IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38232-y.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38232-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38232-y?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    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).
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Bin Li & Wen-Wu Bai & Tao Guo & Zhen-Yu Tang & Xue-Jiao Jing & Ti-Chao Shan & Sen Yin & Ying Li & Fu Wang & Mo-Li Zhu & Jun-Xiu Lu & Yong-Ping Bai & Bo Dong & Peng Li & Shuang-Xi Wang, 2024. "Statins improve cardiac endothelial function to prevent heart failure with preserved ejection fraction through upregulating circRNA-RBCK1," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Roberta Piras & Emily Y. Ko & Connor Barrett & Marco Simone & Xianzhi Lin & Marina T. Broz & Fernando H. G. Tessaro & Mireia Castillo-Martin & Carlos Cordon-Cardo & Helen S. Goodridge & Dolores Vizio , 2022. "circCsnk1g3- and circAnkib1-regulated interferon responses in sarcoma promote tumorigenesis by shaping the immune microenvironment," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Zhenzhen Chen & Qiankun He & Tiankun Lu & Jiayi Wu & Gaoli Shi & Luyun He & Hong Zong & Benyu Liu & Pingping Zhu, 2023. "mcPGK1-dependent mitochondrial import of PGK1 promotes metabolic reprogramming and self-renewal of liver TICs," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    4. Ting-Ting He & Yun-Fan Xu & Xiang Li & Xia Wang & Jie-Yu Li & Dan Ou-Yang & Han-Sen Cheng & Hao-Yang Li & Jia Qin & Yu Huang & Hai-Yan Wang, 2023. "A linear and circular dual-conformation noncoding RNA involved in oxidative stress tolerance in Bacillus altitudinis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Steffen Fuchs & Clara Danßmann & Filippos Klironomos & Annika Winkler & Jörg Fallmann & Louisa-Marie Kruetzfeldt & Annabell Szymansky & Julian Naderi & Stephan H. Bernhart & Laura Grunewald & Konstant, 2023. "Defining the landscape of circular RNAs in neuroblastoma unveils a global suppressive function of MYCN," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    6. Xiaojuan Fan & Yun Yang & Chuyun Chen & Zefeng Wang, 2022. "Pervasive translation of circular RNAs driven by short IRES-like elements," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Federica Conte & Giulia Fiscon & Matteo Chiara & Teresa Colombo & Lorenzo Farina & Paola Paci, 2017. "Role of the long non-coding RNA PVT1 in the dysregulation of the ceRNA-ceRNA network in human breast cancer," PLOS ONE, Public Library of Science, vol. 12(2), pages 1-22, February.
    8. Jian Zhong & Xujia Wu & Yixin Gao & Junju Chen & Maolei Zhang & Huangkai Zhou & Jia Yang & Feizhe Xiao & Xuesong Yang & Nunu Huang & Haoyue Qi & Xiuxing Wang & Fan Bai & Yu Shi & Nu Zhang, 2023. "Circular RNA encoded MET variant promotes glioblastoma tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Tutz, Gerhard & Pößnecker, Wolfgang & Uhlmann, Lorenz, 2015. "Variable selection in general multinomial logit models," Computational Statistics & Data Analysis, Elsevier, vol. 82(C), pages 207-222.
    10. Rui Wang & Naihua Xiu & Kim-Chuan Toh, 2021. "Subspace quadratic regularization method for group sparse multinomial logistic regression," Computational Optimization and Applications, Springer, vol. 79(3), pages 531-559, July.
    11. Mkhadri, Abdallah & Ouhourane, Mohamed, 2013. "An extended variable inclusion and shrinkage algorithm for correlated variables," Computational Statistics & Data Analysis, Elsevier, vol. 57(1), pages 631-644.
    12. Chen, Le-Yu & Lee, Sokbae, 2018. "Best subset binary prediction," Journal of Econometrics, Elsevier, vol. 206(1), pages 39-56.
    13. Sung Jae Jun & Sokbae Lee, 2020. "Causal Inference under Outcome-Based Sampling with Monotonicity Assumptions," Papers 2004.08318, arXiv.org, revised Oct 2023.
    14. Xiangwei Li & Thomas Delerue & Ben Schöttker & Bernd Holleczek & Eva Grill & Annette Peters & Melanie Waldenberger & Barbara Thorand & Hermann Brenner, 2022. "Derivation and validation of an epigenetic frailty risk score in population-based cohorts of older adults," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    15. Christopher J Greenwood & George J Youssef & Primrose Letcher & Jacqui A Macdonald & Lauryn J Hagg & Ann Sanson & Jenn Mcintosh & Delyse M Hutchinson & John W Toumbourou & Matthew Fuller-Tyszkiewicz &, 2020. "A comparison of penalised regression methods for informing the selection of predictive markers," PLOS ONE, Public Library of Science, vol. 15(11), pages 1-14, November.
    16. Heng Chen & Daniel F. Heitjan, 2022. "Analysis of local sensitivity to nonignorability with missing outcomes and predictors," Biometrics, The International Biometric Society, vol. 78(4), pages 1342-1352, December.
    17. S Ariane Christie & Amanda S Conroy & Rachael A Callcut & Alan E Hubbard & Mitchell J Cohen, 2019. "Dynamic multi-outcome prediction after injury: Applying adaptive machine learning for precision medicine in trauma," PLOS ONE, Public Library of Science, vol. 14(4), pages 1-13, April.
    18. Zhu Wang, 2022. "MM for penalized estimation," TEST: An Official Journal of the Spanish Society of Statistics and Operations Research, Springer;Sociedad de Estadística e Investigación Operativa, vol. 31(1), pages 54-75, March.
    19. Ida Kubiszewski & Kenneth Mulder & Diane Jarvis & Robert Costanza, 2022. "Toward better measurement of sustainable development and wellbeing: A small number of SDG indicators reliably predict life satisfaction," Sustainable Development, John Wiley & Sons, Ltd., vol. 30(1), pages 139-148, February.
    20. Gustavo A. Alonso-Silverio & Víctor Francisco-García & Iris P. Guzmán-Guzmán & Elías Ventura-Molina & Antonio Alarcón-Paredes, 2021. "Toward Non-Invasive Estimation of Blood Glucose Concentration: A Comparative Performance," Mathematics, MDPI, vol. 9(20), pages 1-13, October.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38232-y. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.