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The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer

Colorectal cancer (CRC) patients with liver metastases usually obtain less benefit from immunotherapy, and the underlying mechanisms remain understudied. Here, we identify that fibrinogen-like protein 1 (FGL1), secreted from cancer cells and hepatocytes, facilitates the progression of CRC in an intr...

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Autores principales: Li, Jia-Jun, Wang, Jin-Hong, Tian, Tian, Liu, Jia, Zheng, Yong-Qiang, Mo, Hai-Yu, Sheng, Hui, Chen, Yan-Xing, Wu, Qi-Nian, Han, Yi, Liao, Kun, Pan, Yi-Qian, Zeng, Zhao-Lei, Liu, Ze-Xian, Yang, Wei, Xu, Rui-Hua, Ju, Huai-Qiang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10593839/
https://www.ncbi.nlm.nih.gov/pubmed/37872170
http://dx.doi.org/10.1038/s41467-023-42332-0
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author Li, Jia-Jun
Wang, Jin-Hong
Tian, Tian
Liu, Jia
Zheng, Yong-Qiang
Mo, Hai-Yu
Sheng, Hui
Chen, Yan-Xing
Wu, Qi-Nian
Han, Yi
Liao, Kun
Pan, Yi-Qian
Zeng, Zhao-Lei
Liu, Ze-Xian
Yang, Wei
Xu, Rui-Hua
Ju, Huai-Qiang
author_facet Li, Jia-Jun
Wang, Jin-Hong
Tian, Tian
Liu, Jia
Zheng, Yong-Qiang
Mo, Hai-Yu
Sheng, Hui
Chen, Yan-Xing
Wu, Qi-Nian
Han, Yi
Liao, Kun
Pan, Yi-Qian
Zeng, Zhao-Lei
Liu, Ze-Xian
Yang, Wei
Xu, Rui-Hua
Ju, Huai-Qiang
author_sort Li, Jia-Jun
collection PubMed
description Colorectal cancer (CRC) patients with liver metastases usually obtain less benefit from immunotherapy, and the underlying mechanisms remain understudied. Here, we identify that fibrinogen-like protein 1 (FGL1), secreted from cancer cells and hepatocytes, facilitates the progression of CRC in an intraportal injection model by reducing the infiltration of T cells. Mechanistically, tumor-associated macrophages (TAMs) activate NF-ĸB by secreting TNFα/IL-1β in the liver microenvironment and transcriptionally upregulate OTU deubiquitinase 1 (OTUD1) expression, which enhances FGL1 stability via deubiquitination. Disrupting the TAM-OTUD1-FGL1 axis inhibits metastatic tumor progression and synergizes with immune checkpoint blockade (ICB) therapy. Clinically, high plasma FGL1 levels predict poor outcomes and reduced ICB therapy benefits. Benzethonium chloride, an FDA-approved antiseptics, curbs FGL1 secretion, thereby inhibiting liver metastatic tumor growth. Overall, this study uncovers the critical roles and posttranslational regulatory mechanism of FGL1 in promoting metastatic tumor progression, highlighting the TAM-OTUD1-FGL1 axis as a potential target for cancer immunotherapy.
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spelling pubmed-105938392023-10-25 The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer Li, Jia-Jun Wang, Jin-Hong Tian, Tian Liu, Jia Zheng, Yong-Qiang Mo, Hai-Yu Sheng, Hui Chen, Yan-Xing Wu, Qi-Nian Han, Yi Liao, Kun Pan, Yi-Qian Zeng, Zhao-Lei Liu, Ze-Xian Yang, Wei Xu, Rui-Hua Ju, Huai-Qiang Nat Commun Article Colorectal cancer (CRC) patients with liver metastases usually obtain less benefit from immunotherapy, and the underlying mechanisms remain understudied. Here, we identify that fibrinogen-like protein 1 (FGL1), secreted from cancer cells and hepatocytes, facilitates the progression of CRC in an intraportal injection model by reducing the infiltration of T cells. Mechanistically, tumor-associated macrophages (TAMs) activate NF-ĸB by secreting TNFα/IL-1β in the liver microenvironment and transcriptionally upregulate OTU deubiquitinase 1 (OTUD1) expression, which enhances FGL1 stability via deubiquitination. Disrupting the TAM-OTUD1-FGL1 axis inhibits metastatic tumor progression and synergizes with immune checkpoint blockade (ICB) therapy. Clinically, high plasma FGL1 levels predict poor outcomes and reduced ICB therapy benefits. Benzethonium chloride, an FDA-approved antiseptics, curbs FGL1 secretion, thereby inhibiting liver metastatic tumor growth. Overall, this study uncovers the critical roles and posttranslational regulatory mechanism of FGL1 in promoting metastatic tumor progression, highlighting the TAM-OTUD1-FGL1 axis as a potential target for cancer immunotherapy. Nature Publishing Group UK 2023-10-23 /pmc/articles/PMC10593839/ /pubmed/37872170 http://dx.doi.org/10.1038/s41467-023-42332-0 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Jia-Jun
Wang, Jin-Hong
Tian, Tian
Liu, Jia
Zheng, Yong-Qiang
Mo, Hai-Yu
Sheng, Hui
Chen, Yan-Xing
Wu, Qi-Nian
Han, Yi
Liao, Kun
Pan, Yi-Qian
Zeng, Zhao-Lei
Liu, Ze-Xian
Yang, Wei
Xu, Rui-Hua
Ju, Huai-Qiang
The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer
title The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer
title_full The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer
title_fullStr The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer
title_full_unstemmed The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer
title_short The liver microenvironment orchestrates FGL1-mediated immune escape and progression of metastatic colorectal cancer
title_sort liver microenvironment orchestrates fgl1-mediated immune escape and progression of metastatic colorectal cancer
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10593839/
https://www.ncbi.nlm.nih.gov/pubmed/37872170
http://dx.doi.org/10.1038/s41467-023-42332-0
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