Genomic landscape of high-grade meningiomas

被引:144
作者
Bi, Wenya Linda [1 ,2 ,3 ]
Greenwald, Noah F. [1 ,2 ,3 ]
Abedalthagafi, Malak [4 ,5 ,6 ]
Wala, Jeremiah [2 ,3 ]
Gibson, Will J. [2 ,3 ]
Agarwalla, Pankaj K. [2 ,7 ]
Horowitz, Peleg [8 ]
Schumacher, Steven E. [2 ,3 ]
Esaulova, Ekaterina [9 ,10 ]
Mei, Yu [1 ]
Chevalier, Aaron [3 ]
Ducar, Matthew A. [11 ]
Thorner, Aaron R. [11 ]
van Hummelen, Paul [11 ]
Stemmer-Rachamimov, Anat O. [12 ]
Artyomov, Maksym
Al-Mefty, Ossama [1 ]
Dunn, Gavin P. [13 ,14 ]
Santagata, Sandro [4 ]
Dunn, Ian F. [1 ]
Beroukhim, Rameen [2 ,3 ,15 ]
机构
[1] Harvard Med Sch, Brigham & Womens Hosp, Dept Neurosurg, Ctr Skull Base & Pituitary Surg, Boston, MA 02115 USA
[2] Dana Farber Canc Inst, Dept Canc Biol, Boston, MA 02115 USA
[3] Broad Inst MIT & Harvard, Cambridge, MA 02142 USA
[4] Brigham & Womens Hosp, Dept Pathol, Div Neuropathol, 75 Francis St, Boston, MA 02115 USA
[5] King Fahad Med City, Res Ctr, Riyadh, Saudi Arabia
[6] King Abdulaziz City Sci & Technol, Saudi Human Genome Project Lab, Riyadh, Saudi Arabia
[7] Massachusetts Gen Hosp, Dept Neurosurg, Boston, MA 02114 USA
[8] Univ Chicago, Dept Surg, 5841 S Maryland Ave, Chicago, IL 60637 USA
[9] Washington Univ, Sch Med, Dept Pathol & Immunol, St Louis, MO USA
[10] ITMO Univ, Comp Technol Dept, St Petersburg, Russia
[11] Dana Farber Canc Inst, Ctr Canc Genome Discovery, Boston, MA 02115 USA
[12] Massachusetts Gen Hosp, Dept Pathol, Boston, MA 02114 USA
[13] Washington Univ, Sch Med, Dept Neurosurg, St Louis, MO USA
[14] Washington Univ, Sch Med, Ctr Human Immunol & Immunotherapy Programs, St Louis, MO USA
[15] Dana Farber Canc Inst, Dept Med Oncol, Boston, MA 02115 USA
关键词
TERT PROMOTER MUTATIONS; GENETIC-VARIATION; PD-1; BLOCKADE; CANCER; TUMORS; PREDICTION; EVOLUTION; COMMON; AKT1; IMMUNOGENOMICS;
D O I
10.1038/s41525-017-0014-7
中图分类号
Q3 [遗传学];
学科分类号
071007 ; 090102 ;
摘要
High-grade meningiomas frequently recur and are associated with high rates of morbidity and mortality. To determine the factors that promote the development and evolution of these tumors, we analyzed the genomes of 134 high-grade meningiomas and compared this information with data from 595 previously published meningiomas. High-grade meningiomas had a higher mutation burden than low-grade meningiomas but did not harbor any significantly mutated genes aside from NF2. High-grade meningiomas also possessed significantly elevated rates of chromosomal gains and losses, especially among tumors with monosomy 22. Meningiomas previously treated with adjuvant radiation had significantly more copy number alterations than radiation-induced or radiation-naive meningiomas. Across serial recurrences, genomic disruption preceded the emergence of nearly all mutations, remained largely uniform across time, and when present in low-grade meningiomas correlated with subsequent progression to a higher grade. In contrast to the largely stable copy number alterations, mutations were strikingly heterogeneous across tumor recurrences, likely due to extensive geographic heterogeneity in the primary tumor. While high-grade meningiomas harbored significantly fewer overtly targetable alterations than low-grade meningiomas, they contained numerous mutations that are predicted to be neoantigens, suggesting that immunologic targeting may be of therapeutic value.
引用
收藏
页数:14
相关论文
共 66 条
[1]   Oncogenic PI3K mutations are as common as AKT1 and SMO mutations in meningioma [J].
Abedalthagafi, Malak ;
Bi, Wenya Linda ;
Aizer, Ayal A. ;
Merrill, Parker H. ;
Brewster, Ryan ;
Agarwalla, Pankaj K. ;
Listewnik, Marc L. ;
Dias-Santagata, Dora ;
Thorner, Aaron R. ;
Van Hummelen, Paul ;
Brastianos, Priscilla K. ;
Reardon, David A. ;
Wen, Patrick Y. ;
Al-Mefty, Ossama ;
Ramkissoon, Shakti H. ;
Folkerth, Rebecca D. ;
Ligon, Keith L. ;
Ligon, Azra H. ;
Alexander, Brian M. ;
Dunn, Ian F. ;
Beroukhim, Rameen ;
Santagata, Sandro .
NEURO-ONCOLOGY, 2016, 18 (05) :649-655
[2]   ARID1A and TERT promoter mutations in dedifferentiated meningioma [J].
Abedalthagafi, Malak S. ;
Bi, Wenya Linda ;
Merrill, Parker H. ;
Gibson, William J. ;
Rose, Matthew F. ;
Du, Ziming ;
Francis, Joshua M. ;
Du, Rose ;
Dunn, Ian F. ;
Ligon, Azra H. ;
Beroukhim, Rameen ;
Santagata, Sandro .
CANCER GENETICS, 2015, 208 (06) :345-350
[3]   Angiomatous meningiomas have a distinct genetic profile with multiple chromosomal polysomies including polysomy of chromosome 5 [J].
Abedalthagafi, Malak S. ;
Merrill, Parker H. ;
Bi, Wenya Linda ;
Jones, Robert T. ;
Listewnik, Marc L. ;
Ramkissoon, Shakti H. ;
Thorner, Aaron R. ;
Dunn, Ian F. ;
Beroukhim, Rameen ;
Alexander, Brian M. ;
Brastianos, Priscilla K. ;
Francis, Joshua M. ;
Folkerth, Rebecca D. ;
Ligon, Keith L. ;
Van Hummelen, Paul ;
Ligon, Azra H. ;
Santagata, Sandro .
ONCOTARGET, 2014, 5 (21) :10596-10606
[4]   A prognostic cytogenetic scoring system to guide the adjuvant management of patients with atypical meningioma [J].
Aizer, Ayal A. ;
Abedalthagafi, Malak ;
Bi, Wenya Linda ;
Horvath, Margaret C. ;
Arvold, Nils D. ;
Al-Mefty, Ossama ;
Lee, Eudocia Q. ;
Nayak, Lakshmi ;
Rinne, Mikael L. ;
Norden, Andrew D. ;
Reardon, David A. ;
Wen, Patrick Y. ;
Ligon, Keith L. ;
Ligon, Azra H. ;
Beroukhim, Rameen ;
Dunn, Ian F. ;
Santagata, Sandro ;
Alexander, Brian M. .
NEURO-ONCOLOGY, 2016, 18 (02) :269-274
[5]   Signatures of mutational processes in human cancer [J].
Alexandrov, Ludmil B. ;
Nik-Zainal, Serena ;
Wedge, David C. ;
Aparicio, Samuel A. J. R. ;
Behjati, Sam ;
Biankin, Andrew V. ;
Bignell, Graham R. ;
Bolli, Niccolo ;
Borg, Ake ;
Borresen-Dale, Anne-Lise ;
Boyault, Sandrine ;
Burkhardt, Birgit ;
Butler, Adam P. ;
Caldas, Carlos ;
Davies, Helen R. ;
Desmedt, Christine ;
Eils, Roland ;
Eyfjord, Jorunn Erla ;
Foekens, John A. ;
Greaves, Mel ;
Hosoda, Fumie ;
Hutter, Barbara ;
Ilicic, Tomislav ;
Imbeaud, Sandrine ;
Imielinsk, Marcin ;
Jaeger, Natalie ;
Jones, David T. W. ;
Jones, David ;
Knappskog, Stian ;
Kool, Marcel ;
Lakhani, Sunil R. ;
Lopez-Otin, Carlos ;
Martin, Sancha ;
Munshi, Nikhil C. ;
Nakamura, Hiromi ;
Northcott, Paul A. ;
Pajic, Marina ;
Papaemmanuil, Elli ;
Paradiso, Angelo ;
Pearson, John V. ;
Puente, Xose S. ;
Raine, Keiran ;
Ramakrishna, Manasa ;
Richardson, Andrea L. ;
Richter, Julia ;
Rosenstiel, Philip ;
Schlesner, Matthias ;
Schumacher, Ton N. ;
Span, Paul N. ;
Teague, Jon W. .
NATURE, 2013, 500 (7463) :415-+
[6]   Integrating common and rare genetic variation in diverse human populations [J].
Altshuler, David M. ;
Gibbs, Richard A. ;
Peltonen, Leena ;
Dermitzakis, Emmanouil ;
Schaffner, Stephen F. ;
Yu, Fuli ;
Bonnen, Penelope E. ;
de Bakker, Paul I. W. ;
Deloukas, Panos ;
Gabriel, Stacey B. ;
Gwilliam, Rhian ;
Hunt, Sarah ;
Inouye, Michael ;
Jia, Xiaoming ;
Palotie, Aarno ;
Parkin, Melissa ;
Whittaker, Pamela ;
Chang, Kyle ;
Hawes, Alicia ;
Lewis, Lora R. ;
Ren, Yanru ;
Wheeler, David ;
Muzny, Donna Marie ;
Barnes, Chris ;
Darvishi, Katayoon ;
Hurles, Matthew ;
Korn, Joshua M. ;
Kristiansson, Kati ;
Lee, Charles ;
McCarroll, Steven A. ;
Nemesh, James ;
Keinan, Alon ;
Montgomery, Stephen B. ;
Pollack, Samuela ;
Price, Alkes L. ;
Soranzo, Nicole ;
Gonzaga-Jauregui, Claudia ;
Anttila, Verneri ;
Brodeur, Wendy ;
Daly, Mark J. ;
Leslie, Stephen ;
McVean, Gil ;
Moutsianas, Loukas ;
Nguyen, Huy ;
Zhang, Qingrun ;
Ghori, Mohammed J. R. ;
McGinnis, Ralph ;
McLaren, William ;
Takeuchi, Fumihiko ;
Grossman, Sharon R. .
NATURE, 2010, 467 (7311) :52-58
[7]   Punctuated Evolution of Prostate Cancer Genomes [J].
Baca, Sylvan C. ;
Prandi, Davide ;
Lawrence, Michael S. ;
Mosquera, Juan Miguel ;
Romanel, Alessandro ;
Drier, Yotam ;
Park, Kyung ;
Kitabayashi, Naoki ;
MacDonald, Theresa Y. ;
Ghandi, Mahmoud ;
Van Allen, Eliezer ;
Kryukov, Gregory V. ;
Sboner, Andrea ;
Theurillat, Jean-Philippe ;
Soong, T. David ;
Nickerson, Elizabeth ;
Auclair, Daniel ;
Tewari, Ashutosh ;
Beltran, Himisha ;
Onofrio, Robert C. ;
Boysen, Gunther ;
Guiducci, Candace ;
Barbieri, Christopher E. ;
Cibulskis, Kristian ;
Sivachenko, Andrey ;
Carter, Scott L. ;
Saksena, Gordon ;
Voet, Douglas ;
Ramos, Alex H. ;
Winckler, Wendy ;
Cipicchio, Michelle ;
Ardlie, Kristin ;
Kantoff, Philip W. ;
Berger, Michael F. ;
Gabriel, Stacey B. ;
Golub, Todd R. ;
Meyerson, Matthew ;
Lander, Eric S. ;
Elemento, Olivier ;
Getz, Gad ;
Demichelis, Francesca ;
Rubin, Mark A. ;
Garraway, Levi A. .
CELL, 2013, 153 (03) :666-677
[8]   Integrated genomic characterization of IDH1-mutant glioma malignant progression [J].
Bai, Hanwen ;
Harmanci, Akdes Serin ;
Erson-Omay, E. Zeynep ;
Li, Jie ;
Coskun, Sueleyman ;
Simon, Matthias ;
Krischek, Boris ;
Ozduman, Koray ;
Omay, S. Buelent ;
Sorensen, Eric A. ;
Turcan, Sevin ;
Bakirciglu, Mehmet ;
Carrion-Grant, Geneive ;
Murray, Phillip B. ;
Clark, Victoria E. ;
Ercan-Sencicek, A. Gulhan ;
Knight, James ;
Sencar, Leman ;
Altinok, Selin ;
Kaulen, Leon D. ;
Guelez, Burcu ;
Timmer, Marco ;
Schramm, Johannes ;
Mishra-Gorur, Ketu ;
Henegariu, Octavian ;
Moliterno, Jennifer ;
Louvi, Angeliki ;
Chan, Timothy A. ;
Tannheimer, Stacey L. ;
Pamir, M. Necmettin ;
Vortmeyer, Alexander O. ;
Bilguvar, Kaya ;
Yasuno, Katsuhito ;
Guenel, Murat .
NATURE GENETICS, 2016, 48 (01) :59-+
[9]   A comprehensive microRNA expression profile of the backfat tissue from castrated and intact full-sib pair male pigs [J].
Bai, Ying ;
Huang, Jin-Ming ;
Liu, Gang ;
Zhang, Ji-Bin ;
Wang, Jian-Ying ;
Liu, Cheng-Kun ;
Fang, Mei-Ying .
BMC GENOMICS, 2014, 15
[10]   The landscape of somatic copy-number alteration across human cancers [J].
Beroukhim, Rameen ;
Mermel, Craig H. ;
Porter, Dale ;
Wei, Guo ;
Raychaudhuri, Soumya ;
Donovan, Jerry ;
Barretina, Jordi ;
Boehm, Jesse S. ;
Dobson, Jennifer ;
Urashima, Mitsuyoshi ;
Mc Henry, Kevin T. ;
Pinchback, Reid M. ;
Ligon, Azra H. ;
Cho, Yoon-Jae ;
Haery, Leila ;
Greulich, Heidi ;
Reich, Michael ;
Winckler, Wendy ;
Lawrence, Michael S. ;
Weir, Barbara A. ;
Tanaka, Kumiko E. ;
Chiang, Derek Y. ;
Bass, Adam J. ;
Loo, Alice ;
Hoffman, Carter ;
Prensner, John ;
Liefeld, Ted ;
Gao, Qing ;
Yecies, Derek ;
Signoretti, Sabina ;
Maher, Elizabeth ;
Kaye, Frederic J. ;
Sasaki, Hidefumi ;
Tepper, Joel E. ;
Fletcher, Jonathan A. ;
Tabernero, Josep ;
Baselga, Jose ;
Tsao, Ming-Sound ;
Demichelis, Francesca ;
Rubin, Mark A. ;
Janne, Pasi A. ;
Daly, Mark J. ;
Nucera, Carmelo ;
Levine, Ross L. ;
Ebert, Benjamin L. ;
Gabriel, Stacey ;
Rustgi, Anil K. ;
Antonescu, Cristina R. ;
Ladanyi, Marc ;
Letai, Anthony .
NATURE, 2010, 463 (7283) :899-905