Skip to main content
Top
Published in: Acta Neuropathologica 3/2017

01-03-2017 | Original Paper

Global epigenetic profiling identifies methylation subgroups associated with recurrence-free survival in meningioma

Authors: Adriana Olar, Khalida M. Wani, Charmaine D. Wilson, Gelareh Zadeh, Franco DeMonte, David T. W. Jones, Stefan M. Pfister, Erik P. Sulman, Kenneth D. Aldape

Published in: Acta Neuropathologica | Issue 3/2017

Login to get access

Abstract

Meningioma is the most common primary brain tumor and carries a substantial risk of local recurrence. Methylation profiles of meningioma and their clinical implications are not well understood. We hypothesized that aggressive meningiomas have unique DNA methylation patterns that could be used to better stratify patient management. Samples (n = 140) were profiled using the Illumina HumanMethylation450BeadChip. Unsupervised modeling on a training set (n = 89) identified 2 molecular methylation subgroups of meningioma (MM) with significantly different recurrence-free survival (RFS) times between the groups: a prognostically unfavorable subgroup (MM-UNFAV) and a prognostically favorable subgroup (MM-FAV). This finding was validated in the remaining 51 samples and led to a baseline meningioma methylation classifier (bMMC) defined by 283 CpG loci (283-bMMC). To further optimize a recurrence predictor, probes subsumed within the baseline classifier were subject to additional modeling using a similar training/validation approach, leading to a 64-CpG loci meningioma methylation predictor (64-MMP). After adjustment for relevant clinical variables [WHO grade, mitotic index, Simpson grade, sex, location, and copy number aberrations (CNAs)] multivariable analyses for RFS showed that the baseline methylation classifier was not significant (p = 0.0793). The methylation predictor, however, was significantly associated with tumor recurrence (p < 0.0001). CNAs were extracted from the 450k intensity profiles. Tumor samples in the MM-UNFAV subgroup showed an overall higher proportion of CNAs compared to the MM-FAV subgroup tumors and the CNAs were complex in nature. CNAs in the MM-UNFAV subgroup included recurrent losses of 1p, 6q, 14q and 18q, and gain of 1q, all of which were previously identified as indicators of poor outcome. In conclusion, our analyses demonstrate robust DNA methylation signatures in meningioma that correlate with CNAs and stratify patients by recurrence risk.
Appendix
Available only for authorised users
Literature
1.
go back to reference Abedalthagafi M, Bi WL, Aizer AA, Merrill PH, Brewster R, Agarwalla PK, Listewnik ML, Dias-Santagata D, Thorner AR, Van Hummelen P, Brastianos PK, Reardon DA, Wen PY, Al-Mefty O, Ramkissoon SH, Folkerth RD, Ligon KL, Ligon AH, Alexander BM, Dunn IF, Beroukhim R, Santagata S (2016) Oncogenic PI3K mutations are as common as AKT1 and SMO mutations in meningioma. Neuro-oncology 18(5):649–655. doi:10.1093/neuonc/nov316 CrossRefPubMed Abedalthagafi M, Bi WL, Aizer AA, Merrill PH, Brewster R, Agarwalla PK, Listewnik ML, Dias-Santagata D, Thorner AR, Van Hummelen P, Brastianos PK, Reardon DA, Wen PY, Al-Mefty O, Ramkissoon SH, Folkerth RD, Ligon KL, Ligon AH, Alexander BM, Dunn IF, Beroukhim R, Santagata S (2016) Oncogenic PI3K mutations are as common as AKT1 and SMO mutations in meningioma. Neuro-oncology 18(5):649–655. doi:10.​1093/​neuonc/​nov316 CrossRefPubMed
2.
go back to reference Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, Curry WT Jr, Barker FG 2nd (2009) Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64(1):56–60. doi:10.1227/01.NEU.0000330399.55586.63 (discussion 60) Aghi MK, Carter BS, Cosgrove GR, Ojemann RG, Amin-Hanjani S, Martuza RL, Curry WT Jr, Barker FG 2nd (2009) Long-term recurrence rates of atypical meningiomas after gross total resection with or without postoperative adjuvant radiation. Neurosurgery 64(1):56–60. doi:10.​1227/​01.​NEU.​0000330399.​55586.​63 (discussion 60)
3.
go back to reference Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6):716–723CrossRef Akaike H (1974) A new look at the statistical model identification. IEEE Trans Autom Control 19(6):716–723CrossRef
5.
go back to reference Ashktorab H, Rahi H, Wansley D, Varma S, Shokrani B, Lee E, Daremipouran M, Laiyemo A, Goel A, Carethers JM, Brim H (2013) Toward a comprehensive and systematic methylome signature in colorectal cancers. Epigenetics 8(8):807–815. doi:10.4161/epi.25497 CrossRefPubMedPubMedCentral Ashktorab H, Rahi H, Wansley D, Varma S, Shokrani B, Lee E, Daremipouran M, Laiyemo A, Goel A, Carethers JM, Brim H (2013) Toward a comprehensive and systematic methylome signature in colorectal cancers. Epigenetics 8(8):807–815. doi:10.​4161/​epi.​25497 CrossRefPubMedPubMedCentral
6.
go back to reference Aydemir F, Yurtcu E, Balci TB, Sahin FI, Gulsen S, Altinors N (2012) Identification of promoter region methylation patterns of MGMT, CDKN2A, GSTP1, and THBS1 genes in intracranial meningioma patients. Genet Test Mol Biomark 16(5):335–340. doi:10.1089/gtmb.2011.0245 CrossRef Aydemir F, Yurtcu E, Balci TB, Sahin FI, Gulsen S, Altinors N (2012) Identification of promoter region methylation patterns of MGMT, CDKN2A, GSTP1, and THBS1 genes in intracranial meningioma patients. Genet Test Mol Biomark 16(5):335–340. doi:10.​1089/​gtmb.​2011.​0245 CrossRef
8.
go back to reference Bello MJ, Aminoso C, Lopez-Marin I, Arjona D, Gonzalez-Gomez P, Alonso ME, Lomas J, de Campos JM, Kusak ME, Vaquero J, Isla A, Gutierrez M, Sarasa JL, Rey JA (2004) DNA methylation of multiple promoter-associated CpG islands in meningiomas: relationship with the allelic status at 1p and 22q. Acta Neuropathol 108(5):413–421. doi:10.1007/s00401-004-0911-6 CrossRefPubMed Bello MJ, Aminoso C, Lopez-Marin I, Arjona D, Gonzalez-Gomez P, Alonso ME, Lomas J, de Campos JM, Kusak ME, Vaquero J, Isla A, Gutierrez M, Sarasa JL, Rey JA (2004) DNA methylation of multiple promoter-associated CpG islands in meningiomas: relationship with the allelic status at 1p and 22q. Acta Neuropathol 108(5):413–421. doi:10.​1007/​s00401-004-0911-6 CrossRefPubMed
10.
go back to reference Brastianos PK, Horowitz PM, Santagata S, Jones RT, McKenna A, Getz G, Ligon KL, Palescandolo E, Van Hummelen P, Ducar MD, Raza A, Sunkavalli A, Macconaill LE, Stemmer-Rachamimov AO, Louis DN, Hahn WC, Dunn IF, Beroukhim R (2013) Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet 45(3):285–289. doi:10.1038/ng.2526 CrossRefPubMedPubMedCentral Brastianos PK, Horowitz PM, Santagata S, Jones RT, McKenna A, Getz G, Ligon KL, Palescandolo E, Van Hummelen P, Ducar MD, Raza A, Sunkavalli A, Macconaill LE, Stemmer-Rachamimov AO, Louis DN, Hahn WC, Dunn IF, Beroukhim R (2013) Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet 45(3):285–289. doi:10.​1038/​ng.​2526 CrossRefPubMedPubMedCentral
11.
go back to reference Brokinkel B, Fischer BR, Peetz-Dienhart S, Ebel H, Sepehrnia A, Rama B, Albert FK, Stummer W, Paulus W, Hasselblatt M (2010) MGMT promoter methylation status in anaplastic meningiomas. J Neurooncol 100(3):489–490. doi:10.1007/s11060-010-0202-0 CrossRefPubMed Brokinkel B, Fischer BR, Peetz-Dienhart S, Ebel H, Sepehrnia A, Rama B, Albert FK, Stummer W, Paulus W, Hasselblatt M (2010) MGMT promoter methylation status in anaplastic meningiomas. J Neurooncol 100(3):489–490. doi:10.​1007/​s11060-010-0202-0 CrossRefPubMed
13.
go back to reference Clark VE, Erson-Omay EZ, Serin A, Yin J, Cotney J, Ozduman K, Avsar T, Li J, Murray PB, Henegariu O, Yilmaz S, Gunel JM, Carrion-Grant G, Yilmaz B, Grady C, Tanrikulu B, Bakircioglu M, Kaymakcalan H, Caglayan AO, Sencar L, Ceyhun E, Atik AF, Bayri Y, Bai H, Kolb LE, Hebert RM, Omay SB, Mishra-Gorur K, Choi M, Overton JD, Holland EC, Mane S, State MW, Bilguvar K, Baehring JM, Gutin PH, Piepmeier JM, Vortmeyer A, Brennan CW, Pamir MN, Kilic T, Lifton RP, Noonan JP, Yasuno K, Gunel M (2013) Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339(6123):1077–1080. doi:10.1126/science.1233009 CrossRefPubMedPubMedCentral Clark VE, Erson-Omay EZ, Serin A, Yin J, Cotney J, Ozduman K, Avsar T, Li J, Murray PB, Henegariu O, Yilmaz S, Gunel JM, Carrion-Grant G, Yilmaz B, Grady C, Tanrikulu B, Bakircioglu M, Kaymakcalan H, Caglayan AO, Sencar L, Ceyhun E, Atik AF, Bayri Y, Bai H, Kolb LE, Hebert RM, Omay SB, Mishra-Gorur K, Choi M, Overton JD, Holland EC, Mane S, State MW, Bilguvar K, Baehring JM, Gutin PH, Piepmeier JM, Vortmeyer A, Brennan CW, Pamir MN, Kilic T, Lifton RP, Noonan JP, Yasuno K, Gunel M (2013) Genomic analysis of non-NF2 meningiomas reveals mutations in TRAF7, KLF4, AKT1, and SMO. Science 339(6123):1077–1080. doi:10.​1126/​science.​1233009 CrossRefPubMedPubMedCentral
15.
go back to reference Di Vinci A, Brigati C, Casciano I, Banelli B, Borzi L, Forlani A, Ravetti GL, Allemanni G, Melloni I, Zona G, Spaziante R, Merlo DF, Romani M (2012) HOXA7, 9, and 10 are methylation targets associated with aggressive behavior in meningiomas. Transl Res 160(5):355–362. doi:10.1016/j.trsl.2012.05.007 CrossRefPubMed Di Vinci A, Brigati C, Casciano I, Banelli B, Borzi L, Forlani A, Ravetti GL, Allemanni G, Melloni I, Zona G, Spaziante R, Merlo DF, Romani M (2012) HOXA7, 9, and 10 are methylation targets associated with aggressive behavior in meningiomas. Transl Res 160(5):355–362. doi:10.​1016/​j.​trsl.​2012.​05.​007 CrossRefPubMed
17.
go back to reference Domingues PH, Sousa P, Otero A, Goncalves JM, Ruiz L, de Oliveira C, Lopes MC, Orfao A, Tabernero MD (2014) Proposal for a new risk stratification classification for meningioma based on patient age, WHO tumor grade, size, localization, and karyotype. Neuro-oncology 16(5):735–747. doi:10.1093/neuonc/not325 CrossRefPubMedPubMedCentral Domingues PH, Sousa P, Otero A, Goncalves JM, Ruiz L, de Oliveira C, Lopes MC, Orfao A, Tabernero MD (2014) Proposal for a new risk stratification classification for meningioma based on patient age, WHO tumor grade, size, localization, and karyotype. Neuro-oncology 16(5):735–747. doi:10.​1093/​neuonc/​not325 CrossRefPubMedPubMedCentral
19.
go back to reference Fernandez-Delgado M, Cernadas E, Barro S, Amorim D (2014) Do we need hundreds of classifiers to solve real world classification problems? JMLR 15(1):3133–3181 Fernandez-Delgado M, Cernadas E, Barro S, Amorim D (2014) Do we need hundreds of classifiers to solve real world classification problems? JMLR 15(1):3133–3181
20.
go back to reference Florido JP, Pomares H, Rojas I, Urquiza JM, Herrera LJ, Claros MG (2010) Effect of pre-processing methods on microarray-based SVM classifiers in Affymetrix genechips. IEEE, pp 1–6 Florido JP, Pomares H, Rojas I, Urquiza JM, Herrera LJ, Claros MG (2010) Effect of pre-processing methods on microarray-based SVM classifiers in Affymetrix genechips. IEEE, pp 1–6
23.
go back to reference Harrell FE Jr, Califf RM, Pryor DB, Lee KL, Rosati RA (1982) Evaluating the yield of medical tests. JAMA 247(18):2543–2546CrossRefPubMed Harrell FE Jr, Califf RM, Pryor DB, Lee KL, Rosati RA (1982) Evaluating the yield of medical tests. JAMA 247(18):2543–2546CrossRefPubMed
25.
go back to reference Heim S, Sill M, Jones DT, Vasiljevic A, Jouvet A, Fevre-Montange M, Wesseling P, Beschorner R, Mittelbronn M, Kohlhof P, Hovestadt V, Johann P, Kool M, Pajtler KW, Korshunov A, Ruland V, Sperveslage J, Thomas C, Witt H, von Deimling A, Paulus W, Pfister SM, Capper D, Hasselblatt M (2016) Papillary tumor of the pineal region: a distinct molecular entity. Brain Pathol 26(2):199–205. doi:10.1111/bpa.12282 CrossRefPubMed Heim S, Sill M, Jones DT, Vasiljevic A, Jouvet A, Fevre-Montange M, Wesseling P, Beschorner R, Mittelbronn M, Kohlhof P, Hovestadt V, Johann P, Kool M, Pajtler KW, Korshunov A, Ruland V, Sperveslage J, Thomas C, Witt H, von Deimling A, Paulus W, Pfister SM, Capper D, Hasselblatt M (2016) Papillary tumor of the pineal region: a distinct molecular entity. Brain Pathol 26(2):199–205. doi:10.​1111/​bpa.​12282 CrossRefPubMed
26.
go back to reference Herrlinger U, Jones DT, Glas M, Hattingen E, Gramatzki D, Stuplich M, Felsberg J, Bahr O, Gielen GH, Simon M, Wiewrodt D, Schabet M, Hovestadt V, Capper D, Steinbach JP, von Deimling A, Lichter P, Pfister SM, Weller M, Reifenberger G (2016) Gliomatosis cerebri: no evidence for a separate brain tumor entity. Acta Neuropathol 131(2):309–319. doi:10.1007/s00401-015-1495-z CrossRefPubMed Herrlinger U, Jones DT, Glas M, Hattingen E, Gramatzki D, Stuplich M, Felsberg J, Bahr O, Gielen GH, Simon M, Wiewrodt D, Schabet M, Hovestadt V, Capper D, Steinbach JP, von Deimling A, Lichter P, Pfister SM, Weller M, Reifenberger G (2016) Gliomatosis cerebri: no evidence for a separate brain tumor entity. Acta Neuropathol 131(2):309–319. doi:10.​1007/​s00401-015-1495-z CrossRefPubMed
27.
go back to reference Holsken A, Sill M, Merkle J, Schweizer L, Buchfelder M, Flitsch J, Fahlbusch R, Metzler M, Kool M, Pfister SM, von Deimling A, Capper D, Jones DT, Buslei R (2016) Adamantinomatous and papillary craniopharyngiomas are characterized by distinct epigenomic as well as mutational and transcriptomic profiles. Acta Neuropathol Commun 4:20. doi:10.1186/s40478-016-0287-6 CrossRefPubMedPubMedCentral Holsken A, Sill M, Merkle J, Schweizer L, Buchfelder M, Flitsch J, Fahlbusch R, Metzler M, Kool M, Pfister SM, von Deimling A, Capper D, Jones DT, Buslei R (2016) Adamantinomatous and papillary craniopharyngiomas are characterized by distinct epigenomic as well as mutational and transcriptomic profiles. Acta Neuropathol Commun 4:20. doi:10.​1186/​s40478-016-0287-6 CrossRefPubMedPubMedCentral
28.
go back to reference Hovestadt V, Jones DT, Picelli S, Wang W, Kool M, Northcott PA, Sultan M, Stachurski K, Ryzhova M, Warnatz HJ, Ralser M, Brun S, Bunt J, Jager N, Kleinheinz K, Erkek S, Weber UD, Bartholomae CC, von Kalle C, Lawerenz C, Eils J, Koster J, Versteeg R, Milde T, Witt O, Schmidt S, Wolf S, Pietsch T, Rutkowski S, Scheurlen W, Taylor MD, Brors B, Felsberg J, Reifenberger G, Borkhardt A, Lehrach H, Wechsler-Reya RJ, Eils R, Yaspo ML, Landgraf P, Korshunov A, Zapatka M, Radlwimmer B, Pfister SM, Lichter P (2014) Decoding the regulatory landscape of medulloblastoma using DNA methylation sequencing. Nature 510(7506):537–541. doi:10.1038/nature13268 CrossRefPubMed Hovestadt V, Jones DT, Picelli S, Wang W, Kool M, Northcott PA, Sultan M, Stachurski K, Ryzhova M, Warnatz HJ, Ralser M, Brun S, Bunt J, Jager N, Kleinheinz K, Erkek S, Weber UD, Bartholomae CC, von Kalle C, Lawerenz C, Eils J, Koster J, Versteeg R, Milde T, Witt O, Schmidt S, Wolf S, Pietsch T, Rutkowski S, Scheurlen W, Taylor MD, Brors B, Felsberg J, Reifenberger G, Borkhardt A, Lehrach H, Wechsler-Reya RJ, Eils R, Yaspo ML, Landgraf P, Korshunov A, Zapatka M, Radlwimmer B, Pfister SM, Lichter P (2014) Decoding the regulatory landscape of medulloblastoma using DNA methylation sequencing. Nature 510(7506):537–541. doi:10.​1038/​nature13268 CrossRefPubMed
29.
go back to reference Hovestadt V, Remke M, Kool M, Pietsch T, Northcott PA, Fischer R, Cavalli FM, Ramaswamy V, Zapatka M, Reifenberger G, Rutkowski S, Schick M, Bewerunge-Hudler M, Korshunov A, Lichter P, Taylor MD, Pfister SM, Jones DT (2013) Robust molecular subgrouping and copy-number profiling of medulloblastoma from small amounts of archival tumour material using high-density DNA methylation arrays. Acta Neuropathol 125(6):913–916. doi:10.1007/s00401-013-1126-5 CrossRefPubMedPubMedCentral Hovestadt V, Remke M, Kool M, Pietsch T, Northcott PA, Fischer R, Cavalli FM, Ramaswamy V, Zapatka M, Reifenberger G, Rutkowski S, Schick M, Bewerunge-Hudler M, Korshunov A, Lichter P, Taylor MD, Pfister SM, Jones DT (2013) Robust molecular subgrouping and copy-number profiling of medulloblastoma from small amounts of archival tumour material using high-density DNA methylation arrays. Acta Neuropathol 125(6):913–916. doi:10.​1007/​s00401-013-1126-5 CrossRefPubMedPubMedCentral
30.
go back to reference Jabini R, Moradi A, Afsharnezhad S, Ayatollahi H, Behravan J, Raziee HR, Mosaffa F (2014) Pathodiagnostic parameters and evaluation of O(6)- methyl guanine methyl transferase gene promoter methylation in meningiomas. Gene 538(2):348–353. doi:10.1016/j.gene.2013.12.039 CrossRefPubMed Jabini R, Moradi A, Afsharnezhad S, Ayatollahi H, Behravan J, Raziee HR, Mosaffa F (2014) Pathodiagnostic parameters and evaluation of O(6)- methyl guanine methyl transferase gene promoter methylation in meningiomas. Gene 538(2):348–353. doi:10.​1016/​j.​gene.​2013.​12.​039 CrossRefPubMed
31.
go back to reference Johann PD, Hovestadt V, Thomas C, Jeibmann A, Hess K, Bens S, Oyen F, Hawkins C, Pierson CR, Aldape K, Kim SP, Widing E, Sumerauer D, Hauser P, van Landeghem F, Ryzhova M, Korshunov A, Capper D, Jones DT, Pfister SM, Schneppenheim R, Siebert R, Paulus W, Fruhwald MC, Kool M, Hasselblatt M (2016) Cribriform neuroepithelial tumor: molecular characterization of a SMARCB1-deficient non-rhabdoid tumor with favorable long-term outcome. Brain Pathol. doi:10.1111/bpa.12413 Johann PD, Hovestadt V, Thomas C, Jeibmann A, Hess K, Bens S, Oyen F, Hawkins C, Pierson CR, Aldape K, Kim SP, Widing E, Sumerauer D, Hauser P, van Landeghem F, Ryzhova M, Korshunov A, Capper D, Jones DT, Pfister SM, Schneppenheim R, Siebert R, Paulus W, Fruhwald MC, Kool M, Hasselblatt M (2016) Cribriform neuroepithelial tumor: molecular characterization of a SMARCB1-deficient non-rhabdoid tumor with favorable long-term outcome. Brain Pathol. doi:10.​1111/​bpa.​12413
32.
go back to reference Johnson MD, Okedli E, Woodard A, Toms SA, Allen GS (2002) Evidence for phosphatidylinositol 3-kinase-Akt-p7S6K pathway activation and transduction of mitogenic signals by platelet-derived growth factor in meningioma cells. J Neurosurg 97(3):668–675. doi:10.3171/jns.2002.97.3.0668 CrossRefPubMed Johnson MD, Okedli E, Woodard A, Toms SA, Allen GS (2002) Evidence for phosphatidylinositol 3-kinase-Akt-p7S6K pathway activation and transduction of mitogenic signals by platelet-derived growth factor in meningioma cells. J Neurosurg 97(3):668–675. doi:10.​3171/​jns.​2002.​97.​3.​0668 CrossRefPubMed
33.
go back to reference Johnson MD, Woodard A, Kim P, Frexes-Steed M (2001) Evidence for mitogen-associated protein kinase activation and transduction of mitogenic signals by platelet-derived growth factor in human meningioma cells. J Neurosurg 94(2):293–300. doi:10.3171/jns.2001.94.2.0293 CrossRefPubMed Johnson MD, Woodard A, Kim P, Frexes-Steed M (2001) Evidence for mitogen-associated protein kinase activation and transduction of mitogenic signals by platelet-derived growth factor in human meningioma cells. J Neurosurg 94(2):293–300. doi:10.​3171/​jns.​2001.​94.​2.​0293 CrossRefPubMed
35.
go back to reference Kishida Y, Natsume A, Kondo Y, Takeuchi I, An B, Okamoto Y, Shinjo K, Saito K, Ando H, Ohka F, Sekido Y, Wakabayashi T (2012) Epigenetic subclassification of meningiomas based on genome-wide DNA methylation analyses. Carcinogenesis 33(2):436–441. doi:10.1093/carcin/bgr260 CrossRefPubMed Kishida Y, Natsume A, Kondo Y, Takeuchi I, An B, Okamoto Y, Shinjo K, Saito K, Ando H, Ohka F, Sekido Y, Wakabayashi T (2012) Epigenetic subclassification of meningiomas based on genome-wide DNA methylation analyses. Carcinogenesis 33(2):436–441. doi:10.​1093/​carcin/​bgr260 CrossRefPubMed
36.
go back to reference Koelsche C, Hovestadt V, Jones DT, Capper D, Sturm D, Sahm F, Schrimpf D, Adeberg S, Bohmer K, Hagenlocher C, Mechtersheimer G, Kohlhof P, Muhleisen H, Beschorner R, Hartmann C, Braczynski AK, Mittelbronn M, Buslei R, Becker A, Grote A, Urbach H, Staszewski O, Prinz M, Hewer E, Pfister SM, von Deimling A, Reuss DE (2015) Melanotic tumors of the nervous system are characterized by distinct mutational, chromosomal and epigenomic profiles. Brain Pathol 25(2):202–208. doi:10.1111/bpa.12228 CrossRefPubMed Koelsche C, Hovestadt V, Jones DT, Capper D, Sturm D, Sahm F, Schrimpf D, Adeberg S, Bohmer K, Hagenlocher C, Mechtersheimer G, Kohlhof P, Muhleisen H, Beschorner R, Hartmann C, Braczynski AK, Mittelbronn M, Buslei R, Becker A, Grote A, Urbach H, Staszewski O, Prinz M, Hewer E, Pfister SM, von Deimling A, Reuss DE (2015) Melanotic tumors of the nervous system are characterized by distinct mutational, chromosomal and epigenomic profiles. Brain Pathol 25(2):202–208. doi:10.​1111/​bpa.​12228 CrossRefPubMed
37.
go back to reference Korshunov A, Jakobiec FA, Eberhart CG, Hovestadt V, Capper D, Jones DT, Sturm D, Stagner AM, Edward DP, Eagle RC, Proia AD, Koch A, Ryzhova M, Ektova A, Schuller U, Zheludkova O, Lichter P, von Deimling A, Pfister SM, Kool M (2015) Comparative integrated molecular analysis of intraocular medulloepitheliomas and central nervous system embryonal tumors with multilayered rosettes confirms that they are distinct nosologic entities. Neuropathology 35(6):538–544. doi:10.1111/neup.12227 CrossRefPubMed Korshunov A, Jakobiec FA, Eberhart CG, Hovestadt V, Capper D, Jones DT, Sturm D, Stagner AM, Edward DP, Eagle RC, Proia AD, Koch A, Ryzhova M, Ektova A, Schuller U, Zheludkova O, Lichter P, von Deimling A, Pfister SM, Kool M (2015) Comparative integrated molecular analysis of intraocular medulloepitheliomas and central nervous system embryonal tumors with multilayered rosettes confirms that they are distinct nosologic entities. Neuropathology 35(6):538–544. doi:10.​1111/​neup.​12227 CrossRefPubMed
38.
go back to reference Larijani L, Madjd Z, Samadikuchaksaraei A, Younespour S, Zham H, Rakhshan A, Mohammadi F, Rahbari A, Moradi A (2014) Methylation of O6-methyl guanine methyltransferase gene promoter in meningiomas–comparison between tumor grades I, II, and III. Asian Pac J Cancer Prev 15(1):33–38CrossRefPubMed Larijani L, Madjd Z, Samadikuchaksaraei A, Younespour S, Zham H, Rakhshan A, Mohammadi F, Rahbari A, Moradi A (2014) Methylation of O6-methyl guanine methyltransferase gene promoter in meningiomas–comparison between tumor grades I, II, and III. Asian Pac J Cancer Prev 15(1):33–38CrossRefPubMed
40.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO Classification of tumours of the central nervous system, 4th edn. IARC, Lyon (France) Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (2007) WHO Classification of tumours of the central nervous system, 4th edn. IARC, Lyon (France)
41.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Ellison DW, Figarella-Branger D, Perry A, Raifenberger G, von Deimling A (2016) WHO classification of tumours of the central nervous system, 4th revised edn. IARC, Lyon Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Ellison DW, Figarella-Branger D, Perry A, Raifenberger G, von Deimling A (2016) WHO classification of tumours of the central nervous system, 4th revised edn. IARC, Lyon
42.
go back to reference Mack SC, Witt H, Piro RM, Gu L, Zuyderduyn S, Stutz AM, Wang X, Gallo M, Garzia L, Zayne K, Zhang X, Ramaswamy V, Jager N, Jones DT, Sill M, Pugh TJ, Ryzhova M, Wani KM, Shih DJ, Head R, Remke M, Bailey SD, Zichner T, Faria CC, Barszczyk M, Stark S, Seker-Cin H, Hutter S, Johann P, Bender S, Hovestadt V, Tzaridis T, Dubuc AM, Northcott PA, Peacock J, Bertrand KC, Agnihotri S, Cavalli FM, Clarke I, Nethery-Brokx K, Creasy CL, Verma SK, Koster J, Wu X, Yao Y, Milde T, Sin-Chan P, Zuccaro J, Lau L, Pereira S, Castelo-Branco P, Hirst M, Marra MA, Roberts SS, Fults D, Massimi L, Cho YJ, Van Meter T, Grajkowska W, Lach B, Kulozik AE, von Deimling A, Witt O, Scherer SW, Fan X, Muraszko KM, Kool M, Pomeroy SL, Gupta N, Phillips J, Huang A, Tabori U, Hawkins C, Malkin D, Kongkham PN, Weiss WA, Jabado N, Rutka JT, Bouffet E, Korbel JO, Lupien M, Aldape KD, Bader GD, Eils R, Lichter P, Dirks PB, Pfister SM, Korshunov A, Taylor MD (2014) Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 506(7489):445–450. doi:10.1038/nature13108 CrossRefPubMedPubMedCentral Mack SC, Witt H, Piro RM, Gu L, Zuyderduyn S, Stutz AM, Wang X, Gallo M, Garzia L, Zayne K, Zhang X, Ramaswamy V, Jager N, Jones DT, Sill M, Pugh TJ, Ryzhova M, Wani KM, Shih DJ, Head R, Remke M, Bailey SD, Zichner T, Faria CC, Barszczyk M, Stark S, Seker-Cin H, Hutter S, Johann P, Bender S, Hovestadt V, Tzaridis T, Dubuc AM, Northcott PA, Peacock J, Bertrand KC, Agnihotri S, Cavalli FM, Clarke I, Nethery-Brokx K, Creasy CL, Verma SK, Koster J, Wu X, Yao Y, Milde T, Sin-Chan P, Zuccaro J, Lau L, Pereira S, Castelo-Branco P, Hirst M, Marra MA, Roberts SS, Fults D, Massimi L, Cho YJ, Van Meter T, Grajkowska W, Lach B, Kulozik AE, von Deimling A, Witt O, Scherer SW, Fan X, Muraszko KM, Kool M, Pomeroy SL, Gupta N, Phillips J, Huang A, Tabori U, Hawkins C, Malkin D, Kongkham PN, Weiss WA, Jabado N, Rutka JT, Bouffet E, Korbel JO, Lupien M, Aldape KD, Bader GD, Eils R, Lichter P, Dirks PB, Pfister SM, Korshunov A, Taylor MD (2014) Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 506(7489):445–450. doi:10.​1038/​nature13108 CrossRefPubMedPubMedCentral
44.
go back to reference Maillo A, Diaz P, Sayagues JM, Blanco A, Tabernero MD, Ciudad J, Lopez A, Goncalves JM, Orfao A (2001) Gains of chromosome 22 by fluorescence in situ hybridization in the context of an hyperdiploid karyotype are associated with aggressive clinical features in meningioma patients. Cancer 92(2):377–385CrossRefPubMed Maillo A, Diaz P, Sayagues JM, Blanco A, Tabernero MD, Ciudad J, Lopez A, Goncalves JM, Orfao A (2001) Gains of chromosome 22 by fluorescence in situ hybridization in the context of an hyperdiploid karyotype are associated with aggressive clinical features in meningioma patients. Cancer 92(2):377–385CrossRefPubMed
45.
go back to reference Maillo A, Orfao A, Espinosa AB, Sayagues JM, Merino M, Sousa P, Lara M, Tabernero MD (2007) Early recurrences in histologically benign/grade I meningiomas are associated with large tumors and coexistence of monosomy 14 and del(1p36) in the ancestral tumor cell clone. Neuro-oncology 9(4):438–446. doi:10.1215/15228517-2007-026 CrossRefPubMedPubMedCentral Maillo A, Orfao A, Espinosa AB, Sayagues JM, Merino M, Sousa P, Lara M, Tabernero MD (2007) Early recurrences in histologically benign/grade I meningiomas are associated with large tumors and coexistence of monosomy 14 and del(1p36) in the ancestral tumor cell clone. Neuro-oncology 9(4):438–446. doi:10.​1215/​15228517-2007-026 CrossRefPubMedPubMedCentral
46.
go back to reference Maillo A, Orfao A, Sayagues JM, Diaz P, Gomez-Moreta JA, Caballero M, Santamarta D, Santos-Briz A, Morales F, Tabernero MD (2003) New classification scheme for the prognostic stratification of meningioma on the basis of chromosome 14 abnormalities, patient age, and tumor histopathology. J Clin Oncol 21(17):3285–3295. doi:10.1200/JCO.2003.07.156 CrossRefPubMed Maillo A, Orfao A, Sayagues JM, Diaz P, Gomez-Moreta JA, Caballero M, Santamarta D, Santos-Briz A, Morales F, Tabernero MD (2003) New classification scheme for the prognostic stratification of meningioma on the basis of chromosome 14 abnormalities, patient age, and tumor histopathology. J Clin Oncol 21(17):3285–3295. doi:10.​1200/​JCO.​2003.​07.​156 CrossRefPubMed
47.
49.
go back to reference Marzouka NA, Nordlund J, Backlin CL, Lonnerholm G, Syvanen AC, Carlsson Almlof J (2016) CopyNumber450kCancer: baseline correction for accurate copy number calling from the 450k methylation array. Bioinformatics 32(7):1080–1082. doi:10.1093/bioinformatics/btv652 CrossRefPubMed Marzouka NA, Nordlund J, Backlin CL, Lonnerholm G, Syvanen AC, Carlsson Almlof J (2016) CopyNumber450kCancer: baseline correction for accurate copy number calling from the 450k methylation array. Bioinformatics 32(7):1080–1082. doi:10.​1093/​bioinformatics/​btv652 CrossRefPubMed
50.
go back to reference Mawrin C, Sasse T, Kirches E, Kropf S, Schneider T, Grimm C, Pambor C, Vorwerk CK, Firsching R, Lendeckel U, Dietzmann K (2005) Different activation of mitogen-activated protein kinase and Akt signaling is associated with aggressive phenotype of human meningiomas. Clin Cancer Res 11(11):4074–4082. doi:10.1158/1078-0432.CCR-04-2550 CrossRefPubMed Mawrin C, Sasse T, Kirches E, Kropf S, Schneider T, Grimm C, Pambor C, Vorwerk CK, Firsching R, Lendeckel U, Dietzmann K (2005) Different activation of mitogen-activated protein kinase and Akt signaling is associated with aggressive phenotype of human meningiomas. Clin Cancer Res 11(11):4074–4082. doi:10.​1158/​1078-0432.​CCR-04-2550 CrossRefPubMed
51.
go back to reference Merino DM, Shlien A, Villani A, Pienkowska M, Mack S, Ramaswamy V, Shih D, Tatevossian R, Novokmet A, Choufani S, Dvir R, Ben-Arush M, Harris BT, Hwang EI, Lulla R, Pfister SM, Achatz MI, Jabado N, Finlay JL, Weksberg R, Bouffet E, Hawkins C, Taylor MD, Tabori U, Ellison DW, Gilbertson RJ, Malkin D (2015) Molecular characterization of choroid plexus tumors reveals novel clinically relevant subgroups. Clin Cancer Res 21(1):184–192. doi:10.1158/1078-0432.CCR-14-1324 CrossRefPubMed Merino DM, Shlien A, Villani A, Pienkowska M, Mack S, Ramaswamy V, Shih D, Tatevossian R, Novokmet A, Choufani S, Dvir R, Ben-Arush M, Harris BT, Hwang EI, Lulla R, Pfister SM, Achatz MI, Jabado N, Finlay JL, Weksberg R, Bouffet E, Hawkins C, Taylor MD, Tabori U, Ellison DW, Gilbertson RJ, Malkin D (2015) Molecular characterization of choroid plexus tumors reveals novel clinically relevant subgroups. Clin Cancer Res 21(1):184–192. doi:10.​1158/​1078-0432.​CCR-14-1324 CrossRefPubMed
55.
go back to reference Nordlund J, Backlin CL, Wahlberg P, Busche S, Berglund EC, Eloranta ML, Flaegstad T, Forestier E, Frost BM, Harila-Saari A, Heyman M, Jonsson OG, Larsson R, Palle J, Ronnblom L, Schmiegelow K, Sinnett D, Soderhall S, Pastinen T, Gustafsson MG, Lonnerholm G, Syvanen AC (2013) Genome-wide signatures of differential DNA methylation in pediatric acute lymphoblastic leukemia. Genome Biol 14(9):r105. doi:10.1186/gb-2013-14-9-r105 CrossRefPubMedPubMedCentral Nordlund J, Backlin CL, Wahlberg P, Busche S, Berglund EC, Eloranta ML, Flaegstad T, Forestier E, Frost BM, Harila-Saari A, Heyman M, Jonsson OG, Larsson R, Palle J, Ronnblom L, Schmiegelow K, Sinnett D, Soderhall S, Pastinen T, Gustafsson MG, Lonnerholm G, Syvanen AC (2013) Genome-wide signatures of differential DNA methylation in pediatric acute lymphoblastic leukemia. Genome Biol 14(9):r105. doi:10.​1186/​gb-2013-14-9-r105 CrossRefPubMedPubMedCentral
56.
go back to reference Nordlund J, Backlin CL, Zachariadis V, Cavelier L, Dahlberg J, Ofverholm I, Barbany G, Nordgren A, Overnas E, Abrahamsson J, Flaegstad T, Heyman MM, Jonsson OG, Kanerva J, Larsson R, Palle J, Schmiegelow K, Gustafsson MG, Lonnerholm G, Forestier E, Syvanen AC (2015) DNA methylation-based subtype prediction for pediatric acute lymphoblastic leukemia. Clin Epigenet 7:11. doi:10.1186/s13148-014-0039-z CrossRef Nordlund J, Backlin CL, Zachariadis V, Cavelier L, Dahlberg J, Ofverholm I, Barbany G, Nordgren A, Overnas E, Abrahamsson J, Flaegstad T, Heyman MM, Jonsson OG, Kanerva J, Larsson R, Palle J, Schmiegelow K, Gustafsson MG, Lonnerholm G, Forestier E, Syvanen AC (2015) DNA methylation-based subtype prediction for pediatric acute lymphoblastic leukemia. Clin Epigenet 7:11. doi:10.​1186/​s13148-014-0039-z CrossRef
57.
go back to reference Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RG, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape K (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17(5):510–522. doi:10.1016/j.ccr.2010.03.017 CrossRefPubMedPubMedCentral Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RG, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape K (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17(5):510–522. doi:10.​1016/​j.​ccr.​2010.​03.​017 CrossRefPubMedPubMedCentral
58.
go back to reference Olar A, Wani KM, Sulman EP, Mansouri A, Zadeh G, Wilson CD, DeMonte F, Fuller GN, Aldape KD (2015) Mitotic index is an independent predictor of recurrence-free survival in meningioma. Brain Pathol 25(3):266–275. doi:10.1111/bpa.12174 CrossRefPubMed Olar A, Wani KM, Sulman EP, Mansouri A, Zadeh G, Wilson CD, DeMonte F, Fuller GN, Aldape KD (2015) Mitotic index is an independent predictor of recurrence-free survival in meningioma. Brain Pathol 25(3):266–275. doi:10.​1111/​bpa.​12174 CrossRefPubMed
59.
go back to reference Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro-oncology 17(Suppl 4):iv1–iv62. doi:10.1093/neuonc/nov189 Ostrom QT, Gittleman H, Fulop J, Liu M, Blanda R, Kromer C, Wolinsky Y, Kruchko C, Barnholtz-Sloan JS (2015) CBTRUS statistical report: primary brain and central nervous system tumors diagnosed in the United States in 2008–2012. Neuro-oncology 17(Suppl 4):iv1–iv62. doi:10.​1093/​neuonc/​nov189
60.
go back to reference Ozaki S, Nishizaki T, Ito H, Sasaki K (1999) Comparative genomic hybridization analysis of genetic alterations associated with malignant progression of meningioma. J Neurooncol 41(2):167–174CrossRefPubMed Ozaki S, Nishizaki T, Ito H, Sasaki K (1999) Comparative genomic hybridization analysis of genetic alterations associated with malignant progression of meningioma. J Neurooncol 41(2):167–174CrossRefPubMed
61.
go back to reference Perry A, Banerjee R, Lohse CM, Kleinschmidt-DeMasters BK, Scheithauer BW (2002) A role for chromosome 9p21 deletions in the malignant progression of meningiomas and the prognosis of anaplastic meningiomas. Brain Pathol 12(2):183–190PubMed Perry A, Banerjee R, Lohse CM, Kleinschmidt-DeMasters BK, Scheithauer BW (2002) A role for chromosome 9p21 deletions in the malignant progression of meningiomas and the prognosis of anaplastic meningiomas. Brain Pathol 12(2):183–190PubMed
63.
go back to reference Prowald A, Wemmert S, Biehl C, Storck S, Martin T, Henn W, Ketter R, Meese E, Zang KD, Steudel WI, Urbschat S (2005) Interstitial loss and gain of sequences on chromosome 22 in meningiomas with normal karyotype. Int J Oncol 26(2):385–393PubMed Prowald A, Wemmert S, Biehl C, Storck S, Martin T, Henn W, Ketter R, Meese E, Zang KD, Steudel WI, Urbschat S (2005) Interstitial loss and gain of sequences on chromosome 22 in meningiomas with normal karyotype. Int J Oncol 26(2):385–393PubMed
64.
go back to reference Rohrich M, Koelsche C, Schrimpf D, Capper D, Sahm F, Kratz A, Reuss J, Hovestadt V, Jones DT, Bewerunge-Hudler M, Becker A, Weis J, Mawrin C, Mittelbronn M, Perry A, Mautner VF, Mechtersheimer G, Hartmann C, Okuducu AF, Arp M, Seiz-Rosenhagen M, Hanggi D, Heim S, Paulus W, Schittenhelm J, Ahmadi R, Herold-Mende C, Unterberg A, Pfister SM, von Deimling A, Reuss DE (2016) Methylation-based classification of benign and malignant peripheral nerve sheath tumors. Acta Neuropathol 131(6):877–887. doi:10.1007/s00401-016-1540-6 CrossRefPubMed Rohrich M, Koelsche C, Schrimpf D, Capper D, Sahm F, Kratz A, Reuss J, Hovestadt V, Jones DT, Bewerunge-Hudler M, Becker A, Weis J, Mawrin C, Mittelbronn M, Perry A, Mautner VF, Mechtersheimer G, Hartmann C, Okuducu AF, Arp M, Seiz-Rosenhagen M, Hanggi D, Heim S, Paulus W, Schittenhelm J, Ahmadi R, Herold-Mende C, Unterberg A, Pfister SM, von Deimling A, Reuss DE (2016) Methylation-based classification of benign and malignant peripheral nerve sheath tumors. Acta Neuropathol 131(6):877–887. doi:10.​1007/​s00401-016-1540-6 CrossRefPubMed
65.
go back to reference Sahm F, Schrimpf D, Olar A, Koelsche C, Reuss D, Bissel J, Kratz A, Capper D, Schefzyk S, Hielscher T, Wang Q, Sulman EP, Adeberg S, Koch A, Okuducu AF, Brehmer S, Schittenhelm J, Becker A, Brokinkel B, Schmidt M, Ull T, Gousias K, Kessler AF, Lamszus K, Debus J, Mawrin C, Kim YJ, Simon M, Ketter R, Paulus W, Aldape KD, Herold-Mende C, von Deimling A (2016) TERT promoter mutations and risk of recurrence in meningioma. J Natl Cancer Inst. doi:10.1093/jnci/djv377 PubMed Sahm F, Schrimpf D, Olar A, Koelsche C, Reuss D, Bissel J, Kratz A, Capper D, Schefzyk S, Hielscher T, Wang Q, Sulman EP, Adeberg S, Koch A, Okuducu AF, Brehmer S, Schittenhelm J, Becker A, Brokinkel B, Schmidt M, Ull T, Gousias K, Kessler AF, Lamszus K, Debus J, Mawrin C, Kim YJ, Simon M, Ketter R, Paulus W, Aldape KD, Herold-Mende C, von Deimling A (2016) TERT promoter mutations and risk of recurrence in meningioma. J Natl Cancer Inst. doi:10.​1093/​jnci/​djv377 PubMed
67.
go back to reference Sturm D, Orr BA, Toprak UH, Hovestadt V, Jones DT, Capper D, Sill M, Buchhalter I, Northcott PA, Leis I, Ryzhova M, Koelsche C, Pfaff E, Allen SJ, Balasubramanian G, Worst BC, Pajtler KW, Brabetz S, Johann PD, Sahm F, Reimand J, Mackay A, Carvalho DM, Remke M, Phillips JJ, Perry A, Cowdrey C, Drissi R, Fouladi M, Giangaspero F, Lastowska M, Grajkowska W, Scheurlen W, Pietsch T, Hagel C, Gojo J, Lotsch D, Berger W, Slavc I, Haberler C, Jouvet A, Holm S, Hofer S, Prinz M, Keohane C, Fried I, Mawrin C, Scheie D, Mobley BC, Schniederjan MJ, Santi M, Buccoliero AM, Dahiya S, Kramm CM, von Bueren AO, von Hoff K, Rutkowski S, Herold-Mende C, Fruhwald MC, Milde T, Hasselblatt M, Wesseling P, Rossler J, Schuller U, Ebinger M, Schittenhelm J, Frank S, Grobholz R, Vajtai I, Hans V, Schneppenheim R, Zitterbart K, Collins VP, Aronica E, Varlet P, Puget S, Dufour C, Grill J, Figarella-Branger D, Wolter M, Schuhmann MU, Shalaby T, Grotzer M, van Meter T, Monoranu CM, Felsberg J, Reifenberger G, Snuderl M, Forrester LA, Koster J, Versteeg R, Volckmann R, van Sluis P, Wolf S, Mikkelsen T, Gajjar A, Aldape K, Moore AS, Taylor MD, Jones C, Jabado N, Karajannis MA, Eils R, Schlesner M, Lichter P, von Deimling A, Pfister SM, Ellison DW, Korshunov A, Kool M (2016) New brain tumor entities emerge from molecular classification of CNS-PNETs. Cell 164(5):1060–1072. doi:10.1016/j.cell.2016.01.015 CrossRefPubMed Sturm D, Orr BA, Toprak UH, Hovestadt V, Jones DT, Capper D, Sill M, Buchhalter I, Northcott PA, Leis I, Ryzhova M, Koelsche C, Pfaff E, Allen SJ, Balasubramanian G, Worst BC, Pajtler KW, Brabetz S, Johann PD, Sahm F, Reimand J, Mackay A, Carvalho DM, Remke M, Phillips JJ, Perry A, Cowdrey C, Drissi R, Fouladi M, Giangaspero F, Lastowska M, Grajkowska W, Scheurlen W, Pietsch T, Hagel C, Gojo J, Lotsch D, Berger W, Slavc I, Haberler C, Jouvet A, Holm S, Hofer S, Prinz M, Keohane C, Fried I, Mawrin C, Scheie D, Mobley BC, Schniederjan MJ, Santi M, Buccoliero AM, Dahiya S, Kramm CM, von Bueren AO, von Hoff K, Rutkowski S, Herold-Mende C, Fruhwald MC, Milde T, Hasselblatt M, Wesseling P, Rossler J, Schuller U, Ebinger M, Schittenhelm J, Frank S, Grobholz R, Vajtai I, Hans V, Schneppenheim R, Zitterbart K, Collins VP, Aronica E, Varlet P, Puget S, Dufour C, Grill J, Figarella-Branger D, Wolter M, Schuhmann MU, Shalaby T, Grotzer M, van Meter T, Monoranu CM, Felsberg J, Reifenberger G, Snuderl M, Forrester LA, Koster J, Versteeg R, Volckmann R, van Sluis P, Wolf S, Mikkelsen T, Gajjar A, Aldape K, Moore AS, Taylor MD, Jones C, Jabado N, Karajannis MA, Eils R, Schlesner M, Lichter P, von Deimling A, Pfister SM, Ellison DW, Korshunov A, Kool M (2016) New brain tumor entities emerge from molecular classification of CNS-PNETs. Cell 164(5):1060–1072. doi:10.​1016/​j.​cell.​2016.​01.​015 CrossRefPubMed
68.
go back to reference Sturm D, Witt H, Hovestadt V, Khuong-Quang DA, Jones DT, Konermann C, Pfaff E, Tonjes M, Sill M, Bender S, Kool M, Zapatka M, Becker N, Zucknick M, Hielscher T, Liu XY, Fontebasso AM, Ryzhova M, Albrecht S, Jacob K, Wolter M, Ebinger M, Schuhmann MU, van Meter T, Fruhwald MC, Hauch H, Pekrun A, Radlwimmer B, Niehues T, von Komorowski G, Durken M, Kulozik AE, Madden J, Donson A, Foreman NK, Drissi R, Fouladi M, Scheurlen W, von Deimling A, Monoranu C, Roggendorf W, Herold-Mende C, Unterberg A, Kramm CM, Felsberg J, Hartmann C, Wiestler B, Wick W, Milde T, Witt O, Lindroth AM, Schwartzentruber J, Faury D, Fleming A, Zakrzewska M, Liberski PP, Zakrzewski K, Hauser P, Garami M, Klekner A, Bognar L, Morrissy S, Cavalli F, Taylor MD, van Sluis P, Koster J, Versteeg R, Volckmann R, Mikkelsen T, Aldape K, Reifenberger G, Collins VP, Majewski J, Korshunov A, Lichter P, Plass C, Jabado N, Pfister SM (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22(4):425–437. doi:10.1016/j.ccr.2012.08.024 CrossRefPubMed Sturm D, Witt H, Hovestadt V, Khuong-Quang DA, Jones DT, Konermann C, Pfaff E, Tonjes M, Sill M, Bender S, Kool M, Zapatka M, Becker N, Zucknick M, Hielscher T, Liu XY, Fontebasso AM, Ryzhova M, Albrecht S, Jacob K, Wolter M, Ebinger M, Schuhmann MU, van Meter T, Fruhwald MC, Hauch H, Pekrun A, Radlwimmer B, Niehues T, von Komorowski G, Durken M, Kulozik AE, Madden J, Donson A, Foreman NK, Drissi R, Fouladi M, Scheurlen W, von Deimling A, Monoranu C, Roggendorf W, Herold-Mende C, Unterberg A, Kramm CM, Felsberg J, Hartmann C, Wiestler B, Wick W, Milde T, Witt O, Lindroth AM, Schwartzentruber J, Faury D, Fleming A, Zakrzewska M, Liberski PP, Zakrzewski K, Hauser P, Garami M, Klekner A, Bognar L, Morrissy S, Cavalli F, Taylor MD, van Sluis P, Koster J, Versteeg R, Volckmann R, Mikkelsen T, Aldape K, Reifenberger G, Collins VP, Majewski J, Korshunov A, Lichter P, Plass C, Jabado N, Pfister SM (2012) Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22(4):425–437. doi:10.​1016/​j.​ccr.​2012.​08.​024 CrossRefPubMed
69.
go back to reference Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, Beck S (2013) A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450k DNA methylation data. Bioinformatics 29(2):189–196. doi:10.1093/bioinformatics/bts680 CrossRefPubMed Teschendorff AE, Marabita F, Lechner M, Bartlett T, Tegner J, Gomez-Cabrero D, Beck S (2013) A beta-mixture quantile normalization method for correcting probe design bias in Illumina Infinium 450k DNA methylation data. Bioinformatics 29(2):189–196. doi:10.​1093/​bioinformatics/​bts680 CrossRefPubMed
70.
go back to reference Thomas C, Sill M, Ruland V, Witten A, Hartung S, Kordes U, Jeibmann A, Beschorner R, Keyvani K, Bergmann M, Mittelbronn M, Pietsch T, Felsberg J, Monoranu CM, Varlet P, Hauser P, Olar A, Grundy RG, Wolff JE, Korshunov A, Jones DT, Bewerunge-Hudler M, Hovestadt V, von Deimling A, Pfister SM, Paulus W, Capper D, Hasselblatt M (2016) Methylation profiling of choroid plexus tumors reveals 3 clinically distinct subgroups. Neuro-oncology 18(6):790–796. doi:10.1093/neuonc/nov322 CrossRefPubMed Thomas C, Sill M, Ruland V, Witten A, Hartung S, Kordes U, Jeibmann A, Beschorner R, Keyvani K, Bergmann M, Mittelbronn M, Pietsch T, Felsberg J, Monoranu CM, Varlet P, Hauser P, Olar A, Grundy RG, Wolff JE, Korshunov A, Jones DT, Bewerunge-Hudler M, Hovestadt V, von Deimling A, Pfister SM, Paulus W, Capper D, Hasselblatt M (2016) Methylation profiling of choroid plexus tumors reveals 3 clinically distinct subgroups. Neuro-oncology 18(6):790–796. doi:10.​1093/​neuonc/​nov322 CrossRefPubMed
71.
go back to reference Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, Campos C, Fabius AW, Lu C, Ward PS, Thompson CB, Kaufman A, Guryanova O, Levine R, Heguy A, Viale A, Morris LG, Huse JT, Mellinghoff IK, Chan TA (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483(7390):479–483. doi:10.1038/nature10866 CrossRefPubMedPubMedCentral Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, Campos C, Fabius AW, Lu C, Ward PS, Thompson CB, Kaufman A, Guryanova O, Levine R, Heguy A, Viale A, Morris LG, Huse JT, Mellinghoff IK, Chan TA (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483(7390):479–483. doi:10.​1038/​nature10866 CrossRefPubMedPubMedCentral
73.
go back to reference van den Bent MJ, Gravendeel LA, Gorlia T, Kros JM, Lapre L, Wesseling P, Teepen JL, Idbaih A, Sanson M, Smitt PA, French PJ (2011) A hypermethylated phenotype is a better predictor of survival than MGMT methylation in anaplastic oligodendroglial brain tumors: a report from EORTC study 26951. Clin Cancer Res 17(22):7148–7155. doi:10.1158/1078-0432.CCR-11-1274 CrossRefPubMed van den Bent MJ, Gravendeel LA, Gorlia T, Kros JM, Lapre L, Wesseling P, Teepen JL, Idbaih A, Sanson M, Smitt PA, French PJ (2011) A hypermethylated phenotype is a better predictor of survival than MGMT methylation in anaplastic oligodendroglial brain tumors: a report from EORTC study 26951. Clin Cancer Res 17(22):7148–7155. doi:10.​1158/​1078-0432.​CCR-11-1274 CrossRefPubMed
74.
go back to reference Vengoechea J, Sloan AE, Chen Y, Guan X, Ostrom QT, Kerstetter A, Capella D, Cohen ML, Wolinsky Y, Devine K, Selman W, Barnett GH, Warnick RE, McPherson C, Chiocca EA, Elder JB, Barnholtz-Sloan JS (2013) Methylation markers of malignant potential in meningiomas. J Neurosurg 119(4):899–906. doi:10.3171/2013.7.JNS13311 CrossRefPubMed Vengoechea J, Sloan AE, Chen Y, Guan X, Ostrom QT, Kerstetter A, Capella D, Cohen ML, Wolinsky Y, Devine K, Selman W, Barnett GH, Warnick RE, McPherson C, Chiocca EA, Elder JB, Barnholtz-Sloan JS (2013) Methylation markers of malignant potential in meningiomas. J Neurosurg 119(4):899–906. doi:10.​3171/​2013.​7.​JNS13311 CrossRefPubMed
75.
go back to reference Weber RG, Bostrom J, Wolter M, Baudis M, Collins VP, Reifenberger G, Lichter P (1997) Analysis of genomic alterations in benign, atypical, and anaplastic meningiomas: toward a genetic model of meningioma progression. Proc Natl Acad Sci 94(26):14719–14724CrossRefPubMedPubMedCentral Weber RG, Bostrom J, Wolter M, Baudis M, Collins VP, Reifenberger G, Lichter P (1997) Analysis of genomic alterations in benign, atypical, and anaplastic meningiomas: toward a genetic model of meningioma progression. Proc Natl Acad Sci 94(26):14719–14724CrossRefPubMedPubMedCentral
76.
go back to reference Zang KD (2001) Meningioma: a cytogenetic model of a complex benign human tumor, including data on 394 karyotyped cases. Cytogenet Cell Genet 93(3–4):207–220CrossRefPubMed Zang KD (2001) Meningioma: a cytogenetic model of a complex benign human tumor, including data on 394 karyotyped cases. Cytogenet Cell Genet 93(3–4):207–220CrossRefPubMed
Metadata
Title
Global epigenetic profiling identifies methylation subgroups associated with recurrence-free survival in meningioma
Authors
Adriana Olar
Khalida M. Wani
Charmaine D. Wilson
Gelareh Zadeh
Franco DeMonte
David T. W. Jones
Stefan M. Pfister
Erik P. Sulman
Kenneth D. Aldape
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
Acta Neuropathologica / Issue 3/2017
Print ISSN: 0001-6322
Electronic ISSN: 1432-0533
DOI
https://doi.org/10.1007/s00401-017-1678-x

Other articles of this Issue 3/2017

Acta Neuropathologica 3/2017 Go to the issue