5-methylcytosine promotes pathogenesis of bladder cancer through stabilizing mRNAs
Although 5-methylcytosine (m 5 C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m 5 C modifications in human urothelial carcinoma of the...
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| Published in | Nature cell biology Vol. 21; no. 8; pp. 978 - 990 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.08.2019
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Although 5-methylcytosine (m
5
C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m
5
C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m
5
C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m
5
C ‘reader’ recognizing m
5
C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m
5
C methylation site in the
HDGF
3′ untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m
5
C-regulated oncogene activation, providing a potential therapeutic strategy for UCB.
Chen et al. provide an m
5
C landscape in bladder cancer and show m
5
C enrichment at oncogene mRNAs that promotes tumour progression. They identify YBX1 as the m
5
C ‘reader’ that recruits ELAVL1 to stabilize mRNAs. |
|---|---|
| AbstractList | Although 5-methylcytosine (m
5
C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m
5
C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m
5
C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m
5
C ‘reader’ recognizing m
5
C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m
5
C methylation site in the
HDGF
3′ untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m
5
C-regulated oncogene activation, providing a potential therapeutic strategy for UCB.
Chen et al. provide an m
5
C landscape in bladder cancer and show m
5
C enrichment at oncogene mRNAs that promotes tumour progression. They identify YBX1 as the m
5
C ‘reader’ that recruits ELAVL1 to stabilize mRNAs. Although 5-methylcytosine (m.sup.5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m.sup.5C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m.sup.5C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m.sup.5C 'reader' recognizing m.sup.5C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m.sup.5C methylation site in the HDGF 3' untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m.sup.5C-regulated oncogene activation, providing a potential therapeutic strategy for UCB. Chen et al. provide an m.sup.5C landscape in bladder cancer and show m.sup.5C enrichment at oncogene mRNAs that promotes tumour progression. They identify YBX1 as the m.sup.5C 'reader' that recruits ELAVL1 to stabilize mRNAs. Although 5-methylcytosine (m5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m5C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m5C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m5C ‘reader’ recognizing m5C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m5C methylation site in the HDGF 3′ untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m5C-regulated oncogene activation, providing a potential therapeutic strategy for UCB. Although 5-methylcytosine (m C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m C 'reader' recognizing m C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m C methylation site in the HDGF 3' untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m C-regulated oncogene activation, providing a potential therapeutic strategy for UCB. Although 5-methylcytosine (m.sup.5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m.sup.5C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m.sup.5C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m.sup.5C 'reader' recognizing m.sup.5C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m.sup.5C methylation site in the HDGF 3' untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m.sup.5C-regulated oncogene activation, providing a potential therapeutic strategy for UCB. Although 5-methylcytosine (m5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m5C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m5C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m5C 'reader' recognizing m5C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m5C methylation site in the HDGF 3' untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m5C-regulated oncogene activation, providing a potential therapeutic strategy for UCB.Although 5-methylcytosine (m5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain unknown. Here, we provide the single-nucleotide resolution landscape of messenger RNA m5C modifications in human urothelial carcinoma of the bladder (UCB). We identify numerous oncogene RNAs with hypermethylated m5C sites causally linked to their upregulation in UCBs and further demonstrate YBX1 as an m5C 'reader' recognizing m5C-modified mRNAs through the indole ring of W65 in its cold-shock domain. YBX1 maintains the stability of its target mRNA by recruiting ELAVL1. Moreover, NSUN2 and YBX1 are demonstrated to drive UCB pathogenesis by targeting the m5C methylation site in the HDGF 3' untranslated region. Clinically, a high coexpression of NUSN2, YBX1 and HDGF predicts the poorest survival. Our findings reveal an unprecedented mechanism of RNA m5C-regulated oncogene activation, providing a potential therapeutic strategy for UCB. |
| Audience | Academic |
| Author | Ma, Jinbiao Liu, Zhuo-Wei Xie, Dan Yang, Ying Chen, Yu-Sheng Chen, Ri-Xin Yang, Yun-Gui Wei, Wen-Su Wang, Hai-Lin Li, Ang Han, Ya-Nan Zhao, Yong-Liang Zhou, Fang-Jian Zhang, Mengmeng Lyu, Cong Chen, Xin Gao, Chun-Chun Yuan, Xun Luo, Jun-Hang Ma, Xiao-Dan Sun, Bao-Fa Liu, Yanchao Huang, Ying |
| Author_xml | – sequence: 1 givenname: Xin surname: Chen fullname: Chen, Xin organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Department of Urology, Sun Yat-sen University Cancer Center – sequence: 2 givenname: Ang surname: Li fullname: Li, Ang organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 3 givenname: Bao-Fa surname: Sun fullname: Sun, Bao-Fa organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Institute of Stem Cell and Regeneration, Chinese Academy of Sciences – sequence: 4 givenname: Ying surname: Yang fullname: Yang, Ying organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Institute of Stem Cell and Regeneration, Chinese Academy of Sciences – sequence: 5 givenname: Ya-Nan surname: Han fullname: Han, Ya-Nan organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 6 givenname: Xun surname: Yuan fullname: Yuan, Xun organization: State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 7 givenname: Ri-Xin surname: Chen fullname: Chen, Ri-Xin organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center – sequence: 8 givenname: Wen-Su surname: Wei fullname: Wei, Wen-Su organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Department of Urology, Sun Yat-sen University Cancer Center – sequence: 9 givenname: Yanchao orcidid: 0000-0002-6647-8491 surname: Liu fullname: Liu, Yanchao organization: State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 10 givenname: Chun-Chun surname: Gao fullname: Gao, Chun-Chun organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 11 givenname: Yu-Sheng orcidid: 0000-0001-5292-1301 surname: Chen fullname: Chen, Yu-Sheng organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 12 givenname: Mengmeng surname: Zhang fullname: Zhang, Mengmeng organization: State Key Laboratory of Genetic Engineering, Collaborative Innovation Centre of Genetics and Development, Multiscale Research Institute for Complex Systems, Department of Biochemistry, School of Life Sciences, Fudan University – sequence: 13 givenname: Xiao-Dan surname: Ma fullname: Ma, Xiao-Dan organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center – sequence: 14 givenname: Zhuo-Wei surname: Liu fullname: Liu, Zhuo-Wei organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Department of Urology, Sun Yat-sen University Cancer Center – sequence: 15 givenname: Jun-Hang surname: Luo fullname: Luo, Jun-Hang organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center – sequence: 16 givenname: Cong surname: Lyu fullname: Lyu, Cong organization: University of Chinese Academy of Sciences, State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences – sequence: 17 givenname: Hai-Lin surname: Wang fullname: Wang, Hai-Lin organization: University of Chinese Academy of Sciences, State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences – sequence: 18 givenname: Jinbiao orcidid: 0000-0002-0232-1786 surname: Ma fullname: Ma, Jinbiao organization: State Key Laboratory of Genetic Engineering, Collaborative Innovation Centre of Genetics and Development, Multiscale Research Institute for Complex Systems, Department of Biochemistry, School of Life Sciences, Fudan University – sequence: 19 givenname: Yong-Liang surname: Zhao fullname: Zhao, Yong-Liang organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Institute of Stem Cell and Regeneration, Chinese Academy of Sciences – sequence: 20 givenname: Fang-Jian surname: Zhou fullname: Zhou, Fang-Jian organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center, Department of Urology, Sun Yat-sen University Cancer Center – sequence: 21 givenname: Ying orcidid: 0000-0002-2806-2874 surname: Huang fullname: Huang, Ying email: huangy@sibcb.ac.cn organization: State Key Laboratory of Molecular Biology, Shanghai Key Laboratory of Molecular Andrology, CAS Center for Excellence in Molecular Cell Science, Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, University of Chinese Academy of Sciences – sequence: 22 givenname: Dan orcidid: 0000-0003-2242-3138 surname: Xie fullname: Xie, Dan email: xiedan@sysucc.org.cn organization: State Key Laboratory of Oncology in South China, Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University Cancer Center – sequence: 23 givenname: Yun-Gui orcidid: 0000-0002-2821-8541 surname: Yang fullname: Yang, Yun-Gui email: ygyang@big.ac.cn organization: CAS Key Laboratory of Genomic and Precision Medicine, Collaborative Innovation Center of Genetics and Development, College of Future Technology, Beijing Institute of Genomics, Chinese Academy of Sciences, University of Chinese Academy of Sciences, Institute of Stem Cell and Regeneration, Chinese Academy of Sciences |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/31358969$$D View this record in MEDLINE/PubMed |
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| Snippet | Although 5-methylcytosine (m
5
C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain... Although 5-methylcytosine (m C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain... Although 5-methylcytosine (m.sup.5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer)... Although 5-methylcytosine (m5C) is a widespread modification in RNAs, its regulation and biological role in pathological conditions (such as cancer) remain... |
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| SubjectTerms | 101/58 42/70 42/89 45/90 45/91 5-Methylcytosine - metabolism 631/337/1645/2020 631/337/1645/2570 631/67 64/60 82/1 82/83 Animals Biomedical and Life Sciences Bladder Bladder cancer Cancer Cancer Research Carcinoma, Transitional Cell - genetics Carcinoma, Transitional Cell - metabolism Cell Biology Cold shock Cytosine Development and progression Developmental Biology Gene Expression Regulation - genetics Genetic aspects Health aspects Humans Indoles Life Sciences Messenger RNA Methylation Methyltransferases - genetics Mice mRNA stability Nucleotides Pathogenesis Physiological aspects RNA, Messenger - genetics Stem Cells Urinary Bladder Neoplasms - genetics Urinary Bladder Neoplasms - metabolism Urinary Bladder Neoplasms - pathology Urothelial carcinoma Y-Box-Binding Protein 1 - genetics |
| Title | 5-methylcytosine promotes pathogenesis of bladder cancer through stabilizing mRNAs |
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