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Single-cell spatial immune landscapes of primary and metastatic brain tumours

Author

Listed:
  • Elham Karimi

    (McGill University)

  • Miranda W. Yu

    (McGill University
    McGill University)

  • Sarah M. Maritan

    (McGill University
    McGill University)

  • Lucas J. M. Perus

    (McGill University
    McGill University)

  • Morteza Rezanejad

    (University of Toronto)

  • Mark Sorin

    (McGill University
    McGill University)

  • Matthew Dankner

    (McGill University
    McGill University)

  • Parvaneh Fallah

    (McGill University)

  • Samuel Doré

    (McGill University
    McGill University)

  • Dongmei Zuo

    (McGill University)

  • Benoit Fiset

    (McGill University)

  • Daan J. Kloosterman

    (Netherlands Cancer Institute)

  • LeeAnn Ramsay

    (McGill University)

  • Yuhong Wei

    (McGill University)

  • Stephanie Lam

    (McGill University)

  • Roa Alsajjan

    (King Saud University College of Medicine
    McGill University)

  • Ian R. Watson

    (McGill University
    McGill University)

  • Gloria Roldan Urgoiti

    (University of Calgary
    University of Calgary)

  • Morag Park

    (McGill University
    McGill University
    McGill University)

  • Dieta Brandsma

    (Antoni van Leeuwenhoek Hospital)

  • Donna L. Senger

    (McGill University
    Jewish General Hospital)

  • Jennifer A. Chan

    (University of Calgary
    University of Calgary)

  • Leila Akkari

    (Netherlands Cancer Institute)

  • Kevin Petrecca

    (McGill University
    McGill University Health Centre)

  • Marie-Christine Guiot

    (McGill University
    McGill University
    McGill University Health Centre
    McGill University)

  • Peter M. Siegel

    (McGill University
    McGill University
    McGill University
    McGill University)

  • Daniela F. Quail

    (McGill University
    McGill University
    McGill University)

  • Logan A. Walsh

    (McGill University
    McGill University)

Abstract

Single-cell technologies have enabled the characterization of the tumour microenvironment at unprecedented depth and have revealed vast cellular diversity among tumour cells and their niche. Anti-tumour immunity relies on cell–cell relationships within the tumour microenvironment1,2, yet many single-cell studies lack spatial context and rely on dissociated tissues3. Here we applied imaging mass cytometry to characterize the immunological landscape of 139 high-grade glioma and 46 brain metastasis tumours from patients. Single-cell analysis of more than 1.1 million cells across 389 high-dimensional histopathology images enabled the spatial resolution of immune lineages and activation states, revealing differences in immune landscapes between primary tumours and brain metastases from diverse solid cancers. These analyses revealed cellular neighbourhoods associated with survival in patients with glioblastoma, which we leveraged to identify a unique population of myeloperoxidase (MPO)-positive macrophages associated with long-term survival. Our findings provide insight into the biology of primary and metastatic brain tumours, reinforcing the value of integrating spatial resolution to single-cell datasets to dissect the microenvironmental contexture of cancer.

Suggested Citation

  • Elham Karimi & Miranda W. Yu & Sarah M. Maritan & Lucas J. M. Perus & Morteza Rezanejad & Mark Sorin & Matthew Dankner & Parvaneh Fallah & Samuel Doré & Dongmei Zuo & Benoit Fiset & Daan J. Kloosterma, 2023. "Single-cell spatial immune landscapes of primary and metastatic brain tumours," Nature, Nature, vol. 614(7948), pages 555-563, February.
    • Handle: RePEc:nat:nature:v:614:y:2023:i:7948:d:10.1038_s41586-022-05680-3
    DOI: 10.1038/s41586-022-05680-3
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    Citations

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    Cited by:

    1. Frank A. Giordano & Julian P. Layer & Sonia Leonardelli & Lea L. Friker & Roberta Turiello & Dillon Corvino & Thomas Zeyen & Christina Schaub & Wolf Müller & Elena Sperk & Leonard Christopher Schmeel , 2024. "L-RNA aptamer-based CXCL12 inhibition combined with radiotherapy in newly-diagnosed glioblastoma: dose escalation of the phase I/II GLORIA trial," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Caroline S. Jansen & Meghana S. Pagadala & Maria A. Cardenas & Roshan S. Prabhu & Subir Goyal & Chengjing Zhou & Prasanthi Chappa & BaoHan T. Vo & Chengyu Ye & Benjamin Hopkins & Jim Zhong & Adam Klie, 2024. "Pre-operative stereotactic radiosurgery and peri-operative dexamethasone for resectable brain metastases: a two-arm pilot study evaluating clinical outcomes and immunological correlates," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Juan Du & Junlei Zhang & Lin Wang & Xun Wang & Yaxing Zhao & Jiaoying Lu & Tingmin Fan & Meng Niu & Jie Zhang & Fei Cheng & Jun Li & Qi Zhu & Daoqiang Zhang & Hao Pei & Guang Li & Xingguang Liang & He, 2023. "Selective oxidative protection leads to tissue topological changes orchestrated by macrophage during ulcerative colitis," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    4. Augusto Faria Andrade & Alva Annett & Elham Karimi & Danai Georgia Topouza & Morteza Rezanejad & Yitong Liu & Michael McNicholas & Eduardo G. Gonzalez Santiago & Dhana Llivichuzhca-Loja & Arne Gehlhaa, 2024. "Immune landscape of oncohistone-mutant gliomas reveals diverse myeloid populations and tumor-promoting function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. 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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