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Mutation characteristics and molecular evolution of ovarian metastasis from gastric cancer and potential biomarkers for paclitaxel treatment

Author

Listed:
  • Pengfei Yu

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Can Hu

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Guangyu Ding

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Xiaoliang Shi

    (Ltd)

  • Jingli Xu

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Yang Cao

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Xiangliu Chen

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Wei Wu

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Qi Xu

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Jingquan Fang

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Xingmao Huang

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Shaohua Yuan

    (Ltd)

  • Hui Chen

    (Ltd)

  • Zhizheng Wang

    (Ltd)

  • Ling Huang

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Fei Pang

    (Ltd)

  • Yian Du

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

  • Xiangdong Cheng

    (Hangzhou Institute of Medicine (HIM), Chinese Academy of Sciences)

Abstract

Ovarian metastasis is one of the major causes of treatment failure in patients with gastric cancer (GC). However, the genomic characteristics of ovarian metastasis in GC remain poorly understood. In this study, we enroll 74 GC patients with ovarian metastasis, with 64 having matched primary and metastatic samples. Here, we show a characterization of the mutation landscape of this disease, alongside an investigation into the molecular heterogeneity and pathway mutation enrichments between synchronous and metachronous metastasis. We classify patients into distinct clonal evolution patterns based on the distribution of mutations in paired samples. Notably, the parallel evolution group exhibits the most favorable prognosis. Additionally, by analyzing the differential response to chemotherapy, we identify potential biomarkers, including SALL4, CCDC105, and CLDN18, for predicting the efficacy of paclitaxel treatment. Furthermore, we validate that CLDN18 fusion mutations improve tumor response to paclitaxel treatment in GC with ovarian metastasis in vitro and vivo.

Suggested Citation

  • Pengfei Yu & Can Hu & Guangyu Ding & Xiaoliang Shi & Jingli Xu & Yang Cao & Xiangliu Chen & Wei Wu & Qi Xu & Jingquan Fang & Xingmao Huang & Shaohua Yuan & Hui Chen & Zhizheng Wang & Ling Huang & Fei , 2024. "Mutation characteristics and molecular evolution of ovarian metastasis from gastric cancer and potential biomarkers for paclitaxel treatment," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48144-0
    DOI: 10.1038/s41467-024-48144-0
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    References listed on IDEAS

    as
    1. Yang Shu & Weihan Zhang & Qianqian Hou & Linyong Zhao & Shouyue Zhang & Jiankang Zhou & Xiaohai Song & Yan Zhang & Dan Jiang & Xinzu Chen & Peiqi Wang & Xuyang Xia & Fei Liao & Dandan Yin & Xiaolong C, 2018. "Prognostic significance of frequent CLDN18-ARHGAP26/6 fusion in gastric signet-ring cell cancer," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Ludmil B. Alexandrov & Serena Nik-Zainal & David C. Wedge & Samuel A. J. R. Aparicio & Sam Behjati & Andrew V. Biankin & Graham R. Bignell & Niccolò Bolli & Ake Borg & Anne-Lise Børresen-Dale & Sandri, 2013. "Correction: Corrigendum: Signatures of mutational processes in human cancer," Nature, Nature, vol. 502(7470), pages 258-258, October.
    3. Ludmil B. Alexandrov & Serena Nik-Zainal & David C. Wedge & Samuel A. J. R. Aparicio & Sam Behjati & Andrew V. Biankin & Graham R. Bignell & Niccolò Bolli & Ake Borg & Anne-Lise Børresen-Dale & Sandri, 2013. "Signatures of mutational processes in human cancer," Nature, Nature, vol. 500(7463), pages 415-421, August.
    4. Liqun Wu & Herui Yao & Hui Chen & Aodi Wang & Kun Guo & Wenli Gou & Yanfei Yu & Xiang Li & Ming Yao & Shaohua Yuan & Fei Pang & Jinwei Hu & Lijuan Chen & Wenjin Liu & Jicheng Yao & Shuirong Zhang & Xi, 2022. "Landscape of somatic alterations in large-scale solid tumors from an Asian population," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    5. Johannes G. Reiter & Alvin P. Makohon-Moore & Jeffrey M. Gerold & Ivana Bozic & Krishnendu Chatterjee & Christine A. Iacobuzio-Donahue & Bert Vogelstein & Martin A. Nowak, 2017. "Reconstructing metastatic seeding patterns of human cancers," Nature Communications, Nature, vol. 8(1), pages 1-10, April.
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