The subapical compartment: a traffic center in membrane polarity development

Hoekstra, Dick; Tyteca, Donatienne; IJzendoorn, Sven C. D. van

doi:10.1242/jcs.01217

Cited by 131 publications

(135 citation statements)

References 95 publications

(152 reference statements)

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“…The activation of this membrane trafficking pathway has previously been demonstrated to play an important role in apical-basolateral polarity development in HepG2 cells (van IJzendoorn and Hoekstra, 1999a,b;van IJzendoorn et al, 2000;Hoekstra et al, 2004). OSM-stimulated membrane trafficking from SAC to the developing apical surface is dependent on intact microtubules (unpublished data).…”

Section: Discussionmentioning

confidence: 79%

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27^Kip1-Regulated Cell Cycle Dynamics

IJzendoorn

Théard

Wouden

et al. 2004

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Oncostatin M regulates membrane traffic and stimulates apicalization of the cell surface in hepatoma cells in a protein kinase A-dependent manner. Here, we show that oncostatin M enhances the expression of the cyclin-dependent kinase (cdk)2 inhibitor p27 Kip1 , which inhibits G 1 -S phase progression. Forced G 1 -S-phase transition effectively renders presynchronized cells insensitive to the apicalization-stimulating effect of oncostatin M. G 1 -S-phase transition prevents oncostatin M-mediated recruitment of protein kinase A to the centrosomal region and precludes the oncostatin M-mediated activation of a protein kinase A-dependent transport route to the apical surface, which exits the subapical compartment (SAC). This transport route has previously been shown to be crucial for apical plasma membrane biogenesis. Together, our data indicate that oncostatin M-stimulated apicalization of the cell surface is critically dependent on the ability of oncostatin M to control p27 Kip1 /cdk2-mediated G 1 -S-phase progression and suggest that the regulation of apical plasma membrane-directed traffic from SAC is coupled to centrosome-associated signaling pathways. INTRODUCTIONThe establishment and maintenance of apical and basolateral plasma membrane (PM) domains in epithelia require a careful orchestration of extra-and intracellular signals, triggering crucial cytoskeleton-, organelle-, and membrane traffic-linked machineries, as partly elucidated in systems as diverse as yeast, Drosophila, and mammalian cells (Lecuit and Pilot, 2003;Mostov et al., 2003;Baas et al., 2004). Impairment of these events may cause a loss of apical-basolateral asymmetry and may lead to deranged cell growth (Bilder et al., 2000;Vermeer et al., 2003;Baas et al., 2004) or spindle misorientation . Recent studies have reported an evolutionary conserved genetic program that may link the process of polarity development and proliferation (Bilder et al., 2000;Humbert et al., 2003;Rolls et al., 2003;Klezovitch et al., 2004). However, many aspects of such a link remain unclear, e.g., the extent to which cell proliferation can directly affect epithelial cell organization or vice versa. Indeed, epithelial cell proliferation and apical-basolateral polarity may be controlled by different signaling pathways (Liu et al., 2004).Signaling cascades stimulated by interleukin-6 family cytokines, including oncostatin M (OSM), elicit multiple responses in the cell. Originally, as its name indicates, oncostatin M was primarily recognized to inhibit the proliferation of tumor cells (Tanaka and Miyajima, 2003), presumably by modulating cell cycle regulatory proteins, including the cyclin-dependent kinase (cdk)2-inhibitor p27 Kip1 (Kortylewski et al., 1999;Klausen et al., 2000;Li et al., 2001). Disruption of the regulatory system that controls G 1 -phase progression is a common event in human hepatocarcinogenesis (Hui et al., 1998), and p27 Kip1 has been associated with differentiation, invasiveness, and metastasis of hepatocellular carcinoma tumors (Zhou et al., 2003). ...

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Section: Discussionmentioning

confidence: 79%

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27^Kip1-Regulated Cell Cycle Dynamics

IJzendoorn

Théard

Wouden

et al. 2004

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Section: Introductionmentioning

confidence: 99%

“…Many ligands do not recycle but instead are transported from early to late endosomes and eventually to lysosomes for degradation (Mukherjee et al, 1997). In polarized epithelial cells such as cultured Madin-Darby canine kidney (MDCK) cells, an additional layer of complexity in the endocytic pathway contributes to formation and/or maintenance of the specialized apical and basolateral domains (Nelson and Yeaman, 2001;Mostov et al, 2003;Hoekstra et al, 2004). Both the apical and basolateral membranes deliver cargo to early endosomes.…”

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“…Both the apical and basolateral membranes deliver cargo to early endosomes. Basolaterally derived and apical cargo can reach medially located "common endosomes," which can sort cargo from either source to the basolateral PM or to apical recycling endosomes (ARE), which can then ultimately send cargo to the apical PM Wang et al, 2000;Hoekstra et al, 2004).One group of master regulators of trafficking that has come under intense scrutiny are the Rab proteins, members of the Ras superfamily of small GTPases (Zerial and McBride, 2001). The human genome encodes Ͼ60 Rab proteins, whereas the Caenorhabditis elegans genome encodes 29 predicted members (Pereira-Leal and Seabra, 2001).…”

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RAB-10 Is Required for Endocytic Recycling in theCaenorhabditis elegansIntestine

Chen

Schweinsberg

Vashist

et al. 2006

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The endocytic pathway of eukaryotes is essential for the internalization and trafficking of macromolecules, fluid, membranes, and membrane proteins. One of the most enigmatic aspects of this process is endocytic recycling, the return of macromolecules (often receptors) and fluid from endosomes to the plasma membrane. We have previously shown that the EH-domain protein RME-1 is a critical regulator of endocytic recycling in worms and mammals. Here we identify the RAB-10 protein as a key regulator of endocytic recycling upstream of RME-1 in polarized epithelial cells of the Caenorhabditis elegans intestine. rab-10 null mutant intestinal cells accumulate abnormally abundant RAB-5-positive early endosomes, some of which are enlarged by more than 10-fold. Conversely most RME-1-positive recycling endosomes are lost in rab-10 mutants. The abnormal early endosomes in rab-10 mutants accumulate basolaterally recycling transmembrane cargo molecules and basolaterally recycling fluid, consistent with a block in basolateral transport. These results indicate a role for RAB-10 in basolateral recycling upstream of RME-1. We found that a functional GFP-RAB-10 reporter protein is localized to endosomes and Golgi in wild-type intestinal cells consistent with a direct role for RAB-10 in this transport pathway. INTRODUCTIONEndocytosis and endocytic trafficking controls the uptake and sorting of extracellular macromolecules as well as the components of the cell membrane itself, counterbalancing secretion and allowing a complex interplay between cells and their environment that is important for a myriad of cellular activities (Brodsky et al., 2001;Maxfield and McGraw, 2004). The steps involved in the uptake and trafficking of cargo within the endosomal system have been well described, but many of the components mediating these steps at the molecular level remain to be identified (Brodsky et al., 2001;Maxfield and McGraw, 2004). Many receptors and their associated ligands cluster into clathrincoated pits, whereas other types of cargo utilize clathrinindependent uptake mechanisms (Nichols, 2003;Gesbert et al., 2004). Plasma membrane invaginations pinch off into vesicles, uncoat, and then fuse with one another and with early endosomes. In early endosomes some ligand-receptor complexes dissociate because of the reduced pH of the endosomal lumen (Mukherjee et al., 1997). Many receptors then recycle to the plasma membrane (PM) either directly or indirectly via recycling endosomes (Mukherjee et al., 1997;Maxfield and McGraw, 2004). Many ligands do not recycle but instead are transported from early to late endosomes and eventually to lysosomes for degradation (Mukherjee et al., 1997). In polarized epithelial cells such as cultured Madin-Darby canine kidney (MDCK) cells, an additional layer of complexity in the endocytic pathway contributes to formation and/or maintenance of the specialized apical and basolateral domains (Nelson and Yeaman, 2001;Mostov et al., 2003;Hoekstra et al., 2004). Both the apical and basolateral membranes deliver cargo ...

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“…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.…”

Section: Inhibition Of Pka-rii␣ Anchoring At Centrosomes Interferes Wmentioning

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

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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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The subapical compartment: a traffic center in membrane polarity development

Cited by 131 publications

References 95 publications

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27^Kip1-Regulated Cell Cycle Dynamics

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27^Kip1-Regulated Cell Cycle Dynamics

RAB-10 Is Required for Endocytic Recycling in theCaenorhabditis elegansIntestine

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

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The subapical compartment: a traffic center in membrane polarity development

Cited by 131 publications

References 95 publications

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27Kip1-Regulated Cell Cycle Dynamics

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27Kip1-Regulated Cell Cycle Dynamics

RAB-10 Is Required for Endocytic Recycling in theCaenorhabditis elegansIntestine

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

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Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27^Kip1-Regulated Cell Cycle Dynamics

Oncostatin M-stimulated Apical Plasma Membrane Biogenesis Requires p27^Kip1-Regulated Cell Cycle Dynamics