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[Preprint]. 2023 Aug 21:2023.08.19.553966. [Version 1] doi: 10.1101/2023.08.19.553966

Cell-specific crosstalk proteomics reveals cathepsin B signaling as a driver of glioblastoma malignancy near the subventricular zone

Emily S Norton, Lauren A Whaley, Vanessa K Jones, Mieu M Brooks, Marissa N Russo, Dmytro Morderer, Erik Jessen, Paula Schiapparelli, Andres Ramos-Fresnedo, Natanael Zarco, Anna Carrano, Wilfried Rossoll, Yan W Asmann, TuKiet T Lam, Kaisorn L Chaichana, Panos Z Anastasiadis, Alfredo Quiñones-Hinojosa, Hugo Guerrero-Cázares
PMCID: PMC10473635  PMID: 37662251

Summary

Glioblastoma (GBM) is the most prevalent and aggressive malignant primary brain tumor. GBM proximal to the lateral ventricles (LVs) is more aggressive, potentially due to subventricular zone (SVZ) contact. Despite this, crosstalk between GBM and neural stem/progenitor cells (NSC/NPCs) is not well understood. Using cell-specific proteomics, we show that LV-proximal GBM prevents neuronal maturation of NSCs through induction of senescence. Additionally, GBM brain tumor initiating cells (BTICs) increase expression of CTSB upon interaction with NPCs. Lentiviral knockdown and recombinant protein experiments reveal both cell-intrinsic and soluble CTSB promote malignancy-associated phenotypes in BTICs. Soluble CTSB stalls neuronal maturation in NPCs while promoting senescence, providing a link between LV-tumor proximity and neurogenesis disruption. Finally, we show LV-proximal CTSB upregulation in patients, showing the relevance of this crosstalk in human GBM biology. These results demonstrate the value of proteomic analysis in tumor microenvironment research and provide direction for new therapeutic strategies in GBM.

Highlights

  • Periventricular GBM is more malignant and disrupts neurogenesis in a rodent model.

  • Cell-specific proteomics elucidates tumor-promoting crosstalk between GBM and NPCs.

  • NPCs induce upregulated CTSB expression in GBM, promoting tumor progression.

  • GBM stalls neurogenesis and promotes NPC senescence via CTSB.

Full Text Availability

The license terms selected by the author(s) for this preprint version do not permit archiving in PMC. The full text is available from the preprint server.


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