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Chromatin composition alterations and the critical role of MeCP2 for epigenetic silencing of progesterone receptor-B gene in endometrial cancers

Byline: Yongli Chu (1), Yanlin Wang (2), Guanghua Zhang (3), Haibin Chen (4), Sean C. Dowdy (5), Yuning Xiong (5), Fengming Liu (6), Run Zhang (9), Jinping Li (5,7,9), Shi-Wen Jiang (5,7,8,9) Keywords: Progesterone receptor-B; Epigenetic silencing; Endometrial cancer; DNA methylation; Chromatin Abst... Full description

Journal Title: Cellular and Molecular Life Sciences 2014, Vol.71(17), pp.3393-3408
Main Author: Chu, Yongli
Other Authors: Wang, Yanlin , Zhang, Guanghua , Chen, Haibin , Dowdy, Sean , Xiong, Yuning , Liu, Fengming , Zhang, Run , Li, Jinping , Jiang, Shi-Wen
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: ISSN: 1420-682X ; E-ISSN: 1420-9071 ; DOI: 10.1007/s00018-014-1580-9
Link: http://dx.doi.org/10.1007/s00018-014-1580-9
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recordid: springer_jour10.1007/s00018-014-1580-9
title: Chromatin composition alterations and the critical role of MeCP2 for epigenetic silencing of progesterone receptor-B gene in endometrial cancers
format: Article
creator:
  • Chu, Yongli
  • Wang, Yanlin
  • Zhang, Guanghua
  • Chen, Haibin
  • Dowdy, Sean
  • Xiong, Yuning
  • Liu, Fengming
  • Zhang, Run
  • Li, Jinping
  • Jiang, Shi-Wen
subjects:
  • Progesterone receptor-B
  • Epigenetic silencing
  • Endometrial cancer
  • DNA methylation
  • Chromatin
ispartof: Cellular and Molecular Life Sciences, 2014, Vol.71(17), pp.3393-3408
description: Byline: Yongli Chu (1), Yanlin Wang (2), Guanghua Zhang (3), Haibin Chen (4), Sean C. Dowdy (5), Yuning Xiong (5), Fengming Liu (6), Run Zhang (9), Jinping Li (5,7,9), Shi-Wen Jiang (5,7,8,9) Keywords: Progesterone receptor-B; Epigenetic silencing; Endometrial cancer; DNA methylation; Chromatin Abstract: Objective To understand the epigenetic mechanism underlying the PR-B gene silencing in endometrial cancer (EC) cells, we compared the chromatin composition between transcriptionally active and silenced PR-B genes in EC cell lines and cancer tissues. Methods Chromatin Immunoprecipitation (ChIP) assay was performed to measure MBD occupancy and histone acetylation/methylation in transcriptionally active and silenced PR-B genes. PR-B-positive/-negative, as well as epigenetic inhibitor-treated/-untreated EC cells were used as study models. Real-time polymerase chain reaction (PCR) and Western blot analysis were applied to measure the mRNA and protein levels of PR-B, MBD, and histones. Results A close association among PR-B methylation, MBD binding and PR-B gene silencing was observed. Treatment with epigenetic inhibitors led to dynamic changes in the PR-B chromatin composition and gene expression. Increased H3/H4 acetylation and H3-K4 methylation, and decreased H3-K9 methylation were found to be associated with re-activation of silenced PR-B genes. MeCP2 knockdown resulted in a decreased MeCP2 binding to PR-B genes and an increased PR-B expression. ChIP analysis of MeCP2 binding to PR-B genes in the PR-B-positive/-negative EC samples confirmed the significant role of MeCP2 in PR-B silencing. Conclusion PR-B gene expression is regulated by a concerted action of epigenetic factors including DNA methylation, MBD binding, and histone modifications. MeCP2 occupancy of PR-B genes plays a critical role in PR-B gene silencing. These findings enriched our knowledge of the epigenetic regulation of PR-B expression in EC, and suggested that the epigenetic re-activation of PR-B could be explored as a potential strategy to sensitize the PR-B-negative endometrial cancers to progestational therapy. Author Affiliation: (1) Yantai Yuhuangding Hospital Affiliated to Qingdao University, Yantai, 264000, China (2) Department of Reproductive Medicine, Binzhou Medical University Hospital, Binzhou, 256603, China (3) Tianjin Medical University Cancer Hospital, Tianjin, 300060, China (4) Department of Histology and Embryology, Shantou University Medical College, Guangdong, China (5) Depa
language: eng
source:
identifier: ISSN: 1420-682X ; E-ISSN: 1420-9071 ; DOI: 10.1007/s00018-014-1580-9
fulltext: fulltext
issn:
  • 1420-9071
  • 14209071
  • 1420-682X
  • 1420682X
url: Link


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titleChromatin composition alterations and the critical role of MeCP2 for epigenetic silencing of progesterone receptor-B gene in endometrial cancers
creatorChu, Yongli ; Wang, Yanlin ; Zhang, Guanghua ; Chen, Haibin ; Dowdy, Sean ; Xiong, Yuning ; Liu, Fengming ; Zhang, Run ; Li, Jinping ; Jiang, Shi-Wen
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subjectProgesterone receptor-B ; Epigenetic silencing ; Endometrial cancer ; DNA methylation ; Chromatin
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descriptionByline: Yongli Chu (1), Yanlin Wang (2), Guanghua Zhang (3), Haibin Chen (4), Sean C. Dowdy (5), Yuning Xiong (5), Fengming Liu (6), Run Zhang (9), Jinping Li (5,7,9), Shi-Wen Jiang (5,7,8,9) Keywords: Progesterone receptor-B; Epigenetic silencing; Endometrial cancer; DNA methylation; Chromatin Abstract: Objective To understand the epigenetic mechanism underlying the PR-B gene silencing in endometrial cancer (EC) cells, we compared the chromatin composition between transcriptionally active and silenced PR-B genes in EC cell lines and cancer tissues. Methods Chromatin Immunoprecipitation (ChIP) assay was performed to measure MBD occupancy and histone acetylation/methylation in transcriptionally active and silenced PR-B genes. PR-B-positive/-negative, as well as epigenetic inhibitor-treated/-untreated EC cells were used as study models. Real-time polymerase chain reaction (PCR) and Western blot analysis were applied to measure the mRNA and protein levels of PR-B, MBD, and histones. Results A close association among PR-B methylation, MBD binding and PR-B gene silencing was observed. Treatment with epigenetic inhibitors led to dynamic changes in the PR-B chromatin composition and gene expression. Increased H3/H4 acetylation and H3-K4 methylation, and decreased H3-K9 methylation were found to be associated with re-activation of silenced PR-B genes. MeCP2 knockdown resulted in a decreased MeCP2 binding to PR-B genes and an increased PR-B expression. ChIP analysis of MeCP2 binding to PR-B genes in the PR-B-positive/-negative EC samples confirmed the significant role of MeCP2 in PR-B silencing. Conclusion PR-B gene expression is regulated by a concerted action of epigenetic factors including DNA methylation, MBD binding, and histone modifications. MeCP2 occupancy of PR-B genes plays a critical role in PR-B gene silencing. These findings enriched our knowledge of the epigenetic regulation of PR-B expression in EC, and suggested that the epigenetic re-activation of PR-B could be explored as a potential strategy to sensitize the PR-B-negative endometrial cancers to progestational therapy. Author Affiliation: (1) Yantai Yuhuangding Hospital Affiliated to Qingdao University, Yantai, 264000, China (2) Department of Reproductive Medicine, Binzhou Medical University Hospital, Binzhou, 256603, China (3) Tianjin Medical University Cancer Hospital, Tianjin, 300060, China (4) Department of Histology and Embryology, Shantou University Medical College, Guangdong, China (5) Department of Obstetrics and Gynecology, Mayo Clinic and Mayo Medical School, Rochester, MN, 55905, USA (6) Department of Research and Development, Guangxi Medicinal Botanical Institute, Nanning, 530024, China (7) Curtis & Elizabeth Anderson Cancer Institute, Memorial Health University Medical Center, 4700 Waters Avenue, Savannah, GA, 31404, USA (8) Department of Obstetrics and Gynecology, Memorial Health University Medical Center, 4700 Waters Avenue, Savannah, GA, 31404, USA (9) Department of Biomedical Science, Mercer University School of Medicine, Savannah, GA, 31404, USA Article History: Registration Date: 28/01/2014 Received Date: 22/09/2012 Accepted Date: 28/01/2014 Online Date: 15/02/2014 Article note: Y. Chu, Y. Wang, G. Zhang and H. Chen contributed equally.
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