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Single-cell transcriptomic analysis in a mouse model deciphers cell transition states in the multistep development of esophageal cancer

Author

Listed:
  • Jiacheng Yao

    (Tsinghua University)

  • Qionghua Cui

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Wenyi Fan

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Yuling Ma

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Yamei Chen

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Tianyuan Liu

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Xiannian Zhang

    (Capital Medical University)

  • Yiyi Xi

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Chengcheng Wang

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Linna Peng

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Yingying Luo

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Ai Lin

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Wenjia Guo

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Lin Lin

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Yuan Lin

    (Peking University)

  • Wen Tan

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC))

  • Dongxin Lin

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC)
    Chinese Academy of Medical Sciences
    Sun Yat-sen University Cancer Center, State Key Laboratory of Oncology in South China)

  • Chen Wu

    (Chinese Academy of Medical Sciences (CAMS) and Peking Union Medical College (PUMC)
    Nanjing Medical University
    Chinese Academy of Medical Sciences)

  • Jianbin Wang

    (Tsinghua University)

Abstract

Esophageal squamous cell carcinoma (ESCC) is prevalent in some geographical regions of the world. ESCC development presents a multistep pathogenic process from inflammation to invasive cancer; however, what is critical in these processes and how they evolve is largely unknown, obstructing early diagnosis and effective treatment. Here, we create a mouse model mimicking human ESCC development and construct a single-cell ESCC developmental atlas. We identify a set of key transitional signatures associated with oncogenic evolution of epithelial cells and depict the landmark dynamic tumorigenic trajectories. An early downregulation of CD8+ response against the initial tissue damage accompanied by the transition of immune response from type 1 to type 3 results in accumulation and activation of macrophages and neutrophils, which may create a chronic inflammatory environment that promotes carcinogen-transformed epithelial cell survival and proliferation. These findings shed light on how ESCC is initiated and developed.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17492-y
    DOI: 10.1038/s41467-020-17492-y
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    Cited by:

    1. 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.
    2. Mohammad Faujul Kabir & Adam L. Karami & Ricardo Cruz-Acuña & Alena Klochkova & Reshu Saxena & Anbin Mu & Mary Grace Murray & Jasmine Cruz & Annie D. Fuller & Margarette H. Clevenger & Kumaraswamy Nai, 2022. "Single cell transcriptomic analysis reveals cellular diversity of murine esophageal epithelium," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. Naveen Kumar & Pon Ganish Prakash & Christian Wentland & Shilpa Mary Kurian & Gaurav Jethva & Volker Brinkmann & Hans-Joachim Mollenkopf & Tobias Krammer & Christophe Toussaint & Antoine-Emmanuel Sali, 2024. "Decoding spatiotemporal transcriptional dynamics and epithelial fibroblast crosstalk during gastroesophageal junction development through single cell analysis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    4. Yuan Jiang & Yueyuan Zheng & Yuan-Wei Zhang & Shuai Kong & Jinxiu Dong & Fei Wang & Benjamin Ziman & Sigal Gery & Jia-Jie Hao & Dan Zhou & Jianian Zhou & Allen S. Ho & Uttam K. Sinha & Jian Chen & Shu, 2024. "Reciprocal inhibition between TP63 and STAT1 regulates anti-tumor immune response through interferon-γ signaling in squamous cancer," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. E. Koncina & M. Nurmik & V. I. Pozdeev & C. Gilson & M. Tsenkova & R. Begaj & S. Stang & A. Gaigneaux & C. Weindorfer & F. Rodriguez & M. Schmoetten & E. Klein & J. Karta & V. S. Atanasova & K. Grzyb , 2023. "IL1R1+ cancer-associated fibroblasts drive tumor development and immunosuppression in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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