The p53-induced lincRNA-p21 derails somatic cell reprogramming by sustaining H3K9me3 and CpG methylation at pluripotency gene promoters
Recent studies have boosted our understanding of long noncoding RNAs （IncRNAs） in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 （lin...
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| Published in | Cell research Vol. 25; no. 1; pp. 80 - 92 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.01.2015
Nature Publishing Group |
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| Online Access | Get full text |
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| Abstract | Recent studies have boosted our understanding of long noncoding RNAs （IncRNAs） in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 （lincRNAop21） impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation. |
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| AbstractList | Recent studies have boosted our understanding of long noncoding RNAs (lncRNAs) in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 (lincRNA-p21) impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation. Recent studies have boosted our understanding of long noncoding RNAs (lncRNAs) in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 ( lincRNA-p21 ) impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation. Recent studies have boosted our understanding of long noncoding RNAs (lncRNAs) in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 (lincRNA-p21) impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation.Recent studies have boosted our understanding of long noncoding RNAs (lncRNAs) in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 (lincRNA-p21) impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation. Recent studies have boosted our understanding of long noncoding RNAs （IncRNAs） in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 （lincRNAop21） impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation. |
| Author | Xichen Bao Haitao Wu Xihua Zhu Xiangpeng Guo Andrew P Hutchins Zhiwei Luo Hong Song Yongqiang Chen Keyu Lai Menghui Yin Lingxiao Xu Liang Zhou Jiekai Chen Dongye Wang Baoming Qin Jon Frampton Hung-Fat Tse Duanqing Pei Huating Wang Biliang Zhang Miguel A Esteban |
| AuthorAffiliation | Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Guangzhou, Guangdong 510530, China Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, Guangdong 510530, China University of Chinese Academy of Sciences, Beijing 100049, China Laboratory of RNA Chemical Biology, State Key Laboratory of Respiratory Diseases, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, Guangdong 510530, China School of Life Sciences, Shandong University, Jinan, Shandong 250100, China Department of Radiation Medicine, School of Public Health and Tropic Medicine, Southern Medical University, Guangzhou, Guangdong 510515, China Drug Discovery Pipeline Group, Guang- zhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Guangzhou, Guangdong 510530, China Laboratory of Metabolism and Cell Fate, Guangzh |
| Author_xml | – sequence: 1 givenname: Xichen surname: Bao fullname: Bao, Xichen email: bao_xichen@gibh.ac.cn organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 2 givenname: Haitao surname: Wu fullname: Wu, Haitao organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 3 givenname: Xihua surname: Zhu fullname: Zhu, Xihua organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 4 givenname: Xiangpeng surname: Guo fullname: Guo, Xiangpeng organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 5 givenname: Andrew P surname: Hutchins fullname: Hutchins, Andrew P organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 6 givenname: Zhiwei surname: Luo fullname: Luo, Zhiwei organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 7 givenname: Hong surname: Song fullname: Song, Hong organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 8 givenname: Yongqiang surname: Chen fullname: Chen, Yongqiang organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 9 givenname: Keyu surname: Lai fullname: Lai, Keyu organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 10 givenname: Menghui surname: Yin fullname: Yin, Menghui organization: Laboratory of RNA Chemical Biology, State Key Laboratory of Respiratory Diseases, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 11 givenname: Lingxiao surname: Xu fullname: Xu, Lingxiao organization: School of Life Sciences, Shandong University – sequence: 12 givenname: Liang surname: Zhou fullname: Zhou, Liang organization: Department of Radiation Medicine, School of Public Health and Tropic Medicine, Southern Medical University – sequence: 13 givenname: Jiekai surname: Chen fullname: Chen, Jiekai organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 14 givenname: Dongye surname: Wang fullname: Wang, Dongye organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Drug Discovery Pipeline Group, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 15 givenname: Baoming surname: Qin fullname: Qin, Baoming organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Laboratory of Metabolism and Cell Fate, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Hong Kong - Guangdong Joint Laboratory of Stem Cells and Regenerative Medicine, the University of Hong Kong and Guangzhou Institutes of Biomedicine and Health – sequence: 16 givenname: Jon surname: Frampton fullname: Frampton, Jon organization: School of Immunity and Infection, College of Medical and Dental Sciences, University of Birmingham – sequence: 17 givenname: Hung-Fat surname: Tse fullname: Tse, Hung-Fat organization: Hong Kong - Guangdong Joint Laboratory of Stem Cells and Regenerative Medicine, the University of Hong Kong and Guangzhou Institutes of Biomedicine and Health, Cardiology Division, Department of medicine, Queen Mary Hospital, The University of Hong Kong, Shenzhen Institutes of Research and Innovation, The University of Hong Kong – sequence: 18 givenname: Duanqing surname: Pei fullname: Pei, Duanqing organization: Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Hong Kong - Guangdong Joint Laboratory of Stem Cells and Regenerative Medicine, the University of Hong Kong and Guangzhou Institutes of Biomedicine and Health – sequence: 19 givenname: Huating surname: Wang fullname: Wang, Huating organization: Department of Orthopaedics and Traumatology, Li Ka Shing Institute of Health Sciences, The Chinese University of Hong Kong – sequence: 20 givenname: Biliang surname: Zhang fullname: Zhang, Biliang organization: Laboratory of RNA Chemical Biology, State Key Laboratory of Respiratory Diseases, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences – sequence: 21 givenname: Miguel A surname: Esteban fullname: Esteban, Miguel A email: miguel@gibh.ac.cn organization: Laboratory of Chromatin and Human Disease, Chinese Academy of Sciences, Key Laboratory of Regenerative Biology, South China Institute for Stem Cell Biology and Regenerative Medicine, Guangzhou Institutes of Biomedicine and Health, Chinese Academy of Sciences, Hong Kong - Guangdong Joint Laboratory of Stem Cells and Regenerative Medicine, the University of Hong Kong and Guangzhou Institutes of Biomedicine and Health |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25512341$$D View this record in MEDLINE/PubMed |
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| Copyright | Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences 2015 Copyright Nature Publishing Group Jan 2015 Copyright © 2015 Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences 2015 Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences |
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| DocumentTitleAlternate | The p53-induced lincRNA-p21 derails somatic cell reprogramming by sustaining H3K9me3 and CpG methylation at pluripotency gene promoters LincRNA-p21 is an epigenetic barrier for reprogramming |
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| Keywords | DNA methylation long noncoding RNAs somatic cell reprogramming H3K9 methylation p53 heterochromatin |
| Language | English |
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| Notes | somatic cell reprogramming; long noncoding RNAs; p53; lincRNA-p21; heterochromatin; H3K9 methylation;DNA methylation 31-1568/Q Recent studies have boosted our understanding of long noncoding RNAs （IncRNAs） in numerous biological processes, but few have examined their roles in somatic cell reprogramming. Through expression profiling and functional screening, we have identified that the large intergenic noncoding RNA p21 （lincRNAop21） impairs reprogramming. Notably, lincRNA-p21 is induced by p53 but does not promote apoptosis or cell senescence in reprogramming. Instead, lincRNA-p21 associates with the H3K9 methyltransferase SETDB1 and the maintenance DNA methyltransferase DNMT1, which is facilitated by the RNA-binding protein HNRNPK. Consequently, lincRNA-p21 prevents reprogramming by sustaining H3K9me3 and/or CpG methylation at pluripotency gene promoters. Our results provide insight into the role of lncRNAs in reprogramming and establish a novel link between p53 and heterochromatin regulation. ObjectType-Article-1 SourceType-Scholarly Journals-1 content type line 14 ObjectType-Feature-2 content type line 23 These three authors contributed equally to this work. |
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| PublicationTitle | Cell research |
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| PublicationYear | 2015 |
| Publisher | Nature Publishing Group UK Nature Publishing Group |
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| Snippet | Recent studies have boosted our understanding of long noncoding RNAs （IncRNAs） in numerous biological processes, but few have examined their roles in somatic... Recent studies have boosted our understanding of long noncoding RNAs (lncRNAs) in numerous biological processes, but few have examined their roles in somatic... |
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| SubjectTerms | 631/337/176/1988 631/337/384/2568 631/532/2435 Animals Apoptosis Biomedical and Life Sciences Cell Biology Cell Proliferation Cellular Reprogramming CpG CpG Islands DNA (Cytosine-5-)-Methyltransferase 1 DNA (Cytosine-5-)-Methyltransferases - metabolism DNA Methylation Heterochromatin - genetics Heterochromatin - metabolism Histone-Lysine N-Methyltransferase - metabolism Histones - genetics Histones - metabolism Induced Pluripotent Stem Cells - cytology Induced Pluripotent Stem Cells - metabolism Life Sciences Methylation Mice Original original-article p53 Promoter Regions, Genetic RNA, Long Noncoding - metabolism Tumor Suppressor Protein p53 - metabolism 体细胞 全能性 基因启动子 基因诱导 甲基化 重编程 |
| Title | The p53-induced lincRNA-p21 derails somatic cell reprogramming by sustaining H3K9me3 and CpG methylation at pluripotency gene promoters |
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