Trans-acting non-synonymous variant of FOXA1 predisposes to hepatocellular carcinoma through modulating FOXA1-ERα transcriptional program and may have undergone natural selection.


Journal

Carcinogenesis
ISSN: 1460-2180
Titre abrégé: Carcinogenesis
Pays: England
ID NLM: 8008055

Informations de publication

Date de publication:
22 04 2020
Historique:
received: 24 01 2019
revised: 26 06 2019
accepted: 30 07 2019
pubmed: 11 8 2019
medline: 1 9 2020
entrez: 11 8 2019
Statut: ppublish

Résumé

Interplay of pioneer transcription factor forkhead box A1 (FOXA1) and estrogen receptor has been implicated in sexual dimorphism in hepatocellular carcinoma (HCC), but etiological relevance of its polymorphism was unknown. In the case control study (1152 patients versus1242 controls), we observed significant increase in HCC susceptibility in hepatitis B virus carriers associated with a non-synonymous Thr83Ala variant of FOXA1 (odds ratio [OR], 1.28; 95% confidence interval [CI], 1.11-1.48, for Ala83-containing genotype, after validation in an independent population with 933 patients versus 1030 controls), a tightly linked (CGC)5/6or7 repeat polymorphism at its promoter (OR 1.32; 95% CI 1.10-1.60, for (CGC)6or7-repeat-containing genotype), and their combined haplotype (OR 1.50; 95% CI 1.24-1.81, for (CGC)6or7-Ala83 haplotype). The susceptible FOXA1-Ala83 impairs its interaction with ERα, attenuates transactivation toward some of their dual target genes, such as type 1 iodothyronine deiodinase, UDP glucuronosyltransferase 2 family, polypeptide B17 and sodium/taurocholate cotransporting polypeptide, but correlates with strengthened cellular expression of α-fetoprotein (AFP) and elevated AFP serum concentration in HCC patients (n = 1096). The susceptible FOXA1 cis-variant with (CGC)6or7 repeat strengthens the binding to transcription factor early growth response 1 and enhances promoter activity and gene expression. Evolutionary population genetics analyses with public datasets reveal significant population differentiation and unique haplotype structure of the derived protective FOXA1-Thr83 and suggest that it may have undergone positive natural selection in Chinese population. These findings epidemiologically highlight the functional significance of FOXA1-ERα transcriptional program and regulatory network in liver cancer development.

Identifiants

pubmed: 31400761
pii: 5546009
doi: 10.1093/carcin/bgz136
doi:

Substances chimiques

ESR1 protein, human 0
Estrogen Receptor alpha 0
FOXA1 protein, human 0
Hepatocyte Nuclear Factor 3-alpha 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

146-158

Informations de copyright

© The Author(s) 2019. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com.

Auteurs

Sheng Wang (S)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Chan Xiang (C)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Department of Pathology, Shanghai Chest Hospital, Shanghai Jiao Tong University, Shanghai, China.

Lin Mou (L)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Yuan Yang (Y)

The Third Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China.

Rong Zhong (R)

Department of Epidemiology and Biostatistics and State Key Laboratory of Environment Health (Incubation), Ministry of Education Key Laboratory of Environment and Health, Ministry of Environmental Protection Key Laboratory of Environment and Health (Wuhan), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.

Liyan Wang (L)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Chang Sun (C)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Zhaoyu Qin (Z)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Jingmin Yang (J)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Ji Qian (J)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Fudan-Taizhou Institute of Health Sciences, Taizhou, Jiangsu, China.

Yuanyuan Zhao (Y)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Yi Wang (Y)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Xuedong Pan (X)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Jingbo Qie (J)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Yan Jiang (Y)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.

Xiaofeng Wang (X)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Fudan-Taizhou Institute of Health Sciences, Taizhou, Jiangsu, China.

Yajun Yang (Y)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Fudan-Taizhou Institute of Health Sciences, Taizhou, Jiangsu, China.

Wei-Ping Zhou (WP)

The Third Department of Hepatic Surgery, Eastern Hepatobiliary Surgery Hospital, Second Military Medical University, Shanghai, China.

Xiaoping Miao (X)

Department of Epidemiology and Biostatistics and State Key Laboratory of Environment Health (Incubation), Ministry of Education Key Laboratory of Environment and Health, Ministry of Environmental Protection Key Laboratory of Environment and Health (Wuhan), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan, Hubei, China.

Fuchu He (F)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
State Key Laboratory of Proteomics, Beijing Proteome Research Center, National Center for Protein Sciences, Beijing Institute of Lifeomics, Beijing, China.

Li Jin (L)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Fudan-Taizhou Institute of Health Sciences, Taizhou, Jiangsu, China.

Haijian Wang (H)

State Key Laboratory of Genetic Engineering and Collaborative Innovation Center for Genetics and Development, School of Life Sciences; Institutes of Biomedical Sciences, Shanghai Medical College, Fudan University, Shanghai, China.
Fudan-Taizhou Institute of Health Sciences, Taizhou, Jiangsu, China.

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