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Targeting metastasis-initiating cells through the fatty acid receptor CD36

Author

Listed:
  • Gloria Pascual

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Alexandra Avgustinova

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Stefania Mejetta

    (Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology (BIST))

  • Mercè Martín

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Andrés Castellanos

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Camille Stephan-Otto Attolini

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Antoni Berenguer

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Neus Prats

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST))

  • Agustí Toll

    (IMIM, Hospital del Mar)

  • Juan Antonio Hueto

    (Vall D´Hebron Hospital, Barcelona, Universitat Autònoma de Barcelona)

  • Coro Bescós

    (Vall D´Hebron Hospital, Barcelona, Universitat Autònoma de Barcelona)

  • Luciano Di Croce

    (Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology (BIST)
    Catalan Institution for Research and Advanced Studies (ICREA)
    Universitat Pompeu Fabra (UPF))

  • Salvador Aznar Benitah

    (Institute for Research in Biomedicine (IRB Barcelona), The Barcelona Institute of Science and Technology (BIST)
    Catalan Institution for Research and Advanced Studies (ICREA))

Abstract

The fact that the identity of the cells that initiate metastasis in most human cancers is unknown hampers the development of antimetastatic therapies. Here we describe a subpopulation of CD44bright cells in human oral carcinomas that do not overexpress mesenchymal genes, are slow-cycling, express high levels of the fatty acid receptor CD36 and lipid metabolism genes, and are unique in their ability to initiate metastasis. Palmitic acid or a high-fat diet specifically boosts the metastatic potential of CD36+ metastasis-initiating cells in a CD36-dependent manner. The use of neutralizing antibodies to block CD36 causes almost complete inhibition of metastasis in immunodeficient or immunocompetent orthotopic mouse models of human oral cancer, with no side effects. Clinically, the presence of CD36+ metastasis-initiating cells correlates with a poor prognosis for numerous types of carcinomas, and inhibition of CD36 also impairs metastasis, at least in human melanoma- and breast cancer-derived tumours. Together, our results indicate that metastasis-initiating cells particularly rely on dietary lipids to promote metastasis.

Suggested Citation

  • Gloria Pascual & Alexandra Avgustinova & Stefania Mejetta & Mercè Martín & Andrés Castellanos & Camille Stephan-Otto Attolini & Antoni Berenguer & Neus Prats & Agustí Toll & Juan Antonio Hueto & Coro , 2017. "Targeting metastasis-initiating cells through the fatty acid receptor CD36," Nature, Nature, vol. 541(7635), pages 41-45, January.
    • Handle: RePEc:nat:nature:v:541:y:2017:i:7635:d:10.1038_nature20791
    DOI: 10.1038/nature20791
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    Cited by:

    1. Phillip M. Brailey & Lauren Evans & Juan Carlos López-Rodríguez & Anthony Sinadinos & Victoria Tyrrel & Gavin Kelly & Valerie O’Donnell & Peter Ghazal & Susan John & Patricia Barral, 2022. "CD1d-dependent rewiring of lipid metabolism in macrophages regulates innate immune responses," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. Rebekka Wegmann & Ximena Bonilla & Ruben Casanova & Stéphane Chevrier & Ricardo Coelho & Cinzia Esposito & Joanna Ficek-Pascual & Sandra Goetze & Gabriele Gut & Francis Jacob & Andrea Jacobs & Jack Ku, 2024. "Single-cell landscape of innate and acquired drug resistance in acute myeloid leukemia," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Ling Tao & Mahmoud A. Mohammad & Giorgio Milazzo & Myrthala Moreno-Smith & Tajhal D. Patel & Barry Zorman & Andrew Badachhape & Blanca E. Hernandez & Amber B. Wolf & Zihua Zeng & Jennifer H. Foster & , 2022. "MYCN-driven fatty acid uptake is a metabolic vulnerability in neuroblastoma," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Yuying Tan & Junjie Li & Guangyuan Zhao & Kai-Chih Huang & Horacio Cardenas & Yinu Wang & Daniela Matei & Ji-Xin Cheng, 2022. "Metabolic reprogramming from glycolysis to fatty acid uptake and beta-oxidation in platinum-resistant cancer cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    5. Jan Philipp Menzel & Reuben S. E. Young & Aurélie H. Benfield & Julia S. Scott & Puttandon Wongsomboon & Lukáš Cudlman & Josef Cvačka & Lisa M. Butler & Sónia T. Henriques & Berwyck L. J. Poad & Steph, 2023. "Ozone-enabled fatty acid discovery reveals unexpected diversity in the human lipidome," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. Daniela Michelatti & Sven Beyes & Chiara Bernardis & Maria Luce Negri & Leonardo Morelli & Naiara Garcia Bediaga & Vittoria Poli & Luca Fagnocchi & Sara Lago & Sarah D’Annunzio & Nicole Cona & Ilaria , 2024. "Oncogenic enhancers prime quiescent metastatic cells to escape NK immune surveillance by eliciting transcriptional memory," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    7. Ping Yang & Hong Qin & Yiyu Li & Anhua Xiao & Enze Zheng & Han Zeng & Chunxiao Su & Xiaoqing Luo & Qiannan Lu & Meng Liao & Lei Zhao & Li Wei & Zac Varghese & John F. Moorhead & Yaxi Chen & Xiong Z. R, 2022. "CD36-mediated metabolic crosstalk between tumor cells and macrophages affects liver metastasis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Rens Peeters & Jorge Cuenca-Escalona & Esther A. Zaal & Anna T. Hoekstra & Anouk C. G. Balvert & Marcos Vidal-Manrique & Niek Blomberg & Sjoerd J. Deventer & Rinke Stienstra & Julia Jellusova & Martin, 2022. "Fatty acid metabolism in aggressive B-cell lymphoma is inhibited by tetraspanin CD37," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    9. C. Megan Young & Laurent Beziaud & Pierre Dessen & Angela Madurga Alonso & Albert Santamaria-Martínez & Joerg Huelsken, 2023. "Metabolic dependencies of metastasis-initiating cells in female breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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