NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner

Background/Objectives: Head and neck squamous cell carcinoma (HNSCC) is a prevalent and aggressive cancer with high rates of metastasis and poor prognosis. Recent research highlights the role of 5-methylcytosine (m<sup>5</sup>C) in cancer progression. NSUN2, an m<sup>5</sup>C...

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Main Authors: Shuojin Huang, Congyuan Cao, Dongxiao Tang, Yiwen Liu, Wanhang Zhou, Lianlian Liu, Xin Zheng, Qianting He, Anxun Wang
Format: Article
Language:English
Published: MDPI AG 2024-11-01
Series:Biomedicines
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Online Access:https://www.mdpi.com/2227-9059/12/11/2533
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author Shuojin Huang
Congyuan Cao
Dongxiao Tang
Yiwen Liu
Wanhang Zhou
Lianlian Liu
Xin Zheng
Qianting He
Anxun Wang
author_facet Shuojin Huang
Congyuan Cao
Dongxiao Tang
Yiwen Liu
Wanhang Zhou
Lianlian Liu
Xin Zheng
Qianting He
Anxun Wang
author_sort Shuojin Huang
collection DOAJ
description Background/Objectives: Head and neck squamous cell carcinoma (HNSCC) is a prevalent and aggressive cancer with high rates of metastasis and poor prognosis. Recent research highlights the role of 5-methylcytosine (m<sup>5</sup>C) in cancer progression. NSUN2, an m<sup>5</sup>C methyltransferase, has been implicated in various cancers, but its role in HNSCC remains elusive. Methods: NSUN2 expression and its impact on HNSCC were analyzed by using clinical samples and bioinformatic analysis. m<sup>5</sup>C-Bis-Seq was used to assess changes in mRNA m<sup>5</sup>C modification and identify downstream targets. Both in vitro and vivo studies were performed to evaluate the impact of NSUN2 manipulation on tumor growth and metastasis. Results: Results indicated that NSUN2 was significantly upregulated in HNSCC tissues compared to normal tissues and was associated with poor prognosis. NSUN2 knockdown led to decreased cell proliferation, migration, and invasion in vitro and reduced tumorigenicity and lymph node metastasis in vivo. m<sup>5</sup>C-Bis-Seq revealed altered m<sup>5</sup>C-modification patterns upon NSUN2 knockdown, with LAMC2 identified as a key downstream target. Conclusions: NSUN2-mediated m<sup>5</sup>C-modification enhanced LAMC2 stability, promoting epithelial–mesenchymal transition (EMT) signaling pathways. These findings demonstrate that NSUN2 promotes the initiation and progression of HNSCC by stabilizing the LAMC2 transcript through m<sup>5</sup>C-dependent mechanisms, offering a promising epitranscriptomic-targeted therapeutic approach for HNSCC.
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spelling doaj-art-e7b238ce2a0f4bbba09dc7931de7037a2024-11-26T17:53:08ZengMDPI AGBiomedicines2227-90592024-11-011211253310.3390/biomedicines12112533NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent MannerShuojin Huang0Congyuan Cao1Dongxiao Tang2Yiwen Liu3Wanhang Zhou4Lianlian Liu5Xin Zheng6Qianting He7Anxun Wang8Department of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaDepartment of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaDepartment of Stomatology, The Third Affiliated Hospital, Sun Yat-sen University, Guangzhou 510630, ChinaDepartment of Endodontics, Stomatological Hospital, School of Stomatology, Southern Medical University, Guangzhou 510280, ChinaDepartment of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaDepartment of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaDepartment of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaDepartment of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaDepartment of Oral and Maxillofacial Surgery, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, ChinaBackground/Objectives: Head and neck squamous cell carcinoma (HNSCC) is a prevalent and aggressive cancer with high rates of metastasis and poor prognosis. Recent research highlights the role of 5-methylcytosine (m<sup>5</sup>C) in cancer progression. NSUN2, an m<sup>5</sup>C methyltransferase, has been implicated in various cancers, but its role in HNSCC remains elusive. Methods: NSUN2 expression and its impact on HNSCC were analyzed by using clinical samples and bioinformatic analysis. m<sup>5</sup>C-Bis-Seq was used to assess changes in mRNA m<sup>5</sup>C modification and identify downstream targets. Both in vitro and vivo studies were performed to evaluate the impact of NSUN2 manipulation on tumor growth and metastasis. Results: Results indicated that NSUN2 was significantly upregulated in HNSCC tissues compared to normal tissues and was associated with poor prognosis. NSUN2 knockdown led to decreased cell proliferation, migration, and invasion in vitro and reduced tumorigenicity and lymph node metastasis in vivo. m<sup>5</sup>C-Bis-Seq revealed altered m<sup>5</sup>C-modification patterns upon NSUN2 knockdown, with LAMC2 identified as a key downstream target. Conclusions: NSUN2-mediated m<sup>5</sup>C-modification enhanced LAMC2 stability, promoting epithelial–mesenchymal transition (EMT) signaling pathways. These findings demonstrate that NSUN2 promotes the initiation and progression of HNSCC by stabilizing the LAMC2 transcript through m<sup>5</sup>C-dependent mechanisms, offering a promising epitranscriptomic-targeted therapeutic approach for HNSCC.https://www.mdpi.com/2227-9059/12/11/2533NSUN2mRNA m<sup>5</sup>C modificationshead and neck squamous cell carcinomaLAMC2epithelial–mesenchymal transition
spellingShingle Shuojin Huang
Congyuan Cao
Dongxiao Tang
Yiwen Liu
Wanhang Zhou
Lianlian Liu
Xin Zheng
Qianting He
Anxun Wang
NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner
Biomedicines
NSUN2
mRNA m<sup>5</sup>C modifications
head and neck squamous cell carcinoma
LAMC2
epithelial–mesenchymal transition
title NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner
title_full NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner
title_fullStr NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner
title_full_unstemmed NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner
title_short NSUN2 Promotes Head and Neck Squamous Cell Carcinoma Progression by Targeting EMT-Related Gene LAMC2 in an m<sup>5</sup>C-YBX1-Dependent Manner
title_sort nsun2 promotes head and neck squamous cell carcinoma progression by targeting emt related gene lamc2 in an m sup 5 sup c ybx1 dependent manner
topic NSUN2
mRNA m<sup>5</sup>C modifications
head and neck squamous cell carcinoma
LAMC2
epithelial–mesenchymal transition
url https://www.mdpi.com/2227-9059/12/11/2533
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