A Distinct DNA Methylation Shift in a Subset of Glioma CpG Island Methylator Phenotypes during Tumor Recurrence

被引:130
作者
de Souza, Camila Ferreira [1 ,2 ]
Sabedot, Thais S. [1 ,2 ]
Malta, Tathiane M. [1 ,2 ]
Stetson, Lindsay [3 ]
Morozova, Olena [4 ,5 ]
Sokolov, Artem [6 ]
Laird, Peter W. [7 ]
Wiznerowicz, Maciej [8 ,9 ,10 ]
Iavarone, Antonio [11 ,12 ]
Snyder, James [1 ]
deCarvalho, Ana [1 ]
Sanborn, Zachary [13 ]
McDonald, Kerrie L. [14 ]
Friedman, William A. [15 ]
Tirapelli, Daniela [16 ]
Poisson, Laila [1 ,17 ]
Mikkelsen, Tom [1 ]
Carlotti, Carlos G., Jr. [16 ]
Kalkanis, Steven [1 ]
Zenklusen, Jean [18 ]
Salama, Sofie R. [4 ,5 ]
Barnholtz-Sloan, Jill S. [3 ]
Noushmehr, Houtan [1 ,2 ]
机构
[1] Henry Ford Hlth Syst, Dept Neurosurg, Detroit, MI 48202 USA
[2] Univ Sao Paulo, Ribeirao Preto Med Sch, Dept Genet, Ribeirao Preto, SP, Brazil
[3] Case Western Reserve Univ, Sch Med, Case Comprehens Canc Ctr, Cleveland, OH 44106 USA
[4] Univ Calif Santa Cruz, UC Santa Cruz Genom Inst, Santa Cruz, CA 95064 USA
[5] Univ Calif Santa Cruz, Howard Hughes Med Inst, Santa Cruz, CA 95064 USA
[6] Harvard Med Sch, Lab Syst Pharmacol, Boston, MA 02115 USA
[7] Van Andel Res Inst, Ctr Epigenet, Grand Rapids, MI 49503 USA
[8] Greater Poland Canc Ctr, Dept Diagnost & Canc Immunol, Lab Gene Therapy, Poznan, Poland
[9] Poznan Univ Med Sci, Dept Canc Immunol, Poznan, Poland
[10] Int Inst Mol Oncol, Poznan, Poland
[11] Columbia Univ, Dept Pathol & Cell Biol, New York, NY 10032 USA
[12] Columbia Univ, Neurol Inst Canc Genet, New York, NY 10032 USA
[13] NantOmics LLC, Santa Cruz, CA USA
[14] UNSW, Prince Wales Clin Sch, Cure Brain Canc Biomarkers & Translat Res Lab, Sydney, NSW, Australia
[15] Univ Florida, Dept Neurosurg, Gainesville, FL USA
[16] Univ Sao Paulo, Ribeirao Preto Med Sch, Dept Surg & Anat, Ribeirao Preto, Brazil
[17] Henry Ford Hlth Syst, Dept Publ Hlth Sci, Detroit, MI 48202 USA
[18] NCI, Bethesda, MD 20892 USA
基金
巴西圣保罗研究基金会;
关键词
INTEGRATED GENOMIC ANALYSIS; CENTRAL-NERVOUS-SYSTEM; STEM-CELLS; ADJUVANT TEMOZOLOMIDE; GLIOBLASTOMA; BRAIN; IDH1; REVEALS; MUTATIONS; RADIOTHERAPY;
D O I
10.1016/j.celrep.2018.03.107
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Glioma diagnosis is based on histomorphology and grading; however, such classification does not have predictive clinical outcome after glioblastomas have developed. To date, no bona fide biomarkers that significantly translate into a survival benefit to glioblastoma patients have been identified. We previously reported that the IDH mutant G-CIMP-high subtype would be a predecessor to the G-CIMP-low subtype. Here, we performed a comprehensive DNA methylation longitudinal analysis of diffuse gliomas from 77 patients (200 tumors) to enlighten the epigenome-based malignant transformation of initially lower-grade gliomas. Intra-subtype heterogeneity among G-CIMP-high primary tumors allowed us to identify predictive biomarkers for assessing the risk of malignant recurrence at early stages of disease. G-CIMP-low recurrence appeared in 9.5% of all gliomas, and these resembled IDH-wild-type primary glioblastoma. G-CIMP-low recurrence can be characterized by distinct epigenetic changes at candidate functional tissue enhancers with AP-1/SOX binding elements, mesenchymal stem cell-like epigenomic phenotype, and genomic instability. Molecular abnormalities of longitudinal G-CIMP offer possibilities to defy glioblastoma progression.
引用
收藏
页码:637 / 651
页数:15
相关论文
共 48 条
[1]   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-+
[2]   Detailed longitudinal sampling of glioma stem cells in situ reveals Chr7 gain and Chr10 loss as repeated events in primary tumor formation and recurrence [J].
Baysan, Mehmet ;
Woolard, Kevin ;
Cam, Margaret C. ;
Zhang, Wei ;
Song, Hua ;
Kotliarova, Svetlana ;
Balamatsias, Demosthenes ;
Linkous, Amanda ;
Ahn, Susie ;
Walling, Jennifer ;
Belova, Galina I. ;
Fine, Howard A. .
INTERNATIONAL JOURNAL OF CANCER, 2017, 141 (10) :2002-2013
[3]   CONTROLLING THE FALSE DISCOVERY RATE - A PRACTICAL AND POWERFUL APPROACH TO MULTIPLE TESTING [J].
BENJAMINI, Y ;
HOCHBERG, Y .
JOURNAL OF THE ROYAL STATISTICAL SOCIETY SERIES B-STATISTICAL METHODOLOGY, 1995, 57 (01) :289-300
[4]   Mesenchymal Differentiation Mediated by NF-κB Promotes Radiation Resistance in Glioblastoma [J].
Bhat, Krishna P. L. ;
Balasubramaniyan, Veerakumar ;
Vaillant, Brian ;
Ezhilarasan, Ravesanker ;
Hummelink, Karlijn ;
Hollingsworth, Faith ;
Wani, Khalida ;
Heathcock, Lindsey ;
James, Johanna D. ;
Goodman, Lindsey D. ;
Conroy, Siobhan ;
Long, Lihong ;
Lelic, Nina ;
Wang, Suzhen ;
Gumin, Joy ;
Raj, Divya ;
Kodama, Yoshinori ;
Raghunathan, Aditya ;
Olar, Adriana ;
Joshi, Kaushal ;
Pelloski, Christopher E. ;
Heimberger, Amy ;
Kim, Se Hoon ;
Cahill, Daniel P. ;
Rao, Ganesh ;
Den Dunnen, Wilfred F. A. ;
Boddeke, Hendrikus W. G. M. ;
Phillips, Heidi S. ;
Nakano, Ichiro ;
Lang, Frederick F. ;
Colman, Howard ;
Sulman, Erik P. ;
Aldape, Kenneth .
CANCER CELL, 2013, 24 (03) :331-346
[5]   Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas [J].
Brat, Daniel J. ;
Verhaak, Roel G. W. ;
Al-dape, Kenneth D. ;
Yung, W. K. Alfred ;
Salama, Sofie R. ;
Cooper, Lee A. D. ;
Rheinbay, Esther ;
Miller, C. Ryan ;
Vitucci, Mark ;
Morozova, Olena ;
Robertson, A. Gordon ;
Noushmehr, Houtan ;
Laird, Peter W. ;
Cherniack, Andrew D. ;
Akbani, Rehan ;
Huse, Jason T. ;
Ciriello, Giovanni ;
Poisson, Laila M. ;
Barnholtz-Sloan, Jill S. ;
Berger, Mitchel S. ;
Brennan, Cameron ;
Colen, Rivka R. ;
Colman, Howard ;
Flanders, Adam E. ;
Giannini, Caterina ;
Grifford, Mia ;
Iavarone, Antonio ;
Jain, Rajan ;
Joseph, Isaac ;
Kim, Jaegil ;
Kasaian, Katayoon ;
Mikkelsen, Tom ;
Murray, Bradley A. ;
O'Neill, Brian Patrick ;
Pachter, Lior ;
Parsons, Donald W. ;
Sougnez, Carrie ;
Sulman, Erik P. ;
Vandenberg, Scott R. ;
Van Meir, Erwin G. ;
von Deimling, Andreas ;
Zhang, Hailei ;
Crain, Daniel ;
Lau, Kevin ;
Mallery, David ;
Morris, Scott ;
Paulauskis, Joseph ;
Penny, Robert ;
Shelton, Troy ;
Sherman, Mark .
NEW ENGLAND JOURNAL OF MEDICINE, 2015, 372 (26) :2481-2498
[6]   The Somatic Genomic Landscape of Glioblastoma [J].
Brennan, Cameron W. ;
Verhaak, Roel G. W. ;
McKenna, Aaron ;
Campos, Benito ;
Noushmehr, Houtan ;
Salama, Sofie R. ;
Zheng, Siyuan ;
Chakravarty, Debyani ;
Sanborn, J. Zachary ;
Berman, Samuel H. ;
Beroukhim, Rameen ;
Bernard, Brady ;
Wu, Chang-Jiun ;
Genovese, Giannicola ;
Shmulevich, Ilya ;
Barnholtz-Sloan, Jill ;
Zou, Lihua ;
Vegesna, Rahulsimham ;
Shukla, Sachet A. ;
Ciriello, Giovanni ;
Yung, W. K. ;
Zhang, Wei ;
Sougnez, Carrie ;
Mikkelsen, Tom ;
Aldape, Kenneth ;
Bigner, Darell D. ;
Van Meir, Erwin G. ;
Prados, Michael ;
Sloan, Andrew ;
Black, Keith L. ;
Eschbacher, Jennifer ;
Finocchiaro, Gaetano ;
Friedman, William ;
Andrews, David W. ;
Guha, Abhijit ;
Iacocca, Mary ;
O'Neill, Brian P. ;
Foltz, Greg ;
Myers, Jerome ;
Weisenberger, Daniel J. ;
Penny, Robert ;
Kucherlapati, Raju ;
Perou, Charles M. ;
Hayes, D. Neil ;
Gibbs, Richard ;
Marra, Marco ;
Mills, Gordon B. ;
Lander, Eric ;
Spellman, Paul ;
Wilson, Richard .
CELL, 2013, 155 (02) :462-477
[7]   The transcriptional network for mesenchymal transformation of brain tumours [J].
Carro, Maria Stella ;
Lim, Wei Keat ;
Alvarez, Mariano Javier ;
Bollo, Robert J. ;
Zhao, Xudong ;
Snyder, Evan Y. ;
Sulman, Erik P. ;
Anne, Sandrine L. ;
Doetsch, Fiona ;
Colman, Howard ;
Lasorella, Anna ;
Aldape, Ken ;
Califano, Andrea ;
Iavarone, Antonio .
NATURE, 2010, 463 (7279) :318-U68
[8]   Molecular Profiling Reveals Biologically Discrete Subsets and Pathways of Progression in Diffuse Glioma [J].
Ceccarelli, Michele ;
Barthel, Floris P. ;
Malta, Tathiane M. ;
Sabedot, Thais S. ;
Salama, Sofie R. ;
Murray, Bradley A. ;
Morozova, Olena ;
Newton, Yulia ;
Radenbaugh, Amie ;
Pagnotta, Stefano M. ;
Anjum, Samreen ;
Wang, Jiguang ;
Manyam, Ganiraju ;
Zoppoli, Pietro ;
Ling, Shiyun ;
Rao, Arjun A. ;
Grifford, Mia ;
Cherniack, Andrew D. ;
Zhang, Hailei ;
Poisson, Laila ;
Carlotti, Carlos Gilberto, Jr. ;
Tirapelli, Daniela Pretti da Cunha ;
Rao, Arvind ;
Mikkelsen, Tom ;
Lau, Ching C. ;
Yung, W. K. Alfred ;
Rabadan, Raul ;
Huse, Jason ;
Brat, Daniel J. ;
Lehman, Norman L. ;
Barnholtz-Sloan, Jill S. ;
Zheng, Siyuan ;
Hess, Kenneth ;
Rao, Ganesh ;
Meyerson, Matthew ;
Beroukhim, Rameen ;
Cooper, Lee ;
Akbani, Rehan ;
Wrensch, Margaret ;
Haussler, David ;
Aldape, Kenneth D. ;
Laird, Peter W. ;
Gutmann, David H. ;
Noushmehr, Houtan ;
Iavarone, Antonio ;
Verhaak, Roel G. W. .
CELL, 2016, 164 (03) :550-563
[9]   Mitf is the key molecular switch between mouse or human melanoma initiating cells and their differentiated progeny [J].
Cheli, Y. ;
Guiliano, S. ;
Botton, T. ;
Rocchi, S. ;
Hofman, V. ;
Hofman, P. ;
Bahadoran, P. ;
Bertolotto, C. ;
Ballotti, R. .
ONCOGENE, 2011, 30 (20) :2307-2318
[10]   TCGAbiolinks: an R/Bioconductor package for integrative analysis of TCGA data [J].
Colaprico, Antonio ;
Silva, Tiago C. ;
Olsen, Catharina ;
Garofano, Luciano ;
Cava, Claudia ;
Garolini, Davide ;
Sabedot, Thais S. ;
Malta, Tathiane M. ;
Pagnotta, Stefano M. ;
Castiglioni, Isabella ;
Ceccarelli, Michele ;
Bontempi, Gianluca ;
Noushmehr, Houtan .
NUCLEIC ACIDS RESEARCH, 2016, 44 (08) :e71