Association of Rab25 and Rab11a with the Apical Recycling System of Polarized Madin–Darby Canine Kidney Cells

Casanova, James E.; Wang, Xiaoye; Kumar, Ravindra; Bhartur, Sheela G.; Navarre, Jennifer; Woodrum, Julie E.; Altschuler, Yoram; Ray, Greg S.; Goldenring, James R.

doi:10.1091/mbc.10.1.47

Cited by 369 publications

(382 citation statements)

References 51 publications

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“…As described, AREs are enriched with transcytotic dIgA (Apodaca et al, 1994) and Rab 25 (Casanova et al, 1999), but are relatively depleted of Tfn (Apodaca et al, 1994). Results presented in Figure 8, A and B, fulfilled these criteria, hence suggesting that Cav1-positive organelles are either linked or reside in proximity to AREs (Bush et al, 2006).…”

Section: Cav1 Codistributes With Diga-pigr and Rab25-positive Clustersupporting

confidence: 64%

Cholesterol-sensitive Modulation of Transcytosis

Leyt

Melamed-Book

Vaerman

et al. 2007

MBoC

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Cholesterol-rich membrane domains (e.g., lipid rafts) are thought to act as molecular sorting machines, capable of coordinating the organization of signal transduction pathways within limited regions of the plasma membrane and organelles. The significance of these domains in polarized postendocytic sorting is currently not understood. We show that dimeric IgA stimulates the incorporation of its receptor into cholesterol-sensitive detergent-resistant membranes confined to the basolateral surface/basolateral endosomes. A fraction of human transferrin receptor was also found in basolateral detergent-resistant membranes. Disrupting these membrane domains by cholesterol depletion (using methyl-␤-cyclodextrin) before ligand-receptor internalization caused depolarization of traffic from endosomes, suggesting that cholesterol in basolateral lipid rafts plays a role in polarized sorting after endocytosis. In contrast, cholesterol depletion performed after ligand internalization stimulated cargo transcytosis. It also stimulated caveolin-1 phosphorylation on tyrosine 14 and the appearance of the activated protein in dimeric IgA-containing apical organelles. We propose that cholesterol depletion stimulates the coupling of transcytotic and caveolin-1 signaling pathways, consequently prompting the membranes to shuttle from endosomes to the plasma membrane. This process may represent a unique compensatory mechanism required to maintain cholesterol balance on the cell surface of polarized epithelia. INTRODUCTIONIn humans, the major antibody that mediates immunological defense against mucosal infections is dimeric IgA (dIgA). This antibody is produced by plasma cells in the lamina propria located underneath the mucosal surface (reviewed in Lamm et al., 1995;Rojas and Apodaca, 2002) and is carried from the blood to mucosal secretions by the polymeric immunoglobulin receptor (pIgR). The itinerary of pIgR and its ligand was intensively studied in the polarized MadinDarby canine kidney (MDCK) cell line that heterologously expresses rabbit pIgR (for a recent review, see Rojas and Apodaca, 2002). The receptor is initially delivered from the trans-Golgi network (TGN) to the basolateral plasma membrane, where it encounters and binds dIgA. The complex is subsequently internalized and transcytosed to the apical plasma membrane of the cell. At that surface, the ectodomain of pIgR is proteolytically cleaved off to yield the secretory component (SC), which is released together with dIgA into mucosal secretions. In the course of transcytosis, pIgRdIgA complexes traverse various endosomal compartments, among which is an endocytic compartment located immediately underneath the apical surface (Gibson et al., 1998). This apical compartment, defined as apical recycling endosomes (AREs), is enriched in dIgA and is relatively deficient in recycling transferrin (Apodaca et al., 1994;Barroso and Sztul, 1994;Brown et al., 2000). AREs are thought to play a unique role in transcytosis, possibly by exploiting apical recycling mechanisms to shuttle transcy...

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Section: Cav1 Codistributes With Diga-pigr and Rab25-positive Clustersupporting

confidence: 64%

Cholesterol-sensitive Modulation of Transcytosis

Leyt

Melamed-Book

Vaerman

et al. 2007

MBoC

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“…Figure 3C, 2-5). The ARE was visualized using an antibody raised against rab11a, a well-established ARE-associated small GTPase (Casanova et al, 1999;Brown et al, 2000;Leung et al, 2000;Prekeris et al, 2000). In parental HepG2 cells, rab11a labeling was exclusively subapical, as expected (Figure 4, F and G).…”

supporting

confidence: 72%

“…These data suggest that expression of the AKAP-IS peptide and concomitant reduction of centrosome-associated PKA-RII␣ interferes with the subapical positioning of the centrosome and the orientation of a major part of the microtubule net- work in a manner that seems unrelated to the enzymatic activity of PKA. Several endosomal compartments such as the CE/SAC and the rab11a-positive ARE are typically concentrated around the centrosome in epithelial cells (Casanova et al, 1999;Leung et al, 2000;Hobdy-Henderson et al, 2003), and they mediate the transcellular flow of membranes (for review, see Hoekstra et al, 2004), a process that has been shown to be stimulated by OSM (van der Wouden et al, 2002). Therefore, we next examined the subcellular position of the CE/SAC and ARE in control HepG2 cells and HepG2 cells expressing the AKAP-IS peptide.…”

mentioning

confidence: 99%

Anchoring of Protein Kinase A-Regulatory Subunit IIα to Subapically Positioned Centrosomes Mediates Apical Bile Canalicular Lumen Development in Response to Oncostatin M but Not cAMP

Wojtal

Hoekstra

IJzendoorn

2007

MBoC

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Oncostatin M and cAMP signaling stimulate apical surface-directed membrane trafficking and apical lumen development in hepatocytes, both in a protein kinase A (PKA)-dependent manner. Here, we show that oncostatin M, but not cAMP, promotes the A-kinase anchoring protein (AKAP)-dependent anchoring of the PKA regulatory subunit (R)II␣ to subapical centrosomes and that this requires extracellular signal-regulated kinase 2 activation. Stable expression of the RIIdisplacing peptide AKAP-IS, but not a scrambled peptide, inhibits the association of RII␣ with centrosomal AKAPs and results in the repositioning of the centrosome from a subapical to a perinuclear location. Concomitantly, common endosomes, but not apical recycling endosomes, are repositioned from a subapical to a perinuclear location, without significant effects on constitutive or oncostatin M-stimulated basolateral-to-apical transcytosis. Importantly, however, the expression of the AKAP-IS peptide completely blocks oncostatin M-, but not cAMP-stimulated apical lumen development. Together, the data suggest that centrosomal anchoring of RII␣ and the interrelated subapical positioning of these centrosomes is required for oncostatin M-, but not cAMP-mediated, bile canalicular lumen development in a manner that is uncoupled from oncostatin M-stimulated apical lumen-directed membrane trafficking. The results also imply that multiple PKA-mediated signaling pathways control apical lumen development and that subapical centrosome positioning is important in some of these pathways. INTRODUCTIONPolarized hepatocytes, like all epithelial cells, display distinct plasma membrane domains, an apical plasma membrane domain facing the bile canalicular lumen, and a basolateral plasma membrane domain facing the space of Disse. Concomitant with cell surface polarity, also the cell interior displays a polarized organization. A dense cortical actin network is assembled beneath the apical surface and actin filaments extend into apical microvilli with their barbed ends facing the microvilli tips. In addition, part of the microtubule cytoskeleton is oriented parallel to the apicalbasolateral axis with their minus and plus ends facing the apical and basolateral surface, respectively. The cytoskeleton organization influences the position of the centrosome (Burakov et al., 2003), which in various epithelial cells including intestinal Caco-2, kidney Madin-Darby canine kidney (MDCK), and hepatic WIF-B cells, is typically oriented toward the apical surface (Buendia et al., 1990;Meads and Schroer, 1995;Salas, 1999). Polarized positioning of the centrosome is thought to play a role in the establishment of epithelial cell polarity (Zeligs, 1979;Dylewski and Keenan, 1984;Houliston et al., 1987;Rizzolo and Joshi, 1993) and neuronal polarity (de Anda et al., 2005;Higginbotham et al., 2006). A subapical position of the centrosome may be important for the polarized orientation of microtubule-associated organelles such as the Golgi apparatus and recycling endosomes, and, in this way, facilitate the...

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“…This compartment was enriched in TfR and did not contain EEA1, a marker of early sorting endosomes (Wilson et al, 2000), or Rab11, a marker of AREs in MDCK cells (Casanova et al, 1999;Wang et al, 2001; Figure 2A). All of these characteristics are typical of a compartment denominated common RE, involved in the recycling of TfR and LDLR to the basolateral membrane and in the transcytosis of Polymeric IgA Receptor to the apical membrane via ARE (Futter et al, 1998;Brown et al, 2000;Wang et al, 2000).…”

Section: Tgn-vs Ap1b-mediated Sorting Pathwaysmentioning

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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Association of Rab25 and Rab11a with the Apical Recycling System of Polarized Madin–Darby Canine Kidney Cells

Cited by 369 publications

References 51 publications

Cholesterol-sensitive Modulation of Transcytosis

Cholesterol-sensitive Modulation of Transcytosis

Anchoring of Protein Kinase A-Regulatory Subunit IIα to Subapically Positioned Centrosomes Mediates Apical Bile Canalicular Lumen Development in Response to Oncostatin M but Not cAMP

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

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