Functional evaluation of genetic variants associated with endometriosis near GREB1
Abstract
STUDY QUESTION: Do DNA variants in the growth regulation by estrogen in breast cancer 1 (GREB1) region regulate endometrial GREB1 expression and increase the risk of developing endometriosis in women? SUMMARY ANSWER: We identified new single nucleotide polymorphisms (SNPs) with strong association with endometriosis at the GREB1 locus although we did not detect altered GREB1 expression in endometriosis patients with defined genotypes. WHAT IS ALREADY KNOWN: Genome-wide association studies have identified the GREB1 region on chromosome 2p25.1 for increasing endometriosis risk. The differential expression of GREB1 has also been reported by others in association with endometriosis disease phenotype. STUDY DESIGN, SIZE, DURATION: Fine mapping studies comprehensively evaluated SNPs within the GREB1 region in a large-scale data set (>2500 cases and >4000 controls). Publicly available bioinformatics tools were employed to functionally annotate SNPs showing the strongest association signal with endometriosis risk. Endometrial GREB1 mRNA and protein expression was studied with respect to phases of the menstrual cycle (n = 2-45 per cycle stage) and expression quantitative trait loci (eQTL) analysis for significant SNPs were undertaken for GREB1 [mRNA (n = 94) and protein (n = 44) in endometrium]. PARTICIPANTS/MATERIALS, SETTING, METHODS: Participants in this study are females who provided blood and/or endometrial tissue samples in a hospital setting. The key SNPs were genotyped using Sequenom MassARRAY. The functional roles and regulatory annotations for identified SNPs are predicted by various publicly available bioinformatics tools. Endometrial GREB1 expression work employed qRT-PCR, western blotting and immunohistochemistry studies. MAIN RESULTS AND THE ROLE OF CHANCE: Fine mapping results identified a number of SNPs showing stronger association (0.004 < P < 0.032) with endometriosis risk than the original GWAS SNP (rs13394619) (P = 0.034). Some of these SNPs were predicted to have functional roles, for example, interaction with transcription factor motifs. The haplotype (a combination of alleles) formed by the risk alleles from two common SNPs showed significant association (P = 0.026) with endometriosis and epistasis analysis showed no evidence for interaction between the two SNPs, suggesting an additive effect of SNPs on endometriosis risk. In normal human endometrium, GREB1 protein expression was altered depending on the cycle stage (significantly different in late proliferative versus late secretory, P < 0.05) and cell type (glandular epithelium, not stromal cells). However, GREB1 expression in endometriosis cases versus controls and eQTL analyses did not reveal any significant changes. LIMITATIONS, REASONS FOR CAUTION: In silico prediction tools are generally based on cell lines different to our tissue and disease of interest. Functional annotations drawn from these analyses should be considered with this limitation in mind. We identified cell-specific and hormone-specific changes in GREB1 protein expression. The lack of a significant difference observed following our GREB1 expression studies may be the result of moderate power on mixed cell populations in the endometrial tissue samples. WIDER IMPLICATIONS OF THE FINDINGS: This study further implicates the GREB1 region on chromosome 2p25.1 and the GREB1 gene with involvement in endometriosis risk. More detailed functional studies are required to determine the role of the novel GREB1 transcripts in endometriosis pathophysiology. STUDY FUNDING/COMPETING INTERESTS: Funding for this work was provided by NHMRC Project Grants APP1012245, APP1026033, APP1049472 and APP1046880. There are no competing interests.
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Certain genetic variants that are significantly more common in endometriosis appear to be good functional candidates for the genetic factors responsible for the onset of endometriosis.
“Literature data on GWAS studies suggest that certain genetic variants, significantly more common in endometriosis, appear to be good functional candidates for the genetic factors responsible for the onset of this disease [185].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [185]
The 2p25.1 region, located near the GREB1 gene, is linked to the risk of endometriosis.
“Research indicates a link between the 2p25.1 region, located near the GREB1 gene, and the risk of endometriosis [185].”
From Endometriosis: Epidemiology, Classification, Pathogenesis, Treatment and Genetics (Review of Literature) (2021) · cites this paper as [185]
The index SNP associated with endometriosis on chromosome 2p25.1 is a common splice variant in GREB1 and SNPs associated with endometriosis on chromosome 12q22 increase expression of VEZT in RNA from blood and endometrium.
“The index SNP associated with endometriosis on chromosome 2p25.1 is a common splice variant in the oestrogen-responsive growth regulation by oestrogen in breast cancer 1 (GREB1) gene3337 and SNPs associated with endometriosis on chromosome 12q22 increase expression of the transmembrane adherens junctions protein coding gene vezatin (VEZT) in RNA from blood and endometrium38.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [37]
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- Authors
- Fung, J. N., Holdsworth-Carson, S. J., Sapkota, Y., Zhao, Z. Z., Jones, L., Girling, J. E., Paiva, P., Healey, M., Nyholt, D. R., Rogers, P. A. W., & Montgomery, G. W.
- Affiliations
- QIMR Berghofer Medical Research Institute (AU)
- Royal Women's Hospital (AU)
- Corresponding author
- Fung, Jenny N.
- ORCID
- Venue
- Human Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2015-03-18
- Volume
- 30
- Issue
- 5
- Pages
- 1263-1275
- ISSN
- 0268-1161 (ISSN-L)
- 1460-2350
- OpenAlex
- W2130576072
- Cited by
- 46
- References
- 49
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 5 · 2023: 1 · 2022: 2 · 2021: 6 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 7 · 2016: 4 · 2015: 2
- FWCI
- 6.47
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction (publishedVersion)
- PubMed (publishedVersion)
- Faculty of Health; Institute of Health and Biomedical Innovation
- Funders
- QIMR Berghofer Medical Research Institute
- National Health and Medical Research Council (613674, 1078399, 1013774)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Plant and fungal interactions
- Keywords
- endometriosis, GREB1, single nucleotide polymorphisms, fine mapping, endometrial gene expression, expression quantitative trait loci, haplotype association, epistasis, estrogen regulation, menstrual cycle, transcription factor binding motifs, genetic risk variants, endometrium, epigenetic regulation
- MeSH terms
- Chromosome Mapping, Endometriosis, Endometrium, Female, Gene Expression Regulation, Genotype, Humans, Immunohistochemistry, Neoplasm Proteins, Phenotype, Genetic Variation, Computational Biology, Polymorphism, Single Nucleotide, Quantitative Trait Loci, Genome-Wide Association Study
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