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ARF6–JIP3/4 regulate endosomal tubules for MT1-MMP exocytosis in cancer invasion

Marchesin, Valentina, Castro-Castro, Antonio, Lodillinsky, Catalina, Castagnino, Alessia, Cyrta, Joanna, Bonsang-Kitzis, Hélène, Fuhrmann, Laetitia, Irondelle, Marie, Infante, Elvira, Montagnac, Guillaume, Reyal, Fabien, Vincent-Salomon, Anne, Chavrier, Philippe·2015·Journal of Cell Biology
DOI 10.1083/jcb.201506002PMC PMC4621834
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Abstract

Invasion of cancer cells into collagen-rich extracellular matrix requires membrane-tethered membrane type 1–matrix metalloproteinase (MT1-MMP) as the key protease for collagen breakdown. Understanding how MT1-MMP is delivered to the surface of tumor cells is essential for cancer cell biology. In this study, we identify ARF6 together with c-Jun NH2-terminal kinase–interacting protein 3 and 4 (JIP3 and JIP4) effectors as critical regulators of this process. Silencing ARF6 or JIP3/JIP4 in breast tumor cells results in MT1-MMP endosome mispositioning and reduces MT1-MMP exocytosis and tumor cell invasion. JIPs are recruited by Wiskott-Aldrich syndrome protein and scar homologue (WASH) on MT1-MMP endosomes on which they recruit dynein–dynactin and kinesin-1. The interaction of plasma membrane ARF6 with endosomal JIPs coordinates dynactin–dynein and kinesin-1 activity in a tug-of-war mechanism, leading to MT1-MMP endosome tubulation and exocytosis. In addition, we find that ARF6, MT1-MMP, and kinesin-1 are up-regulated in high-grade triple-negative breast cancers. These data identify a critical ARF6–JIP–MT1-MMP–dynein–dynactin–kinesin-1 axis promoting an invasive phenotype of breast cancer cells.

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Metadata

Authors
Marchesin, V., Castro-Castro, A., Lodillinsky, C., Castagnino, A., Cyrta, J., Bonsang-Kitzis, H., Fuhrmann, L., Irondelle, M., Infante, E., Montagnac, G., Reyal, F., Vincent-Salomon, A., & Chavrier, P.
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2015-10-26
Volume
211
Issue
2
Pages
339-358
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.201506002
PMC
PMC4621834
Cited by
160
References
3
Language
en

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