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VC-resist glioblastoma cell state: vessel co-option as a key driver of chemoradiation resistance

Author

Listed:
  • Cathy Pichol-Thievend

    (Paris-Saclay University)

  • Oceane Anezo

    (Paris-Saclay University)

  • Aafrin M. Pettiwala

    (Paris-Saclay University
    PSL University)

  • Guillaume Bourmeau

    (Paris-Saclay University)

  • Remi Montagne

    (PSL University
    INSERM U900
    PSL Research University)

  • Anne-Marie Lyne

    (PSL University
    INSERM U900
    PSL Research University)

  • Pierre-Olivier Guichet

    (ProDiCeT
    Laboratoire de Cancérologie Biologique)

  • Pauline Deshors

    (Paris-Saclay University)

  • Alberto Ballestín

    (Paris-Saclay University)

  • Benjamin Blanchard

    (Paris-Saclay University)

  • Juliette Reveilles

    (Paris-Saclay University)

  • Vidhya M. Ravi

    (Medical Center - University of Freiburg)

  • Kevin Joseph

    (Medical Center - University of Freiburg)

  • Dieter H. Heiland

    (Medical Center - University of Freiburg)

  • Boris Julien

    (Paris-Saclay University)

  • Sophie Leboucher

    (Institut Curie)

  • Laetitia Besse

    (Multimodal Imaging Center)

  • Patricia Legoix

    (ICGex Next-Generation Sequencing Platform)

  • Florent Dingli

    (CurieCoreTech Spectrométrie de Masse Protéomique)

  • Stephane Liva

    (PSL University
    INSERM U900
    PSL Research University)

  • Damarys Loew

    (CurieCoreTech Spectrométrie de Masse Protéomique)

  • Elisa Giani

    (Humanitas University)

  • Valentino Ribecco

    (Paris-Saclay University)

  • Charita Furumaya

    (Paris-Saclay University)

  • Laura Marcos-Kovandzic

    (Paris-Saclay University)

  • Konstantin Masliantsev

    (ProDiCeT
    Laboratoire de Cancérologie Biologique)

  • Thomas Daubon

    (UMR5095)

  • Lin Wang

    (City of Hope)

  • Aaron A. Diaz

    (University of California, San Francisco)

  • Oliver Schnell

    (Medical Center - University of Freiburg)

  • Jürgen Beck

    (Medical Center - University of Freiburg)

  • Nicolas Servant

    (PSL University
    INSERM U900
    PSL Research University)

  • Lucie Karayan-Tapon

    (ProDiCeT
    Laboratoire de Cancérologie Biologique)

  • Florence M. G. Cavalli

    (PSL University
    INSERM U900
    PSL Research University)

  • Giorgio Seano

    (Paris-Saclay University)

Abstract

Glioblastoma (GBM) is a highly lethal type of cancer. GBM recurrence following chemoradiation is typically attributed to the regrowth of invasive and resistant cells. Therefore, there is a pressing need to gain a deeper understanding of the mechanisms underlying GBM resistance to chemoradiation and its ability to infiltrate. Using a combination of transcriptomic, proteomic, and phosphoproteomic analyses, longitudinal imaging, organotypic cultures, functional assays, animal studies, and clinical data analyses, we demonstrate that chemoradiation and brain vasculature induce cell transition to a functional state named VC-Resist (vessel co-opting and resistant cell state). This cell state is midway along the transcriptomic axis between proneural and mesenchymal GBM cells and is closer to the AC/MES1-like state. VC-Resist GBM cells are highly vessel co-opting, allowing significant infiltration into the surrounding brain tissue and homing to the perivascular niche, which in turn induces even more VC-Resist transition. The molecular and functional characteristics of this FGFR1-YAP1-dependent GBM cell state, including resistance to DNA damage, enrichment in the G2M phase, and induction of senescence/stemness pathways, contribute to its enhanced resistance to chemoradiation. These findings demonstrate how vessel co-option, perivascular niche, and GBM cell plasticity jointly drive resistance to therapy during GBM recurrence.

Suggested Citation

  • Cathy Pichol-Thievend & Oceane Anezo & Aafrin M. Pettiwala & Guillaume Bourmeau & Remi Montagne & Anne-Marie Lyne & Pierre-Olivier Guichet & Pauline Deshors & Alberto Ballestín & Benjamin Blanchard & , 2024. "VC-resist glioblastoma cell state: vessel co-option as a key driver of chemoradiation resistance," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47985-z
    DOI: 10.1038/s41467-024-47985-z
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