v-SNARE cellubrevin is required for basolateral sorting of AP-1B–dependent cargo in polarized epithelial cells

Fields, Ian C.; Shteyn, Elina; Pypaert, Marc; Proux-Gillardeaux, Véronique; Kang, Richard S.; Galli, Thierry; Fölsch, Heike

doi:10.1083/jcb.200610047

Cited by 77 publications

(122 citation statements)

References 58 publications

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“…Docking of apical transporters depends on the T-SNARE syntaxin 3 in MDCK cells (Low et al, 1996) and on a tetanus-insensitive V-SNARE (Galli et al, 1998;Low et al, 1998;Lafont et al, 1999). Docking of basolateral transporters requires syntaxin 4 (Low et al, 1996), rab 8 (Huber et al, 1993) and a V-SNARE, cellubrevin, which cooperates with AP-1B in basolateral membrane trafficking (Fields et al, 2007), as well as the exocyst (Grindstaff et al, 1998;Shipitsin and Feig, 2004; The EPP: machineries involved and their hijacking by cancer B Tanos and E Rodriguez-Boulan Yeaman et al, 2004b;Langevin et al, 2005), a multiprotein particle that is also a key regulator of yeast's secretory route (Potenza et al, 1992;TerBush and Novick, 1995;TerBush et al, 1996). Interestingly, the exocyst interacts with the clathrin adaptor AP1B (Folsch et al, 2003) and participates not only in biosynthetic delivery, but, also, in postendocytic recycling to both basolateral and apical membranes, the latter in association with the small GTPase Rab11a (Oztan et al, 2007).…”

Section: Polarized Trafficking Machinerymentioning

confidence: 99%

The epithelial polarity program: machineries involved and their hijacking by cancer

2008

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The Epithelial Polarity Program (EPP) adapts and integrates three ancient cellular machineries to construct an epithelial cell. The polarized trafficking machinery adapts the cytoskeleton and ancestral secretory and endocytic machineries to the task of sorting and delivering different plasma membrane (PM) proteins to apical and basolateral surface domains. The domain-identity machinery builds a tight junctional fence (TJ) between apical and basolateral PM domains and adapts ancient polarity proteins and polarity lipids on the cytoplasmic side of the PM, which have evolved to perform a diversity of polarity tasks across cells and species, to provide 'identity' to each epithelial PM domain. The 3D organization machinery utilizes adhesion molecules as positional sensors of other epithelial cells and the basement membrane and small GTPases as integrators of positional information with the activities of the domain-identity and polarized trafficking machineries. Cancer is a disease mainly of epithelial cells (90% of human cancers are carcinomas that derive from epithelial cells) that hijacks the EPP machineries, resulting in loss of epithelial polarity, which often correlates in extent with the aggressiveness of the tumor. Here, we review how the EPP integrates its three machineries and the strategies used by cancer to hijack them.

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Section: Polarized Trafficking Machinerymentioning

confidence: 99%

The epithelial polarity program: machineries involved and their hijacking by cancer

2008

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“…Finally, a recent study (Fields et al, 2007) reported the interaction of various basolateral proteins with different AP adaptors by a yeast two-hybrid approach, but the data obtained provide no information on specific routes in which these adaptors perform their function or on the role of RE in biosynthetic transport. Thus, the role of RE in biosynthetic transport and the sorting role of AP1B in RE is currently supported only by circumstantial evidence.…”

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confidence: 99%

“…However, the experiments did not quantitatively demonstrate the transport of basolateral proteins between TGN and RE or directly show that the sorting role of AP1B took place at RE. Similarly, another report demonstrated that ablation of RE with horseradish peroxidase (HRP)-peroxidase blocked transport of VSVG in the biosynthetic route, but did not demonstrate that under those conditions a significant mass of VSVG had left the TGN and quantitatively moved to RE, and more precisely, to RE containing AP1B.Finally, a recent study (Fields et al, 2007) reported the interaction of various basolateral proteins with different AP adaptors by a yeast two-hybrid approach, but the data obtained provide no information on specific routes in which these adaptors perform their function or on the role of RE in biosynthetic transport. Thus, the role of RE in biosynthetic transport and the sorting role of AP1B in RE is currently supported only by circumstantial evidence.…”

mentioning

confidence: 99%

Antibody to AP1B Adaptor Blocks Biosynthetic and Recycling Routes of Basolateral Proteins at Recycling Endosomes

Cancino

Torrealba

Soza

et al. 2007

MBoC

117

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The epithelial-specific adaptor AP1B sorts basolateral plasma membrane (PM) proteins in both biosynthetic and recycling routes, but the site where it carries out this function remains incompletely defined. Here, we have investigated this topic in Fischer rat thyroid (FRT) epithelial cells using an antibody against the medium subunit 1〉. This antibody was suitable for immunofluorescence and blocked the function of AP1B in these cells. The antibody blocked the basolateral recycling of two basolateral PM markers, Transferrin receptor (TfR) and LDL receptor (LDLR), in a perinuclear compartment with marker and functional characteristics of recycling endosomes (RE). Live imaging experiments demonstrated that in the presence of the antibody two newly synthesized GFP-tagged basolateral proteins (vesicular stomatitis virus G [VSVG] protein and TfR) exited the trans-Golgi network (TGN) normally but became blocked at the RE within 3-5 min.By contrast, the antibody did not block trafficking of green fluorescent protein (GFP)-LDLR from the TGN to the PM but stopped its recycling after internalization into RE in ϳ45 min. Our experiments conclusively demonstrate that 1) AP1B functions exclusively at RE; 2) TGN-to-RE transport is very fast and selective and is mediated by adaptors different from AP1B; and 3) the TGN and AP1B-containing RE cooperate in biosynthetic basolateral sorting. INTRODUCTIONEpithelial cells display an asymmetric distribution of plasma membrane (PM) proteins into apical and basolateral PM domains (Yeaman et al., 1999;Mostov et al., 2003; RodriguezBoulan et al., 2005). Early studies demonstrated that this polarity was achieved by sorting of newly synthesized proteins at the level of the trans-Golgi network (TGN; Rindler et al., 1984;Fuller et al., 1985;Griffiths and Simons, 1986) and of endocytosed proteins at the level of recycling endosomes (RE;Mostov and Cardone, 1995;Odorizzi and Trowbridge, 1997). Trafficking in both biosynthetic and recycling routes is controlled by apical sorting signals (e.g., N-and O-glycans, lipid anchors, and protein domains with affinity for lipid rafts), by microtubule motor determinants (Rodriguez-Boulan and Gonzalez, 1999;Schuck and Simons, 2004;Rodriguez-Boulan et al., 2005) and by basolateral sorting signals (e.g., tyrosine, dileucine, and monoleucine motifs, some similar to endocytic determinants, and noncanonic motifs not yet matching any consensus sequence; Rodriguez-Boulan et al., 2005). Tyrosine-based signals are recognized by a family of organelle-specific tetrameric AP (adaptor protein) adaptors via their subunit, whereas dileucine motifs may be recognized via large (␥ and ␦) and small ( 1, 3) subunits of AP adaptors acting together (Bonifacino and Lippincott-Schwartz, 2003;Janvier et al., 2003).The early paradigm of two separate sorting sites for proteins in biosynthetic or recycling pathways has, however, progressively shifted over the past decade to a different paradigm in which both TGN and RE share a sorting role in the biosynthetic route. This new paradigm emer...

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“…More recently, the RE has been increasingly recognized as a way station for post-Golgi exocytosis and sorting of membrane and soluble cargo proteins destined for the cell surface (2,6,12,17,25,29). In nonpolarized or early-polarized cells, basolateral proteins travel from the Golgi complex to the cell surface via the RE (2,24), where, according to recent studies, these proteins are also sorted (12). Some apical proteins also appear to traverse the RE, although this route remains more controversial (10).…”

mentioning

confidence: 99%

“…The RE compartment was initially designated for recycling proteins, such as transferrin-loaded transferrin receptor (TfR), back to the cell surface following endocytosis (31,42). More recently, the RE has been increasingly recognized as a way station for post-Golgi exocytosis and sorting of membrane and soluble cargo proteins destined for the cell surface (2,6,12,17,25,29). In nonpolarized or early-polarized cells, basolateral proteins travel from the Golgi complex to the cell surface via the RE (2,24), where, according to recent studies, these proteins are also sorted (12).…”

mentioning

confidence: 99%

Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis

Desclozeaux

Venturato²,

Wylie³

et al. 2008

American Journal of Physiology-Cell Physiology

135

141

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herin (E-cadherin) is a major determinant for the acquisition of epithelial cell polarity and for the maintenance of epithelial integrity. The compartments and trafficking components required to sort and transport Ecadherin to the basolateral cell surface remain to be fully defined. On the basis of previous data, we know that E-cadherin is trafficked via the recycling endosome (RE) in nonpolarized and newly polarized cells. Here we explore the role of the RE throughout epithelial morphogenesis in MDCK monolayers and cysts. Time-lapse microscopy in live cells, altering RE function biochemically, and expressing a dominant-negative form of Rab11 (DN-Rab11), each showed that the RE is always requisite for E-cadherin sorting and trafficking. The RE remained important for E-cadherin trafficking in MDCK cells from a nonpolarized state through to fully formed, polarized epithelial monolayers. During the development of epithelial cysts, DN-Rab11 disrupted E-cadherin targeting and trafficking, the subapical localization of pERM and actin, and cyst lumen formation. This final effect demonstrated an early and critical interdependence of Rab11 and the RE for E-cadherin targeting, apical membrane formation, and cell polarity in cysts.

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v-SNARE cellubrevin is required for basolateral sorting of AP-1B–dependent cargo in polarized epithelial cells

Cited by 77 publications

References 58 publications

The epithelial polarity program: machineries involved and their hijacking by cancer

The epithelial polarity program: machineries involved and their hijacking by cancer

Antibody to AP1B Adaptor Blocks Biosynthetic and Recycling Routes of Basolateral Proteins at Recycling Endosomes

Active Rab11 and functional recycling endosome are required for E-cadherin trafficking and lumen formation during epithelial morphogenesis

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