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LncRNA CACClnc promotes chemoresistance of colorectal cancer by modulating alternative splicing of RAD51

Oncogene volume 42, pages 1374–1391 (2023)Cite this article

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Abstract

Long non-coding RNAs (lncRNAs) play important roles in carcinogenesis. However, the effect of lncRNA on chemoresistance and RNA alternative splicing remains largely unknown. In this study, we identified a novel lncRNA, CACClnc, which was upregulated and associated with chemoresistance and poor prognosis in colorectal cancer (CRC). CACClnc promoted CRC resistance to chemotherapy via promoting DNA repair and enhancing homologous recombination in vitro and in vivo. Mechanistically, CACClnc specifically bound to Y-box binding protein 1 (YB1, a splicing factor) and U2AF65 (a subunit of U2AF splicing factor), promoting the interaction between YB1 and U2AF65, and then modulated alternative splicing (AS) of RAD51 mRNA, and consequently altered CRC cell biology. In addition, expression of exosomal CACClnc in peripheral plasma of CRC patients can effectively predict the chemotherapy effect of patients before treatment. Thus, measuring and targeting CACClnc and its associated pathway could yield valuable insight into clinical management and might ameliorate CRC patients’ outcomes.

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Fig. 1: CACClnc is associated with chemotherapy response and recurrence of CRC patients.
Fig. 2: CACClnc promotes chemoresistance in CRC.
Fig. 3: CACClnc is regulated by m6A modification in CRC cells.
Fig. 4: CACClnc promotes chemoresistance and is involved in homologous recombination repair in CRC.
Fig. 5: YB1 is responsible for CACClnc mediated chemoresistance.
Fig. 6: CACClnc inhibits aberrant RNA splicing of RAD51.
Fig. 7: CACClnc inhibits aberrant alternative splicing (AS) of RAD51 via binding with YB1 and U2AF65.
Fig. 8: RAD51 participates in CACClnc-mediated chemoresistance.

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Data availability

The RNA sequence data have been deposited in NCBI’s Gene Expression Omnibus (GEO, http://www.ncbi.nlm.nih.gov/geo/) and are accessible through GEO Series accession number GSE158559.

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Acknowledgements

This work was supported by National Natural Science Foundation (82230016, 82272979, 82073115, 81891901, 82200603); Shanghai Municipal Education Commission—Gaofeng Clinical Medicine Grant Support (No.20152512, 20161309); Guangzhou Municipality Bureau of Science and Technology (No.202201020281).

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  1. These authors contributed equally: Xinyu Zhang, Dan Ma, Baoqin Xuan, Debing Shi, Jie He, Minhao Yu, Hua Xiong.

Authors and Affiliations

  1. State Key Laboratory for Oncogenes and Related Genes, NHC Key Laboratory of Digestive Diseases, Division of Gastroenterology and Hepatology, Shanghai Institute of Digestive Disease, Shanghai Cancer Institute, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China

    Xinyu Zhang, Dan Ma, Baoqin Xuan, Hua Xiong, Yanru Ma, Chaoqin Shen, Fangfang Guo, Yingying Cao, Yuqing Yan, Ziyun Gao, Tianying Tong, Xiaoqiang Zhu, Jing-Yuan Fang, Haoyan Chen & Jie Hong

  2. Department of Gastroenterology, the First Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, China

    Dan Ma

  3. Department of Colorectal Surgery, Fudan University Shanghai Cancer Center, Shanghai, China

    Debing Shi

  4. Department of Oncology, Shanghai Medical College, Fudan University, Shanghai, China

    Debing Shi

  5. Guangzhou Key Laboratory of Digestive Disease, Guangzhou Digestive Disease Center, Guangzhou First People’s Hospital and The Second Affiliated Hospital, South China University of Technology School of Medicine, Guangzhou, China

    Jie He

  6. Department of Gastrointestinal Surgery, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China

    Minhao Yu

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Contributions

JH, HYC designed the experiments; XYZ, DM, BQX, DBS, JH, MHY conducted the experiments; XYZ wrote the original draft; JH, BQX and HYC reviewed and edited the paper.

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Correspondence to Haoyan Chen or Jie Hong.

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Zhang, X., Ma, D., Xuan, B. et al. LncRNA CACClnc promotes chemoresistance of colorectal cancer by modulating alternative splicing of RAD51. Oncogene 42, 1374–1391 (2023). https://doi.org/10.1038/s41388-023-02657-y

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