Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway

Abstract Posttranscriptional modifications are involved in cancer progression. However, the function and regulatory mechanism of mRNA acetylation modification remains largely unknown. Here, we discover an unexpected role of N4-acetylcytidine (ac4C) RNA acetyltransferase NAT10 in reshaping the tumor...

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Main Authors: Wan-cheng Liu, Yi-hong Wei, Jin-feng Chen, Xiang-ling Xing, He-xiao Jia, Xin-yu Yang, Ying-jian Huang, Xiao-min Liu, Ke Xiao, Xiao-dong Guo, Can Can, A-min Zhang, Na He, Hai-lei Zhang, Dao-xin Ma
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60293-4
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author Wan-cheng Liu
Yi-hong Wei
Jin-feng Chen
Xiang-ling Xing
He-xiao Jia
Xin-yu Yang
Ying-jian Huang
Xiao-min Liu
Ke Xiao
Xiao-dong Guo
Can Can
A-min Zhang
Na He
Hai-lei Zhang
Dao-xin Ma
author_facet Wan-cheng Liu
Yi-hong Wei
Jin-feng Chen
Xiang-ling Xing
He-xiao Jia
Xin-yu Yang
Ying-jian Huang
Xiao-min Liu
Ke Xiao
Xiao-dong Guo
Can Can
A-min Zhang
Na He
Hai-lei Zhang
Dao-xin Ma
author_sort Wan-cheng Liu
collection DOAJ
description Abstract Posttranscriptional modifications are involved in cancer progression. However, the function and regulatory mechanism of mRNA acetylation modification remains largely unknown. Here, we discover an unexpected role of N4-acetylcytidine (ac4C) RNA acetyltransferase NAT10 in reshaping the tumor immune microenvironment. By analyzing patients’ data, we find that NAT10 is upregulated in tumor tissues, and negatively correlated with immune cell infiltration and overall survival. Loss of tumoral NAT10 enhances tumor-specific cellular immune response and suppresses tumor growth. Mechanistically, MYC is identified as a key downstream target of NAT10 via enhancing mRNA ac4C modification. Inhibition of NAT10 blocks the MYC/CDK2/DNMT1 pathway, enhances double-stranded RNA (dsRNA) formation, which triggers type I interferon response and improves tumor specific CD8+ T cell response in vivo. More importantly, the inhibition of NAT10, using either small molecule inhibitor (Remodelin) or PEI/PC7A/siNAT10 nanoparticles, synergize PD-1 blockade in elevating anti-tumor immune response and repressing tumor progression. Our findings thus uncover the crucial role of tumor-intrinsic NAT10 in tumor immune microenvironment, which represents a promising target for enhancing cancer immunotherapy.
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spelling doaj-art-c61d0b73f46f4eacb8bd477c49aeb9c92025-08-20T02:30:42ZengNature PortfolioNature Communications2041-17232025-06-0116112110.1038/s41467-025-60293-4Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathwayWan-cheng Liu0Yi-hong Wei1Jin-feng Chen2Xiang-ling Xing3He-xiao Jia4Xin-yu Yang5Ying-jian Huang6Xiao-min Liu7Ke Xiao8Xiao-dong Guo9Can Can10A-min Zhang11Na He12Hai-lei Zhang13Dao-xin Ma14Department of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversitySuzhou Institute of Nano-Tech and Nano-Bionics (SINANO), Chinese Academy of SciencesDepartment of Radiation Oncology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Dermatology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Clinical Laboratory, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityDepartment of Hematology, Qilu Hospital of Shandong UniversityAbstract Posttranscriptional modifications are involved in cancer progression. However, the function and regulatory mechanism of mRNA acetylation modification remains largely unknown. Here, we discover an unexpected role of N4-acetylcytidine (ac4C) RNA acetyltransferase NAT10 in reshaping the tumor immune microenvironment. By analyzing patients’ data, we find that NAT10 is upregulated in tumor tissues, and negatively correlated with immune cell infiltration and overall survival. Loss of tumoral NAT10 enhances tumor-specific cellular immune response and suppresses tumor growth. Mechanistically, MYC is identified as a key downstream target of NAT10 via enhancing mRNA ac4C modification. Inhibition of NAT10 blocks the MYC/CDK2/DNMT1 pathway, enhances double-stranded RNA (dsRNA) formation, which triggers type I interferon response and improves tumor specific CD8+ T cell response in vivo. More importantly, the inhibition of NAT10, using either small molecule inhibitor (Remodelin) or PEI/PC7A/siNAT10 nanoparticles, synergize PD-1 blockade in elevating anti-tumor immune response and repressing tumor progression. Our findings thus uncover the crucial role of tumor-intrinsic NAT10 in tumor immune microenvironment, which represents a promising target for enhancing cancer immunotherapy.https://doi.org/10.1038/s41467-025-60293-4
spellingShingle Wan-cheng Liu
Yi-hong Wei
Jin-feng Chen
Xiang-ling Xing
He-xiao Jia
Xin-yu Yang
Ying-jian Huang
Xiao-min Liu
Ke Xiao
Xiao-dong Guo
Can Can
A-min Zhang
Na He
Hai-lei Zhang
Dao-xin Ma
Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway
Nature Communications
title Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway
title_full Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway
title_fullStr Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway
title_full_unstemmed Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway
title_short Inhibition of tumor-intrinsic NAT10 enhances antitumor immunity by triggering type I interferon response via MYC/CDK2/DNMT1 pathway
title_sort inhibition of tumor intrinsic nat10 enhances antitumor immunity by triggering type i interferon response via myc cdk2 dnmt1 pathway
url https://doi.org/10.1038/s41467-025-60293-4
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