Sorting Nexin-1 Mediates Tubular Endosome-to-TGN Transport through Coincidence Sensing of High- Curvature Membranes and 3-Phosphoinositides

Carlton, Jeremy G.; Bujny, Miriam V.; Peter, Brian J.; Oorschot, Viola; Rutherford, Anna C.; Mellor, Harry; Klumperman, Judith; McMahon, Harvey T.; Cullen, Peter J.

doi:10.1016/j.cub.2004.09.077

Cited by 431 publications

(613 citation statements)

References 37 publications

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“…One should be cautious to interpret data of knockdown and overexpression experiments because they often contradict. It was shown by siRNA that knockdown of SNX1 showed no effect on EGF receptor degradation (Gullapalli et al, 2004;Carlton et al, 2004) or on transferrin receptor trafficking (Carlton et al, 2004), whereas SNX1 is required for proper endosome retrieval of the CI-MPR (Carlton et al, 2005). This contrasts with the findings of previous studies using overexpression showing that overexpression of SNX1 enhances EGF receptor degradation (Kurten et al, 1996;Chin et al, 2001;Zheng et al, 2001), whereas other groups were unable to demonstrate that overexpression of SNX1 or SNX2, 3, or 4 increases the turnover of insulin or EGF receptors (Haft et al, 1998).…”

Section: Ehrab7a Overexpression Caused a Decrease Of Cp Activity Whimentioning

confidence: 67%

A Retromerlike Complex Is a Novel Rab7 Effector That Is Involved in the Transport of the Virulence Factor Cysteine Protease in the Enteric Protozoan ParasiteEntamoeba histolytica

Nakada‐Tsukui

Saito‐Nakano

Ali

et al. 2005

MBoC

137

173

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Vesicular trafficking plays an important role in a virulence mechanism of the enteric protozoan parasite Entamoeba histolytica as secreted and lysosomal cysteine protease (CP) contributes to both cytolysis of tissues and degradation of internalized host cells. Despite the primary importance of intracellular sorting in pathogenesis, the molecular mechanism of CP trafficking remains largely unknown. In this report we demonstrate that transport of CP is regulated through a specific interaction of Rab7A small GTPase (EhRab7A) with the retromerlike complex. The amoebic retromerlike complex composed of Vps26, Vps29, and Vps35 was identified as EhRab7A-binding proteins. The amoebic retromerlike complex specifically bound to GTP-EhRab7A, but not GDP-EhRab7A through the direct binding via the carboxy terminus of EhVps26. In erythrophagocytosis the retromerlike complex was recruited to prephagosomal vacuoles, the unique preparatory vacuole of digestive enzymes, and later to phagosomes. This dynamism was indistinguishable from that of EhRab7A, and consistent with the premise that the retromerlike complex is involved in the retrograde transport of putative hydrolase receptor(s) from preparatory vacuoles and phagosomes to the Golgi apparatus. EhRab7A overexpression caused enlargement of lysosomes and decrease of the cellular CP activity. The reduced CP activity was restored by the coexpression of EhVps26, implying that the EhRab7A-mediated transport of CP to phagosomes is regulated by the retromerlike complex. INTRODUCTIONRab GTPases play an essential role to regulate intracellular membrane trafficking. The compartmentalization and functions of Rab proteins are modulated at multiple layers of mechanisms including isoprenylation of the carboxy terminus, nucleotide exchange, and binding of specific effector molecules (Stenmark and Olkkonen, 2001;Takai et al., 2001;Tuvim et al., 2001). Among these modulators, effectors play key roles in the control of 7-90 Rab proteins depending on organisms from fission yeast and amoeba to mammals and plants. A variety of effectors have been identified and shown to interact with specific Rab protein. For instance, regulatory secretions of neurotransmitters from neurons or insulin from pancreatic ␤-cells are regulated by the specific interaction of Rab3 with its effectors (Jahn and Sudhof, 1999). At least four proteins, Rabphilin3, Rim1, Rim2, and Noc2, are known to bind Rab3 and recruit cAMP-GEFII, 14 -3-3, and zyxin, respectively, to regulate cAMP responsiveness, phosphoserine-dependent signaling, and the interaction with cytoskeleton (Kotake et al., 1997;Ozaki et al., 2000;Sun et al., 2003). The specificity of the Rab-effector interaction is attributable to primary sequence motifs in only a few cases including exophilins or Slip/Slac2, Rab3, and Rab27 effectors (Izumi et al., 2003). However, the majority of Rab effectors lack recognizable conserved binding motifs. For instance, Rab5 effectors, rabaptin-5, Rabex-5, EEA1, Rabenosyn-5, hVps34/p150, p110␤/p35␣, rabip4Ј, and rabankyrin-5, which a...

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Section: Ehrab7a Overexpression Caused a Decrease Of Cp Activity Whimentioning

confidence: 67%

A Retromerlike Complex Is a Novel Rab7 Effector That Is Involved in the Transport of the Virulence Factor Cysteine Protease in the Enteric Protozoan ParasiteEntamoeba histolytica

Nakada‐Tsukui

Saito‐Nakano

Ali

et al. 2005

MBoC

137

173

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“…In contrast, TfR-cluster were negative for SNX15 (Figure 18a, b), which was previously implicated in earlier sorting events such as the progression of CCVs to PI(3)P-enriched early endosomes (Danson, Brown et al 2013). Many SNXs contain BAR domains with membrane deforming activities (Carlton, Bujny et al 2004), some of which we found enriched on TfR-containing endosomes upon MTM1 depletion. Accordingly, we frequently observed strong tubulation of the endosomal recycling compartment in MTM1 knockdown cells (Figure 18c).…”

Section: Sub-plasma Membrane Early and Recycling Endosomes Accumulatementioning

confidence: 69%

“…Asn-Pro-x-Tyr (NPxY) motifs or PDZ (post synaptic density) -ligands, within the cytoplasmic domain of cargo proteins. Although SNX-BAR proteins can stabilize and drive tubule formation in vitro (Carlton, Bujny et al 2004), it remains unclear if SNX-BAR proteins are targeted to preexisting, tubular, PI-enriched endosomal subdomains or remodel the endosomal membrane themselves.…”

Section: Endosomal Sorting Occurs Via Tubular Cargo-enriched Subdomainsmentioning

confidence: 99%

A phosphoinositide conversion mechanism for exit from endosomes

Ketel¹,

Krauß²,

Nicot³

et al. 2016

Nature

161

177

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I owe special thanks to Marnix Wieffer and Michael Krauß, who spent a lot of time helping me to get started in the lab, to overcome numerous experimental problem, I was not sure how to deal with, and frequently joined in discussions about my project with excellent advice. I am really grateful for your experimental support, Michael, and the time you invested in the project during our paper revision.Further, I would like to thank Jocelyn Laporte and his group, especially Anne-Sophie Nicot, at the IGBMC in Strasbourg for their support and a very fruitful collaboration, and Carsten Schultz and his group at the EMBL in Heidelberg for their support and constant supply with PIP/AMs. I owe special thanks to Dmytro Puchkov for the ultrastructural analysis and Eberhard Krause for mass spectrometry done within this project. I also need to acknowledge Markus Wenk and Federico Torta at the Singapore Lipidomics Incubator for joining the project at a very late stage, when we urgently needed help from lipidomics specialists. It was a pity that experiments did not work out as planned.I would further like to express my gratitude to two very skilled technicians in the AG Haucke lab: Silke Zillmann and Delia Löwe. Without your help it would have been impossible to achieve so much within the limited amount of time I had during the paper revision. by VPS34-IN1 treatment................................................... 52 2.3.11 Fluorescence microscopy................................................................................. 53 2.3.12 Flow cytometry............................................................................................ III SummaryPhosphoinositides (PIs) are a minor class of short-lived phospholipids that serve as crucial signposts of membrane identity. Thereby, PIs full fill important functions in cell signaling and membrane transport. PI 4-phosphates such as phosphatitylinositol-4-phosphate (PI(4)P) and phosphatitylinositol-4,5-bisphosphate (PI(4,5)P 2 ) are enriched at the plasma membrane (PM), on secretory organelles and lysosomes, while PI 3-phosphates, i.e.phosphatitylinositol-3-phosphate (PI(3)P), are a hallmark of the endosomal system.Directional transport between these compartments, thus, requires regulated PI conversion.However, PI conversion in exit from PI(3)P-enriched endosomes en route to the PI(4)P-and PI(4,5)P 2 -positive PM in endosomal recycling remained unknown.Here, we report that cargo exit from endosomes requires removal of PI(3)P by the PI(3)P 3-phosphatase myotubularin 1 (MTM1), and concomitant PI(4)P synthesis by PI 4-kinase type II α (PI4K2α). Loss of MTM1 causes endosomal accumulation of PI(3)P and PI(3)P effector proteins, i.e. sorting nexins, Kif16b-mediated outward traffic of PI(3)P containing endosomes and sub-plasmalemmal accumulation of exocytosis-deficient endosomes. As PI4K2α associates with MTM1 and thereby facilitates membrane recruitment of MTM1, these phenotypic changes are mimicked by loss of PI4K2α. The conversion of PI(3)P-to-PI(4)P is paralleled by a switch i...

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“…Canonical BAR domains including ASAP1 BAR consist of three long, kinked ␣-helices that are bundled to form crescent-shaped homodimers . Several BAR domains found in amphipysin, endophilin, sorting nexins and Arf GAPs such as ACAP1 and ASAP1 sense or induce membrane curvature (Takei et al, 1999;Carlton et al, 2004;Peter et al, 2004;Masuda et al, 2006;Nie et al, 2006). Other BAR proteins, arfaptin 2 and APPL1, interact with small G proteins (Tarricone et al, 2001;Miaczynska et al, 2004).…”

Section: Discussionmentioning

confidence: 99%

Arf GTPase-activating Protein ASAP1 Interacts with Rab11 Effector FIP3 and Regulates Pericentrosomal Localization of Transferrin Receptor–positive Recycling Endosome

Inoue

Prekeris

et al. 2008

MBoC

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ADP-ribosylation factors (Arfs) and Arf GTPase-activating proteins (GAPs) are key regulators of membrane trafficking and the actin cytoskeleton. The Arf GAP ASAP1 contains an N-terminal BAR domain, which can induce membrane tubulation. Here, we report that the BAR domain of ASAP1 can also function as a protein binding site. Two-hybrid screening identified FIP3, which is a putative Arf6-and Rab11-effector, as a candidate ASAP1 BAR domain-binding protein. Both coimmunoprecipitation and in vitro pulldown assays confirmed that ASAP1 directly binds to FIP3 through its BAR domain. ASAP1 formed a ternary complex with Rab11 through FIP3. FIP3 binding to the BAR domain stimulated ASAP1 GAP activity against Arf1, but not Arf6. ASAP1 colocalized with FIP3 in the pericentrosomal endocytic recycling compartment. Depletion of ASAP1 or FIP3 by small interfering RNA changed the localization of transferrin receptor, which is a marker of the recycling endosome, in HeLa cells. The depletion also altered the trafficking of endocytosed transferrin. These results support the conclusion that ASAP1, like FIP3, functions as a component of the endocytic recycling compartment. INTRODUCTIONArf family GTP-binding proteins and their GTPase-activating proteins (Arf GAPs) play crucial roles for membrane traffic and actin remodeling (D'Souza-Schorey and Chavrier, 2006;Gillingham and Munro, 2007). Arf GAPs share the same catalytic domain, the Arf GAP domain, which is responsible for GTP hydrolysis. In humans, 31 genes encoding proteins with Arf GAP domains have been found. They are classified into several subfamilies based on their domain structures Inoue and Randazzo, 2007). Three subfamilies, ArfGAPs, SMAPs, and GITs, have an Arf GAP domain at the N-terminus of the molecules. In contrast, the others, which are called AZAP-family Arf GAPs, contain an Arf GAP domain following a pleckstrin homology (PH) domain in the middle of the protein. They are subdivided into four subfamilies, ASAPs, ACAPs, ARAPs, and AGAPs.ASAP1 is one of the best-characterized Arf GAPs. In addition to PH and Arf GAP domains, ASAP1 contains an N-terminal Bin, Amphiphysin, and Rvs167/Rvs161 (BAR) domain and, in the C-terminal half of the protein, a proline (Pro)-rich domain and Src homology 3 (SH3) domain. Other ASAP isoforms, ASAP2 and ASAP3, have similar domain structures and high homology, especially in the Arf GAP domains, although ASAP3 lacks C-terminal SH3 domain (Ha et al., 2008). Through its Pro-rich and SH3 domains, ASAP1 interacts with a number of proteins, which are mainly adhesion-and actin cytoskeleton-related proteins including Src, focal adhesion kinase (FAK), Crk/CrkL, and cortactin (Brown et al., 1998;Liu et al., 2002;Oda et al., 2003;Onodera et al., 2005;Bharti et al., 2007). ASAP1 is a component of three integrated membrane/actin cytoskeleton structures: focal adhesions, circular dorsal ruffles (CDRs) and invadopodia/podosomes. ASAP1 associates with focal adhesions in fibroblasts . The focal adhesion localization depends on the interaction of ASAP1 with FA...

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Sorting Nexin-1 Mediates Tubular Endosome-to-TGN Transport through Coincidence Sensing of High- Curvature Membranes and 3-Phosphoinositides

Abstract: We conclude that through coincidence detection SNX1 associates with a microdomain of the early endosome-characterized by high membrane curvature and the presence of 3-phosphoinositides-from where it regulates tubular-based endosome-to-TGN retrieval of the CI-MPR.

Cited by 431 publications

References 37 publications

A Retromerlike Complex Is a Novel Rab7 Effector That Is Involved in the Transport of the Virulence Factor Cysteine Protease in the Enteric Protozoan ParasiteEntamoeba histolytica

A Retromerlike Complex Is a Novel Rab7 Effector That Is Involved in the Transport of the Virulence Factor Cysteine Protease in the Enteric Protozoan ParasiteEntamoeba histolytica

A phosphoinositide conversion mechanism for exit from endosomes

Arf GTPase-activating Protein ASAP1 Interacts with Rab11 Effector FIP3 and Regulates Pericentrosomal Localization of Transferrin Receptor–positive Recycling Endosome

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