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Metastatic-niche labelling reveals parenchymal cells with stem features

Author

Listed:
  • Luigi Ombrato

    (The Francis Crick Institute)

  • Emma Nolan

    (The Francis Crick Institute)

  • Ivana Kurelac

    (The Francis Crick Institute
    Università di Bologna)

  • Antranik Mavousian

    (University of Cambridge)

  • Victoria Louise Bridgeman

    (The Francis Crick Institute)

  • Ivonne Heinze

    (Leibniz Institute on Aging, Fritz Lipmann Institute (FLI))

  • Probir Chakravarty

    (The Francis Crick Institute)

  • Stuart Horswell

    (The Francis Crick Institute)

  • Estela Gonzalez-Gualda

    (The Francis Crick Institute)

  • Giulia Matacchione

    (The Francis Crick Institute)

  • Anne Weston

    (The Francis Crick Institute)

  • Joanna Kirkpatrick

    (Leibniz Institute on Aging, Fritz Lipmann Institute (FLI))

  • Ehab Husain

    (Aberdeen Royal Infirmary)

  • Valerie Speirs

    (University of Aberdeen)

  • Lucy Collinson

    (The Francis Crick Institute)

  • Alessandro Ori

    (Leibniz Institute on Aging, Fritz Lipmann Institute (FLI))

  • Joo-Hyeon Lee

    (University of Cambridge
    University of Cambridge)

  • Ilaria Malanchi

    (The Francis Crick Institute)

Abstract

Direct investigation of the early cellular changes induced by metastatic cells within the surrounding tissue remains a challenge. Here we present a system in which metastatic cancer cells release a cell-penetrating fluorescent protein, which is taken up by neighbouring cells and enables spatial identification of the local metastatic cellular environment. Using this system, tissue cells with low representation in the metastatic niche can be identified and characterized within the bulk tissue. To highlight its potential, we applied this strategy to study the cellular environment of metastatic breast cancer cells in the lung. We report the presence of cancer-associated parenchymal cells, which exhibit stem-cell-like features, expression of lung progenitor markers, multi-lineage differentiation potential and self-renewal activity. In ex vivo assays, lung epithelial cells acquire a cancer-associated parenchymal-cell-like phenotype when co-cultured with cancer cells and support their growth. These results highlight the potential of this method as a platform for new discoveries.

Suggested Citation

  • Luigi Ombrato & Emma Nolan & Ivana Kurelac & Antranik Mavousian & Victoria Louise Bridgeman & Ivonne Heinze & Probir Chakravarty & Stuart Horswell & Estela Gonzalez-Gualda & Giulia Matacchione & Anne , 2019. "Metastatic-niche labelling reveals parenchymal cells with stem features," Nature, Nature, vol. 572(7771), pages 603-608, August.
  • Handle: RePEc:nat:nature:v:572:y:2019:i:7771:d:10.1038_s41586-019-1487-6
    DOI: 10.1038/s41586-019-1487-6
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    Citations

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    Cited by:

    1. Jing Huang & Weijun Huang & Junzhe Yi & Yiwen Deng & Ruijie Li & Jieying Chen & Jiahao Shi & Yuan Qiu & Tao Wang & Xiaoyong Chen & Xiaoran Zhang & Andy Peng Xiang, 2023. "Mesenchymal stromal cells alleviate depressive and anxiety-like behaviors via a lung vagal-to-brain axis in male mice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Anna Cioce & Beatriz Calle & Tatiana Rizou & Sarah C. Lowery & Victoria L. Bridgeman & Keira E. Mahoney & Andrea Marchesi & Ganka Bineva-Todd & Helen Flynn & Zhen Li & Omur Y. Tastan & Chloe Roustan &, 2022. "Cell-specific bioorthogonal tagging of glycoproteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Bingjie Guan & Youdong Liu & Bowen Xie & Senlin Zhao & Abudushalamu Yalikun & Weiwei Chen & Menghua Zhou & Qi Gu & Dongwang Yan, 2024. "Mitochondrial genome transfer drives metabolic reprogramming in adjacent colonic epithelial cells promoting TGFβ1-mediated tumor progression," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Misa Minegishi & Takahiro Kuchimaru & Kaori Nishikawa & Takayuki Isagawa & Satoshi Iwano & Kei Iida & Hiromasa Hara & Shizuka Miura & Marika Sato & Shigeaki Watanabe & Akifumi Shiomi & Yo Mabuchi & Hi, 2023. "Secretory GFP reconstitution labeling of neighboring cells interrogates cell–cell interactions in metastatic niches," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    5. Kristina Handler & Karsten Bach & Costanza Borrelli & Salvatore Piscuoglio & Xenia Ficht & Ilhan E. Acar & Andreas E. Moor, 2023. "Fragment-sequencing unveils local tissue microenvironments at single-cell resolution," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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