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The Retromer, Sorting Nexins and the Plant Endomembrane Protein Trafficking Nicole Heucken and Rumen Ivanov*

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The Retromer, Sorting Nexins and the Plant Endomembrane Protein Trafficking Nicole Heucken and Rumen Ivanov* © 2018. Published by The Company of Biologists Ltd | Journal of Cell Science (2018) 131, jcs203695. doi:10.1242/jcs.203695 REVIEW SPECIAL ISSUE: PLANT CELL BIOLOGY The retromer, sorting nexins and the plant endomembrane protein trafficking Nicole Heucken and Rumen Ivanov* ABSTRACT to distinct subdomains of the compartment. This shows that the Protein sorting in the endomembrane system is responsible for the many functions of the TGN might, to a certain extent, be spatially coordination of cellular functions. Plant intracellular trafficking has its separated (Bassham et al., 2000; Sanderfoot et al., 2001; Staehelin own unique features, which include specific regulatory aspects of and Kang, 2008). endosomal sorting and recycling of cargo proteins, mediated by the The late endosome is a structure with smaller internal (luminal) retromer complex. Recent work has led to significant progress in vesicles, giving it the name multivesicular body (MVB). From understanding the role of Arabidopsis retromer subunits in recycling the TGN, proteins performing functions in the tonoplast or in the vacuolar sorting receptors and plasma membrane proteins. As a vacuole, or those targeted for vacuolar degradation, pass through the consequence, members of the sorting nexin (SNX) protein family and MVB (Fig. 1). The MVB was shown to originate from the TGN their interaction partners have emerged as critical protein trafficking (Scheuring et al., 2011), supporting the idea that endomembrane regulators, in particular with regard to adaptation to environmental compartments represent continuous stages, rather than static structures change, such as temperature fluctuations and nutrient deficiency. In (Robinson and Neuhaus, 2016). However, it needs to be noted that other this Review, we discuss the known and proposed functions of the transport routes are known, such as secretion from the Golgi to the PM comparatively small Arabidopsis SNX protein family. We review the bypassing the TGN and direct ER-to-vacuole transport (Crowell et al., available information on the role of the three Bin-Amphiphysin-Rvs 2009; Viotti et al., 2013), whose prominence remains to be determined. (BAR)-domain-containing Arabidopsis thaliana (At)SNX proteins and Transport between compartments is bidirectional and proteins discuss their function in the context of their potential participation in may undergo retrograde transport towards a preceding trafficking the plant retromer complex. We also summarize the role of AtSNX1- stage (Fig. 1). A form of retrograde transport is the recycling of interacting proteins in different aspects of SNX-dependent protein vacuolar sorting receptors (VSRs) and PM proteins. In the first case, trafficking and comment on the potential function of three novel, as yet soluble cargo proteins, such as acid hydrolases, move towards the unexplored, Arabidopsis SNX proteins. vacuole owing to their interaction with VSRs already at the ER (Kunzl et al., 2016; Niemes et al., 2010a). The conditions in the KEY WORDS: Retromer, Sorting nexin, Protein sorting, Vacuolar TGN lumen promote the dissociation of the complex, and whereas sorting receptor, Transporter recycling, Environmental response the soluble cargos proceed with the flow towards the vacuole, the VSRs are transported backwards (recycled) towards the ER (Kunzl Introduction et al., 2016; Robinson and Neuhaus, 2016). Similarly, endocytosed The correct distribution of proteins in the endomembrane system is PM proteins – such as transporters and transmembrane receptors – critical for the maintenance of cellular functions and the survival of can be recycled back to the PM by being actively diverted from the the organism. In plants, trafficking towards the plasma membrane default vacuolar degradation pathway (Barberon et al., 2011; (PM) or the vacuole is a multistep process occurring through several Dhonukshe et al., 2007; Ivanov et al., 2014; Kasai et al., 2011; Luo intracellular compartments. Transmembrane or soluble luminal et al., 2015; Viotti et al., 2010). The wealth of often contradictory proteins are synthesized at the endoplasmic reticulum (ER) and data suggests that the sorting events that underlie these recycling transported towards the Golgi (Fig. 1). The cis-Golgi cisternae processes occur at the TGN and most probably involve the early accept material from the ER and gradually mature. Ultimately, they stages of MVB maturation (Robinson and Neuhaus, 2016). form a new tubular-vesicular structure, the trans-Golgi network The retromer is a key protein complex involved in cargo recycling (TGN), which contains the ER-derived proteins. In plants, the TGN and retrograde transport. Its components were identified in screens exists close to the trans-Golgi face, but also as a Golgi-independent for yeast (Saccharomyces cerevisiae) mutants defective in vacuolar compartment (Kang et al., 2011; Viotti et al., 2010). It is a major trafficking (Paravicini et al., 1992; Seaman et al., 1998). The hub where the two transport routes – one leading to the PM and the retromer consists of two subcomplexes, the core retromer and the other to the vacuole – are separated. The TGN fulfills the role of an sorting nexin (SNX) subcomplex (Fig. 2A). In this Review, we early endosome (Dettmer et al., 2006; Lam et al., 2007), and is also discuss the role of the retromer complex and SNXs in plant protein responsible for sorting and recycling material to or from the Golgi, sorting. By drawing comparison to the yeast and mammalian the PM and the lytic pathway (Gu et al., 2001; Kunzl et al., 2016; systems, we outline the common and specific functions of the plant Luo et al., 2015; Paez Valencia et al., 2016; Reguera et al., 2015). retromer. We further concentrate on the plant SNX protein family, Consistent with this, certain TGN-localized protein markers localize which consists of three previously known and three novel, as yet uncharacterized, proteins, and we discuss their localization, Institute of Botany, Heinrich-Heine University, Universitätsstrasse 1, 40225 regulation and functions. Düsseldorf, Germany. The retromer complex in yeast and mammals *Author for correspondence ([email protected]) In yeast, the core retromer complex is composed of three proteins: R.I., 0000-0001-7909-4123 vacuolar protein sorting 35 (Vps35p), Vps29p and Vps26p (also Journal of Cell Science 1 REVIEW Journal of Cell Science (2018) 131, jcs203695. doi:10.1242/jcs.203695 A SNX dimer Core retromer MVB VPS26 VPS29 VPS35 SNX1 SNX2 PM Vacuole B 302 AtVPS26a (At5g53530) AtVPS26b (At4g27690) 303 190 AtVPS29 (At3g47810) 787 AtVPS35a (At2g17790) 790 AtVPS35b (At1g75850) TGN 790 AtVPS35c (At3g51310) Golgi Nucleus C S16 402 AtSNX1 (At5g06140) ER 587 AtSNX2a (At5g58440) 572 AtSNX2b (At5g07120) Key Secretion Endocytosis 706 AtSNX3.1 (At1g15240.1) Degradation Recycling 1020 AtSNX3.2 (At1g15240.2) AtSNX3.3 (At1g15240.3) 1012 Fig. 1. Endomembrane trafficking pathways in plant cells. Proteins leaving the ER pass the Golgi and localize to the TGN, where the pathways towards the 994 cell surface and the vacuole split (dark gray arrows). Proteins destined for AtSNX4 (At2g15900) the vacuole are transported into the MVB. PM material is endocytosed towards 938 the TGN (blue arrow) and sent for vacuolar degradation via the MVB (orange AtSNX5 (At3g48195) arrows). During the early stages of MVB maturation, certain proteins can be retrieved from the vacuolar pathway and be recycled (green arrows). D 1127 Mdm1p (NM_001182466) known as Pep8p). Vps35p functions as the binding factor for 957 membranes of the prevacuolar compartment and is responsible for the HsSNX13 (NM_015132) interaction with the sorting receptors which are to be recycled (Hierro HsSNX14 (AY044865) 886 992 et al., 2007; Seaman et al., 1998). The classical SNX subcomplex is a HsSNX19 (AF395843) Vps5p–Vps17p heterodimer. Its function is to sense and/or induce HsSNX25 (AY601647) 840 membrane curvature through the Bin-Amphiphysin-Rvs (BAR) domains in both proteins (Peter et al., 2004), which drives the Key retromer towards the forming of endosomal tubules. PX SNX1/2-like MPP signature RGS Retromer components exist in all eukaryotes (Cullen and PX19-like Vps35 signature TM helix Korswagen, 2012). In humans (Homo sapiens), homologs to four PXA BAR Arrestin_N signature of the five yeast retromer proteins have been identified. The Vps17p RING9 PXC protein appears to have no direct homolog, whereas Vps5p has two, SNX1 and SNX2 (Haft et al., 1998; Horazdovsky et al., 1997). Loss Arabidopsis of both proteins causes the human retromer to dissociate from the Fig. 2. The retromer and the SNX protein family. (A) The retromer is a pentamer consisting of two subcomplexes: the core retromer, a endosomal membrane and leads to failure in the trafficking of trimer of the subunits VPS26, VPS29 and VPS35 (light to dark blue), and a SNX the mannose 6-phosphate receptors back to the TGN (Rojas et al., heterodimer (yellow). VPS35 and the SNX proteins, but not VPS26 and VPS29 2007). In addition to the BAR domain, sorting nexins are interact with the membrane surface. In yeast and mammals, the VPS29 subunit characterized by the presence of a specific type of PHOX- interacts with the SNX subcomplex (not depicted). In plants, an interaction homology (PX) domain that allows them to bind to membrane between the two subcomplexes has thus far not been demonstrated. (B) The phosphoinositides (Ponting, 1996; Seaman and Williams, 2002; Arabidopsis genome contains two VPS26-encoding genes, one encoding VPS29 and three encoding VPS35.
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