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Cargo-selective SNX-BAR proteins mediate retromer trimer independent retrograde transport

Kvainickas, Arunas, Jimenez-Orgaz, Ana, Nägele, Heike, Hu, Zehan, Dengjel, Jörn, Steinberg, Florian·2017·Journal of Cell Biology
DOI 10.1083/jcb.201702137PMC PMC5674888
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Abstract

The retromer complex, which recycles the cation-independent mannose 6-phosphate receptor (CI-MPR) from endosomes to the trans-Golgi network (TGN), is thought to consist of a cargo-selective VPS26–VPS29–VPS35 trimer and a membrane-deforming subunit of sorting nexin (SNX)–Bin, Amphyphysin, and Rvs (BAR; SNX-BAR) proteins. In this study, we demonstrate that heterodimers of the SNX-BAR proteins, SNX1, SNX2, SNX5, and SNX6, are the cargo-selective elements that mediate the retrograde transport of CI-MPR from endosomes to the TGN independently of the core retromer trimer. Using quantitative proteomics, we also identify the IGF1R, among more potential cargo, as another SNX5 and SNX6 binding receptor that recycles through SNX-BAR heterodimers, but not via the retromer trimer, in a ligand- and activation-dependent manner. Overall, our data redefine the mechanics of retromer-based sorting and call into question whether retromer indeed functions as a complex of SNX-BAR proteins and the VPS26–VPS29–VPS35 trimer.

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  • These data support that in metazoans retromer and ESCPE-1 have evolved into functionally distinct complexes.

    “These data therefore support the in vivo evidence that in metazoans retromer and ESCPE-1 have evolved into functionally distinct complexes (Kvainickas et al., 2017; Simonetti et al., 2017, 2019; Strutt et al., 2019).”

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

  • The metazoan equivalent assembly has evolved into two functionally distinct complexes, the retromer (VPS26-VPS35-VPS29) and the ESCPE-1 (SNX1/SNX2 and SNX5/SNX6) complexes.

    “An increasing body of biochemical, cellular and in vivo functional data are consistent with the equivalent metazoan assembly having evolved into two functionally distinct complexes, the retromer (VPS26–VPS35–VPS29) and the ESCPE-1 (SNX1/SNX2 and SNX5/SNX6) complexes (Norwood et al., 2011; Swarbrick et al., 2011; Kvainickas et al., 2017; Simonetti et al., 2017, 2019; Strutt et al., 2019).”

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

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Metadata

Authors
Kvainickas, A., Jimenez-Orgaz, A., Nägele, H., Hu, Z., Dengjel, J., & Steinberg, F.
Affiliations
  • Center for Biological Systems Analysis, Albert Ludwigs Universitaet Freiburg, Freiburg, Germany 1
  • Department of Biology, Fribourg University, Fribourg, Switzerland 3
ORCID
Venue
Journal of Cell Biology
Publisher
Rockefeller University Press
Published
2017-09-21
Volume
216
Issue
11
Pages
3677-3693
ISSN
  • 0021-9525
  • 1540-8140
DOI
10.1083/jcb.201702137
PMC
PMC5674888
Cited by
190
References
2
Language
en
Licence
Funders
Deutsche Forschungsgemeinschaft (DFG STE2310/1-1)

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