Differential expression and methylation of brain developmental genes define location-specific subsets of pilocytic astrocytoma

Acta Neuropathologica

Volumn 126, Issue 2, 2013, Pages 291-301

  Lambert, Sally R ^a   Witt, Hendrik ^b,c   Hovestadt, Volker ^b   Zucknick, Manuela ^b   Kool, Marcel ^b   Pearson, Danita M ^a   Korshunov, Andrey ^b,d   Ryzhova, Marina ^e   Ichimura, Koichi ^f   Jabado, Nada ^g   Fontebasso, Adam M ^g   Lichter, Peter ^b   Pfister, Stefan M ^b,c   Collins, V Peter ^a   Jones, David T W ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e BURDENKO NEUROSURGICAL INSTITUTE   (Russian Federation)

^f NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^g RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Development; DNA methylation; Pilocytic astrocytoma; SUZ12

Indexed keywords

ARTICLE; BINDING SITE; BRAIN FOURTH VENTRICLE; BRAIN REGION; BRAIN STEM; BRAIN THIRD VENTRICLE; CARCINOGENESIS; CEREBELLUM; CONTROLLED STUDY; DEVELOPMENTAL GENE; DIENCEPHALON; DNA METHYLATION; EN2 GENE; FEZF2 GENE; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; NR2E1 GENE; NUCLEOTIDE SEQUENCE; OPTIC NERVE; PAX3 GENE; PILOCYTIC ASTROCYTOMA; PRIORITY JOURNAL; PYROSEQUENCING; SUZ12 GENE; TUMOR LOCALIZATION; VAX1 GENE;

ASTROCYTOMA; BINDING SITES; BRAIN NEOPLASMS; CEREBELLAR NEOPLASMS; CHILD; DNA METHYLATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, DEVELOPMENTAL; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYCOMB REPRESSIVE COMPLEX 2;

EID: 84881092752     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-013-1124-7     Document Type: Article

References (35)

1. Armstrong GT, Conklin HM, Huang S et al (2011) Survival and long-term health and cognitive outcomes after low-grade glioma. Neuro Oncol 13:223-234. doi: 10.1093/neuonc/noq178
2. Bert SA, Robinson MD, Strbenac D et al (2013) Regional activation of the cancer genome by long-range epigenetic remodeling. Cancer Cell 23:9-22. doi: 10.1016/j.ccr.2012.11.006
3. Bertuzzi S, Hindges R, Mui SH, O'Leary DD, Lemke G (1999) The homeodomain protein vax1 is required for axon guidance and major tract formation in the developing forebrain. Genes Dev 13:3092-3105
4. Cheng Y, Sudarov A, Szulc KU et al (2010) The Engrailed homeobox genes determine the different foliation patterns in the vermis and hemispheres of the mammalian cerebellum. Development 137:519-529. doi: 10.1242/dev.027045
5. Dirven CM, Mooij JJ, Molenaar WM (1997) Cerebellar pilocytic astrocytoma: a treatment protocol based upon analysis of 73 cases and a review of the literature. Childs Nerv Syst 13:17-23
6. Esteller M, Hamilton SR, Burger PC, Baylin SB, Herman JG (1999) Inactivation of the DNA repair gene O6-methylguanine-DNA methyltransferase by promoter hypermethylation is a common event in primary human neoplasia. Cancer Res 59:793-797
7. Forshew T, Tatevossian RG, Lawson AR et al (2009) Activation of the ERK/MAPK pathway: a signature genetic defect in posterior fossa pilocytic astrocytomas. J Pathol 218:172-181. doi: 10.1002/path.2558
8. Gnekow AK, Falkenstein F, von Hornstein S et al (2012) Long-term follow-up of the multicenter, multidisciplinary treatment study HIT-LGG-1996 for low-grade glioma in children and adolescents of the German Speaking Society of Pediatric Oncology and Hematology. Neuro Oncol 14:1265-1284. doi: 10.1093/neuonc/nos202
9. Gronych J, Korshunov A, Bageritz J et al (2011) An activated mutant BRAF kinase domain is sufficient to induce pilocytic astrocytoma in mice. J Clin Invest 121:1344-1348. doi: 10.1172/JCI44656
10. Hellman A, Chess A (2007) Gene body-specific methylation on the active X chromosome. Science 315:1141-1143. doi: 10.1126/science.1136352
11. Ichimura K, Pearson DM, Kocialkowski S et al (2009) IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro Oncol 11:341-347. doi: 10.1215/15228517-2009-025
12. Jacob K, Quang-Khuong DA, Jones DTW et al (2011) Genetic aberrations leading to MAPK pathway activation mediate oncogene-induced senescence in sporadic pilocytic astrocytomas. Clin Cancer Res 17:4650-4660. doi: 10.1158/1078-0432.CCR-11-0127
13. Jones DTW, Gronych J, Lichter P, Witt O, Pfister SM (2012) MAPK pathway activation in pilocytic astrocytoma. Cell Mol Life Sci 69:1799-1811. doi: 10.1007/s00018-011-0898-9
14. Jones DTW, Ichimura K, Liu L, Pearson DM, Plant K, Collins VP (2006) Genomic analysis of pilocytic astrocytomas at 0.97 Mb resolution shows an increasing tendency toward chromosomal copy number change with age. J Neuropathol Exp Neurol 65:1049-1058. doi: 10.1097/01.jnen.0000240465.33628.87
15. Jones DTW, Kocialkowski S, Liu L et al (2008) Tandem duplication producing a novel oncogenic BRAF fusion gene defines the majority of pilocytic astrocytomas. Cancer Res 68:8673-8677. doi: 10.1158/0008-5472.CAN-08-2097
16. Kelly TK, de Carvalho DD, Jones PA (2010) Epigenetic modifications as therapeutic targets. Nat Biotechnol 28:1069-1078. doi: 10.1038/nbt.1678
17. Lee DY, Gianino SM, Gutmann DH (2012) Innate neural stem cell heterogeneity determines the patterning of glioma formation in children. Cancer Cell 22:131-138. doi: 10.1016/j.ccr.2012.05.036
18. Lindroth AM, Park YJ, McLean CM et al (2008) Antagonism between DNA and H3K27 methylation at the imprinted Rasgrf1 locus. PLoS Genet 4:e1000145. doi: 10.1371/journal.pgen.1000145
19. Liu HK, Wang Y, Belz T et al (2010) The nuclear receptor tailless induces long-term neural stem cell expansion and brain tumor initiation. Genes Dev 24:683-695. doi: 10.1101/gad.560310
20. Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343-349. doi: 10.1038/nature09784
21. Ohgaki H, Eibl RH, Schwab M et al (1993) Mutations of the p53 tumor suppressor gene in neoplasms of the human nervous system. Mol Carcinog 8:74-80
22. Pfister S, Janzarik WG, Remke M et al (2008) BRAF gene duplication constitutes a mechanism of MAPK pathway activation in low-grade astrocytomas. J Clin Invest 118:1739-1749. doi: 10.1172/JCI33656
23. Raabe EH, Lim KS, Kim JM et al (2011) BRAF activation induces transformation and then senescence in human neural stem cells: a pilocytic astrocytoma model. Clin Cancer Res 17:3590-3599. doi: 10.1158/1078-0432.CCR-10- 3349
24. Rasheed BK, McLendon RE, Herndon JE et al (1994) Alterations of the TP53 gene in human gliomas. Cancer Res 54:1324-1330
25. Rauch TA, Wu X, Zhong X, Riggs AD, Pfeifer GP (2009) A human B cell methylome at 100-base pair resolution. Proc Natl Acad Sci USA 106:671-678. doi: 10.1073/pnas.0812399106
26. Rogers HA, Kilday JP, Mayne C et al (2012) 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 Neuropathol 123:711-725. doi: 10.1007/s00401-011-0904-1
27. Sharma MK, Mansur DB, Reifenberger G et al (2007) Distinct genetic signatures among pilocytic astrocytomas relate to their brain region origin. Cancer Res 67:890-900. doi: 10.1158/0008-5472.CAN-06-0973
28. Sievert AJ, Jackson EM, Gai X et al (2009) Duplication of 7q34 in pediatric low-grade astrocytomas detected by high-density single-nucleotide polymorphism-based genotype arrays results in a novel BRAF fusion gene. Brain Pathol 19:449-458. doi: 10.1111/j.1750-3639.2008.00225.x
29. Squazzo SL, O'Geen H, Komashko VM et al (2006) Suz12 binds to silenced regions of the genome in a cell-type-specific manner. Genome Res 16:890-900. doi: 10.1101/gr.5306606
30. Stokland T, Liu JF, Ironside JW et al (2010) A multivariate analysis of factors determining tumor progression in childhood low-grade glioma: a population-based cohort study (CCLG CNS9702). Neuro Oncol 12:1257-1268. doi: 10.1093/neuonc/noq092
31. Sturm D, Witt H, Hovestadt V et al (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22:425-437. doi: 10.1016/j.ccr.2012.08.024
32. Szulwach KE, Li X, Li Y et al (2011) 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 14:1607-1616. doi: 10.1038/nn.2959
33. Tchoghandjian A, Fernandez C, Colin C et al (2009) Pilocytic astrocytoma of the optic pathway: a tumour deriving from radial glia cells with a specific gene signature. Brain 132:1523-1535. doi: 10.1093/brain/awp048
34. Yu RT, Chiang MY, Tanabe T et al (2000) The orphan nuclear receptor Tlx regulates Pax2 and is essential for vision. Proc Natl Acad Sci USA 97:2621-2625. doi: 10.1073/pnas.050566897
35. Zhu CC, Dyer MA, Uchikawa M, Kondoh H, Lagutin OV, Oliver G (2002) Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors. Development 129:2835-2849