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Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation

The recently described role of RNA methylation in regulating immune cell infiltration into tumors has attracted interest, given its potential impact on immunotherapy response. YTHDF1 is a versatile and powerful m6A reader, but the understanding of its impact on immune evasion is limited. Here, we re...

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Autores principales: Lin, Wanzun, Chen, Li, Zhang, Haojiong, Qiu, Xianxin, Huang, Qingting, Wan, Fangzhu, Le, Ziyu, Geng, Shikai, Zhang, Anlan, Qiu, Sufang, Chen, Long, Kong, Lin, Lu, Jiade J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9845301/
https://www.ncbi.nlm.nih.gov/pubmed/36650153
http://dx.doi.org/10.1038/s41467-022-35710-7
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author Lin, Wanzun
Chen, Li
Zhang, Haojiong
Qiu, Xianxin
Huang, Qingting
Wan, Fangzhu
Le, Ziyu
Geng, Shikai
Zhang, Anlan
Qiu, Sufang
Chen, Long
Kong, Lin
Lu, Jiade J.
author_facet Lin, Wanzun
Chen, Li
Zhang, Haojiong
Qiu, Xianxin
Huang, Qingting
Wan, Fangzhu
Le, Ziyu
Geng, Shikai
Zhang, Anlan
Qiu, Sufang
Chen, Long
Kong, Lin
Lu, Jiade J.
author_sort Lin, Wanzun
collection PubMed
description The recently described role of RNA methylation in regulating immune cell infiltration into tumors has attracted interest, given its potential impact on immunotherapy response. YTHDF1 is a versatile and powerful m6A reader, but the understanding of its impact on immune evasion is limited. Here, we reveal that tumor-intrinsic YTHDF1 drives immune evasion and immune checkpoint inhibitor (ICI) resistance. Additionally, YTHDF1 deficiency converts cold tumors into responsive hot tumors, which improves ICI efficacy. Mechanistically, YTHDF1 deficiency inhibits the translation of lysosomal genes and limits lysosomal proteolysis of the major histocompatibility complex class I (MHC-I) and antigens, ultimately restoring tumor immune surveillance. In addition, we design a system for exosome-mediated CRISPR/Cas9 delivery to target YTHDF1 in vivo, resulting in YTHDF1 depletion and antitumor activity. Our findings elucidate the role of tumor-intrinsic YTHDF1 in driving immune evasion and its underlying mechanism.
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spelling pubmed-98453012023-01-19 Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation Lin, Wanzun Chen, Li Zhang, Haojiong Qiu, Xianxin Huang, Qingting Wan, Fangzhu Le, Ziyu Geng, Shikai Zhang, Anlan Qiu, Sufang Chen, Long Kong, Lin Lu, Jiade J. Nat Commun Article The recently described role of RNA methylation in regulating immune cell infiltration into tumors has attracted interest, given its potential impact on immunotherapy response. YTHDF1 is a versatile and powerful m6A reader, but the understanding of its impact on immune evasion is limited. Here, we reveal that tumor-intrinsic YTHDF1 drives immune evasion and immune checkpoint inhibitor (ICI) resistance. Additionally, YTHDF1 deficiency converts cold tumors into responsive hot tumors, which improves ICI efficacy. Mechanistically, YTHDF1 deficiency inhibits the translation of lysosomal genes and limits lysosomal proteolysis of the major histocompatibility complex class I (MHC-I) and antigens, ultimately restoring tumor immune surveillance. In addition, we design a system for exosome-mediated CRISPR/Cas9 delivery to target YTHDF1 in vivo, resulting in YTHDF1 depletion and antitumor activity. Our findings elucidate the role of tumor-intrinsic YTHDF1 in driving immune evasion and its underlying mechanism. Nature Publishing Group UK 2023-01-17 /pmc/articles/PMC9845301/ /pubmed/36650153 http://dx.doi.org/10.1038/s41467-022-35710-7 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Lin, Wanzun
Chen, Li
Zhang, Haojiong
Qiu, Xianxin
Huang, Qingting
Wan, Fangzhu
Le, Ziyu
Geng, Shikai
Zhang, Anlan
Qiu, Sufang
Chen, Long
Kong, Lin
Lu, Jiade J.
Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation
title Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation
title_full Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation
title_fullStr Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation
title_full_unstemmed Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation
title_short Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation
title_sort tumor-intrinsic ythdf1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting mhc-i degradation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9845301/
https://www.ncbi.nlm.nih.gov/pubmed/36650153
http://dx.doi.org/10.1038/s41467-022-35710-7
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