field JK, et al. 2006. Downregulation of the KIP family members p27(KIP1) and p57(KIP2) by SKP2 and the role of methylation in p57(KIP2) inactivation in nonsmall cell lung cancer. Int J Cancer 119: 2546-2556.
27. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, Russell R, Bayani J, Head R, Lee M, Bernstein M, et al. 2009. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4: 568-580.
28. Qiu H, Zhu J, Yuan C, Yan S, Yang Q, Kong B. 2010. Frequent hypermethylation and loss of heterozygosity of the testis derived transcript gene in ovarian cancer. Cancer Sci 101: 1255-1260.
29. Rizwana R, Hahn PJ. 1998. CpG islands and double-minute chromosomes. Genomics 51: 207-215.
30. Ron-Bigger S, Bar-Nur O, Isaac S, Bocker M, Lyko F, Eden A. 2010. Aberrant epigenetic silencing of tumor suppressor genes is reversed by direct reprogramming. Stem Cells 28: 1349-1354.
31. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, Eden E, Yakhini Z, Ben-Shushan E, Reubinoff BE, et al. 2007. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet 39: 232-236.
32. Schwartzentruber J, Korshunov A, Liu X-Y, Jones DTW, Pfaff E, Jacob K, Sturm D, Fontebasso AM, Quang D-AK, Tönjes M, et al. 2012. Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482: 226-231.
33. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res 63: 5821-5828.
34. Sturm D, Witt H, Hovestadt V, Khuong-Quang D-A, Jones DTW, Konermann C, Pfaff E, Tönjes M, Sill M, Bender S, et al. 2012. Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22: 425-437.
35. Sun Y, Pollard S, Conti L, Toselli M, Biella G, Parkin G, Willatt L, Falk A, Cattaneo E, Smith A. 2008. Long-term tripotent differentiation capacity of human neural stem (NS) cells in adherent culture. Mol Cell Neurosci 38: 245-258.
36. Suzuki H, Watkins DN, Jair K-W, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M, et al. 2004. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 36: 417-422.
37. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. 2007. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131: 861-872.
38. Tatarelli C, Linnenbach A, Mimori K, Croce CM. 2000. Characterization of the human TESTIN gene localized in the FRA7G region at 7q31.2. Genomics 68: 1-12.
39. Tobias ES, Hurlstone AF, MacKenzie E, McFarlane R, Black DM. 2001. The TES gene at 7q31.1 is methylated in tumours and encodes a novel growth-suppressing LIM domain protein. Oncogene 20: 2844-2853.
40. Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, Miller CR, Ding L, Golub T, Mesirov JP, et al. 2010. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 17: 98-110.
41. Ward RJ, Dirks PB. 2007. Cancer stem cells: At the headwaters of tumor development. Annu Rev Pathol 2: 175-189.
42. Weeks RJ, Kees UR, Song S, Morison IM. 2010. Silencing of TESTIN by dense biallelic promoter methylation is the most common molecular event in childhood acute lymphoblastic leukaemia. Mol Cancer 9: 163.
43. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, Weisenberger DJ, Campan M, Young J, Jacobs I, et al. 2007. Epigenetic stem cell signature in cancer. Nat Genet 39: 157-158.