m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer

Background: Altered lipid metabolism is a well-known hallmark of cancer. However, the underlying mechanisms of altered lipid metabolism in colorectal cancer (CRC) progression requires further investigation. Previously we have revealed that DEAD-box RNA helicase 21 (DDX21) promotes CRC metastasis via...

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Main Authors: Huabin Gao, Shuai Zheng, Jiangtao Liang, Yuting Wang, Lin Chen, Hui Li, Yongyu Chen, Fenfen Zhang, Huijuan Shi, Anjia Han
Format: Article
Language:English
Published: Elsevier 2025-05-01
Series:Translational Oncology
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Online Access:http://www.sciencedirect.com/science/article/pii/S1936523325001044
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author Huabin Gao
Shuai Zheng
Jiangtao Liang
Yuting Wang
Lin Chen
Hui Li
Yongyu Chen
Fenfen Zhang
Huijuan Shi
Anjia Han
author_facet Huabin Gao
Shuai Zheng
Jiangtao Liang
Yuting Wang
Lin Chen
Hui Li
Yongyu Chen
Fenfen Zhang
Huijuan Shi
Anjia Han
author_sort Huabin Gao
collection DOAJ
description Background: Altered lipid metabolism is a well-known hallmark of cancer. However, the underlying mechanisms of altered lipid metabolism in colorectal cancer (CRC) progression requires further investigation. Previously we have revealed that DEAD-box RNA helicase 21 (DDX21) promotes CRC metastasis via liquid-liquid phase separation. In this study, we identify DDX21 as a novel regulator of lipid metabolism in CRC. Methods: In vitro and in vivo assays illustrated the biological role of DDX21 and YTH N6-methyladenosine RNA binding protein 1 (YTHDF1) in CRC lipid metabolism and progression. Bioinformatics analysis, ChIP, meRIP, RIP, RNA stability assay and dual-luciferase reporter assay were applied to explore the underlying molecular mechanisms. The expression levels and prognostic role of YTHDF1/DDX21/HMGCS1 axis in CRC patients were analyzed by immunohistochemical staining and Kaplan-Meier plotter. Results: DDX21 enhanced CRC progression via promoting lipid metabolism. Mechanistically, YTHDF1 enhanced DDX21 mRNA stability by recognizing its m6A-modified sites. DDX21 further binded to 3‑hydroxy-3-methylglutaryl-CoA synthase 1 (HMGCS1) promoter region and directly activated HMGCS1 transcription. Moreover, our clinical data showed that a simultaneously high expression of YTHDF1, DDX21 and HMGCS1 predicted an unfavorable overall survival in CRC patients. Conclusions: Our study demonstrates that the YTHDF1/DDX21/HMGCS1 axis promotes CRC progression via regulating lipid metabolism and DDX21 might be a promising target for CRC therapy.
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spelling doaj-art-09bc6ff65e9e4b1ab2b0eba73e98bf332025-08-20T03:03:27ZengElsevierTranslational Oncology1936-52332025-05-015510237310.1016/j.tranon.2025.102373m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancerHuabin Gao0Shuai Zheng1Jiangtao Liang2Yuting Wang3Lin Chen4Hui Li5Yongyu Chen6Fenfen Zhang7Huijuan Shi8Anjia Han9Department of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaDepartment of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaCorresponding authors at: Department of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, 58, Zhongshan Road II, Guangzhou 510080, China.; Department of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaCorresponding authors at: Department of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, 58, Zhongshan Road II, Guangzhou 510080, China.; Department of Pathology, the First Affiliated Hospital, Sun Yat-Sen University, Guangzhou 510080, ChinaBackground: Altered lipid metabolism is a well-known hallmark of cancer. However, the underlying mechanisms of altered lipid metabolism in colorectal cancer (CRC) progression requires further investigation. Previously we have revealed that DEAD-box RNA helicase 21 (DDX21) promotes CRC metastasis via liquid-liquid phase separation. In this study, we identify DDX21 as a novel regulator of lipid metabolism in CRC. Methods: In vitro and in vivo assays illustrated the biological role of DDX21 and YTH N6-methyladenosine RNA binding protein 1 (YTHDF1) in CRC lipid metabolism and progression. Bioinformatics analysis, ChIP, meRIP, RIP, RNA stability assay and dual-luciferase reporter assay were applied to explore the underlying molecular mechanisms. The expression levels and prognostic role of YTHDF1/DDX21/HMGCS1 axis in CRC patients were analyzed by immunohistochemical staining and Kaplan-Meier plotter. Results: DDX21 enhanced CRC progression via promoting lipid metabolism. Mechanistically, YTHDF1 enhanced DDX21 mRNA stability by recognizing its m6A-modified sites. DDX21 further binded to 3‑hydroxy-3-methylglutaryl-CoA synthase 1 (HMGCS1) promoter region and directly activated HMGCS1 transcription. Moreover, our clinical data showed that a simultaneously high expression of YTHDF1, DDX21 and HMGCS1 predicted an unfavorable overall survival in CRC patients. Conclusions: Our study demonstrates that the YTHDF1/DDX21/HMGCS1 axis promotes CRC progression via regulating lipid metabolism and DDX21 might be a promising target for CRC therapy.http://www.sciencedirect.com/science/article/pii/S1936523325001044DDX21Colorectal cancerLipid metabolism
spellingShingle Huabin Gao
Shuai Zheng
Jiangtao Liang
Yuting Wang
Lin Chen
Hui Li
Yongyu Chen
Fenfen Zhang
Huijuan Shi
Anjia Han
m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer
Translational Oncology
DDX21
Colorectal cancer
Lipid metabolism
title m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer
title_full m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer
title_fullStr m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer
title_full_unstemmed m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer
title_short m6A-induced DEAD-box RNA helicase 21 enhances lipid metabolism via 3‑hydroxy-3-methylglutaryl-CoA synthases 1 in colorectal cancer
title_sort m6a induced dead box rna helicase 21 enhances lipid metabolism via 3 hydroxy 3 methylglutaryl coa synthases 1 in colorectal cancer
topic DDX21
Colorectal cancer
Lipid metabolism
url http://www.sciencedirect.com/science/article/pii/S1936523325001044
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