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Receptor-mediated transport of vacuolar proteins: a critical analysis and a new model

  • New Ideas in Cell Biology
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Abstract

In this article we challenge the widely accepted view that receptors for soluble vacuolar proteins (VSRs) bind to their ligands at the trans-Golgi network (TGN) and transport this cargo via clathrin-coated vesicles (CCV) to a multivesicular prevacuolar compartment. This notion, which we term the “classical model” for vacuolar protein sorting, further assumes that low pH in the prevacuolar compartment causes VSR–ligand dissociation, resulting in a retromer-mediated retrieval of the VSRs to the TGN. We have carefully evaluated the literature with respect to morphology and function of the compartments involved, localization of key components of the sorting machinery, and conclude that there is little direct evidence in its favour. Firstly, unlike mammalian cells where the sorting receptor for lysosomal hydrolases recognizes its ligand in the TGN, the available data suggests that in plants VSRs interact with vacuolar cargo ligands already in the endoplasmic reticulum. Secondly, the evidence supporting the packaging of VSR–ligand complexes into CCV at the TGN is not conclusive. Thirdly, the prevacuolar compartment appears to have a pH unsuitable for VSR–ligand dissociation and lacks the retromer core and the sorting nexins needed for VSR recycling. We present an alternative model for protein sorting in the TGN that draws attention to the much overlooked role of Ca2+ in VSR–ligand interactions and which may possibly also be a factor in the sequestration of secretory proteins.

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Abbreviations

BFA:

Brefeldin A

CCV:

Clathrin-coated vesicle

ER:

Endoplasmic reticulum

ESCRT:

Endosomal sorting complex required for transport

LBD:

Lumenal binding domain

MPR:

Mannose 6-phosphate receptor

MVB:

Multivesicular body

TGN:

trans-Golgi network

VSR:

Vacuolar sorting receptor

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Acknowledgments

We thank Nadine Paris (Institut National de la Recherche Agronomique/Montpellier SupAgro/Universite´ Montpellier, France) and Karin Schumacher (Centre for Organismal Studies, University of Heidelberg, Germany) for allowing us to cite unpublished results. The financial support of the Deutsche Forschungsgemeinschaft (PI 769/1-2 and RO 440/11-4) is gratefully acknowledged.

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The authors declare that they have no conflict of interest.

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  1. Centre for Organismal Studies (COS), University of Heidelberg, Heidelberg, Germany

    David G. Robinson

  2. Center for Plant Molecular Biology (ZMBP), University of Tübingen, Auf der Morgenstelle 3, 72076, Tübingen, Germany

    Peter Pimpl

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Robinson, D.G., Pimpl, P. Receptor-mediated transport of vacuolar proteins: a critical analysis and a new model. Protoplasma 251, 247–264 (2014). https://doi.org/10.1007/s00709-013-0542-7

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