DNA hypermethylation profiles associated with glioma subtypes and EZH2 and IGFBP2 mRNA expression

Neuro-Oncology

Volumn 13, Issue 3, 2011, Pages 280-289

  Zheng, Shichun ^a   Houseman, E Andres ^b   Morrison, Zachary ^a   Wrensch, Margaret R ^a   Patoka, Joseph S ^a   Ramos, Christian ^a   Haas Kogan, Daphne A ^a   McBride, Sean ^a   Marsit, Carmen J ^b   Christensen, Brock C ^b   Nelson, Heather H ^d   Stokoe, David ^c   Wiemels, Joseph L ^a   Chang, Susan M ^a   Prados, Michael D ^a   Tihan, Tarik ^a   Vandenberg, Scott R ^a   Kelsey, Karl T ^b   Berger, Mitchel S ^a   Wiencke, John K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BROWN UNIVERSITY   (United States)

^c GENENTECH INC   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

DNA methylation; EZH2; Glioma; PI3K Akt; Polycomb

Indexed keywords

MEMBRANE PROTEIN; MESSENGER RNA; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MYELIN PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN EMP3; PROTEIN RFX1; PROTEIN TMS1; PROTEIN ZNF342; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; SLIT2 PROTEIN; SOMATOMEDIN BINDING PROTEIN 2; SUPPRESSOR OF CYTOKINE SIGNALING 1; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ADULT; ARTICLE; ASTROCYTOMA; BRAIN TISSUE; CANCER SURVIVAL; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME DELETION; CLUSTER ANALYSIS; DNA METHYLATION; DNA STRUCTURE; FEMALE; GENE EXPRESSION; GLIOBLASTOMA; GLIOMA; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; LONG INTERSPERSED NUCLEAR ELEMENT 1; MAJOR CLINICAL STUDY; MALE; OLIGODENDROGLIOMA; PHENOTYPE; POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL TIME;

ADOLESCENT; ADULT; BRAIN NEOPLASMS; DNA METHYLATION; DNA, NEOPLASM; DNA-BINDING PROTEINS; FEMALE; GENE AMPLIFICATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 2; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; MIDDLE AGED; POLYMERASE CHAIN REACTION; PROGNOSIS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, MESSENGER; SURVIVAL RATE; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS; YOUNG ADULT;

EID: 79955765058     PISSN: 15228517     EISSN: 15235866     Source Type: Journal    
DOI: 10.1093/neuonc/noq190     Document Type: Article

References (62)

1. Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol (Berl). 2007;114(2):97-109. (Pubitemid 47103521)
2. Wiencke JK, Aldape K, McMillan A, et al. Molecular features of adult glioma associated with patient race/ethnicity, age, and a polymorphism in O6-methylguanine-DNA-methyltransferase. Cancer Epidemiol Biomarkers Prev. 2005;14(7):1774-1783. (Pubitemid 40995094)
3. Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol. 2007;170(5):1445-1453. (Pubitemid 47339290)
4. Furnari FB, Fenton T, Bachoo RM, et al. Malignant astrocytic glioma: Genetics, biology, and paths to treatment. Genes Dev. 2007;21(21):2683-2710. (Pubitemid 350070717)
5. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128(4):683-692. (Pubitemid 46273572)
6. Kunitz A, Wolter M, van den Boom J, et al. DNA hypermethylation and aberrant expression of the EMP3 gene at 19q13.3 in human gliomas. Brain Pathol. 2007;17(4):363-370. (Pubitemid 47537593)
7. Nakamura M, Ishida E, Shimada K, et al. Frequent LOH on 22q12.3 and TIMP-3 inactivation occur in the progression to secondary glioblastomas. Lab Invest. 2005;85(2):165-175. (Pubitemid 40208920)
8. Nakamura M, Watanabe T, Yonekawa Y, Kleihues P, Ohgaki H. Promoter methylation of the DNA repair gene MGMT in astrocytomas is frequently associated with G:C -. A:T mutations of the TP53 tumor suppressor gene. Carcinogenesis. 2001;22(10):1715-1719.
9. Nakamura M, Yonekawa Y, Kleihues P, Ohgaki H. Promoter hypermethylation of the RB1 gene in glioblastomas. Lab Invest. 2001;81(1):77-82. (Pubitemid 32108641)
10. Wiencke JK, Zheng S, Jelluma N, et al. Methylation of the PTEN promoter defines low-grade gliomas and secondary glioblastoma. Neuro Oncol. 2007;9(3):271-279. (Pubitemid 47169659)
11. Costello JF, Plass C, Cavenee WK. Aberrant methylation of genes in low-grade astrocytomas. Brain Tumor Pathol. 2000;17(2):49-56.
12. Dong SM, Pang JC, Poon WS, et al. Concurrent hypermethylation of multiple genes is associated with grade of oligodendroglial tumors. J Neuropathol Exp Neurol. 2001;60(8):808-816. (Pubitemid 32678261)
13. Uhlmann K, Rohde K, Zeller C, et al. Distinct methylation profiles of glioma subtypes. Int J Cancer. 2003;106(1):52-59. (Pubitemid 36750387)
14. Weller M, Stupp R, Reifenberger G, et al. MGMT promoter methylation in malignant gliomas: Ready for personalized medicine? Nat Rev Neurol. 2010;6(1):39-51.
15. Michalowski MB, de Fraipont F, Michelland S, et al. Methylation of RASSF1A and TRAIL pathway-related genes is frequent in childhood intracranial ependymomas and benign choroid plexus papilloma. Cancer Genet Cytogenet. 2006;166(1):74-81.
16. Ohashi Y, Ueda M, Kawase T, Kawakami Y, Toda M. Identification of an epigenetically silenced gene, RFX1, in human glioma cells using restriction landmark genomic scanning. Oncogene. 2004;23(47): 7772-7779. (Pubitemid 39457027)
17. Alaminos M, Davalos V, Ropero S, et al. EMP3, a myelin-related gene located in the critical 19q13.3 region, is epigenetically silenced and exhibits features of a candidate tumor suppressor in glioma and neuroblastoma. Cancer Res. 2005;65(7):2565-2571. (Pubitemid 40490052)
18. Stone AR, Bobo W, Brat DJ, Devi NS, Van Meir EG, Vertino PM. Aberrant methylation and down-regulation of TMS1/ASC in human glioblastoma. Am J Pathol. 2004;165(4):1151-1161. (Pubitemid 39297722)
19. Hong C, Bollen AW, Costello JF. The contribution of genetic and epigenetic mechanisms to gene silencing in oligodendrogliomas. Cancer Res. 2003;63(22):7600-7605. (Pubitemid 37466680)
20. Martini M, Pallini R, Luongo G, Cenci T, Lucantoni C, Larocca LM. Prognostic relevance of SOCS3 hypermethylation in patients with glioblastoma multiforme. Int J Cancer. 2008;123(12):2955-2960.
21. Maegawa S, Yoshioka H, Itaba N, et al. Epigenetic silencing of PEG3 gene expression in human glioma cell lines. Mol Carcinog. 2001;31(1):1-9. (Pubitemid 32520662)
22. Yu J, Zhang H, Gu J, et al. Methylation profiles of thirty four promoter-CpG islands and concordant methylation behaviours of sixteen genes that may contribute to carcinogenesis of astrocytoma. BMC Cancer. 2004;4(1):65.
23. Alaminos M, Davalos V, Cheung NK, Gerald WL, Esteller M. Clustering of gene hypermethylation associated with clinical risk groups in neuroblastoma. J Natl Cancer Inst. 2004;96(16):1208-1219. (Pubitemid 39232712)
24. Dallol A, Krex D, Hesson L, Eng C, Maher ER, Latif F. Frequent epigenetic inactivation of the SLIT2 gene in gliomas. Oncogene. 2003;22(29):4611-4616. (Pubitemid 36920705)
25. Ohm JE, McGarvey KM, Yu X, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat Genet. 2007;39(2):237-242. (Pubitemid 46184356)
26. Rajasekhar VK, Dalerba P, Passegue E, Lagasse E, Najbauer J. Stem cells, cancer, and context dependence. Stem Cells. 2007;26:292-298.
27. Vire E, Brenner C, Deplus R, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature. 2006;439(7078):871-874. (Pubitemid 43255707)
28. Keshet I, Schlesinger Y, Farkash S, et al. Evidence for an instructive mechanism of de novo methylation in cancer cells. Nat Genet. 2006;38(2):149-153. (Pubitemid 43177227)
29. Ohm JE, Baylin SB. Stem cell chromatin patterns: An instructive mechanism for DNA hypermethylation? Cell Cycle. 2007;6(9):1040-1043. (Pubitemid 46708576)
30. Schlesinger Y, Straussman R, Keshet I, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nat Genet. 2007;39(2):232-236. (Pubitemid 46184355)
31. Bachmann N, Hoegel J, Haeusler J, et al. Mutation screen and association study of EZH2 as a susceptibility gene for aggressive prostate cancer. Prostate. 2005;65(3):252-259. (Pubitemid 41443730)
32. Berezovska OP, Glinskii AB, Yang Z, Li XM, Hoffman RM, Glinsky GV. Essential role for activation of the Polycomb group (PcG) protein chromatin silencing pathway in metastatic prostate cancer. Cell Cycle. 2006;5(16):1886-1901. (Pubitemid 44435335)
33. Collett K, Eide GE, Arnes J, et al. Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Clin Cancer Res. 2006;12(4):1168-1174. (Pubitemid 43342505)
34. Raman JD, Mongan NP, Tickoo SK, Boorjian SA, Scherr DS, Gudas LJ. Increased expression of the polycomb group gene, EZH2, in transitional cell carcinoma of the bladder. Clin Cancer Res. 2005;11(24 Pt 1): 8570-8576. (Pubitemid 43005902)
35. van Leenders GJ, Dukers D, Hessels D, et al. Polycomb-group oncogenes EZH2, BMI1, and RING1 are overexpressed in prostate cancer with adverse pathologic and clinical features. Eur Urol. 2007;52(2):455-463. (Pubitemid 46963432)
36. Varambally S, Dhanasekaran SM, Zhou M, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature. 2002;419(6907):624- 629.
37. Weikert S, Christoph F, Kollermann J, et al. Expression levels of the EZH2 polycomb transcriptional repressor correlate with aggressiveness and invasive potential of bladder carcinomas. Int J Mol Med. 2005;16(2):349-353.
38. Yu J, Rhodes DR, Tomlins SA, et al. A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res. 2007;67(22):10657-10663. (Pubitemid 350145890)
39. Hinz S, Kempkensteffen C, Weikert S, et al. EZH2 polycomb transcriptional repressor expression correlates with methylation of the APAF-1 gene in superficial transitional cell carcinoma of the bladder. Tumour Biol. 2007;28(3):151-157. (Pubitemid 46976001)
40. Beke L, Nuytten M, Van Eynde A, Beullens M, Bollen M. The gene encoding the prostatic tumor suppressor PSP94 is a target for repression by the Polycomb group protein EZH2. Oncogene. 2007;26(31):4590-4595. (Pubitemid 47037047)
41. Cha TL, Zhou BP, Xia W, et al. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science. 2005;310(5746):306- 310. (Pubitemid 41457195)
42. Levitt RJ, Georgescu MM, Pollak M. PTEN-induction in U251 glioma cells decreases the expression of insulin-like growth factor binding protein-2. Biochem Biophys Res Commun. 2005;336(4):1056-1061. (Pubitemid 41383429)
43. Mehrian-Shai R, Chen CD, Shi T, et al. Insulin growth factor-binding protein 2 is a candidate biomarker for PTEN status and PI3K/Akt pathway activation in glioblastoma and prostate cancer. Proc Natl Acad Sci U S A. 2007;104(13):5563-5568. (Pubitemid 47175720)
44. Dunlap SM, Celestino J, Wang H, et al. Insulin-like growth factor binding protein 2 promotes glioma development and progression. Proc Natl Acad Sci U S A. 2007;104(28):11736-11741. (Pubitemid 47175082)
45. Jiang R, Mircean C, Shmulevich I, et al. Pathway alterations during glioma progression revealed by reverse phase protein lysate arrays. Proteomics. 2006;6(10):2964-2971. (Pubitemid 43806395)
46. McDonald KL, O'Sullivan MG, Parkinson JF, et al. IQGAP1 and IGFBP2: Valuable biomarkers for determining prognosis in glioma patients. J Neuropathol Exp Neurol. 2007;66(5):405-417. (Pubitemid 46701323)
47. Fuller GN, Hess KR, Rhee CH, et al. Molecular classification of human diffuse gliomas by multidimensional scaling analysis of gene expression profiles parallels morphology-based classification, correlates with survival, and reveals clinically-relevant novel glioma subsets. Brain Pathol. 2002;12(1):108-116. (Pubitemid 33131367)
48. Fuller GN, Rhee CH, Hess KR, et al. Reactivation of insulin-like growth factor binding protein 2 expression in glioblastoma multiforme: A revelation by parallel gene expression profiling. Cancer Res. 1999;59(17):4228-4232. (Pubitemid 29418733)
49. Godard S, Getz G, Delorenzi M, et al. Classification of human astrocytic gliomas on the basis of gene expression: A correlated group of genes with angiogenic activity emerges as a strong predictor of subtypes. Cancer Res. 2003;63(20):6613-6625. (Pubitemid 37322939)
50. Rickman DS, Bobek MP, Misek DE, et al. Distinctive molecular profiles of high-grade and low-grade gliomas based on oligonucleotide microarray analysis. Cancer Res. 2001;61(18):6885-6891. (Pubitemid 32896514)
51. Sallinen SL, Sallinen PK, Haapasalo HK, et al. Identification of differentially expressed genes in human gliomas by DNA microarray and tissue chip techniques. Cancer Res. 2000;60(23):6617-6622.
52. van Hattem WA, Carvalho R, Li A, Offerhaus GJ, Goggins M. Amplification of EMSY Gene in a Subset of Sporadic Pancreatic Adenocarcinomas. Int J Clin Exp Pathol. 2008;1(4):343-351.
53. Depreter M, Vandesompele J, Espeel M, Speleman F, Roels F. Modulation of the peroxisomal gene expression pattern by dehydroepiandrosterone and vitamin D: Therapeutic implications. J Endocrinol. 2002;175(3):779-792. (Pubitemid 36054247)
54. Wilhelm CS, Kelsey KT, Butler R, et al. Implications of LINE1methylation for bladder cancer risk in women. Clin Cancer Res. 2010;6(5):1682-1689.
55. Banfield JD, Raftery AE. Model-based Gaussian and non-Gaussian clustering. Biometrics. 1993;49:803-821. (Pubitemid 23298358)
56. Fraga MF, Esteller M. DNA methylation: A profile of methods and applications. Biotechniques. 2002;33(3):632, 634, 636-649.
57. Fraley C, Raftery AE. Enhanced Software for model-based clustering, discriminant analysis, and density estimation: MCLUST. Journal of Classification. 2003;20:263-286. (Pubitemid 38157158)
58. Houseman EA, Christensen BC, Yeh RF, et al. Model-based clustering of DNA methylation array data: A recursive-partitioning algorithm for high-dimensional data arising as a mixture of beta distributions. BMC Bioinformatics. 2008;9:365.
59. Schwartzbaum J, Jonsson F, Ahlbom A, et al. Prior hospitalization for epilepsy, diabetes, and stroke and subsequent glioma and meningioma risk. Cancer Epidemiol Biomarkers Prev. 2005;14(3):643-650. (Pubitemid 40489209)
60. Hobert O, Jallal B, Ullrich A. Interaction of Vav with ENX-1, a putative transcriptional regulator of homeobox gene expression. Mol Cell Biol. 1996;16(6):3066-3073. (Pubitemid 26163376)
61. Shahrzad S, Bertrand K, Minhas K, Coomber BL. Induction of DNA hypomethylation by tumor hypoxia. Epigenetics. 2007;2(2):119-125. (Pubitemid 351682006)
62. Kondo Y, Shen L, Cheng AS, et al. Gene silencing in cancer by histone H3 lysine 27 trimethylation independent of promoter DNA methylation. Nat Genet. 2008;40(6):741-750. (Pubitemid 351748874)