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Identification of CircRNA signature associated with tumor immune infiltration to predict therapeutic efficacy of immunotherapy

Author

Listed:
  • Yu Dong

    (Furong Laboratory
    Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine
    Lin Gang Laboratory)

  • Qian Gao

    (Furong Laboratory
    Xiangya Hospital
    Xiangya Hospital, Central South University)

  • Yong Chen

    (Fudan University Shanghai Cancer Center
    Fudan University)

  • Zhao Zhang

    (McGovern Medical School at The University of Texas Health Science Center at Houston
    Fudan University)

  • Yanhua Du

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Yuan Liu

    (McGovern Medical School at The University of Texas Health Science Center at Houston
    Texas A&M University
    Texas A&M University)

  • Guangxiong Zhang

    (Lin Gang Laboratory
    Xiangya Hospital)

  • Shengli Li

    (Shanghai Jiao Tong University School of Medicine (SJTU-SM))

  • Gaoyang Wang

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

  • Xiang Chen

    (Furong Laboratory
    Xiangya Hospital)

  • Hong Liu

    (Furong Laboratory
    Xiangya Hospital)

  • Leng Han

    (McGovern Medical School at The University of Texas Health Science Center at Houston
    Texas A&M University
    Texas A&M University)

  • Youqiong Ye

    (Shanghai Jiao Tong University School of Medicine
    Shanghai Jiao Tong University School of Medicine)

Abstract

Circular RNAs (circRNAs) play important roles in the regulation of cancer. However, the clinical implications and regulatory networks of circRNAs in cancer patients receiving immune checkpoint blockades (ICB) have not been fully elucidated. Here, we characterize circRNA expression profiles in two independent cohorts of 157 ICB-treated advanced melanoma patients and reveal overall overexpression of circRNAs in ICB non-responders in both pre-treatment and early during therapy. Then, we construct circRNA-miRNA-mRNA regulatory networks to reveal circRNA-related signaling pathways in the context of ICB treatment. Further, we construct an ICB-related circRNA signature (ICBcircSig) score model based on progression-free survival-related circRNAs to predict immunotherapy efficacy. Mechanistically, the overexpression of ICBcircSig circTMTC3 and circFAM117B could increase PD-L1 expression via the miR-142-5p/PD-L1 axis, thus reducing T cell activity and leading to immune escape. Overall, our study characterizes circRNA profiles and regulatory networks in ICB-treated patients, and highlights the clinical utility of circRNAs as predictive biomarkers of immunotherapy.

Suggested Citation

  • Yu Dong & Qian Gao & Yong Chen & Zhao Zhang & Yanhua Du & Yuan Liu & Guangxiong Zhang & Shengli Li & Gaoyang Wang & Xiang Chen & Hong Liu & Leng Han & Youqiong Ye, 2023. "Identification of CircRNA signature associated with tumor immune infiltration to predict therapeutic efficacy of immunotherapy," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38232-y
    DOI: 10.1038/s41467-023-38232-y
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    1. Sebastian Memczak & Marvin Jens & Antigoni Elefsinioti & Francesca Torti & Janna Krueger & Agnieszka Rybak & Luisa Maier & Sebastian D. Mackowiak & Lea H. Gregersen & Mathias Munschauer & Alexander Lo, 2013. "Circular RNAs are a large class of animal RNAs with regulatory potency," Nature, Nature, vol. 495(7441), pages 333-338, March.
    2. Jinyang Zhang & Shuai Chen & Jingwen Yang & Fangqing Zhao, 2020. "Accurate quantification of circular RNAs identifies extensive circular isoform switching events," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. Thomas B. Hansen & Trine I. Jensen & Bettina H. Clausen & Jesper B. Bramsen & Bente Finsen & Christian K. Damgaard & Jørgen Kjems, 2013. "Natural RNA circles function as efficient microRNA sponges," Nature, Nature, vol. 495(7441), pages 384-388, March.
    4. Friedman, Jerome H. & Hastie, Trevor & Tibshirani, Rob, 2010. "Regularization Paths for Generalized Linear Models via Coordinate Descent," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 33(i01).
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    1. Chi Zhou & Wenxin Li & Zhenxing Liang & Xianrui Wu & Sijing Cheng & Jianhong Peng & Kaixuan Zeng & Weihao Li & Ping Lan & Xin Yang & Li Xiong & Ziwei Zeng & Xiaobin Zheng & Liang Huang & Wenhua Fan & , 2024. "Mutant KRAS-activated circATXN7 fosters tumor immunoescape by sensitizing tumor-specific T cells to activation-induced cell death," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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