Supratentorial and spinal pediatric ependymomas display a hypermethylated phenotype which includes the loss of tumor suppressor genes involved in the control of cell growth and death

Acta Neuropathologica

Volumn 123, Issue 5, 2012, Pages 711-725

  Rogers, Hazel A ^a   Kilday, John Paul ^a   Mayne, Cerys ^a   Ward, Jennifer ^a   Adamowicz Brice, Martyna ^a   Schwalbe, Ed C ^b   Clifford, Steven C ^b   Coyle, Beth ^a   Grundy, Richard G ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Apoptosis; Ependymoma; Immune system; JNK pathway; Methylation

Indexed keywords

CASPASE RECRUITMENT DOMAIN PROTEIN 15; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; JANUS KINASE; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A;

APOPTOSIS; ARTICLE; BRAIN REGION; CELL DEATH; CELL GROWTH; CONTROLLED STUDY; CPG ISLAND; DNA EXTRACTION; DNA METHYLATION; DOWN REGULATION; EPENDYMOMA; EPIGENETICS; GENE DOSAGE; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOSS; GENE SILENCING; HUMAN; IMMUNE SYSTEM; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SPINAL CORD TUMOR; TUMOR SUPPRESSOR GENE; UPREGULATION;

APOPTOSIS; CELL PROLIFERATION; CHILD; CLUSTER ANALYSIS; COHORT STUDIES; DNA METHYLATION; EPENDYMOMA; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HUMANS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; SIGNAL TRANSDUCTION; SPINAL NEOPLASMS; STATISTICS AS TOPIC; SUPRATENTORIAL NEOPLASMS;

EID: 84862649418     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0904-1     Document Type: Article

References (76)

1. Agathanggelou A, Cooper WN, Latif F (2005) Role of the Rasassociation domain family 1 tumor suppressor gene in human cancers. Cancer Res 65:3497-3508 (Pubitemid 40616319)
2. Alonso ME, Bello MJ, Gonzalez-Gomez P et al (2004) Aberrant CpG island methylation of multiple genes in ependymal tumors. J Neurooncol 67:159-165 (Pubitemid 38418264)
3. Benedetti E, Galzio R, Cinque B et al (2008) Biomolecular characterization of human glioblastoma cells in primary cultures: differentiating and antiangiogenic effects of natural and synthetic PPARgamma agonists. J Cell Physiol 217:93-102
4. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc B Methodol 57:289-300
5. Bestor TH (2000) The DNA methyltransferases of mammals. Hum Mol Genet 9:2395-2402
6. Bird AP, Wolffe AP (1999) Methylation-induced repression: belts, braces, and chromatin. Cell 99:451-454 (Pubitemid 129746827)
7. Borsani G, DeGrandi A, Ballabio A et al (1999) EYA4, a novel vertebrate gene related to Drosophila eyes absent. Hum Mol Genet 8:11-23 (Pubitemid 29039044)
8. Cairns JM, Dunning MJ, Ritchie ME, Russell R, Lynch AG (2008) BASH: a tool for managing BeadArray spatial artefacts. Bioinformatics 24:2921-2922
9. Chen Y, Miller C, Mosher R et al (2003) Identification of cervical cancer markers by cDNA and tissue microarrays. Cancer Res 63:1927-1935 (Pubitemid 36460860)
10. Christensen BC, Smith AA, Zheng S et al (2011) DNA methylation, isocitrate dehydrogenase mutation, and survival in glioma. J Natl Cancer Inst 103:143-153
11. Cimini A, Cristiano L, Colafarina S et al (2005) PPARgammadependent effects of conjugated linoleic acid on the human glioblastoma cell line (ADF). Int J Cancer 117:923-933 (Pubitemid 41688566)
12. Conway K, Edmiston SN, Khondker ZS et al (2011) DNAmethylation profiling distinguishes malignant melanomas from benign nevi. Pigment Cell Melanoma Res 24:352-360
13. Costello JF, Fruhwald MC, Smiraglia DJ et al (2000) Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat Genet 24:132-138 (Pubitemid 30094712)
14. Davis RJ (2000) Signal transduction by the JNK group of MAP kinases. Cell 103:239-252
15. De Filippis L, Lamorte G, Snyder EY, Malgaroli A, Vescovi AL (2007) A novel, immortal, and multipotent human neural stem cell line generating functional neurons and oligodendrocytes. Stem Cells 25:2312-2321 (Pubitemid 47480490)
16. Donson AM, Birks DK, Barton VN et al (2009) Immune gene and cell enrichment is associated with a good prognosis in ependymoma. J Immunol 183:7428-7440
17. Dunn GP, Old LJ, Schreiber RD (2004) The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21: 137-148 (Pubitemid 39094044)
18. Eden A, Gaudet F, Waghmare A, Jaenisch R (2003) Chromosomal instability and tumors promoted by DNA hypomethylation. Science 300:455 (Pubitemid 36444319)
19. Feinberg AP, Gehrke CW, Kuo KC, Ehrlich M (1988) Reduced genomic 5-methylcytosine content in human colonic neoplasia. Cancer Res 48:1159-1161 (Pubitemid 18075525)
20. Gibbs JR, van der Brug MP, Hernandez DG et al (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet 6:e1000952
21. Grommes C, Landreth GE, Sastre M et al (2006) Inhibition of in vivo glioma growth and invasion by peroxisome proliferatoractivated receptor gamma agonist treatment. Mol Pharmacol 70:1524-1533
22. Hamilton DW, Lusher ME, Lindsey JC, Ellison DW, Clifford SC (2005) Epigenetic inactivation of the RASSF1A tumour suppressor gene in ependymoma. Cancer Lett 227:75-81 (Pubitemid 41033094)
23. Hermann A, Gowher H, Jeltsch A (2004) Biochemistry and biology of mammalian DNA methyltransferases. Cell Mol Life Sci 61:2571-2587 (Pubitemid 39586518)
24. Houshdaran S, Hawley S, Palmer C et al (2010) DNA methylation profiles of ovarian epithelial carcinoma tumors and cell lines. PLoS One 5:e9359
25. Huang da W, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1-13
26. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57
27. Issa JP (2003) Methylation and prognosis: of molecular clocks and hypermethylator phenotypes. Clin Cancer Res 9:2879-2881
28. Johnson RA, Wright KD, Poppleton H et al (2010) Cross-species genomics matches driver mutations and cell compartments to model ependymoma. Nature 466:632-636
29. Khin SS, Kitazawa R, Kondo T et al (2011) Epigenetic alteration by DNA promoter hypermethylation of genes related to transforming growth factor-b (TGF-b) signaling in cancer. Cancers 3:982-993
30. Kilday JP, Rahman R, Dyer S et al (2009) Pediatric ependymoma: biological perspectives. Mol Cancer Res 7:765-786
31. Kim TK, Kim T, Kim TY, Lee WG, Yim J (2000) Chemotherapeutic DNA-damaging drugs activate interferon regulatory factor-7 by the mitogen-activated protein kinase kinase-4-cJun NH2-terminal kinase pathway. Cancer Res 60:1153-1156 (Pubitemid 30151972)
32. Kuan CY, Whitmarsh AJ, Yang DD et al (2003) A critical role of neural-specific JNK3 for ischemic apoptosis. Proc Natl Acad Sci USA 100:15184-15189 (Pubitemid 37518037)
33. Kuan CY, Yang DD, Samanta Roy DR, Davis RJ, Rakic P, Flavell RA (1999) The Jnk1 and Jnk2 protein kinases are required for regional specific apoptosis during early brain development. Neuron 22:667-676 (Pubitemid 29203491)
34. Ladd-Acosta C, Pevsner J, Sabunciyan S et al (2007) DNA methylation signatures within the human brain. Am J Hum Genet 81:1304-1315 (Pubitemid 350211460)
35. Laffaire J, Everhard S, Idbaih A et al (2011) Methylation profiling identifies 2 groups of gliomas according to their tumorigenesis. Neuro Oncol 13:84-98
36. Liang P, Song F, Ghosh S et al (2011) Genome-wide survey reveals dynamic widespread tissue-specific changes in DNA methylation during development. BMC Genomics 12:231
37. Liu RZ, Mita R, Beaulieu M, Gao Z, Godbout R (2010) Fatty acid binding proteins in brain development and disease. Int J Dev Biol 54:1229-1239
38. Louis DN, Ohgaki H, Wiestler OD et al (2007) The 2007 WHO Classification of Tumours of the Central Nervous System. Acta Neuropathol (Berl) 114:97-109 (Pubitemid 47103521)
39. Ma XJ, Salunga R, Tuggle JT et al (2003) Gene expression profiles of human breast cancer progression. Proc Natl Acad Sci USA 100:5974-5979 (Pubitemid 36576916)
40. Mack SC, Taylor MD (2009) The genetic and epigenetic basis of ependymoma. Childs Nerv Syst 25:1195-1201
41. Mao R, Wang X, Spitznagel EL Jr et al (2005) Primary and secondary transcriptional effects in the developing human Down syndrome brain and heart. Genome Biol 6:R107
42. Martin JH, Mohit AA, Miller CA (1996) Developmental expression in the mouse nervous system of the p493F12 SAP kinase. Brain Res Mol Brain Res 35:47-57
43. Matallanas D, Romano D, Yee K et al (2007) RASSF1A elicits apoptosis through an MST2 pathway directing proapoptotic transcription by the p73 tumor suppressor protein. Mol Cell 27: 962-975 (Pubitemid 47495894)
44. McCabe MT, Brandes JC, Vertino PM (2009) Cancer DNA methylation: molecular mechanisms and clinical implications. Clin Cancer Res 15:3927-3937
45. McGuire CS, Sainani KL, Fisher PG (2009) Both location and age predict survival in ependymoma: a SEER study. Pediatr Blood Cancer 52:65-69
46. Michalowski MB, de Fraipont F, Michelland S et al (2006) Methylation of RASSF1A and TRAIL pathway-related genes is frequent in childhood intracranial ependymomas and benign choroid plexus papilloma. Cancer Genet Cytogenet 166:74-81
47. Miremadi A, Oestergaard MZ, Pharoah PD, Caldas C (2007) Cancer genetics of epigenetic genes. Hum Mol Genet 16 Spec No 1:R28-R49 (Pubitemid 47241841)
48. Modena P, Lualdi E, Facchinetti F et al (2006) Identification of tumor-specific molecular signatures in intracranial ependymoma and association with clinical characteristics. J Clin Oncol 24: 5223-5233 (Pubitemid 46631366)
49. Noushmehr H, Weisenberger DJ, Diefes K et al (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17:510-522
50. Oster B, Thorsen K, Lamy P et al (2011) Identification and validation of highly frequent CpG island hypermethylation in colorectal adenomas and carcinomas. Int J Cancer 129(12): 2855-2866
51. Owada Y, Yoshimoto T, Kondo H (1996) Spatio-temporally differential expression of genes for three members of fatty acid binding proteins in developing and mature rat brains. J Chem Neuroanat 12:113-122 (Pubitemid 27056799)
52. Palm T, Figarella-Branger D, Chapon F et al (2009) Expression profiling of ependymomas unravels localization and tumor gradespecific tumorigenesis. Cancer 115:3955-3968
53. Pancione M, Di Blasi A, Sabatino L et al (2011) A novel case of rhabdoid colon carcinoma associated with a positive CpG island methylator phenotype and BRAF mutation. Hum Pathol 42(7): 1047-1052
54. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45
55. Pike BL, Greiner TC, Wang X et al (2008) DNA methylation profiles in diffuse large B-cell lymphoma and their relationship to gene expression status. Leukemia 22:1035-1043 (Pubitemid 351689886)
56. Rauch TA, Zhong X, Wu X et al (2008) High-resolution mapping of DNA hypermethylation and hypomethylation in lung cancer. Proc Natl Acad Sci U S A 105:252-257
57. Richter AM, Pfeifer GP, Dammann RH (2009) The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim Biophys Acta 1796:114-128
58. Rousseau E, Ruchoux MM, Scaravilli F et al (2003) CDKN2A, CDKN2B and p14ARF are frequently and differentially methylated in ependymal tumours. Neuropathol Appl Neurobiol 29: 574-583 (Pubitemid 37548352)
59. Schwartzbaum JA, Huang K, Lawler S, Ding B, Yu J, Chiocca EA (2010) Allergy and inflammatory transcriptome is predominantly negatively correlated with CD133 expression in glioblastoma. Neuro Oncol 12:320-327
60. Smiraglia DJ, Rush LJ, Fruhwald MC et al (2001) Excessive CpG island hypermethylation in cancer cell lines versus primary human malignancies. Hum Mol Genet 10:1413-1419 (Pubitemid 32640670)
61. Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22:1540-1542 (Pubitemid 43985330)
62. Taylor MD, Poppleton H, Fuller C et al (2005) Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8:323-335 (Pubitemid 41443417)
63. Toyota M, Ahuja N, Ohe-Toyota M, Herman JG, Baylin SB, Issa JP (1999) CpG island methylator phenotype in colorectal cancer. Proc Natl Acad Sci U S A 96:8681-8686 (Pubitemid 29354851)
64. Waha A, Koch A, Hartmann W et al (2004) Analysis of HIC-1 methylation and transcription in human ependymomas. Int J Cancer 110:542-549 (Pubitemid 38658019)
65. Wang Q, Williamson M, Bott S et al (2007) Hypomethylation of WNT5A, CRIP1 and S100P in prostate cancer. Oncogene 26:6560-6565 (Pubitemid 47530597)
66. Wei J, Barr J, Kong LY et al (2010) Glioma-associated cancerinitiating cells induce immunosuppression. Clin Cancer Res 16: 461-473
67. Weisenberger DJ, Siegmund KD, Campan M et al (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38:787-793 (Pubitemid 43980599)
68. Wright KD, Gajjar A (2009) New chemotherapy strategies and biological agents in the treatment of childhood ependymoma. Childs Nerv Syst 25:1275-1282
69. Xie H, Wang M, Bonaldo Mde F et al (2010) Epigenomic analysis of Alu repeats in human ependymomas. Proc Natl Acad Sci U S A 107:6952-6957
70. Xu PX, Adams J, Peters H, Brown MC, Heaney S, Maas R (1999) Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia. Nat Genet 23:113-117 (Pubitemid 29418800)
71. Yang DD, Kuan CY, Whitmarsh AJ et al (1997) Absence of excitotoxicity-induced apoptosis in the hippocampus of mice lacking the Jnk3 gene. Nature 389:865-870 (Pubitemid 27462982)
72. Ying J, Li H, Cui Y, Wong AH, Langford C, Tao Q (2006) Epigenetic disruption of two proapoptotic genes MAPK10/JNK3 and PTPN13/FAP-1 in multiple lymphomas and carcinomas through hypermethylation of a common bidirectional promoter. Leukemia 20:1173-1175 (Pubitemid 43797318)
73. Yoshida S, Fukino K, Harada H et al (2001) The c-Jun NH2- terminal kinase3 (JNK3) gene: genomic structure, chromosomal assignment, and loss of expression in brain tumors. J Hum Genet 46:182-187 (Pubitemid 32435600)
74. Yuen RK, Neumann SM, Fok AK et al (2011) Extensive epigenetic reprogramming in human somatic tissues between fetus and adult. Epigenetics Chromatin 4:7
75. Zacharoulis S, Levy A, Chi SN et al (2007) Outcome for young children newly diagnosed with ependymoma, treated with intensive induction chemotherapy followed by myeloablative chemotherapy and autologous stem cell rescue. Pediatr Blood Cancer 49:34-40 (Pubitemid 46847065)
76. Zou H, Osborn NK, Harrington JJ et al (2005) Frequent methylation of eyes absent 4 gene in Barrett's esophagus and esophageal adenocarcinoma. Cancer Epidemiol Biomarkers Prev 14:830-834 (Pubitemid 40478544)