Allelic Imbalance in Regulation of ANRIL through Chromatin Interaction at 9p21 Endometriosis Risk Locus
Open accessAbstract
Genome-wide association studies (GWASs) have discovered numerous single nucleotide polymorphisms (SNPs) associated with human complex disorders. However, functional characterization of the disease-associated SNPs remains a formidable challenge. Here we explored regulatory mechanism of a SNP on chromosome 9p21 associated with endometriosis by leveraging "allele-specific" functional genomic approaches. By re-sequencing 1.29 Mb of 9p21 region and scrutinizing DNase-seq data from the ENCODE project, we prioritized rs17761446 as a candidate functional variant that was in perfect linkage disequilibrium with the original GWAS SNP (rs10965235) and located on DNase I hypersensitive site. Chromosome conformation capture followed by high-throughput sequencing revealed that the protective G allele of rs17761446 exerted stronger chromatin interaction with ANRIL promoter. We demonstrated that the protective allele exhibited preferential binding affinities to TCF7L2 and EP300 by bioinformatics and chromatin immunoprecipitation (ChIP) analyses. ChIP assays for histone H3 lysine 27 acetylation and RNA polymerase II reinforced the enhancer activity of the SNP site. The allele specific expression analysis for eutopic endometrial tissues and endometrial carcinoma cell lines showed that rs17761446 was a cis-regulatory variant where G allele was associated with increased ANRIL expression. Our work illuminates the allelic imbalances in a series of transcriptional regulation from factor binding to gene expression mediated by chromatin interaction underlie the molecular mechanism of 9p21 endometriosis risk locus. Functional genomics on common disease will unlock functional aspect of genotype-phenotype correlations in the post-GWAS stage.
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Functional studies in mammalian cells show that ANRIL overexpression accelerated proliferation, increased adhesion and decreased apoptosis.
“Functional studies in mammalian cells show that ANRIL overexpression accelerated proliferation, increased adhesion and decreased apoptosis5456.”
From Meta-analysis identifies five novel loci associated with endometriosis highlighting key genes involved in hormone metabolism (2017) · cites this paper as [54]
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- Authors
- Nakaoka, H., Gurumurthy, A., Hayano, T., Ahmadloo, S., Omer, W. H., Yoshihara, K., Yamamoto, A., Kurose, K., Enomoto, T., Akira, S., Hosomichi, K., & Inoue, I.
- Affiliations
- National Institute of Genetics (JP)
- Niigata University (JP)
- Nippon Medical School (JP)
- Kanazawa University (JP)
- Corresponding author
- Inoue, Ituro
- ORCID
- Venue
- PLOS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-04-07
- Volume
- 12
- Issue
- 4
- Pages
- e1005893
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC4824487
- OpenAlex
- W2326815424
- Cited by
- 46
- References
- 68
- Citations by year
- 2026: 3 · 2025: 2 · 2023: 1 · 2022: 5 · 2021: 4 · 2020: 2 · 2019: 9 · 2018: 9 · 2017: 10 · 2016: 1
- FWCI
- 5.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Japan Society for the Promotion of Science (15K15598, 26640126, 15H02373)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Keywords
- endometriosis, 9p21, ANRIL, allelic imbalance, cis-regulatory variation, enhancer activity, TCF7L2, EP300, H3K27 acetylation, RNA polymerase II, DNase I hypersensitive sites, chromatin looping, allele-specific expression, endometrial cancer, genotype-phenotype correlation
- MeSH terms
- Chromatin, Chromosomes, Human, Pair 9, Endometriosis, Female, Haplotypes, Humans, Promoter Regions, Genetic, Polymorphism, Single Nucleotide, Allelic Imbalance, Cell Line, Tumor, E1A-Associated p300 Protein, Genome-Wide Association Study, Transcription Factor 7-Like 2 Protein, RNA, Long Noncoding
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