Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1

Abstract Platelets play a critical role in tumor progression across various cancers. However, little is known about the molecular mechanisms and biological roles of exosomal long non-coding RNAs (lncRNAs) produced from platelets in colorectal cancer (CRC). Using RNA sequencing, we identified LINC001...

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Main Authors: Guoqing Su, Jinghang Qian, Yi Wang, Yu Zhu, Yanyan Chen, Jingru Shen, Jiayuan Jiang, Yuepeng Cao, Nannan Wang, Xing Huang, Chengshuai Si, Xu Zhang, Peng Shao, Yongxia Ye, Yang Wang, Jun Bao, Liu Yang
Format: Article
Language:English
Published: Nature Publishing Group 2025-08-01
Series:Cell Death and Disease
Online Access:https://doi.org/10.1038/s41419-025-07914-4
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author Guoqing Su
Jinghang Qian
Yi Wang
Yu Zhu
Yanyan Chen
Jingru Shen
Jiayuan Jiang
Yuepeng Cao
Nannan Wang
Xing Huang
Chengshuai Si
Xu Zhang
Peng Shao
Yongxia Ye
Yang Wang
Jun Bao
Liu Yang
author_facet Guoqing Su
Jinghang Qian
Yi Wang
Yu Zhu
Yanyan Chen
Jingru Shen
Jiayuan Jiang
Yuepeng Cao
Nannan Wang
Xing Huang
Chengshuai Si
Xu Zhang
Peng Shao
Yongxia Ye
Yang Wang
Jun Bao
Liu Yang
author_sort Guoqing Su
collection DOAJ
description Abstract Platelets play a critical role in tumor progression across various cancers. However, little is known about the molecular mechanisms and biological roles of exosomal long non-coding RNAs (lncRNAs) produced from platelets in colorectal cancer (CRC). Using RNA sequencing, we identified LINC00183 as the most upregulated lncRNA in platelet-derived exosomes (PLT-Exos) from CRC patients, compared to healthy individuals. Analysis of CRC tissue microarrays and TCGA-CRC patient data indicated that LINC00183 is often overexpressed in CRC, in association with advanced tumor stage and poor survival. Effective transfer of exosomal LINC00183 to human CRC cells was verified by FISH, western blotting, and RT-qPCR analyses. Co-incubation with PLT-Exos from CRC patients and overexpression of LINC00183 stimulated the proliferative and invasive capacities of CRC cells. RNA pull-down and RNA immunoprecipitation assays revealed that LINC00183 interacts with enolase 1 (ENO1). This interaction rescues ENO1 from ubiquitin-proteasome-mediated degradation by masking a critical K262 residue. Co-immunoprecipitation, western blotting, CUT&Tag, and gene knockdown and overexpression assays further revealed that the LINC00183-ENO1 interaction activates glycolysis in CRC cells, leading to lactate accumulation, H3K18 lactylation, and transcriptional upregulation of the oncogene GDF15. These results highlight LINC00183 as a possible therapeutic target for CRC.
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spelling doaj-art-2ea1b94eabd44b7c82f93650ab33a4f42025-08-20T03:42:10ZengNature Publishing GroupCell Death and Disease2041-48892025-08-0116111810.1038/s41419-025-07914-4Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1Guoqing Su0Jinghang Qian1Yi Wang2Yu Zhu3Yanyan Chen4Jingru Shen5Jiayuan Jiang6Yuepeng Cao7Nannan Wang8Xing Huang9Chengshuai Si10Xu Zhang11Peng Shao12Yongxia Ye13Yang Wang14Jun Bao15Liu Yang16Department of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Medical Oncology, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Medical Oncology, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Medical Oncology, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchGastrointestinal Surgery, Beijing Shijitan Hospital, Capital Medical UniversityDepartment of Pathology, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Medical Oncology, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Medical Oncology, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchDepartment of Colorectal Surgery, The Affiliated Cancer Hospital of Nanjing Medical University & Jiangsu Cancer Hospital & Jiangsu Institute of Cancer ResearchAbstract Platelets play a critical role in tumor progression across various cancers. However, little is known about the molecular mechanisms and biological roles of exosomal long non-coding RNAs (lncRNAs) produced from platelets in colorectal cancer (CRC). Using RNA sequencing, we identified LINC00183 as the most upregulated lncRNA in platelet-derived exosomes (PLT-Exos) from CRC patients, compared to healthy individuals. Analysis of CRC tissue microarrays and TCGA-CRC patient data indicated that LINC00183 is often overexpressed in CRC, in association with advanced tumor stage and poor survival. Effective transfer of exosomal LINC00183 to human CRC cells was verified by FISH, western blotting, and RT-qPCR analyses. Co-incubation with PLT-Exos from CRC patients and overexpression of LINC00183 stimulated the proliferative and invasive capacities of CRC cells. RNA pull-down and RNA immunoprecipitation assays revealed that LINC00183 interacts with enolase 1 (ENO1). This interaction rescues ENO1 from ubiquitin-proteasome-mediated degradation by masking a critical K262 residue. Co-immunoprecipitation, western blotting, CUT&Tag, and gene knockdown and overexpression assays further revealed that the LINC00183-ENO1 interaction activates glycolysis in CRC cells, leading to lactate accumulation, H3K18 lactylation, and transcriptional upregulation of the oncogene GDF15. These results highlight LINC00183 as a possible therapeutic target for CRC.https://doi.org/10.1038/s41419-025-07914-4
spellingShingle Guoqing Su
Jinghang Qian
Yi Wang
Yu Zhu
Yanyan Chen
Jingru Shen
Jiayuan Jiang
Yuepeng Cao
Nannan Wang
Xing Huang
Chengshuai Si
Xu Zhang
Peng Shao
Yongxia Ye
Yang Wang
Jun Bao
Liu Yang
Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1
Cell Death and Disease
title Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1
title_full Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1
title_fullStr Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1
title_full_unstemmed Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1
title_short Platelet-derived exosomal LINC00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing ENO1
title_sort platelet derived exosomal linc00183 facilitate colorectal cancer malignant progression driven by histone lactylation through stabilizing eno1
url https://doi.org/10.1038/s41419-025-07914-4
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