NSUN2-mediated RNA 5-methylcytosine promotes esophageal squamous cell carcinoma progression via LIN28B-dependent GRB2 mRNA stabilization

5-Methylcytosine (m 5 C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m 5 C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m 5 C methylat...

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Published inOncogene Vol. 40; no. 39; pp. 5814 - 5828
Main Authors Su, Jiachun, Wu, Guandi, Ye, Ying, Zhang, Jialiang, Zeng, Lingxing, Huang, Xudong, Zheng, Yanfen, Bai, Ruihong, Zhuang, Lisha, Li, Mei, Pan, Ling, Deng, Junge, Li, Rui, Deng, Shuang, Zhang, Shaoping, Zuo, Zhixiang, Liu, Zexian, Lin, Junzhong, Lin, Dongxin, Zheng, Jian
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 30.09.2021
Nature Publishing Group
Subjects
1-Phosphatidylinositol 3-kinase
13/1
13/109
13/51
13/89
38/39
38/90
38/91
5-Methylcytosine - analogs & derivatives
5-Methylcytosine - metabolism
631/337/1645
631/337/176
631/67/1504/1477
64/110
82/58
AKT protein
Animal models
Animals
Apoptosis
Cancer
Cell Biology
Cell Line, Tumor
Development and progression
Disease Progression
E2F1 protein
Esophageal cancer
Esophageal Neoplasms - genetics
Esophageal Neoplasms - metabolism
Esophageal Neoplasms - pathology
Esophageal Squamous Cell Carcinoma - genetics
Esophageal Squamous Cell Carcinoma - metabolism
Esophageal Squamous Cell Carcinoma - pathology
Esophagus
Female
Gene Expression Regulation, Neoplastic
Genetic aspects
Genetic transcription
GRB2 Adaptor Protein - genetics
GRB2 Adaptor Protein - metabolism
Grb2 protein
Health aspects
Human Genetics
Humans
Internal Medicine
Male
MAP kinase
Medicine
Medicine & Public Health
Messenger RNA
Methylation
Methyltransferase
Methyltransferases
Methyltransferases - genetics
Methyltransferases - metabolism
Mice
Mice, Knockout
Oncology
Oncology, Experimental
Post-transcription
RNA modification
RNA Stability - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-Binding Proteins - genetics
RNA-Binding Proteins - metabolism
Squamous cell carcinoma
Transcriptomes
Tumorigenesis
China
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Abstract 5-Methylcytosine (m 5 C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m 5 C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m 5 C methylation in ESCC tumors due to the overexpressed m 5 C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m 5 C modification of growth factor receptor-bound protein 2 ( GRB2 ) and stabilized its mRNA, which was mediated by a novel m 5 C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m 5 C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.
AbstractList 5-Methylcytosine (m 5 C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m 5 C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m 5 C methylation in ESCC tumors due to the overexpressed m 5 C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m 5 C modification of growth factor receptor-bound protein 2 ( GRB2 ) and stabilized its mRNA, which was mediated by a novel m 5 C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m 5 C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.
5-Methylcytosine (m5C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m5C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m5C methylation in ESCC tumors due to the overexpressed m5C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m5C modification of growth factor receptor-bound protein 2 (GRB2) and stabilized its mRNA, which was mediated by a novel m5C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m5C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.5-Methylcytosine (m5C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m5C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m5C methylation in ESCC tumors due to the overexpressed m5C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m5C modification of growth factor receptor-bound protein 2 (GRB2) and stabilized its mRNA, which was mediated by a novel m5C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m5C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.
5-Methylcytosine (m C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m C methylation in ESCC tumors due to the overexpressed m C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m C modification of growth factor receptor-bound protein 2 (GRB2) and stabilized its mRNA, which was mediated by a novel m C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.
5-Methylcytosine (m.sup.5C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m.sup.5C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m.sup.5C methylation in ESCC tumors due to the overexpressed m.sup.5C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m.sup.5C modification of growth factor receptor-bound protein 2 (GRB2) and stabilized its mRNA, which was mediated by a novel m.sup.5C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m.sup.5C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.
5-Methylcytosine (m5C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear. Here, by detecting the transcriptome-wide m5C profiling in esophageal squamous cell carcinoma (ESCC), we showed increased m5C methylation in ESCC tumors due to the overexpressed m5C methyltransferase NSUN2. Aberrant expression of NSUN2 was positively regulated by E2F Transcription Factor 1 (E2F1). High NSUN2 levels predicted poor survival of ESCC patients. Moreover, silencing NSUN2 suppressed ESCC tumorigenesis and progression in Nsun2 knockout mouse models. Mechanistically, NSUN2 induced m5C modification of growth factor receptor-bound protein 2 (GRB2) and stabilized its mRNA, which was mediated by a novel m5C mediator, protein lin-28 homolog B (LIN28B). Elevated GRB2 levels increased the activation of PI3K/AKT and ERK/MAPK signalling. These results demonstrate that NSUN2 enhances the initiation and progression of ESCC via m5C-LIN28B dependent stabilization of GRB2 transcript, providing a promising epitranscriptomic-targeted therapeutic strategy for ESCC.
Audience Academic
Author Li, Mei
Deng, Junge
Lin, Dongxin
Deng, Shuang
Ye, Ying
Zeng, Lingxing
Zhuang, Lisha
Zheng, Jian
Zhang, Jialiang
Huang, Xudong
Wu, Guandi
Bai, Ruihong
Su, Jiachun
Zuo, Zhixiang
Liu, Zexian
Li, Rui
Pan, Ling
Zhang, Shaoping
Lin, Junzhong
Zheng, Yanfen
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/34345012$$D View this record in MEDLINE/PubMed
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Snippet 5-Methylcytosine (m 5 C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain...
5-Methylcytosine (m C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear....
5-Methylcytosine (m.sup.5C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain...
5-Methylcytosine (m5C) is a posttranscriptional RNA modification participating in many critical bioprocesses, but its functions in human cancer remain unclear....
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StartPage 5814
SubjectTerms 1-Phosphatidylinositol 3-kinase
13/1
13/109
13/51
13/89
38/39
38/90
38/91
5-Methylcytosine - analogs & derivatives
5-Methylcytosine - metabolism
631/337/1645
631/337/176
631/67/1504/1477
64/110
82/58
AKT protein
Animal models
Animals
Apoptosis
Cancer
Cell Biology
Cell Line, Tumor
Development and progression
Disease Progression
E2F1 protein
Esophageal cancer
Esophageal Neoplasms - genetics
Esophageal Neoplasms - metabolism
Esophageal Neoplasms - pathology
Esophageal Squamous Cell Carcinoma - genetics
Esophageal Squamous Cell Carcinoma - metabolism
Esophageal Squamous Cell Carcinoma - pathology
Esophagus
Female
Gene Expression Regulation, Neoplastic
Genetic aspects
Genetic transcription
GRB2 Adaptor Protein - genetics
GRB2 Adaptor Protein - metabolism
Grb2 protein
Health aspects
Human Genetics
Humans
Internal Medicine
Male
MAP kinase
Medicine
Medicine & Public Health
Messenger RNA
Methylation
Methyltransferase
Methyltransferases
Methyltransferases - genetics
Methyltransferases - metabolism
Mice
Mice, Knockout
Oncology
Oncology, Experimental
Post-transcription
RNA modification
RNA Stability - genetics
RNA, Messenger - genetics
RNA, Messenger - metabolism
RNA-Binding Proteins - genetics
RNA-Binding Proteins - metabolism
Squamous cell carcinoma
Transcriptomes
Tumorigenesis
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Title NSUN2-mediated RNA 5-methylcytosine promotes esophageal squamous cell carcinoma progression via LIN28B-dependent GRB2 mRNA stabilization
URI https://link.springer.com/article/10.1038/s41388-021-01978-0
https://www.ncbi.nlm.nih.gov/pubmed/34345012
https://www.proquest.com/docview/2577913138
https://www.proquest.com/docview/2558088403
https://pubmed.ncbi.nlm.nih.gov/PMC8484015
Volume 40
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