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Spatial transcriptomics analysis of esophageal squamous precancerous lesions and their progression to esophageal cancer

Author

Listed:
  • Xuejiao Liu

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute)

  • Simin Zhao

    (China-US (Henan) Hormel Cancer Institute
    Affiliated Cancer Hospital of Zhengzhou University
    Zhengzhou University)

  • Keke Wang

    (China-US (Henan) Hormel Cancer Institute)

  • Liting Zhou

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University)

  • Ming Jiang

    (China-US (Henan) Hormel Cancer Institute)

  • Yunfeng Gao

    (China-US (Henan) Hormel Cancer Institute)

  • Ran Yang

    (China-US (Henan) Hormel Cancer Institute)

  • Shiwen Yan

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University)

  • Wen Zhang

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University)

  • Bingbing Lu

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University)

  • Feifei Liu

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University)

  • Ran Zhao

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute)

  • Wenting Liu

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute)

  • Zihan Zhang

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University)

  • Kangdong Liu

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University
    The Collaborative Innovation Center of Henan Province for Cancer Chemoprevention)

  • Xiang Li

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University
    The Collaborative Innovation Center of Henan Province for Cancer Chemoprevention)

  • Zigang Dong

    (Zhengzhou University
    China-US (Henan) Hormel Cancer Institute
    Zhengzhou University
    The Collaborative Innovation Center of Henan Province for Cancer Chemoprevention)

Abstract

Esophageal squamous precancerous lesions (ESPL) are the precursors of esophageal squamous cell carcinoma (ESCC) including low-grade and high-grade intraepithelial neoplasia. Due to the absence of molecular indicators, which ESPL will eventually develop into ESCC and thus should be treated is not well defined. Indicators, for predicting risks of ESCC at ESPL stages, are an urgent need. We perform spatial whole-transcriptome atlas analysis, which can eliminate other tissue interference by sequencing the specific ESPL regions. In this study, the expression of TAGLN2 significantly increases, while CRNN expression level decreases along the progression of ESCC. Additionally, TAGLN2 protein level significantly increases in paired after-progression tissues compared with before-progression samples, while CRNN expression decreases. Functional studies suggest that TAGLN2 promotes ESCC progression, while CRNN inhibits it by regulating cell proliferation. Taken together, TAGLN2 and CRNN are suggested as candidate indicators for the risk of ESCC at ESPL stages.

Suggested Citation

  • Xuejiao Liu & Simin Zhao & Keke Wang & Liting Zhou & Ming Jiang & Yunfeng Gao & Ran Yang & Shiwen Yan & Wen Zhang & Bingbing Lu & Feifei Liu & Ran Zhao & Wenting Liu & Zihan Zhang & Kangdong Liu & Xia, 2023. "Spatial transcriptomics analysis of esophageal squamous precancerous lesions and their progression to esophageal cancer," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40343-5
    DOI: 10.1038/s41467-023-40343-5
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    as
    1. Jiacheng Yao & Qionghua Cui & Wenyi Fan & Yuling Ma & Yamei Chen & Tianyuan Liu & Xiannian Zhang & Yiyi Xi & Chengcheng Wang & Linna Peng & Yingying Luo & Ai Lin & Wenjia Guo & Lin Lin & Yuan Lin & We, 2020. "Single-cell transcriptomic analysis in a mouse model deciphers cell transition states in the multistep development of esophageal cancer," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    2. Xiannian Zhang & Linna Peng & Yingying Luo & Shaosen Zhang & Yang Pu & Yamei Chen & Wenjia Guo & Jiacheng Yao & Mingming Shao & Wenyi Fan & Qionghua Cui & Yiyi Xi & Yanxia Sun & Xiangjie Niu & Xuan Zh, 2021. "Dissecting esophageal squamous-cell carcinoma ecosystem by single-cell transcriptomic analysis," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    3. Yingxia Zheng & Zheyi Chen & Yichao Han & Li Han & Xin Zou & Bingqian Zhou & Rui Hu & Jie Hao & Shihao Bai & Haibo Xiao & Wei Vivian Li & Alex Bueker & Yanhui Ma & Guohua Xie & Junyao Yang & Shiyu Che, 2020. "Immune suppressive landscape in the human esophageal squamous cell carcinoma microenvironment," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    4. Daniel S. Chen & Ira Mellman, 2017. "Elements of cancer immunity and the cancer–immune set point," Nature, Nature, vol. 541(7637), pages 321-330, January.
    5. Patrick Danaher & Youngmi Kim & Brenn Nelson & Maddy Griswold & Zhi Yang & Erin Piazza & Joseph M. Beechem, 2022. "Advances in mixed cell deconvolution enable quantification of cell types in spatial transcriptomic data," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    6. Akira Yokoyama & Nobuyuki Kakiuchi & Tetsuichi Yoshizato & Yasuhito Nannya & Hiromichi Suzuki & Yasuhide Takeuchi & Yusuke Shiozawa & Yusuke Sato & Kosuke Aoki & Soo Ki Kim & Yoichi Fujii & Kenichi Yo, 2019. "Age-related remodelling of oesophageal epithelia by mutated cancer drivers," Nature, Nature, vol. 565(7739), pages 312-317, January.
    7. Kieran R Campbell & Christopher Yau, 2018. "Uncovering pseudotemporal trajectories with covariates from single cell and bulk expression data," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    8. Xi-Xi Chen & Qian Zhong & Yang Liu & Shu-Mei Yan & Zhang-Hua Chen & Shan-Zhao Jin & Tian-Liang Xia & Ruo-Yan Li & Ai-Jun Zhou & Zhe Su & Yu-Hua Huang & Qi-Tao Huang & Li-Yun Huang & Xing Zhang & Yan-N, 2017. "Genomic comparison of esophageal squamous cell carcinoma and its precursor lesions by multi-region whole-exome sequencing," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
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