Cited by 5,784Endometrial and Cervical Cancer TreatmentsCancer Genomics and DiagnosticsChromatin Remodeling and Cancer

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Integrated genomic characterization of endometrial carcinoma

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The Cancer Genome Atlas Research Network, Levine, Douglas A.·2013·Nature

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SummaryWe performed an integrated genomic, transcriptomic, and proteomic characterization of 373 endometrial carcinomas using array- and sequencing-based technologies. Uterine serous tumors and ~25% of high-grade endometrioid tumors have extensive copy number alterations, few DNA methylation changes, low ER/PR levels, and frequent TP53 mutations. Most endometrioid tumors have few copy number alterations or TP53 mutations but frequent mutations in PTEN, CTNNB1, PIK3CA, ARID1A, KRAS and novel mutations in the SWI/SNF gene ARID5B. A subset of endometrioid tumors we identified had a dramatically increased transversion mutation frequency, and newly identified hotspot mutations in POLE. Our results classified endometrial cancers into four categories: POLE ultramutated, microsatellite instability hypermutated, copy number low, and copy number high. Uterine serous carcinomas share genomic features with ovarian serous and basal-like breast carcinomas. We demonstrated that the genomic features of endometrial carcinomas permit a reclassification that may impact post-surgical adjuvant treatment for women with aggressive tumors.

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Figure 1 SCNAs in endometrial carcinomas. a, Tumours were hierarchically clustered into four groups based on SCNAs. The heat map shows SCNAs in each tumour (horizontal axis) plotted by chromosomal location (vertical axis). Chr., chromosome. b, Kaplan–Meier curves of progression-free survival for each copy-number cluster. PowerPoint slideCC BY-NC-SA · PubMed Central

Figure 2 Mutation spectra across endometrial carcinomas. a, Mutation frequencies (vertical axis, top panel) plotted for each tumour (horizontal axis). Nucleotide substitutions are shown in the middle panel, with a high frequency of C-to-A transversions in the samples with POLE exonuclease mutations. CN, copy number. b, Tumours were stratified into the four groups by (1) nucleotide substitution frequencies and patterns, (2) MSI status, and (3) copy-number cluster. SNV, single nucleotide variant. c, POLE-mutant tumours have significantly better progression-free survival, whereas copy-number high tumours have the poorest outcome. d, Recurrently mutated genes are different between the four subgroups. Shown are the mutation frequencies of all genes that were significantly mutated in at least one of the four subgroups (MUSiC, asterisk denotes FDR < 0.05). PowerPoint slideCC BY-NC-SA · PubMed Central

Figure 3 Gene expression across integrated subtypes in endometrial carcinomas. a, Supervised analysis of ∼1,500 genes significantly associated with integrated subtypes. b, Heat map of protein expression clusters, supervised by integrated subtypes. Samples are in columns; genes or proteins are in rows. PowerPoint slideCC BY-NC-SA · PubMed Central

Figure 4 Pathway alterations in endometrial carcinomas. a, The RTK/RAS/β-catenin pathway is altered through several mechanisms that exhibit mutually exclusive patterns. Alteration frequencies are expressed as a percentage of all cases. The right panel shows patterns of occurrence. b, The PI(3)K pathway has mutually exclusive PIK3CA and PIK3R1 alterations that frequently co-occur with PTEN alterations in the MSI and copy-number low subgroups. c, Heat map display of top 1,000 varying pathway features within PARADIGM consensus clusters. Samples were arranged in order of their consensus cluster membership. The genomic subtype for each sample is displayed below the consensus clusters. PowerPoint slideCC BY-NC-SA · PubMed Central

Figure 5 Genomic relationships between endometrial serous-like, ovarian serous, and basal-like breast carcinomas. a, SCNAs for each tumour type. b, Frequency of genomic alterations present in at least 10% of one tumour type. PowerPoint slideCC BY-NC-SA · PubMed Central

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“For example, the most common PTEN (phosphate and tension homology deleted on chromosome ten) and PIK3CA (p110α catalytic subunit of PI3 kinase) gene mutations are found in all the above four types of endometrial cancer [8].”
Background
Specific Biomarker Expression Patterns in the Diagnosis of Residual and Recurrent Endometrial Precancers After Progestin Treatment
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“8) 33 (24-40) 30 (20-72) Yes 8 0 Complete response 26 (48.”
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“Since PTEN, CTNNB1, PIK3CA, ARID1A, and KRAS play important roles in the pathogenesis of UCEC [20], we further evaluated whether the variation (SNV or CNV) of m6A regulatory genes was associated with changes in the above five genes.”
Background
Targeted Molecular Testing in Endometrial Carcinoma: Validation of a Clinically Driven Selective ProMisE Testing Protocol
Talhouk, A., Jamieson, A., Crosbie, E. J., et al. (2022) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000000898 · Cited by 31
“6) POLEmut 45 (57) 14 (35) 45 (5) 14 (3.”
BackgroundInfluential
HER-2 Amplification in Uterine Serous Carcinoma and Serous Endometrial Intraepithelial Carcinoma
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“Breast score 0/1+ 29 (83) 27 (90) 0 2 (50)* 2+ 6 (17) 3 (10) 1 (100) 2 (50) 3+ 0 0 0 0 Total # of cases 35 30 1 4 GI score”
HER2 Overexpression and Amplification in Uterine Carcinosarcomas With Serous Morphology
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Corded and Hyalinized and Spindled Endometrioid Endometrial Carcinoma
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A Multiplex SNaPshot Assay is a Rapid and Cost-Effective Method for Detecting POLE Exonuclease Domain Mutations in Endometrial Carcinoma
Devereaux, K. A., Steiner, D. F., Ho, C. C., Gomez, A. J., Gilks, C. B., Longacre, T. A., Zehnder, J. L., Howitt, B. E., & Suarez, C. J. (2021) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000000841 · Cited by 29
“In other words, the assay covers the most common mutation positions, accounting for approximately 90-95% of all clinically relevant POLE EDMs variants reported in ECs (1,2,17,35,39,40).”
BackgroundMethodInfluential
Nivolumab for mismatch-repair-deficient or hypermutated gynecologic cancers: a phase 2 trial with biomarker analyses
Friedman, C. F., Manning‐Geist, B. L., Zhou, Q. C., Soumerai, T. E., Holland, A., Paula, A. D. C., Green, H., Ozsoy, M. A., Iasonos, A. E., Hollmann, T. J., et al. (2024) · Nature Medicine · doi:10.1038/s41591-024-02942-7 · Cited by 30
“This patient had progression of disease at her first follow-up copy number-low and copy number-high 5 .”
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BRG1, INI1, and ARID1B Deficiency in Endometrial Carcinoma
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NEK10 tyrosine phosphorylates p53 and controls its transcriptional activity
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Prognostic implications of tumor-infiltrating T cells in early-stage endometrial cancer
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The oncogenic landscape of the idiopathic pulmonary fibrosis: a narrative review
Stella, G. M., D’Agnano, V., Piloni, D., Saracino, L., Lettieri, S., Mariani, F., Lancia, A., Bortolotto, C., Rinaldi, P., Falanga, F., et al. (2022) · Translational Lung Cancer Research · doi:10.21037/tlcr-21-880 · Cited by 25
“Interestingly, it is also associated to the enhancement of kirsten rat sarcoma (KRAS)-driven adenocarcinogenesis (82-84).”
Background
Data Set for the Reporting of Ovarian, Fallopian Tube and Primary Peritoneal Carcinoma: Recommendations From the International Collaboration on Cancer Reporting (ICCR)
Gilks, C. B., Selinger, C. I., Davidson, B., et al. (2022) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000000908 · Cited by 27
Endometrial Carcinomas With Subclonal Loss of Mismatch Repair Proteins
Mendoza, R. P., Wang, P., Schulte, J. J., Tjota, M. Y., Jani, I., Martinez, A. C., Haridas, R., Wanjari, P., Steinhardt, G., Brown, N. A., et al. (2023) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000002031 · Cited by 30
Early‐stage endometrial cancer, CTNNB1 mutations, and the relation between lymphovascular space invasion and recurrence
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“epithelial cells DNA quality was assessed with the qBiomarker Human DNA qual‐ ity control plate (Qiagen) with wild‐type sequences of 7 genes (protooncogene B‐raf [BRAF], k‐ras [KRAS], v‐Ha‐Ras Harvey rat sarcoma viral oncogene [HRAS], neuroblastoma‐Ras [NRAS], mi‐ togen‐activated protein kinase kinase 1 [MEK1], phosph…”
BackgroundInfluential
Fibroblast growth factor receptor signaling as therapeutic targets in female reproductive system cancers
Zhu, D., Tuo, X.-M., Rong, Y., et al. (2020) · Journal of Cancer · doi:10.7150/jca.44727 · Cited by 26
“FGFR1 and FGFR3 amplifications are also found in endometrial cancer through integrating genomic characterization of somatic copy number alterations [58].”
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Data Set for the Reporting of Endometrial Cancer: Recommendations From the International Collaboration on Cancer Reporting (ICCR)
Matías‐Guiu, X., Selinger, C. I., Anderson, L. A., Buza, N., Ellenson, L. H., Fadare, O., Ganesan, R., Ip, P. P. C., Palacios, J., Parra‐Herran, C., et al. (2022) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000000901 · Cited by 24
“In the 2020 edition of the WHO Classification (5), it is suggested that patients with clonally related low-risk tumors be managed conservatively (as if they were 2 independent primaries) when the following criteria are met: (1) low-grade endometrioid morphology, (2) no more than superficial myometrial invasion, (3) ab…”
BackgroundMethodInfluential
Therapeutic targeting of mismatch repair-deficient cancers
Johannet, P. M., Rousseau, B., Aghajanian, C. A., Foote, M. B., & Diaz, L. A. (2025) · Nature Reviews Clinical Oncology · doi:10.1038/s41571-025-01054-6 · Cited by 35
“MMRd tumours were historically thought of as chromosomally stable, and MSI-H was viewed as mutually exclusive with chromosomal instability 112–114 .”
Mismatch repair deficiency and clinical implications in prostate cancer
Graham, L. S., & Schweizer, M. T. (2022) · The Prostate · doi:10.1002/pros.24343 · Cited by 30
Lynch syndrome screening in gynaecological cancers: results of an international survey with recommendations for uniform reporting terminology for mismatch repair immunohistochemistry results
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“Furthermore, it highlights the disconnection between research and clinical practice; the identification of MMRd tumours has key prognostic and therapeutic implications for patients, which could be ignored if clinicians are unaware of them.(25,26) A high percentage of the pathologists who undertook the survey were invo…”
Background
Detection of somatic mutations in peritoneal lavages and plasma of endometrial cancer patients: A proof‐of‐concept study
Mayo‐de‐las‐Casas, C., Velasco, A., Guzman, D. R. S., et al. (2020) · International Journal of Cancer · doi:10.1002/ijc.32872 · Cited by 24
“In addition, the Cancer Genome Atlas (TCGA) has shown that they have different mutation profiles.(26) The most frequently mutated genes in EEC were PTEN (78%), PIK3CA (53%) and KRAS (25%) compared to TP53 (91%) and PIK3CA (42%) in SC.”
Background
Dendritic cell vaccination combined with carboplatin/paclitaxel for metastatic endometrial cancer patients: results of a phase I/II trial
Koeneman, B. J., Schreibelt, G., Gorris, M. A. J., Hins - de Bree, S., Westdorp, H., Ottevanger, P. B., & de Vries, I. J. M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1368103 · Cited by 24
miRNA-576-5p promotes endometrial cancer cell growth and metastasis by targeting ZBTB4
Chen, C., Zhang, Q., & Kong, B. (2022) · Clinical & Translational Oncology · doi:10.1007/s12094-022-02976-8 · Cited by 23
Mesonephric‐like adenocarcinoma harbours characteristic copy number variations and a distinct DNA methylation signature closely related to mesonephric adenocarcinoma of the cervix
Kommoss, F., Lee, C.-H., Tessier-Cloutier, B., Gilks, C., Stewart, C. J. R., von Deimling, A., & Köbel, M. (2023) · Journal of Pathology · doi:10.1002/path.6217 · Cited by 22
c-KIT Analysis and Targeted Molecular Sequencing of Mesonephric Carcinomas of the Female Genital Tract
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Prognostic significance of mutant-allele tumor heterogeneity in uterine corpus endometrial carcinoma
Hou, Y., Li, T., Gan, W., Lv, S., Zeng, Z., Zheng, Y., Wang, W., & Yang, M. H. (2020) · Annals of Translational Medicine · doi:10.21037/atm.2020.02.136 · Cited by 21
“The molecular type of each sample was downloaded from attachment files of the article “Integrated Genomic Characterization of Endometrial Carcinoma” (23).”
Method
Recent advances in smooth muscle tumors with PGR and PLAG1 gene fusions and myofibroblastic uterine neoplasms
Chiang, S. (2020) · Genes Chromosomes and Cancer · doi:10.1002/gcc.22920 · Cited by 23
CDK2 heterobifunctional degraders co-degrade CDK2 and cyclin E resulting in efficacy in CCNE1-amplified and overexpressed cancers
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Expression of DNA repair proteins in endometrial cancer predicts disease outcome
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KRAS, YWHAE, SP1 and MSRA as biomarkers in endometrial cancer
Yang, Y., Sang, Z., Ma, J., Zhu, Y., & Wu, S. (2021) · Translational Cancer Research · doi:10.21037/tcr-20-2969 · Cited by 19
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Method
Dostarlimab for recurrent mismatch repair‐deficient endometrial cancer: A cost‐effectiveness study
Dioun, S. M., Chen, L., Melamed, A., Gockley, A. A., Clair, C. M. S., Hou, J. Y., Khoury‐Collado, F., Hur, C., Elkin, E. B., Accordino, M. K., et al. (2022) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.17338 · Cited by 20
Utility of a PAX2, PTEN, and β-catenin Panel in the Diagnosis of Atypical Hyperplasia/Endometrioid Intraepithelial Neoplasia in Endometrial Polyps
Lucas, E., Niu, S., Aguilar, M., et al. (2023) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000002076 · Cited by 22
Long-range gene regulation in hormone-dependent cancer
Tettey, T. T., Rinaldi, L., & Hager, G. L. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00603-4 · Cited by 23
Omics-based molecular classifications empowering in precision oncology
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The Value of DICER1 Mutation Analysis in “Subtle” Diagnostically Challenging Embryonal Rhabdomyosarcomas of the Uterine Cervix
Yoon, J., Apellániz-Ruiz, M., Chong, A., et al. (2020) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0000000000000718 · Cited by 22
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Magnetic resonance-based radiomics nomogram for predicting microsatellite instability status in endometrial cancer
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“In our study, approximately 33% of EC had MSI, and this prevalence was similar to that of other studies (5,32).”
Mismatch repair markers in preoperative and operative endometrial cancer samples; expression concordance and prognostic value
Berg, H. F., Engerud, H., Myrvold, M., Lien, H. E., Hjelmeland, M. E., Halle, M. K., Woie, K., Høivik, E. A., Haldorsen, I. S., Vintermyr, O. K., et al. (2022) · British Journal of Cancer · doi:10.1038/s41416-022-02063-3 · Cited by 21
“Patients with MSI-hypermutated tumours have an intermediate prognosis [5] and may be eligible for treatment with immune checkpoint inhibitors [6], although this is seldom used in clinical routine.”
BackgroundResultInfluential
Incorporating Intratumoral Heterogeneity into Weakly-Supervised Deep Learning Models via Variance Pooling
Carmichael, I., Song, A. H., Chen, R. J., Williamson, D. F. K., Chen, T. Y., & Mahmood, F. (2022) · Lecture Notes in Computer Science · doi:10.1007/978-3-031-16434-7_38 · Cited by 20
Common DNA methylation dynamics in endometriod adenocarcinoma and glioblastoma suggest universal epigenomic alterations in tumorigenesis
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Malignancy and lymphoid proliferation in primary immune deficiencies; hard to define, hard to treat
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“Symptom of age of PID (month) (median, range) 6 (1-108)”
Background

Authors: The Cancer Genome Atlas Research Network, & Levine, D. A.
Affiliations: Memorial Sloan Kettering Cancer Center (US)
Corresponding author: Levine, Douglas A.
ORCID: Levine, Douglas A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2013-05-01
Volume: 497
Issue: 7447
Pages: 67-73
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature12113
PMC: PMC3704730
OpenAlex: W2041440766
Cited by: 5,784
References: 40
Citations by year: 2026: 467 · 2025: 580 · 2024: 559 · 2023: 595 · 2022: 591 · 2021: 572 · 2020: 455 · 2019: 384 · 2018: 320 · 2017: 328 · 2016: 313 · 2015: 285 · 2014: 231 · 2013: 96
FWCI: 345.78
Type: journal article
Language: en
Update notices: erratum (2013-06-12)
Open access: hybrid
doi.org
Licence: cc-by-nc-sa
creativecommons.org/licenses/by-nc-sa/3.0/ (tdm)
creativecommons.org/licenses/by-nc-sa/3.0/ (vor)
Locations: Nature (publishedVersion, cc-by-nc-sa)
PubMed Central (publishedVersion, cc-by-nc-sa)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: National Institutes of Health
National Human Genome Research Institute (U54HG003067, U54HG003079, U54HG003273)
National Cancer Institute (P50CA098258, U24CA143882, R01CA180006, U24CA143843, U24CA143840, U24CA143858, U24CA144025, U24CA143866, U24CA143883, U24CA143845, U24CA143867, U24CA143848, U24CA143799, U24CA143835, P30CA008748, P30CA016672, P30CA016056, P30CA016086)
Topics: Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: endometrial cancer, uterine serous carcinoma, endometrioid carcinoma, copy number alterations, TP53 mutation, POLE mutation, microsatellite instability, ARID5B, SWI/SNF chromatin remodeling, CTNNB1, PIK3CA, KRAS, PTEN, DNA methylation, oestrogen receptor, progesterone receptor, adjuvant therapy, genomic profiling
MeSH terms: Poly-ADP-Ribose Binding Proteins, Breast Neoplasms, Chromosome Aberrations, DNA Mutational Analysis, DNA Polymerase II, DNA-Binding Proteins, Female, Humans, Ovarian Neoplasms, Transcription Factors, Signal Transduction, Genome, Human, Gene Expression Regulation, Neoplastic, Endometrial Neoplasms, Genomics, DNA Copy Number Variations, Exome

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