Receptor Salvage from the Prevacuolar Compartment Is Essential for Efficient Vacuolar Protein Targeting

DaSilva, Luis; Taylor, James L.; Hadlington, Jane L.; Hanton, Sally L.; Snowden, C.M.; Fox, Sarah Jane; Foresti, Ombretta; Brandizzí, Federica; Denecke, Jürgen

doi:10.1105/tpc.104.026351

Cited by 164 publications

(277 citation statements)

References 66 publications

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“…In plant cells, wortmannin also blocks the trafficking of some vacuolar proteins (Matsuoka et al, 1995;Di Sansebastiano et al, 1998) and prevents the recycling of VSR proteins from the PVC to the Golgi apparatus (daSilva et al, 2005(daSilva et al, , 2006. Morphologically, wortmannin induces the vacuolation of BP-80-labeled PVCs/MVBs in BY-2 cells (Tse et al, 2004;Lo and Jiang, 2006), and it seems that such a vacuolation is a general response to wortmannin treatment in various plant cell types and species (Miao et al, 2006;Tse et al, 2006).…”

Section: Wortmannin Targets Both Early and Late Endosomes (Pvc) In Tomentioning

confidence: 99%

Rice SCAMP1 Defines Clathrin-Coated,trans-Golgi–Located Tubular-Vesicular Structures as an Early Endosome in Tobacco BY-2 Cells

et al. 2007

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We recently identified multivesicular bodies (MVBs) as prevacuolar compartments (PVCs) in the secretory and endocytic pathways to the lytic vacuole in tobacco (Nicotiana tabacum) BY-2 cells. Secretory carrier membrane proteins (SCAMPs) are post-Golgi, integral membrane proteins mediating endocytosis in animal cells. To define the endocytic pathway in plants, we cloned the rice (Oryza sativa) homolog of animal SCAMP1 and generated transgenic tobacco BY-2 cells expressing yellow fluorescent protein (YFP)-SCAMP1 or SCAMP1-YFP fusions. Confocal immunofluorescence and immunogold electron microscopy studies demonstrated that YFP-SCAMP1 fusions and native SCAMP1 localize to the plasma membrane and mobile structures in the cytoplasm of transgenic BY-2 cells. Drug treatments and confocal immunofluorescence studies demonstrated that the punctate cytosolic organelles labeled by YFP-SCAMP1 or SCAMP1 were distinct from the Golgi apparatus and PVCs. SCAMP1-labeled organelles may represent an early endosome because the internalized endocytic markers FM4-64 and AM4-64 reached these organelles before PVCs. In addition, wortmannin caused the redistribution of SCAMP1 from the early endosomes to PVCs, probably as a result of fusions between the two compartments. Immunogold electron microscopy with high-pressure frozen/freeze-substituted samples identified the SCAMP1-positive organelles as tubular-vesicular structures at the trans-Golgi with clathrin coats. These early endosomal compartments resemble the previously described partially coated reticulum and trans-Golgi network in plant cells.

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Section: Wortmannin Targets Both Early and Late Endosomes (Pvc) In Tomentioning

confidence: 99%

Rice SCAMP1 Defines Clathrin-Coated,trans-Golgi–Located Tubular-Vesicular Structures as an Early Endosome in Tobacco BY-2 Cells

et al. 2007

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“…The 'Alanine zipper' also participates in the coiled coil formation as a result of its interaction with aromatic and/or large hydrophobic side-chain residues as Leu, Tyr and Ile. A highly conserved neighboring Leu [64] and Glu [68] patch binds directly to the C-terminal acidic region of CHMP1B, one of the human VPS46 homologs [64].…”

Section: Vps4mentioning

confidence: 99%

Exploring the ESCRTing machinery in eukaryotes

Winter

Hauser

2006

Trends in Plant Science

170

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The profile of protein sorting into multivesicular bodies (MVBs) has risen recently with the identification of three heteromeric complexes known as ESCRT-I,-II,-III (Endosomal Sorting Complex Required for Transport). Genetic analyses in yeast have identified up to 15 soluble class E VPS (vacuolar protein sorting) proteins that have been assigned to the ESCRT machinery and function in cargo recognition and sorting, complex assembly, vesicle formation and dissociation. Despite their functional importance in yeast and mammalian cells, little is known about their presence and function in other organisms including plants. We have made use of the fully sequenced genomes of Arabidopsis thaliana and Oryza sativa, Drosophila melanogaster and Caenorhabditis elegans to explore the identity, structural characteristics and phylogenetic relationships of proteins assigned to the ESCRT machinery.Multivesicular bodies (MVBs) are late endosomal organelles with up to several hundred interluminal vesicles that originate by invagination and budding of the limiting endosomal membrane (Figure 1) [1,2]. MVBs are also prevacuolar compartments involved in the retrograde endocytotic pathway where, upon fusion to vacuoles or lysosomes, the interluminal vesicles are released [3][4][5][6]. In yeast and mammals, MVBs are involved in sorting and degradation of transmembrane surface proteins as transporters (e.g. GAP1, STE6 and PDR5), receptors (e.g. EGFR, GHR, STE3 and STE2), in budding of viruses (e.g. HIV, MuLV and RSV) and in lipid partitioning [7,8]. However, MVBs are also central for sorting vacuolar proteins directly from the late Golgi to the anterograde and biosynthetic pathway ( Figure 1) [9]. Furthermore, MVBs operate in the exocytotic pathway and the secreted interluminal vesicles are known as exosomes (Figure 1) [10][11][12]. Thus, MVBs act as an intermediate station for cargo on the way to degradation, intracellular recycling and secretion ( Figure 1). Although MVBs have been described in plants, little is known about their biogenesis, cargos and function [2,4,[13][14][15][16]. These studies show that plant MVBs are prevacuolar compartments and are labeled by vacuolar sorting receptor (VSR) antibodies such as BP80 [5,17]. Plant MVBs are not only involved in the transport of proteins to lytic but also to protein-storage vacuoles. As plasmalemmasomes in tobacco, MVBs have been implicated in the internalization of arabinogalactanrich plasma membrane proteins that are sequestered within the vacuole [18] Upstream cargo recognition and sorting system of the ESCRT machineryThe entry of membrane proteins into the MVB pathway starts with the binding of monoubiquitinated cargos to the outer endosomal membrane and the recruitment of the ESCRT-I complex. This membrane association is mediated by ubiquitin-binding proteins that contain one or two UIMs or a GAT domain in combination with protein domains that had been implicated in binding to membranes such as the phosphatidylinositol-3 phosphate (PI3P) binding FYVE finger domain (Figure...

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“…This marker is a truncated form of the binding protein of 80 kDa (BP80), an extensively studied pea VSR (Brandizzi et al, 2002;Paris and Neuhaus, 2002;daSilva et al, 2005;Tse et al, 2004). The intra-luminal part of BP80, involved in interaction with the transported lytic enzymes (e.g.…”

Section: Atsnx1 Endosomes and Pvc Define A Similar Compartment In Aramentioning

confidence: 99%

“…The dissociation between VSRs and their ligands is thought to take place within the PVC due to the low luminal pH of this compartment. Then VSRs are recycled back to the TGN for an additional round of sorting, while lytic enzymes are routed towards the lytic vacuoles (daSilva et al, 2005). As AtSNX1 is a putative component of the Arabidopsis retromer complex, we surmised that AtSNX1 would also be localized to the PVC, like the other three proteins of the retromer analysed so far.…”

Section: Introductionmentioning

confidence: 99%

Evidence for a sorting endosome in Arabidopsis root cells

et al. 2007

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SummaryIn eukaryotic cells, the endocytic and secretory pathways are key players in several physiological processes. These pathways are largely inter-connected in animal and yeast cells through organelles named sorting endosomes. Sorting endosomes are multi-vesicular compartments that redirect proteins towards various destinations, such as the lysosomes or vacuoles for degradation, the trans-Golgi network for retrograde transport and the plasma membrane for recycling. In contrast, cross-talk between the endocytic and secretory pathways has not been clearly established in plants, especially in terms of cargo protein trafficking. Here we show by co-localization analyses that endosomes labelled with the AtSORTING NEXIN1 (AtSNX1) protein overlap with the pre-vacuolar compartment in Arabidopsis root cells. In addition, alteration of the routing functions of AtSNX1 endosomes by drug treatments leads to mis-routing of endocytic and secretory cargo proteins. Based on these results, we propose that the AtSNX1 endosomal compartment represents a sorting endosome in root cells, and that this specialized organelle is conserved throughout eukaryotes.

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Receptor Salvage from the Prevacuolar Compartment Is Essential for Efficient Vacuolar Protein Targeting

Cited by 164 publications

References 66 publications

Rice SCAMP1 Defines Clathrin-Coated,trans-Golgi–Located Tubular-Vesicular Structures as an Early Endosome in Tobacco BY-2 Cells

Rice SCAMP1 Defines Clathrin-Coated,trans-Golgi–Located Tubular-Vesicular Structures as an Early Endosome in Tobacco BY-2 Cells

Exploring the ESCRTing machinery in eukaryotes

Evidence for a sorting endosome in Arabidopsis root cells

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