Cited by 112Glioma Diagnosis and TreatmentCellular Mechanics and InteractionsCancer Cells and Metastasis

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p120-catenin-dependent collective brain infiltration by glioma cell networks

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Gritsenko, Pavlo G., Atlasy, Nader, Dieteren, Cindy E. J., Navis, Anna C., Venhuizen, Jan-Hendrik, Veelken, Cornelia, Schubert, Dirk, Acker-Palmer, Amparo, Westerman, Bart A., Wurdinger, Thomas, Leenders, William, Wesseling, Pieter, Stunnenberg, Hendrik G., Friedl, Peter·2020·Nature Cell Biology

DOI 10.1038/s41556-019-0443-xPMC PMC6952556

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Abstract

Diffuse brain infiltration by glioma cells causes detrimental disease progression, but its multicellular coordination is poorly understood. We show here that glioma cells infiltrate the brain collectively as multicellular networks. Contacts between moving glioma cells are adaptive epithelial-like or filamentous junctions stabilized by N-cadherin, β-catenin and p120-catenin, which undergo kinetic turnover, transmit intercellular calcium transients and mediate directional persistence. Downregulation of p120-catenin compromises cell-cell interaction and communication, disrupts collective networks, and both the cadherin and RhoA binding domains of p120-catenin are required for network formation and migration. Deregulating p120-catenin further prevents diffuse glioma cell infiltration of the mouse brain with marginalized microlesions as the outcome. Transcriptomics analysis has identified p120-catenin as an upstream regulator of neurogenesis and cell cycle pathways and a predictor of poor clinical outcome in glioma patients. Collective glioma networks infiltrating the brain thus depend on adherens junctions dynamics, the targeting of which may offer an unanticipated strategy to halt glioma progression.

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Screening for Tumor Microtube–Targeting Drugs Identifies PKC Modulators as Multipotent Inhibitors of Glioblastoma Progression
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ECM Substrates Impact RNAi Localization at Adherens Junctions of Colon Epithelial Cells
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TTK Inhibition Alleviates Postinjury Neointimal Formation and Atherosclerosis
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Jamming Transitions in Astrocytes and Glioblastoma Are Induced by Cell Density and Tension
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Retracted
miR-302e Suppresses Glioma Progression by Targeting VEGFA
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Retracted
Alteration of long non-coding RNAs and mRNAs expression profiles by compound heterozygous ASXL3 mutations in the mouse brain
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Targeting network circuitry in glioma
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Authors: Gritsenko, P. G., Atlasy, N., Dieteren, C. E. J., Navis, A. C., Venhuizen, J.-H., Veelken, C., Schubert, D., Acker-Palmer, A., Westerman, B. A., Wurdinger, T., Leenders, W., Wesseling, P., Stunnenberg, H. G., & Friedl, P.
Affiliations: Radboud University Medical Center (NL)
Radboud University Nijmegen (NL)
Karolinska Institutet (SE)
Amsterdam UMC Location Vrije Universiteit Amsterdam (NL)
Princess Máxima Center (NL)
The University of Texas MD Anderson Cancer Center (US)
Corresponding author: Friedl, Peter
ORCID: Atlasy, Nader
Navis, Anna C.
Venhuizen, Jan-Hendrik
Schubert, Dirk
Westerman, Bart A.
Wurdinger, Thomas
Leenders, William
Wesseling, Pieter
Stunnenberg, Hendrik G.
Friedl, Peter
Venue: Nature Cell Biology
Publisher: Springer Science and Business Media LLC
Published: 2020-01
Volume: 22
Issue: 1
Pages: 97-107
ISSN: 1465-7392 (ISSN-L)
1476-4679
DOI: 10.1038/s41556-019-0443-x
PMC: PMC6952556
OpenAlex: W2997878069
Cited by: 112
References: 82
Citations by year: 2026: 7 · 2025: 15 · 2024: 19 · 2023: 17 · 2022: 23 · 2021: 15 · 2020: 16
FWCI: 9.19
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Cell Biology (publishedVersion)
PubMed (publishedVersion)
Amsterdam UMC (VU Amsterdam) - Institutional Repository (publishedVersion)
PubMed Central (acceptedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Pure Amsterdam UMC (submittedVersion, other-oa)
MPG.PuRe (Max Planck Society) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion)
Apollo (University of Cambridge) (submittedVersion)
Apollo
Funders: Brain Tumour Charity (GN-000429)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (918.11.626, 863.13.019)
National Cancer Institute (U54CA210184, P30CA016672)
Topics: Health Sciences › Medicine › Oncology › Glioma Diagnosis and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular Mechanics and Interactions
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Keywords: p120 catenin, glioma, brain infiltration, collective cell migration, multicellular networks, N-cadherin, β-catenin, adherens junctions, intercellular calcium signaling, RhoA, directional persistence, intercellular communication, neurogenesis, cell cycle, clinical outcome prediction
MeSH terms: Delta Catenin, Animals, Brain, Cell Adhesion, Glioma, Phosphoproteins, Phosphorylation, Down-Regulation, Cadherins, Adherens Junctions, Cell Line, Tumor, Catenins

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