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ID1 expressing macrophages support cancer cell stemness and limit CD8+ T cell infiltration in colorectal cancer

Author

Listed:
  • Shuang Shang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Chen Yang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Fei Chen

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Ren-shen Xiang

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

  • Huan Zhang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Shu-yuan Dai

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Jing Liu

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Xiao-xi Lv

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Cheng Zhang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    China–Japan Friendship Hospital)

  • Xiao-tong Liu

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Qi Zhang

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

  • Shuai-bing Lu

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

  • Jia-wei Song

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Jiao-jiao Yu

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Ji-chao Zhou

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Xiao-wei Zhang

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Bing Cui

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Ping-ping Li

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

  • Sheng-tao Zhu

    (Beijing Friendship Hospital
    Beijing Friendship Hospital)

  • Hai-zeng Zhang

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

  • Fang Hua

    (Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College
    Chinese Academy of Medical Sciences & Peking Union Medical College)

Abstract

Elimination of cancer stem cells (CSCs) and reinvigoration of antitumor immunity remain unmet challenges for cancer therapy. Tumor-associated macrophages (TAMs) constitute the prominant population of immune cells in tumor tissues, contributing to the formation of CSC niches and a suppressive immune microenvironment. Here, we report that high expression of inhibitor of differentiation 1 (ID1) in TAMs correlates with poor outcome in patients with colorectal cancer (CRC). ID1 expressing macrophages maintain cancer stemness and impede CD8+ T cell infiltration. Mechanistically, ID1 interacts with STAT1 to induce its cytoplasmic distribution and inhibits STAT1-mediated SerpinB2 and CCL4 transcription, two secretory factors responsible for cancer stemness inhibition and CD8+ T cell recruitment. Reducing ID1 expression ameliorates CRC progression and enhances tumor sensitivity to immunotherapy and chemotherapy. Collectively, our study highlights the pivotal role of ID1 in controlling the protumor phenotype of TAMs and paves the way for therapeutic targeting of ID1 in CRC.

Suggested Citation

  • Shuang Shang & Chen Yang & Fei Chen & Ren-shen Xiang & Huan Zhang & Shu-yuan Dai & Jing Liu & Xiao-xi Lv & Cheng Zhang & Xiao-tong Liu & Qi Zhang & Shuai-bing Lu & Jia-wei Song & Jiao-jiao Yu & Ji-cha, 2023. "ID1 expressing macrophages support cancer cell stemness and limit CD8+ T cell infiltration in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43548-w
    DOI: 10.1038/s41467-023-43548-w
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    1. Marianna Papaspyridonos & Irina Matei & Yujie Huang & Maria do Rosario Andre & Helene Brazier-Mitouart & Janelle C. Waite & April S. Chan & Julie Kalter & Ilyssa Ramos & Qi Wu & Caitlin Williams & Jed, 2015. "Id1 suppresses anti-tumour immune responses and promotes tumour progression by impairing myeloid cell maturation," Nature Communications, Nature, vol. 6(1), pages 1-13, November.
    2. Xuan Li & Xiao-Qi Wu & Rong Deng & Dan-Dan Li & Jun Tang & Wen-Dan Chen & Jing-Hong Chen & Jiao Ji & Lin Jiao & Shan Jiang & Fen Yang & Gong-Kan Feng & Ravichandran Senthilkumar & Fei Yue & Hai-Liang , 2017. "CaMKII-mediated Beclin 1 phosphorylation regulates autophagy that promotes degradation of Id and neuroblastoma cell differentiation," Nature Communications, Nature, vol. 8(1), pages 1-16, December.
    3. Naoko Ohtani & Zoe Zebedee & Thomas J. G. Huot & Julie A. Stinson & Masataka Sugimoto & Yasuhiro Ohashi & Andrew D. Sharrocks & Gordon Peters & Eiji Hara, 2001. "Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence," Nature, Nature, vol. 409(6823), pages 1067-1070, February.
    4. Oscar R. Colegio & Ngoc-Quynh Chu & Alison L. Szabo & Thach Chu & Anne Marie Rhebergen & Vikram Jairam & Nika Cyrus & Carolyn E. Brokowski & Stephanie C. Eisenbarth & Gillian M. Phillips & Gary W. Cli, 2014. "Functional polarization of tumour-associated macrophages by tumour-derived lactic acid," Nature, Nature, vol. 513(7519), pages 559-563, September.
    5. Flora Castellino & Alex Y. Huang & Grégoire Altan-Bonnet & Sabine Stoll & Clemens Scheinecker & Ronald N. Germain, 2006. "Chemokines enhance immunity by guiding naive CD8+ T cells to sites of CD4+ T cell–dendritic cell interaction," Nature, Nature, vol. 440(7086), pages 890-895, April.
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