Lowered H3K27me3 and DNA hypomethylation define poorly prognostic pediatric posterior fossa ependymomas

Science Translational Medicine

Volumn 8, Issue 366, 2016, Pages

  Bayliss, Jill ^a   Mukherjee, Piali ^b   Lu, Chao ^c   Jain, Siddhant U ^d   Chung, Chan ^a   Martinez, Daniel ^e   Sabari, Benjamin ^c   Margol, Ashley S ^f   Panwalkar, Pooja ^a   Parolia, Abhijit ^a,g   Pekmezci, Melike ^h   McEachin, Richard C ^a   Cieslik, Marcin ^a,g   Tamrazi, Benita ^f   Garcia, Benjamin A ⁱ   La Rocca, Gaspare ^j   Santi, Mariarita ^e   Lewis, Peter W ^d   Hawkins, Cynthia ^k,l   Melnick, Ari ^b   Allis, C David ^c   Thompson, Craig B ^j   Chinnaiyan, Arul M ^a,g   Judkins, Alexander R ^m   Venneti, Sriram ^a   more..

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^h UNIVERSITY OF CALIFORNIA   (United States)

ⁱ UNIVERSITY OF PENNSYLVANIA   (United States)

^j MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^k HOSPITAL FOR SICK CHILDREN   (Canada)

^l UNIVERSITY OF TORONTO   (Canada)

^m UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE H3; HISTONE H3K27ME3; UNCLASSIFIED DRUG; HISTONE;

ADULT; ARTICLE; CANCER TISSUE; CEREBELLUM; CHILD; CHILDHOOD CANCER; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA MODIFICATION; EPENDYMOMA; EPIGENETICS; FEMALE; GENE EXPRESSION; GENE LOCUS; GLIA; GLIOMA; HUMAN; HUMAN TISSUE; MALE; POSTERIOR CRANIAL FOSSA TUMOR; POSTERIOR FOSSA EPENDYMOMA; PRIORITY JOURNAL; PROGNOSIS; WESTERN BLOTTING; BRAIN TUMOR; CENTRAL NERVOUS SYSTEM; CHEMISTRY; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENETICS; HUMAN GENOME; METABOLISM; MUTATION; PATHOLOGY; TREATMENT OUTCOME;

BRAIN NEOPLASMS; CENTRAL NERVOUS SYSTEM; CHILD; CPG ISLANDS; DNA METHYLATION; EPENDYMOMA; EPIGENESIS, GENETIC; GENE EXPRESSION PROFILING; GENOME, HUMAN; HISTONES; HUMANS; MUTATION; PROGNOSIS; TREATMENT OUTCOME;

EID: 84997794993     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aah6904     Document Type: Article

References (30)

1. D. N. Louis, A. Perry, G. Reifenberger, A. von Deimling, D. Figarella-Branger, W. K. Cavenee, H. Ohgaki, O. D. Wiestler, P. Kleihues, D. W. Ellison, The 2016 World Health Organization classification of tumors of the central nervous system: A summary. Acta Neuropathol. 131, 803-820 (2016).
2. K. W. Pajtler, H. Witt, M. Sill, D. T. W. Jones, V. Hovestadt, F. Kratochwil, K. Wani, R. Tatevossian, C. Punchihewa, P. Johann, J. Reimand, H.-J. Warnatz, M. Ryzhova, S. Mack, V. Ramaswamy, D. Capper, L. Schweizer, L. Sieber, A. Wittmann, Z. Huang, P. van Sluis, R. Volckmann, J. Koster, R. Versteeg, D. Fults, H. Toledano, S. Avigad, L. M. Hoffman, A. M. Donson, N. Foreman, E. Hewer, K. Zitterbart, M. Gilbert, T. S. Armstrong, N. Gupta, J. C. Allen, M. A. Karajannis, D. Zagzag, M. Hasselblatt, A. E. Kulozik, O. Witt, V. P. Collins, K. von Hoff, S. Rutkowski, T. Pietsch, G. Bader, M.-L. Yaspo, A. von Deimling, P. Lichter, M. D. Taylor, R. Gilbertson, D. W. Ellison, K. Aldape, A. Korshunov, M. Kool, S. M. Pfister, Molecular classification of ependymal tumors across all CNS compartments, histopathological grades, and age groups. Cancer Cell 27, 728-743 (2015).
3. R. G. Grundy, S. A. Wilne, C. L. Weston, K. Robinson, L. S. Lashford, J. Ironside, T. Cox, W. K. Chong, R. H. A. Campbell, C. C. Bailey, R. Gattamaneni, S. Picton, N. Thorpe, C. Mallucci, M. W. English, J. A. G. Punt, D. A. Walker, D. W. Ellison, D. Machin; Children's Cancer and Leukaemia Group (formerly UKCCSG) Brain Tumour Committee, Primary postoperative chemotherapy without radiotherapy for intracranial ependymoma in children: The UKCCSG/SIOP prospective study. Lancet Oncol. 8, 696-705 (2007).
4. T. E. Merchant, R. K. Mulhern, M. J. Krasin, L. E. Kun, T. Williams, C. Li, X. Xiong, R. B. Khan, R. H. Lustig, F. A. Boop, R. A. Sanford, Preliminary results from a phase II trial of conformal radiation therapy and evaluation of radiation-related CNS effects for pediatric patients with localized ependymoma. J. Clin. Oncol. 22, 3156-3162 (2004).
5. M. Parker, K. M. Mohankumar, C. Punchihewa, R. Weinlich, J. D. Dalton, Y. Li, R. Lee, R. G. Tatevossian, T. N. Phoenix, R. Thiruvenkatam, E. White, B. Tang, W. Orisme, K. Gupta, M. Rusch, X. Chen, Y. Li, P. Nagahawhatte, E. Hedlund, D. Finkelstein, G. Wu, S. Shurtleff, J. Easton, K. Boggs, D. Yergeau, B. Vadodaria, H. L. Mulder, J. Becksfort, P. Gupta, R. Huether, J. Ma, G. Song, A. Gajjar, T. Merchant, F. Boop, A. A. Smith, L. Ding, C. Lu, K. Ochoa, D. Zhao, R. S. Fulton, L. L. Fulton, E. R. Mardis, R. K. Wilson, J. R. Downing, D. R. Green, J. Zhang, D. W. Ellison, R. J. Gilbertson, C11orf95-RELA fusions drive oncogenic NF-kB signalling in ependymoma. Nature 506, 451-455 (2014).
6. H. Witt, S. C. Mack, M. Ryzhova, S. Bender, M. Sill, R. Isserlin, A. Benner, T. Hielscher, T. Milde, M. Remke, D. T. Jones, P. A. Northcott, L. Garzia, K. C. Bertrand, A. Wittmann, Y. Yao, S. S. Roberts, L. Massimi, T. Van Meter, W. A. Weiss, N. Gupta, W. Grajkowska, B. Lach, Y. J. Cho, A. von Deimling, A. E. Kulozik, O. Witt, G. D. Bader, C. E. Hawkins, U. Tabori, A. Guha, J. T. Rutka, P. Lichter, A. Korshunov, M. D. Taylor, S. M. Pfister, Delineation of two clinically and molecularly distinct subgroups of posterior fossa ependymoma. Cancer Cell 20, 143-157 (2011).
7. S. C. Mack, H. Witt, R. M. Piro, L. Gu, S. Zuyderduyn, A. M. Stütz, X. Wang, M. Gallo, L. Garzia, K. Zayne, X. Zhang, V. Ramaswamy, N. Jäger, D. T. Jones, M. Sill, T. J. Pugh, M. Ryzhova, K. M. Wani, D. J. Shih, R. Head, M. Remke, S. D. Bailey, T. Zichner, C. C. Faria, M. Barszczyk, S. Stark, H. Seker-Cin, S. Hutter, P. Johann, S. Bender, V. Hovestadt, T. Tzaridis, A. M. Dubuc, P. A. Northcott, J. Peacock, K. C. Bertrand, S. Agnihotri, F. M. Cavalli, I. Clarke, K. Nethery-Brokx, C. L. Creasy, S. K. Verma, J. Koster, X. Wu, Y. Yao, T. Milde, P. Sin-Chan, J. Zuccaro, L. Lau, S. Pereira, P. Castelo-Branco, M. Hirst, M. A. Marra, S. S. Roberts, D. Fults, L. Massimi, Y. J. Cho, T. Van Meter, W. Grajkowska, B. Lach, A. E. Kulozik, A. von Deimling, O. Witt, S. W. Scherer, X. Fan, K. M. Muraszko, M. Kool, S. L. Pomeroy, N. Gupta, J. Phillips, A. Huang, U. Tabori, C. Hawkins, D. Malkin, P. N. Kongkham, W. A. Weiss, N. Jabado, J. T. Rutka, E. Bouffet, J. O. Korbel, M. Lupien, K. D. Aldape, G. D. Bader, R. Eils, P. Lichter, P. B. Dirks, S. M. Pfister, A. Korshunov, M. D. Taylor, Epigenomic alterations define lethal CIMP-positive ependymomas of infancy. Nature 506, 445-450 (2014).
8. V. Ramaswamy, T. Hielscher, S. C. Mack, A. Lassaletta, T. Lin, K. W. Pajtler, D. T. Jones, B. Luu, F. M. Cavalli, K. Aldape, M. Remke, M. Mynarek, S. Rutkowski, S. Gururangan, R. E. McLendon, E. S. Lipp, C. Dunham, J. Hukin, D. D. Eisenstat, D. Fulton, F. K. H. van Landeghem, M. Santi, M. L. C. van Veelen, E. G. Van Meir, S. Osuka, X. Fan, K. M. Muraszko, D. P. C. Tirapelli, S. M. Oba-Shinjo, S. K. N. Marie, C. G. Carlotti, J. Y. Lee, A. A. Rao, C. Giannini, C. C. Faria, S. Nunes, J. Mora, R. L. Hamilton, P. Hauser, N. Jabado, K. Petrecca, S. Jung, L. Massimi, M. Zollo, G. Cinalli, L. Bognár, A. Klekner, T. Hortobágyi, S. Leary, R. P. Ermoian, J. M. Olson, J. R. Leonard, C. Gardner, W. A. Grajkowska, L. B. Chambless, J. Cain, C. G. Eberhart, S. Ahsan, M. Massimino, F. Giangaspero, F. R. Buttarelli, R. J. Packer, L. Emery, W. H. Yong, H. Soto, L. M. Liau, R. Everson, A. Grossbach, T. Shalaby, M. Grotzer, M. A. Karajannis, D. Zagzag, H. Wheeler, K. von Hoff, M. M. Alonso, T. Tuñon, U. Schüller, K. Zitterbart, J. Sterba, J. A. Chan, M. Guzman, S. K. Elbabaa, H. Colman, G. Dhall, P. G. Fisher, M. Fouladi, A. Gajjar, S. Goldman, E. Hwang, M. Kool, H. Ladha, E. Vera-Bolanos, K. Wani, F. Lieberman, T. Mikkelsen, A. M. Omuro, I. F. Pollack, M. Prados, H. I. Robins, R. Soffietti, J. Wu, P. Metellus, U. Tabori, U. Bartels, E. Bouffet, C. E. Hawkins, J. T. Rutka, P. Dirks, S. M. Pfister, T. E. Merchant, M. R. Gilbert, T. S. Armstrong, A. Korshunov, D. W. Ellison, M. D. Taylor, Therapeutic impact of cytoreductive surgery and irradiation of posterior fossa ependymoma in the molecular era: A retrospective multicohort analysis. J. Clin. Oncol. 34, 2468-2477 (2016).
9. S. Venneti, M. T. Garimella, L. M. Sullivan, D. Martinez, J. T. Huse, A. Heguy, M. Santi, C. B. Thompson, A. R. Judkins, Evaluation of histone 3 lysine 27 trimethylation (H3K27me3) and enhancer of Zest 2 (EZH2) in pediatric glial and glioneuronal tumors shows decreased H3K27me3 in H3F3A K27M mutant glioblastomas. Brain Pathol. 23, 558-564 (2013).
10. P. W. Lewis, M. M. Muller, M. S. Koletsky, F. Cordero, S. Lin, L. A. Banaszynski, B. A. Garcia, T. W. Muir, O. J. Becher, C. D. Allis, Inhibition of PRC2 activity by a gain-of-function H3 mutation found in pediatric glioblastoma. Science 340, 857-861 (2013).
11. M. D. Taylor, H. Poppleton, C. Fuller, X. Su, Y. Liu, P. Jensen, S. Magdaleno, J. Dalton, C. Calabrese, J. Board, T. Macdonald, J. Rutka, A. Guha, A. Gajjar, T. Curran, R. J. Gilbertson, Radial glia cells are candidate stem cells of ependymoma. Cancer Cell 8, 323-335 (2005).
12. A. M. Li, C. Dunham, U. Tabori, A.-S. Carret, P. D. McNeely, D. Johnston, L. Lafay-Cousin, B. Wilson, D. D. Eisenstat, N. Jabado, S. Zelcer, M. Silva, K. Scheinemann, C. Fryer, G. Hendson, A. Fotovati, C. Hawkins, S. Yip, S. E. Dunn, J. Hukin, EZH2 expression is a prognostic factor in childhood intracranial ependymoma: A Canadian Pediatric Brain Tumor Consortium study. Cancer 121, 1499-1507 (2015).
13. E. M. Mendenhall, R. P. Koche, T. Truong, V. W. Zhou, B. Issac, A. S. Chi, M. Ku, B. E. Bernstein, GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLOS Genet. 6, e1001244 (2010).
14. J. P. Reddington, S. M. Perricone, C. E. Nestor, J. Reichmann, N. A. Youngson, M. Suzuki, D. Reinhardt, D. S. Dunican, J. G. Prendergast, H. Mjoseng, B. H. Ramsahoye, E. Whitelaw, J. M. Greally, I. R. Adams, W. A. Bickmore, R. R. Meehan, Redistribution of H3K27me3 upon DNA hypomethylation results in de-repression of Polycomb target genes. Genome Biol. 14, R25 (2013).
15. A. Yoshizawa, Y. Nakahara, T. Izawa, T. Ishitani, M. Tsutsumi, A. Kuroiwa, M. Itoh, Y. Kikuchi, Zebrafish Dmrta2 regulates neurogenesis in the telencephalon. Genes Cells 16, 1097-1109 (2011).
16. L. C.-L. Hsu, S. Nam, Y. Cui, C. P. Chang, C. F. Wang, H.-C. Kuo, J. D. Touboul, S.-J. Chou, Lhx2 regulates the timing of b-catenin-dependent cortical neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 112, 12199-12204 (2015).
17. J. Schwartzentruber, A. Korshunov, X. Y. Liu, D. T. Jones, E. Pfaff, K. Jacob, D. Sturm, A. M. Fontebasso, D.-A. K. Quang, M. Tönjes, V. Hovestadt, S. Albrecht, M. Kool, A. Nantel, C. Konermann, A. Lindroth, N. Jäger, T. Rausch, M. Ryzhova, J. O. Korbel, T. Hielscher, P. Hauser, M. Garami, A. Klekner, L. Bognar, M. Ebinger, M. U. Schuhmann, W. Scheurlen, A. Pekrun, M. C. Fruhwald, W. Roggendorf, C. Kramm, M. Durken, J. Atkinson, P. Lepage, A. Montpetit, M. Zakrzewska, K. Zakrzewski, P. P. Liberski, Z. Dong, P. Siegel, A. E. Kulozik, M. Zapatka, A. Guha, D. Malkin, J. Felsberg, G. Reifenberger, A. von Deimling, K. Ichimura, V. P. Collins, H. Witt, T. Milde, O. Witt, C. Zhang, P. Castelo-Branco, P. Lichter, D. Faury, U. Tabori, C. Plass, J. Majewski, S. M. Pfister, N. Jabado, Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226-231 (2012).
18. G. Wu, A. Broniscer, T. A. McEachron, C. Lu, B. S. Paugh, J. Becksfort, C. Qu, L. Ding, R. Huether, M. Parker, J. Zhang, A. Gajjar, M. A. Dyer, C. G. Mullighan, R. J. Gilbertson, E. R. Mardis, R. K. Wilson, J. R. Downing, D. W. Ellison, S. J. Baker; St. Jude Children's Research Hospital-Washington University Pediatric Cancer Genome Project, Somatic histone H3 alterations in pediatric diffuse intrinsic pontine gliomas and non-brainstem glioblastomas. Nat. Genet. 44, 251-253 (2012).
19. S. Bender, Y. Tang, A. M. Lindroth, V. Hovestadt, D. T. Jones, M. Kool, M. Zapatka, P. A. Northcott, D. Sturm, W. Wang, B. Radlwimmer, J. W. Højfeldt, N. Truffaux, D. Castel, S. Schubert, M. Ryzhova, H. Seker-Cin, J. Gronych, P. D. Johann, S. Stark, J. Meyer, T. Milde, M. Schuhmann, M. Ebinger, C. M. Monoranu, A. Ponnuswami, S. Chen, C. Jones, O. Witt, V. P. Collins, A. von Deimling, N. Jabado, S. Puget, J. Grill, K. Helin, A. Korshunov, P. Lichter, M. Monje, C. Plass, Y.-J. Cho, S. M. Pfister, Reduced H3K27me3 and DNA hypomethylation are major drivers of gene expression in K27M mutant pediatric high-grade gliomas. Cancer Cell 24, 660-672 (2013).
20. D. Sturm, H. Witt, V. Hovestadt, D.-A. Khuong-Quang, D. T. W. Jones, C. Konermann, E. Pfaff, M. Tonjes, M. Sill, S. Bender, M. Kool, M. Zapatka, N. Becker, M. Zucknick, T. Hielscher, X. Y. Liu, A. M. Fontebasso, M. Ryzhova, S. Albrecht, K. Jacob, M. Wolter, M. Ebinger, M. U. Schuhmann, T. van Meter, M. C. Frühwald, H. Hauch, A. Pekrun, B. Radlwimmer, T. Niehues, G. von Komorowski, M. Dürken, A. E. Kulozik, J. Madden, A. Donson, N. K. Foreman, R. Drissi, M. Fouladi, W. Scheurlen, A. von Deimling, C.-M. Monoranu, W. Roggendorf, C. Herold-Mende, A. Unterberg, C. M. Kramm, J. Felsberg, C. Hartmann, B. Wiestler, W. Wick, T. Milde, O. Witt, A. M. Lindroth, J. Schwartzentruber, D. Faury, A. Fleming, M. Zakrzewska, P. P. Liberski, K. Zakrzewski, P. Hauser, M. Garami, A. Klekner, L. Bognar, S. Morrissy, F. Cavalli, M. D. Taylor, P. van Sluis, J. Koster, R. Versteeg, R. Volckmann, T. Mikkelsen, K. Aldape, G. Reifenberger, V. P. Collins, J. Majewski, A. Korshunov, P. Lichter, C. Plass, N. Jabado, S. M. Pfister, Hotspot mutations in H3F3A and IDH1 define distinct epigenetic and biological subgroups of glioblastoma. Cancer Cell 22, 425-437 (2012).
21. K.-M. Chan, D. Fang, H. Gan, R. Hashizume, C. Yu, M. Schroeder, N. Gupta, S. Mueller, C. D. James, R. Jenkins, J. Sarkaria, Z. Zhang, The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev. 27, 985-990 (2013).
22. K. Funato, T. Major, P. W. Lewis, C. D. Allis, V. Tabar, Use of human embryonic stem cells to model pediatric gliomas with H3.3K27M histone mutation. Science 346, 1529-1533 (2014).
23. J. H. Lui, T. J. Nowakowski, A. A. Pollen, A. Javaherian, A. R. Kriegstein, M. C. Oldham, Radial glia require PDGFD-PDGFRb signalling in human but not mouse neocortex. Nature 515, 264-268 (2014).
24. D. N. Louis, H. Ohgaki, O. D. Wiestler, W. K. Cavenee, P. C. Burger, A. Jouvet, B. W. Scheithauer, P. Kleihues, The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 114, 97-109 (2007).
25. R. A. Johnson, K. D. Wright, H. Poppleton, K. M. Mohankumar, D. Finkelstein, S. B. Pounds, V. Rand, S. E. S. Leary, E. White, C. Eden, T. Hogg, P. Northcott, S. Mack, G. Neale, Y. D. Wang, B. Coyle, J. Atkinson, M. DeWire, T. A. Kranenburg, Y. Gillespie, J. C. Allen, T. Merchant, F. A. Boop, R. A. Sanford, A. Gajjar, D. W. Ellison, M. D. Taylor, R. G. Grundy, R. J. Gilbertson, Cross-species genomics matches driver mutations and cell compartments to model ependymoma. Nature 466, 632-636 (2010).
26. C. De Juan Romero, V. Borrell, Coevolution of radial glial cells and the cerebral cortex. Glia 63, 1303-1319 (2015).
27. C. L. Frank, F. Liu, R. Wijayatunge, L. Song, M. T. Biegler, M. G. Yang, C. M. Vockley, A. Safi, C. A. Gersbach, G. E. Crawford, A. E. West, Regulation of chromatin accessibility and Zic binding at enhancers in the developing cerebellum. Nat. Neurosci. 18, 647-656 (2015).
28. A. A. Pollen, T. J. Nowakowski, J. Chen, H. Retallack, C. Sandoval-Espinosa, C. R. Nicholas, J. Shuga, S. J. Liu, M. C. Oldham, A. Diaz, D. A. Lim, A. A. Leyrat, J. A. West, A. R. Kriegstein, Molecular identity of human outer radial glia during cortical development. Cell 163, 55-67 (2015).
29. S. Koirala, G. Corfas, Identification of novel glial genes by single-cell transcriptional profiling of Bergmann glial cells from mouse cerebellum. PLOS ONE 5, e9198 (2010).
30. F. Mohn, M. Weber, M. Rebhan, T. C. Roloff, J. Richter, M. B. Stadler, M. Bibel, D. Schübeler, Lineage-specific polycomb targets and de novo DNA methylation define restriction and potential of neuronal progenitors. Mol. Cell 30, 755-766 (2008).