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HRS-WASH axis governs actin-mediated endosomal recycling and cell invasion

MacDonald, Ewan, Brown, Louise, Selvais, Arnaud, Liu, Han, Waring, Thomas, Newman, Daniel, Bithell, Jessica, Grimes, Douglas, Urbé, Sylvie, Clague, Michael J., Zech, Tobias·2018·Journal of Cell Biology
DOI 10.1083/jcb.201710051PMC PMC6028553
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Abstract

Transmembrane proteins in the sorting endosome are either recycled to their point of origin or destined for lysosomal degradation. Lysosomal sorting is mediated by interaction of ubiquitylated transmembrane proteins with the endosomal sorting complex required for transport (ESCRT) machinery. In this study, we uncover an alternative role for the ESCRT-0 component hepatocyte growth factor–regulated tyrosine kinase substrate (HRS) in promoting the constitutive recycling of transmembrane proteins. We find that endosomal localization of the actin nucleating factor Wiscott-Aldrich syndrome protein and SCAR homologue (WASH) requires HRS, which occupies adjacent endosomal subdomains. Depletion of HRS results in defective constitutive recycling of epidermal growth factor receptor and the matrix metalloproteinase MT1–MMP, leading to their accumulation in internal compartments. We show that direct interactions with endosomal actin are required for efficient recycling and use a model system of chimeric transferrin receptor trafficking to show that an actin-binding motif can counteract an ubiquitin signal for lysosomal sorting. Directed receptor recycling is used by cancer cells to achieve invasive migration. Accordingly, abrogating HRS- and actin-dependent MT1-MMP recycling results in defective matrix degradation and invasion of triple-negative breast cancer cells.

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  • A significant amount of the WASH complex is retained on endosomes even after retromer knocksideways.

    “Supporting evidence that a sub-population of the WASH complex is associated with endosomes independently of retromer (McNally et al., 2017; MacDonald et al., 2018), a significant amount of the WASH complex was retained on endosomes even after retromer knocksideways (Fig. 2C,E; Fig. S2B,D,E).”

    From Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting (2020) · cites this paper as MacDonald et al., 2018

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Metadata

Authors
MacDonald, E., Brown, L., Selvais, A., Liu, H., Waring, T., Newman, D., Bithell, J., Grimes, D., Urbé, S., Clague, M. J., & Zech, T.
Affiliations
  • Institute of Translational Medicine, Cellular and Molecular Physiology, University of Liverpool, Liverpool, England, UK 1
  • Institute of Cancer Stem Cell, Dalian Medical University, Dalian, China 2
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2018-06-11
Volume
217
Issue
7
Pages
2549-2564
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.201710051
PMC
PMC6028553
Cited by
62
References
2
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (vor, 465 d)
Funders
  • North West Cancer Research (1032, 932)
  • Breast Cancer Now (2014MayPR292)
  • Wellcome Trust (105350/Z/14/A, 105353)
  • Discovery Medicine North
  • Biotechnology and Biological Sciences Research Council (BB/M011186/1/1797330)

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