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Tumour-associated macrophages secrete pleiotrophin to promote PTPRZ1 signalling in glioblastoma stem cells for tumour growth

Author

Listed:
  • Yu Shi

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Yi-Fang Ping

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Wenchao Zhou

    (Lerner Research Institute, Cleveland Clinic)

  • Zhi-Cheng He

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Cong Chen

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China
    Lerner Research Institute, Cleveland Clinic)

  • Bai-Shi-Jiao Bian

    (Southwest Hospital, The Third Military Medical University)

  • Lin Zhang

    (Xijing Hospital, The Fourth Military Medical University)

  • Lu Chen

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Xun Lan

    (Stanford University)

  • Xian-Chao Zhang

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Kai Zhou

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Qing Liu

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Hua Long

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Ti-Wei Fu

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Xiao-Ning Zhang

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Mian-Fu Cao

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Zhi Huang

    (Lerner Research Institute, Cleveland Clinic)

  • Xiaoguang Fang

    (Lerner Research Institute, Cleveland Clinic)

  • Xiuxing Wang

    (Lerner Research Institute, Cleveland Clinic)

  • Hua Feng

    (Southwest Hospital, The Third Military Medical University)

  • Xiao-Hong Yao

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Shi-Cang Yu

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • You-Hong Cui

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Xia Zhang

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China)

  • Jeremy N Rich

    (Lerner Research Institute, Cleveland Clinic)

  • Shideng Bao

    (Lerner Research Institute, Cleveland Clinic)

  • Xiu-Wu Bian

    (Institute of Pathology and Southwest Cancer Centre, Southwest Hospital, The Third Military Medical University
    The Key Laboratory of Tumour Immunopathology, The Ministry of Education of China
    Collaborative Innovation Center for Cancer Medicine, Sun Yat-sen University)

Abstract

Intense infiltration of tumour-associated macrophages (TAMs) facilitates malignant growth of glioblastoma (GBM), but the underlying mechanisms remain undefined. Herein, we report that TAMs secrete abundant pleiotrophin (PTN) to stimulate glioma stem cells (GSCs) through its receptor PTPRZ1 thus promoting GBM malignant growth through PTN–PTPRZ1 paracrine signalling. PTN expression correlates with infiltration of CD11b+/CD163+ TAMs and poor prognosis of GBM patients. Co-implantation of M2-like macrophages (MLCs) promoted GSC-driven tumour growth, but silencing PTN expression in MLCs mitigated their pro-tumorigenic activity. The PTN receptor PTPRZ1 is preferentially expressed in GSCs and also predicts GBM poor prognosis. Disrupting PTPRZ1 abrogated GSC maintenance and tumorigenic potential. Moreover, blocking the PTN–PTPRZ1 signalling by shRNA or anti-PTPRZ1 antibody potently suppressed GBM tumour growth and prolonged animal survival. Our study uncovered a critical molecular crosstalk between TAMs and GSCs through the PTN–PTPRZ1 paracrine signalling to support GBM malignant growth, indicating that targeting this signalling axis may have therapeutic potential.

Suggested Citation

  • Yu Shi & Yi-Fang Ping & Wenchao Zhou & Zhi-Cheng He & Cong Chen & Bai-Shi-Jiao Bian & Lin Zhang & Lu Chen & Xun Lan & Xian-Chao Zhang & Kai Zhou & Qing Liu & Hua Long & Ti-Wei Fu & Xiao-Ning Zhang & M, 2017. "Tumour-associated macrophages secrete pleiotrophin to promote PTPRZ1 signalling in glioblastoma stem cells for tumour growth," Nature Communications, Nature, vol. 8(1), pages 1-17, August.
    • Handle: RePEc:nat:natcom:v:8:y:2017:i:1:d:10.1038_ncomms15080
    DOI: 10.1038/ncomms15080
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    Cited by:

    1. Nourhan Abdelfattah & Parveen Kumar & Caiyi Wang & Jia-Shiun Leu & William F. Flynn & Ruli Gao & David S. Baskin & Kumar Pichumani & Omkar B. Ijare & Stephanie L. Wood & Suzanne Z. Powell & David L. H, 2022. "Single-cell analysis of human glioma and immune cells identifies S100A4 as an immunotherapy target," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Yuanning Zheng & Francisco Carrillo-Perez & Marija Pizurica & Dieter Henrik Heiland & Olivier Gevaert, 2023. "Spatial cellular architecture predicts prognosis in glioblastoma," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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