Comprehensive molecular portraits of human breast tumours
Open accessAbstract
We analysed primary breast cancers by genomic DNA copy number arrays, DNA methylation, exome sequencing, messenger RNA arrays, microRNA sequencing and reverse-phase protein arrays. Our ability to integrate information across platforms provided key insights into previously defined gene expression subtypes and demonstrated the existence of four main breast cancer classes when combining data from five platforms, each of which shows significant molecular heterogeneity. Somatic mutations in only three genes (TP53, PIK3CA and GATA3) occurred at >10% incidence across all breast cancers; however, there were numerous subtype-associated and novel gene mutations including the enrichment of specific mutations in GATA3, PIK3CA and MAP3K1 with the luminal A subtype. We identified two novel protein-expression-defined subgroups, possibly produced by stromal/microenvironmental elements, and integrated analyses identified specific signalling pathways dominant in each molecular subtype including a HER2/phosphorylated HER2/EGFR/phosphorylated EGFR signature within the HER2-enriched expression subtype. Comparison of basal-like breast tumours with high-grade serous ovarian tumours showed many molecular commonalities, indicating a related aetiology and similar therapeutic opportunities. The biological finding of the four main breast cancer subtypes caused by different subsets of genetic and epigenetic abnormalities raises the hypothesis that much of the clinically observable plasticity and heterogeneity occurs within, and not across, these major biological subtypes of breast cancer. The Cancer Genome Atlas Network describe their multifaceted analyses of primary breast cancers, shedding light on breast cancer heterogeneity; although only three genes (TP53, PIK3CA and GATA3) are mutated at a frequency greater than 10% across all breast cancers, numerous subtype-associated and novel mutations were identified. This Article from the Cancer Genome Atlas consortium describes a multifaceted analysis of primary breast cancers in 825 people. Exome sequencing, copy number variation, DNA methylation, messenger RNA arrays, microRNA sequencing and proteomic analyses were performed and integrated to shed light on breast-cancer heterogeneity. Just three genes — TP53, PIK3CA and GATA3 — are mutated at greater than 10% frequency across all breast cancers. Many subtype-associated and novel mutations were identified, as well as two breast-cancer subgroups with specific signalling-pathway signatures. The analyses also suggest that much of the clinically observable plasticity and heterogeneity occurs within, and not across, the major subtypes of breast cancer.
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HIF-1α is a master transcription factor that is highly expressed in cancer tissues, including breast cancer, and is particularly enriched in triple-negative breast cancer (TNBC).
“Hypoxia-inducible factor 1α (HIF-1α) is a master transcription factor that is highly expressed in cancer tissues, including breast cancer, and is particularly enriched in triple-negative breast cancer (TNBC)2.”
From Liposomal Formulation of HIF-1α Inhibitor Echinomycin Eliminates Established Metastases of Triple-negative Breast Cancer (2020) · cites this paper as [2]
The Basal-like summary analysis (page unavailable) identifies hyperactivated HIF1α/ARNT regulatory hubs and high pathway activity in basal-like breast cancers, most of which are TNBC. It does not establish that HIF-1α itself is highly expressed in cancer tissues generally or measured as enriched in TNBC; its finding concerns inferred pathway activity in the basal-like subtype. (LLM, conf=0.88)
Experimental — accuracy not yet measuredA recent analysis found that the PI3K/Akt pathway is elevated in basal-like cancers compared with luminal or HER2+ cancers.
“A recent analysis, combining mutation, mRNA expression and protein levels, determined that the PI3K/Akt pathway was elevated in basal-like cancers as compared with luminal or HER2+ (47).”
From Mislocalization of the Cell Polarity Protein Scribble Promotes Mammary Tumorigenesis and Is Associated with Basal Breast Cancer (2014) · cites this paper as [47]
In breast cancer, hypoxia is more evident in TNBC than in other breast cancer subtypes.
“In breast cancer, hypoxia is more evident in TNBC than in other breast cancer subtypes11,12.”
The hypoxia gene signature is inversely correlated with immune effector genes (IFNG, TNF, GZMB, PRF1), IFNγ-responsive genes, and TIL-associated genes in TNBC (n = 99) in the TCGA dataset.
“data analysis of The Cancer Genome Atlas (TCGA) dataset11 identified that hypoxic gene signature, which includes commonly documented hypoxia-responsive genes26, was inversely correlated with immune effector genes (IFNG, TNF, GZMB, PRF1), IFNγ-responsive genes, as well as genes associated with tumor-infiltrating lymphocytes (TILs) in TNBC (n = 99) (also referred as a basal subtype of breast cancer)”
TNBC patients with higher hypoxia gene signature are associated with worse overall survival and distant metastasis-free survival compared to those with lower expression of the hypoxia gene signature.
“Kaplan–Meier analysis using public breast cancer meta-analysis database11,30 reveals that TNBC patients with higher hypoxia gene signature are associated with worse disease outcomes, including both overall survival (OS) and distant metastasis-free survival (DMFS), compared to those with lower expression of hypoxia gene signature (Fig. 1h).”
Triple-negative breast cancers have a wide diversity of somatic mutations, none of which are found at high frequency.
“Analysis of hundreds of triple-negative breast cancers revealed a wide diversity of somatic mutations none of which were found at high frequency [4].”
From The hypoxic tumor microenvironment: A driving force for breast cancer progression (2016) · cites this paper as [4]
HIF target genes are remarkably overexpressed in triple-negative breast cancer.
“Given the remarkable overexpression of HIF target genes in triple-negative breast cancer [4, 21], the master regulatory role of HIFs in metastasis (Fig. 5), and their involvement in chemotherapy resistance, HIF inhibitors may represent a targeted therapy for these breast cancers.”
From The hypoxic tumor microenvironment: A driving force for breast cancer progression (2016) · cites this paper as [4]
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RetractedIntegrative multi-omics approaches in cancer research: from biological networks to clinical subtypes
Heo, Y. J., Hwa, C., Lee, G.-H., Park, J.-M., & An, J.-Y. (2021) · Molecules and Cells · doi:10.14348/molcells.2021.0042 · Cited by 294 · see citing works
Saal, L. H., Vallon-Christersson, J., Häkkinen, J., Hegardt, C., Grabau, D., Winter, C., Brueffer, C., Tang, M.-H. E., Reuterswärd, C., Schulz, R., et al. (2015) · Genome Medicine · doi:10.1186/s13073-015-0131-9 · Cited by 255 · see citing works
Distinct structural classes of activating FOXA1 alterations in advanced prostate cancer
Parolia, A., Cieslik, M., Chu, S.-C., Xiao, L., Ouchi, T., Zhang, Y., Wang, X., Vats, P., Cao, X., Pitchiaya, S., et al. (2019) · Nature · doi:10.1038/s41586-019-1347-4 · Cited by 284 · see citing works
- Authors
- The Cancer Genome Atlas Network
- Corresponding author
- The Cancer Genome Atlas Network
- Venue
- Nature
- Published
- 2012-09-23
- Volume
- 490
- Issue
- 7418
- Pages
- 61-70
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3465532
- OpenAlex
- W4301159569
- Cited by
- 12,129
- References
- 57
- Citations by year
- 2026: 552 · 2025: 690 · 2024: 761 · 2023: 781 · 2022: 918 · 2021: 1164 · 2020: 1005 · 2019: 961 · 2018: 942 · 2017: 949 · 2016: 979 · 2015: 909 · 2014: 879 · 2013: 590 · 2012: 40
- FWCI
- 256.76
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Nature (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- U.S. Department of Defense
- Breast Cancer Research Foundation (P50CA116201)
- Henry M. Jackson Foundation
- National Institutes of Health
- National Human Genome Research Institute (U54HG003067, U54HG003079, U54HG004028)
- National Cancer Institute (R01CA094143, U24CA143882, U01CA084955, U24CA143840, U24CA143858, U24CA144025, K08CA148912, U24CA143866, U24CA143883, U24CA143845, U24CA143867, U24CA143848, U24CA143799, U24CA143835, P50 CA 58223, P30CA016672, P30CA016058, P50CA058223, P50CA116201, P30CA016086)
- U.S. National Library of Medicine (R01LM009722)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Breast Lesions and Carcinomas
- Keywords
- breast cancer, molecular subtypes, tumor heterogeneity, somatic mutations, TP53, PIK3CA, GATA3, MAP3K1, luminal A, HER2-enriched breast cancer, basal-like breast cancer, high-grade serous ovarian cancer, DNA methylation, copy number variation, gene expression signatures, signaling pathways, tumor microenvironment, multi-omics integration
- MeSH terms
- Breast Neoplasms, DNA Mutational Analysis, Female, Humans, Mutation, Ovarian Neoplasms, Receptors, Estrogen, RNA, Messenger, RNA, Neoplasm, Genome, Human, Gene Expression Regulation, Neoplastic, Genes, p53, Retinoblastoma Protein, Genes, erbB-2, Genetic Heterogeneity, DNA Methylation, Genes, BRCA1, Phosphatidylinositol 3-Kinases, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Genomics, MicroRNAs, Protein Array Analysis, Proteomics, MAP Kinase Kinase Kinase 1, GATA3 Transcription Factor, Genes, Neoplasm, DNA Copy Number Variations, Class I Phosphatidylinositol 3-Kinases, Exome
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