The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells

doi:10.1083/jcb.107.6.2377

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The polarized distribution of an apical cell surface glycoprotein is maintained by interactions with the cytoskeleton of Madin-Darby canine kidney cells

GK Ojakian and R Schwimmer
Department of Anatomy and Cell Biology, State University of New York Health Science Center, Brooklyn 11203.

A monoclonal antibody made against a 135-kD glycoprotein (gp135) on the plasma membrane of Madin-Darby canine kidney (MDCK) cells was used to study the development and maintenance of epithelial cell surface polarity. Immunofluorescence microscopy and immunogold electron microscopy of confluent monolayers demonstrated that gp135 had a polarized cell surface distribution and was only localized on the apical surface. The role of membrane contacts in establishing gp135 polarity was determined by plating cells in low Ca++-medium to prevent the formation of intercellular junctions. Quantitative immunogold electron microscopy demonstrated that gp135 had a polarized distribution on cells lacking membrane contacts and was observed on the apical surface at a density 24 times that of the basal membrane contacting the substratum. The possibility that gp135 was associated with components of the apical cytoskeleton was investigated using cytoskeleton-disrupting drugs. Incubation in cytochalasin D produced a clustering of both actin and gp135, and double-label fluorescence microscopy demonstrated that these proteins were colocalized. Experiments using nocodazole had no effect, suggesting that gp135 could be interacting with actin microfilaments, but not microtubules. Treatment with Triton X-100 extracted approximately 50% of the gp135 and immunofluorescence microscopy indicated that the gp135 which remained associated with the detergent-insoluble cytoskeleton had a distribution identical to that of control cells. Experiments demonstrating that gp23, a nonpolarized glycoprotein, was preferentially extracted from the apical membrane suggested that the improperly sorted apical gp23 did not interact with the cytoskeleton. These results provided evidence that the polarized cell surface distribution of gp135 was maintained through its interaction with actin in the apical cytoskeleton.
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Mak, G. Z., Kavanaugh, G. M., Buschmann, M. M., Stickley, S. M., Koch, M., Goss, K. H., Waechter, H., Zuk, A., Matlin, K. S. (2006). Regulated Synthesis and Functions of Laminin 5 in Polarized Madin-Darby Canine Kidney Epithelial Cells. Mol. Biol. Cell 17: 3664-3677 [Abstract] [Full Text]
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Warner, F. J., Lew, R. A., Smith, A. I., Lambert, D. W., Hooper, N. M., Turner, A. J. (2005). Angiotensin-converting Enzyme 2 (ACE2), But Not ACE, Is Preferentially Localized to the Apical Surface of Polarized Kidney Cells. J. Biol. Chem. 280: 39353-39362 [Abstract] [Full Text]
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Roux, K. J., Amici, S. A., Fletcher, B. S., Notterpek, L. (2005). Modulation of Epithelial Morphology, Monolayer Permeability, and Cell Migration by Growth Arrest Specific 3/Peripheral Myelin Protein 22. Mol. Biol. Cell 16: 1142-1151 [Abstract] [Full Text]
Vogelmann, R., Nelson, W. J. (2005). Fractionation of the Epithelial Apical Junctional Complex: Reassessment of Protein Distributions in Different Substructures. Mol. Biol. Cell 16: 701-716 [Abstract] [Full Text]
Meder, D., Shevchenko, A., Simons, K., Fullekrug, J. (2005). Gp135/podocalyxin and NHERF-2 participate in the formation of a preapical domain during polarization of MDCK cells. JCB 168: 303-313 [Abstract] [Full Text]
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Rajasekaran, S. A., Palmer, L. G., Moon, S. Y., Peralta Soler, A., Apodaca, G. L., Harper, J. F., Zheng, Y., Rajasekaran, A. K. (2001). Na,K-ATPase Activity Is Required for Formation of Tight Junctions, Desmosomes, and Induction of Polarity in Epithelial Cells. Mol. Biol. Cell 12: 3717-3732 [Abstract] [Full Text]
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Tai, A. W., Chuang, J.-Z., Sung, C.-H. (2001). Cytoplasmic Dynein Regulation by Subunit Heterogeneity and Its Role in Apical Transport. JCB 153: 1499-1510 [Abstract] [Full Text]
Suzuki, A., Yamanaka, T., Hirose, T., Manabe, N., Mizuno, K., Shimizu, M., Akimoto, K., Izumi, Y., Ohnishi, T., Ohno, S. (2001). Atypical Protein Kinase C Is Involved in the Evolutionarily Conserved Par Protein Complex and Plays a Critical Role in Establishing Epithelia-Specific Junctional Structures. JCB 152: 1183-1196 [Abstract] [Full Text]
Ojakian, G., Ratcliffe, D., Schwimmer, R (2001). Integrin regulation of cell-cell adhesion during epithelial tubule formation. J. Cell Sci. 114: 941-952 [Abstract]
Troxell, M., Loftus, D., Nelson, W., Marrs, J. (2001). Mutant cadherin affects epithelial morphogenesis and invasion, but not transformation. J. Cell Sci. 114: 1237-1246 [Abstract]
Mo, C., Schneeberger, E. E., Arvin, A. M. (2000). Glycoprotein E of Varicella-Zoster Virus Enhances Cell-Cell Contact in Polarized Epithelial Cells. J. Virol. 74: 11377-11387 [Abstract] [Full Text]
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Brunet, J.-P., Cotte-Laffitte, J., Linxe, C., Quero, A.-M., Géniteau-Legendre, M., Servin, A. (2000). Rotavirus Infection Induces an Increase in Intracellular Calcium Concentration in Human Intestinal Epithelial Cells: Role in Microvillar Actin Alteration. J. Virol. 74: 2323-2332 [Abstract] [Full Text]
Trotter, K. W., Fraser, I. D.C., Scott, G. K., Stutts, M. J., Scott, J. D., Milgram, S. L. (1999). Alternative Splicing Regulates the Subcellular Localization of a-Kinase Anchoring Protein 18 Isoforms. JCB 147: 1481-1492 [Abstract] [Full Text]
Tsukamoto, T., Nigam, S. K. (1999). Cell-Cell Dissociation upon Epithelial Cell Scattering Requires a Step Mediated by the Proteasome. J. Biol. Chem. 274: 24579-24584 [Abstract] [Full Text]
Corbeil, D, Roper, K, Hannah, M., Hellwig, A, Huttner, W. (1999). Selective localization of the polytopic membrane protein prominin in microvilli of epithelial cells - a combination of apical sorting and retention in plasma membrane protrusions. J. Cell Sci. 112: 1023-1033 [Abstract]
YEAMAN, C., GRINDSTAFF, K. K., NELSON, W. J. (1999). New Perspectives on Mechanisms Involved in Generating Epithelial Cell Polarity. Physiol. Rev. 79: 73-98 [Abstract] [Full Text]
Lafont, F., Lecat, S., Verkade, P., Simons, K. (1998). Annexin XIIIb Associates with Lipid Microdomains to Function in Apical Delivery. JCB 142: 1413-1427 [Abstract] [Full Text]
Jourdan, N., Brunet, J. P., Sapin, C., Blais, A., Cotte-Laffitte, J., Forestier, F., Quero, A.-M., Trugnan, G., Servin, A. L. (1998). Rotavirus Infection Reduces Sucrase-Isomaltase Expression in Human Intestinal Epithelial Cells by Perturbing Protein Targeting and Organization of Microvillar Cytoskeleton. J. Virol. 72: 7228-7236 [Abstract] [Full Text]
Jou, T.-S., James Nelson, W. (1998). Effects of Regulated Expression of Mutant RhoA and Rac1 Small GTPases on the Development of Epithelial (MDCK) Cell Polarity. JCB 142: 85-100 [Abstract] [Full Text]
Grindstaff, K. K., Bacallao, R. L., Nelson, W. J. (1998). Apiconuclear Organization of Microtubules Does Not Specify Protein Delivery from the Trans-Golgi Network to Different Membrane Domains in Polarized Epithelial Cells. Mol. Biol. Cell 9: 685-699 [Abstract] [Full Text]
Saunders, C., Limbird, L. E. (1997). Disruption of Microtubules Reveals Two Independent Apical Targeting Mechanisms for G-protein-coupled Receptors in Polarized Renal Epithelial Cells. J. Biol. Chem. 272: 19035-19045 [Abstract] [Full Text]
Salas, P. J.I., Rodriguez, M. L., Viciana, A. L., Vega-Salas, D. E., Hauri, H.-P. (1997). The Apical Submembrane Cytoskeleton Participates in the Organization of the Apical Pole in Epithelial Cells. JCB 137: 359-375 [Abstract] [Full Text]
Haller, C., Schick, C. S., Zorn, M., Kubler, W. (1997). Cytotoxicity of radiocontrast agents on polarized renal epithelial cell monolayers. Cardiovasc Res 33: 655-665 [Abstract]
Ojakian, G., Nelson, W., Beck, K. (1997). Mechanisms for de novo biogenesis of an apical membrane compartment in groups of simple epithelial cells surrounded by extracellular matrix. J. Cell Sci. 110: 2781-2794 [Abstract]
Saunders, C., Keefer, J. R., Kennedy, A. P., Wells, J. N., Limbird, L. E. (1996). Receptors Coupled to Pertussis Toxin-sensitive G-proteins Traffic to Opposite Surfaces in Madin-Darby Canine Kidney Cells. J. Biol. Chem. 271: 995-1002 [Abstract] [Full Text]
Mayer, A, Ivanov, I., Gravotta, D, Adesnik, M, Sabatini, D. (1996). Cell-free reconstitution of the transport of viral glycoproteins from the TGN to the basolateral plasma membrane of MDCK cells. J. Cell Sci. 109: 1667-1676 [Abstract]
Zuk, A, Matlin, K. (1996). Apical beta 1 integrin in polarized MDCK cells mediates tubulocyst formation in response to type I collagen overlay. J. Cell Sci. 109: 1875-1889 [Abstract]
Bao, Q, Hughes, R. (1995). Galectin-3 expression and effects on cyst enlargement and tubulogenesis in kidney epithelial MDCK cells cultured in three-dimensional matrices in vitro. J. Cell Sci. 108: 2791-2800 [Abstract]
Schwimmer, R, Ojakian, G. (1995). The alpha 2 beta 1 integrin regulates collagen-mediated MDCK epithelial membrane remodeling and tubule formation. J. Cell Sci. 108: 2487-2498 [Abstract]
Rodriguez, M., Brignoni, M, Salas, P. (1994). A specifically apical sub-membrane intermediate filament cytoskeleton in non-brush-border epithelial cells. J. Cell Sci. 107: 3145-3151 [Abstract]
Ojakian, G., Schwimmer, R (1994). Regulation of epithelial cell surface polarity reversal by beta 1 integrins. J. Cell Sci. 107: 561-576 [Abstract]
Ojakian, G. K., Schwimmer, R. (1992). Antimicrotubule drugs inhibit the polarized insertion of an intracellular glycoprotein pool into the apical membrane of Madin-Darby canine kidney (MDCK) cells. J. Cell Sci. 103: 677-687 [Abstract]
Nelson, W.J., Wilson, R., Wollner, D., Mays, R., McNeill, H., Siemers, K. (1992). Regulation of Epithelial Cell Polarity: A View from the Cell Surface. Cold Spring Harb Symp Quant Biol 57: 621-630 [Abstract]
Hammerton, R., Krzeminski, K., Mays, R., Ryan, T., Wollner, D., Nelson, W. (1991). Mechanism for regulating cell surface distribution of Na+,K(+)-ATPase in polarized epithelial cells. Science 254: 847-850 [Abstract]
Rodriguez-Boulan, E, Nelson, W. (1989). Morphogenesis of the polarized epithelial cell phenotype. Science 245: 718-725 [Abstract]