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Sequence-dependent cargo recognition by SNX-BARs mediates retromer-independent transport of CI-MPR

Simonetti, Boris, Danson, Chris M., Heesom, Kate J., Cullen, Peter J.·2017·Journal of Cell Biology
DOI 10.1083/jcb.201703015
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Abstract

Endosomal recycling of transmembrane proteins requires sequence-dependent recognition of motifs present within their intracellular cytosolic domains. In this study, we have reexamined the role of retromer in the sequence-dependent endosome-to–trans-Golgi network (TGN) transport of the cation-independent mannose 6-phosphate receptor (CI-MPR). Although the knockdown or knockout of retromer does not perturb CI-MPR transport, the targeting of the retromer-linked sorting nexin (SNX)–Bin, Amphiphysin, and Rvs (BAR) proteins leads to a pronounced defect in CI-MPR endosome-to-TGN transport. The retromer-linked SNX-BAR proteins comprise heterodimeric combinations of SNX1 or SNX2 with SNX5 or SNX6 and serve to regulate the biogenesis of tubular endosomal sorting profiles. We establish that SNX5 and SNX6 associate with the CI-MPR through recognition of a specific WLM endosome-to-TGN sorting motif. From validating the CI-MPR dependency of SNX1/2–SNX5/6 tubular profile formation, we provide a mechanism for coupling sequence-dependent cargo recognition with the biogenesis of tubular profiles required for endosome-to-TGN transport. Therefore, the data presented in this study reappraise retromer’s role in CI-MPR transport.

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  • SNX5 knocksideways in SNX5/SNX6 double-knockout HeLa cells led to the time-resolved appearance of a CI-MPR missorting phenotype, defined by reduced enrichment of the CI-MPR at the Golgin97 or TGN46-labelled TGN, with maximum penetrance at 6 h.

    “Consistent with the role of SNX5 in the ESCPE-1-mediated endosome-to-TGN transport of the CI-MPR (Kvainickas et al., 2017; Simonetti et al., 2017, 2019), SNX5 knocksideways in SNX5/SNX6 double-knockout HeLa cells led to the time-resolved appearance of a CI-MPR missorting phenotype as defined by a reduced enrichment of the CI-MPR at the Golgin97 or TGN46-labelled TGN with a maximum penetrance at 6”

    From Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting (2020) · cites this paper as Simonetti et al., 2017

  • The authors and others have recently questioned the precise role of retromer in CI-MPR transport.

    “However, we, and others, have recently questioned the precise role of retromer in this pathway (Kvainickas et al., 2017; Simonetti et al., 2017).”

    From Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting (2020) · cites this paper as Simonetti et al., 2017

  • Given that endosome-to-TGN transport of the CI-MPR is considered to occur over about 20 to 30 min, acute perturbation of retromer function does not appear to lead to a detectable defect in the endosomal sorting of the CI-MPR.

    “Given that the endosome-to-TGN transport of the CI-MPR is considered to occur over a period of ∼20 to 30 min (Seaman, 2004), the acute perturbation of retromer function does not appear to lead to a detectable defect in the endosomal sorting of the CI-MPR (Kvainickas et al., 2017; Simonetti et al., 2017).”

    From Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting (2020) · cites this paper as Simonetti et al., 2017

  • Expression of the GFP-FRB-SNX5 chimera in a previously isolated and characterised SNX5/SNX6 double-knockout HeLa cell line reverted the observed missorting of the CI-MPR and allowed the receptor to return to its normal steady-state localisation.

    “Expression of the GFP–FRB–SNX5 chimera in a previously isolated and characterised SNX5/SNX6 double-knockout HeLa cell line (Simonetti et al., 2017) reverted the observed missorting of the CI-MPR and allowed the receptor to return to its normal steady-state localisation (Fig. S4A,B).”

    From Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting (2020) · cites this paper as Simonetti et al., 2017

  • A subpopulation of the WASH complex is associated to endosomes independently of retromer.

    “That said, increasing evidence suggests that a subpopulation of the WASH complex is associated to endosomes independently of retromer (McNally et al., 2017; Kvainickas et al., 2017; Simonetti et al., 2017; MacDonald et al., 2018).”

    From Acute inactivation of retromer and ESCPE-1 leads to time-resolved defects in endosomal cargo sorting (2020) · cites this paper as Simonetti et al., 2017

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Metadata

Authors
Simonetti, B., Danson, C. M., Heesom, K. J., & Cullen, P. J.
Affiliations
  • School of Biochemistry, University of Bristol, Bristol, England, UK 1
  • Proteomics Facility, School of Biochemistry, University of Bristol, Bristol, England, UK 2
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2017-09-21
Volume
216
Issue
11
Pages
3695-3712
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.201703015
Cited by
214
References
2
Language
en
Licence
Funders
Wellcome Trust (089928, 104568, 083474)

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