Apical Sorting by Galectin‐3‐Dependent Glycoprotein Clustering

Delacour, Delphine; Greb, Christoph; Koch, Annett; Salomonsson, Emma; Leffler, Hakon; Bivic, André Le; Jacob, Ralf

doi:10.1111/j.1600-0854.2007.00539.x

Cited by 150 publications

(155 citation statements)

References 44 publications

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“…This lectin was detected in raft-independent apical carrier vesicles in MDCK cells (15). Galectin-3 has been found to directly interact with three apical glycopro- teins, lactase-phlorizin hydrolase, transmembrane neurotrophin receptor p75, and gp114 (15,17). This interaction is competitively inhibited by lactose, suggesting that galectin-3 binds to the glycans attached to these proteins.…”

Section: Putative Apical Sorting Machinery That Recognizes N-glycansmentioning

confidence: 91%

“…Additionally, the mechanisms by which sorting information encoded by N-glycans is recognized by cellular sorting machinery have not been defined. Two lectins have been identified as potential sorting receptors that recognize N-glycans as apical sorting signals (15,17,34,35). However, it is not clear how glycan-lectin interactions that must occur in the luminal compartments of TGN/endosomes are converted into a cascade of cytoplasmic events resulting in apical delivery of N-glycosylated proteins.…”

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confidence: 99%

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Role of N-glycosylation in trafficking of apical membrane proteins in epithelia

Vagin

Kraut²,

Sachs³

2009

American Journal of Physiology-Renal Physiology

168

157

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ized distribution of plasma membrane transporters and receptors in epithelia is essential for vectorial functions of epithelia. This polarity is maintained by sorting of membrane proteins into apical or basolateral transport containers in the transGolgi network and/or endosomes followed by their delivery to the appropriate plasma membrane domains. Sorting depends on the recognition of sorting signals in proteins by specific sorting machinery. In the present review, we summarize experimental evidence for and against the hypothesis that N-glycans attached to the membrane proteins can act as apical sorting signals. Furthermore, we discuss the roles of N-glycans in the apical sorting event per se and their contribution to folding and quality control of glycoproteins in the endoplasmic reticulum or retention of glycoproteins in the plasma membrane. Finally, we review existing hypotheses on the mechanism of apical sorting and discuss the potential roles of the lectins, VIP36 and galectin-3, as putative apical sorting receptors. apical sorting; apical membrane retention; H-K-ATPase ␤-subunit; lectin EPITHELIAL CELLS CARRY OUT vectorial transport that requires polarized distribution of transporters and receptors to apical or basolateral membrane domains. These domains are separated by tight junctions that connect neighboring cells in the epithelial monolayer and act as diffusion barriers to prevent mixing of apical and basolateral membrane components (22). Asymmetric distribution of plasma membrane proteins is accomplished by their sorting into apical and basolateral containers in the trans-Golgi network (TGN) and/or endosomes followed by vectorial transport of these containers and insertion and retention of the proteins in the appropriate plasma membrane domains. Sorting depends on recognition of apical and basolateral sorting signals within the proteins by cellular sorting machinery (20,58,59,75,76).Numerous studies have indicated that both O-and N-glycans attached to the extracellular domains of some membrane proteins are important for apical location of these proteins. This review will focus on the role of N-glycans in polarized distribution of plasma membrane proteins in epithelia. The role of O-glycans in apical sorting has been described in several recent excellent reviews (18, 71) and will not be discussed further here.A putative role of N-glycans as apical sorting signals was postulated more than 10 years ago (24, 31). However, this hypothesis remains controversial primarily because N-glycans are important for the processes that precede or follow the actual sorting event, such as protein folding, quality control, endoplasmic reticulum (ER)-associated degradation, ER-to-Golgi trafficking, and retention of glycoproteins in the apical membrane. Therefore, merely examining the effect of altering the number or the nature of N-linked glycans on the relative abundance of the glycoprotein in the apical membrane, as has been done in many of the studies reported, does not allow one to distinguish between effects on apica...

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Section: Putative Apical Sorting Machinery That Recognizes N-glycansmentioning

confidence: 91%

mentioning

confidence: 99%

Role of N-glycosylation in trafficking of apical membrane proteins in epithelia

Vagin

Kraut²,

Sachs³

2009

American Journal of Physiology-Renal Physiology

168

157

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“…An important objective for the future is to understand how the selectivity of a particular organization of the actin cytoskeleton for a particular cargo is established. In particular, we want to know how p75 sorting signals, previously defined as the O-glycan cluster in its ectodomin (Yeaman et al, 1997) upon clustering with galectin 3 (Delacour et al, 2007) are coupled to the actin regulatory mechanisms required for vesicle fission. Another major challenge is to identify the mechanisms that couple the actin-dependent fission mechanisms described here with our recent observation that kinesin 5B is essential for generation and transport of p75 carrier vesicles from Golgi to PM (Jaulin et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

LIM Kinase 1 and Cofilin Regulate Actin Filament Population Required for Dynamin-dependent Apical Carrier Fission from theTrans-Golgi Network

Salvarezza

Deborde

Schreiner

et al. 2009

MBoC

108

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The functions of the actin cytoskeleton in post-Golgi trafficking are still poorly understood. Here, we report the role of LIM Kinase 1 (LIMK1) and its substrate cofilin in the trafficking of apical and basolateral proteins in Madin-Darby canine kidney cells. Our data indicate that LIMK1 and cofilin organize a specialized population of actin filaments at the Golgi complex that is selectively required for the emergence of an apical cargo route to the plasma membrane (PM). Quantitative pulse-chase live imaging experiments showed that overexpression of kinase-dead LIMK1 (LIMK1-KD), or of LIMK1 small interfering RNA, or of an activated cofilin mutant (cofilin S3A), selectively slowed down the exit from the trans-Golgi network (TGN) of the apical PM marker p75-green fluorescent protein (GFP) but did not interfere with the apical PM marker glycosyl phosphatidylinositol-YFP or the basolateral PM marker neural cell adhesion molecule-GFP. Highresolution live imaging experiments of carrier formation and release by the TGN and analysis of peri-Golgi actin dynamics using photoactivatable GFP suggest a scenario in which TGN-localized LIMK1-cofilin regulate a population of actin filaments required for dynamin-syndapin-cortactin-dependent generation and/or fission of precursors to p75 transporters. INTRODUCTIONThe organization of polarized intracellular trafficking to the plasma membrane (PM) involves a close cooperation between cargo proteins, adaptors and cytoskeletal elements that takes place at major sorting organelles, e.g., the Golgi complex and recycling endosomes (Bonifacino and Traub, 2003;Rodriguez-Boulan et al., 2005). Newly synthesized proteins destined for endosomes, lysosomes, and the basolateral PM of epithelial cells segregate into nascent post-Golgi or postendosomal vesicles via tyrosine, dileucine, or monoleucine sorting signals, clathrin adaptors, and accessory proteins (Bonifacino and Traub, 2003;Rodriguez-Boulan et al., 2005;Deborde et al., 2008).By contrast, proteins destined for the apical PM are sorted into nascent post-Golgi transporters via N-and O-glycans, specialized transmembrane or cytoplasmic domains or glycosyl phosphatidylinositol (GPI)-anchors that interact with lipid domains (rafts), lectins, or microtubule (MT) motors (Scheiffele et al., 1995;Simons and Ikonen, 1997;Yeaman et al., 1997;Delacour et al., 2005Delacour et al., , 2006Rodriguez-Boulan et al., 2005). It is very well established that MT motors of the kinesin or dynein families play key roles in the generation and transcytoplasmic transport of tubular and vesicular transporters destined to the apical PM of Madin-Darby canine kidney (MDCK) cells (Kreitzer et al., 2000;Noda et al., 2001;Tai et al., 2001;Allan et al., 2002;Musch, 2004;Jaulin et al., 2007). By contrast, our knowledge of the specific roles of the actin cytoskeleton in intracellular transport routes remains fragmentary, unlike the situation at the PM, where various mechanisms involving the actin cytoskeleton in endocytic routes have been well documented (Erickson et al., 1...

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“…A third group of apical sorting signals includes N-glycans (Fiedler and Simons, 1995) and Oglycans (Yeaman et al, 1997), which may also act by promoting association with lipid rafts (Naim et al, 1999;Jacob and Naim, 2001). However, not all apical PM proteins associate with lipid rafts; for example, the apical PM protein 75 neurotrophin receptor (p75) uses O-glycans as its apical sorting signal (Yeaman et al, 1997) through clustering by the lectin galectin 3 (Delacour et al, 2006(Delacour et al, , 2007. Yet a fourth apical sorting mechanism, also lipid raft-independent, is that of rhodopsin, which binds to the microtubule (MT) motor dynein by cytoplasmic determinants as an apical sorting strategy (Tai et al, 1999).…”

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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Apical Sorting by Galectin‐3‐Dependent Glycoprotein Clustering

Cited by 150 publications

References 44 publications

Role of N-glycosylation in trafficking of apical membrane proteins in epithelia

Role of N-glycosylation in trafficking of apical membrane proteins in epithelia

LIM Kinase 1 and Cofilin Regulate Actin Filament Population Required for Dynamin-dependent Apical Carrier Fission from theTrans-Golgi Network

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

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