Comprehensive, Integrative Genomic Analysis of Diffuse Lower-Grade Gliomas
Open accessAbstract
BACKGROUND: Diffuse low-grade and intermediate-grade gliomas (which together make up the lower-grade gliomas, World Health Organization grades II and III) have highly variable clinical behavior that is not adequately predicted on the basis of histologic class. Some are indolent; others quickly progress to glioblastoma. The uncertainty is compounded by interobserver variability in histologic diagnosis. Mutations in IDH, TP53, and ATRX and codeletion of chromosome arms 1p and 19q (1p/19q codeletion) have been implicated as clinically relevant markers of lower-grade gliomas. METHODS: We performed genomewide analyses of 293 lower-grade gliomas from adults, incorporating exome sequence, DNA copy number, DNA methylation, messenger RNA expression, microRNA expression, and targeted protein expression. These data were integrated and tested for correlation with clinical outcomes. RESULTS: Unsupervised clustering of mutations and data from RNA, DNA-copy-number, and DNA-methylation platforms uncovered concordant classification of three robust, nonoverlapping, prognostically significant subtypes of lower-grade glioma that were captured more accurately by IDH, 1p/19q, and TP53 status than by histologic class. Patients who had lower-grade gliomas with an IDH mutation and 1p/19q codeletion had the most favorable clinical outcomes. Their gliomas harbored mutations in CIC, FUBP1, NOTCH1, and the TERT promoter. Nearly all lower-grade gliomas with IDH mutations and no 1p/19q codeletion had mutations in TP53 (94%) and ATRX inactivation (86%). The large majority of lower-grade gliomas without an IDH mutation had genomic aberrations and clinical behavior strikingly similar to those found in primary glioblastoma. CONCLUSIONS: The integration of genomewide data from multiple platforms delineated three molecular classes of lower-grade gliomas that were more concordant with IDH, 1p/19q, and TP53 status than with histologic class. Lower-grade gliomas with an IDH mutation either had 1p/19q codeletion or carried a TP53 mutation. Most lower-grade gliomas without an IDH mutation were molecularly and clinically similar to glioblastoma. (Funded by the National Institutes of Health.).
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IDH mutations that increase enzyme activity are early events that define major clinical and prognostic groups of gliomas.
“Gain-of-function IDH mutations are initiating events that define major clinical and prognostic classes of gliomas1,2.”
From Insulator dysfunction and oncogene activation in IDH mutant gliomas (2016) · cites this paper as [2]
The Results (Mutational Landscape of Lower-Grade Gliomas; page not provided) suggest that IDH mutation is an initial event in molecular progression. The Results (Clinical Characteristics and Outcomes; page not provided) and Discussion show that IDH status, together with 1p/19q status, distinguishes groups with different clinical outcomes. Our copy does not characterize the IDH mutations as gain-of-function or establish increased enzyme activity, and it presents the proposed sequence as a suggestion rather than a proven initiating event. (LLM, conf=0.86)
Experimental — accuracy not yet measuredTERT, FUBP1, and CIC mutations are common alterations in oligodendroglioma but not clinically relevant.
“Our patient’s tumor harbored mutations in TERT, FUBP1, and CIC, which are common alterations in oligodendroglioma, but not clinically relevant [46,47].”
From BPC 157 Therapy of Myotendinous Junction Injury in Rats (2025) · cites this paper as [47]
The Results section (page not provided) reports CIC mutations in 62%, FUBP1 mutations in 29%, and TERT promoter mutations in 96% of lower-grade gliomas with an IDH mutation and 1p/19q codeletion, supporting their frequency in this oligodendroglioma-associated subtype. It does not say these mutations are not clinically relevant; it describes the subtype as prognostically significant without establishing the clinical relevance of each mutation individually. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIDH WT astrocytomas are, for the most part, highly aggressive, having a median survival of 18 mo.
“IDH WT astrocytomas are, for the most part, highly aggressive, having a median survival of 18 mo”
From Predicting cancer outcomes from histology and genomics using convolutional networks (2018) · cites this paper as [37]
Predicted risks are consistent with the published expected overall survivals associated with molecular subtypes.
“Second, predicted risks are consistent with the published expected overall survivals associated with molecular subtypes (37).”
From Predicting cancer outcomes from histology and genomics using convolutional networks (2018) · cites this paper as [37]
Oligodendrogliomas have the lowest overall predicted risks, consistent with overall survivals of 10+ y.
“and these have the lowest overall predicted risks consistent with overall survivals of 10+ y (37, 39).”
From Predicting cancer outcomes from histology and genomics using convolutional networks (2018) · cites this paper as [37]
IDH mutant astrocytomas are another subtype with considerably better overall survival ranging from 3 to 8 y.
“IDH mutant astrocytomas are another subtype with considerably better overall survival ranging from 3 to 8 y”
From Predicting cancer outcomes from histology and genomics using convolutional networks (2018) · cites this paper as [37]
Mutations in IDH1/2 are the most frequently mutated metabolic genes in human cancer.
“In recent years, two landmark genomic studies carried out in human glioma and acute myeloid leukaemia (AML) found mutations in IDH1/2 and it is now appreciated that these enzymes (which drive elevated production of D-2-HG) are the most frequently mutated metabolic genes in human cancer112-114.”
From Coupling Krebs cycle metabolites to signalling in immunity and cancer (2018) · cites this paper as [114]
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Molecular imaging in oncology: Current impact and future directions
Rowe, S. P., & Pomper, M. G. (2021) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.21713 · Cited by 342 · see citing works
Buda, M., Saha, A., & Mazurowski, M. A. (2019) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2019.05.002 · Cited by 339 · see citing works
Wijnenga, M. M. J., French, P. J., Dubbink, H. J., Dinjens, W. N. M., Atmodimedjo, P. N., Kros, J. M., Smits, M., Gahrmann, R., Rutten, G.-J. M., Verheul, J. B., et al. (2017) · Neuro-Oncology · doi:10.1093/neuonc/nox176 · Cited by 337 · see citing works
- Authors
- The Cancer Genome Atlas Research Network
- Affiliations
- Emory University (US)
- Corresponding author
- The Cancer Genome Atlas Research Network
- Venue
- New England Journal of Medicine
- Publisher
- Massachusetts Medical Society
- Published
- 2015-06-25
- Volume
- 372
- Issue
- 26
- Pages
- 2481-2498
- ISSN
- 0028-4793 (ISSN-L)
- 1533-4406
- PMC
- PMC4530011
- OpenAlex
- W1812256879
- Cited by
- 3,148
- References
- 54
- Citations by year
- 2026: 139 · 2025: 196 · 2024: 248 · 2023: 282 · 2022: 371 · 2021: 341 · 2020: 366 · 2019: 314 · 2018: 311 · 2017: 284 · 2016: 226 · 2015: 60 · 2014: 3 · 2013: 1
- FWCI
- 164.44
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- New England Journal of Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, other-oa)
- IRIS (submittedVersion)
- SERVAL (Université de Lausanne) (submittedVersion)
- Funders
- National Institutes of Health
- National Human Genome Research Institute (U54HG003067, U54HG003079, U54HG003273, U54HG007990)
- National Cancer Institute (U24CA194362, U24CA126554, U24CA143882, U24CA143843, U24CA143840, U24CA126546, U24CA143858, U24CA126543, U24CA144025, U24CA126563, U01CA168394, U24CA143866, U24CA143883, U24CA143845, U24CA126544, R01CA163722, U24CA180951, U24CA143867, U24CA143848, U24CA143799, U24CA126551, U24CA143835, U24CA126561, P30CA008748, P30CA016672, U24CA143731)
- National Institute of Neurological Disorders and Stroke (R01NS081125)
- Topics
- Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
- Keywords
- glioma molecular subtypes, IDH mutation, 1p/19q codeletion, TP53 mutation, TERT promoter mutation, NOTCH1 mutation, CIC mutation, glioblastoma, prognostic factors, DNA methylation, DNA copy number, gene expression, microRNA expression
- MeSH terms
- Adolescent, Adult, Aged, Chromosomes, Human, Pair 1, Chromosomes, Human, Pair 19, DNA, Neoplasm, Female, Glioblastoma, Glioma, Humans, Male, Middle Aged, Mutation, Signal Transduction, Cluster Analysis, Proportional Hazards Models, Genes, p53, Sequence Analysis, DNA, Kaplan-Meier Estimate, Neoplasm Grading
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