Transport of vesicular stomatitis virus G protein to the cell surface is signal mediated in polarized and nonpolarized cells

doi:10.1083/jcb.133.3.543

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Transport of vesicular stomatitis virus G protein to the cell surface is signal mediated in polarized and nonpolarized cells

A Musch, H Xu, D Shields and E Rodriguez-Boulan
Department of Cell Biology. Cornell University Medical School, New York, New York 10021, USA.

Current model propose that in nonpolarized cells, transport of plasma membrane proteins to the surface occurs by default. In contrast, compelling evidence indicates that in polarized epithelial cells, plasma membrane proteins are sorted in the TGN into at least two vectorial routes to apical and basolateral surface domains. Since both apical and basolateral proteins are also normally expressed by both polarized and nonpolarized cells, we explored here whether recently described basolateral sorting signals in the cytoplasmic domain of basolateral proteins are recognized and used for post TGN transport by nonpolarized cells. To this end, we compared the inhibitory effect of basolateral signal peptides on the cytosol-stimulated release of two basolateral and one apical marker in semi-intact fibroblasts (3T3), pituitary (GH3), and epithelial (MDCK) cells. A basolateral signal peptide (VSVGp) corresponding to the 29-amino acid cytoplasmic tail of vesicular stomatitis virus G protein (VSVG) inhibited with identical potency the vesicular release of VSVG from the TGN of all three cell lines. On the other hand, the VSVG peptide did not inhibit the vesicular release of HA in MDCK cells not of two polypeptide hormones (growth hormone and prolactin) in GH3 cells, whereas in 3T3 cells (influenza) hemagglutinin was inhibited, albeit with a 3x lower potency than VSVG. The results support the existence of a basolateral-like, signal-mediated constitutive pathway from TGN to plasma membrane in all three cell types, and suggest that an apical-like pathway may be present in fibroblast. The data support cargo protein involvement, not bulk flow, in the formation of post-TGN vesicles and predict the involvement of distinct cytosolic factors in the assembly of apical and basolateral transport vesicles.
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Low, S. H., Miura, M., Roche, P. A., Valdez, A. C., Mostov, K. E., Weimbs, T. (2000). Intracellular Redirection of Plasma Membrane Trafficking after Loss of Epithelial Cell Polarity. Mol. Biol. Cell 11: 3045-3060 [Abstract] [Full Text]
Screaton, R. A., DeMarte, L., Draber, P., Stanners, C. P. (2000). The Specificity for the Differentiation Blocking Activity of Carcinoembryonic Antigen Resides in Its Glycophosphatidyl-Inositol Anchor. JCB 150: 613-626 [Abstract] [Full Text]
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Hansen, G. H., Niels-Christiansen, L.-L., Thorsen, E., Immerdal, L., Danielsen, E. M. (2000). Cholesterol Depletion of Enterocytes. EFFECT ON THE GOLGI COMPLEX AND APICAL MEMBRANE TRAFFICKING. J. Biol. Chem. 275: 5136-5142 [Abstract] [Full Text]
Ostermeyer, A. G., Beckrich, B. T., Ivarson, K. A., Grove, K. E., Brown, D. A. (1999). Glycosphingolipids Are Not Essential for Formation of Detergent-resistant Membrane Rafts in Melanoma Cells. METHYL-beta -CYCLODEXTRIN DOES NOT AFFECT CELL SURFACE TRANSPORT OF A GPI-ANCHORED PROTEIN. J. Biol. Chem. 274: 34459-34466 [Abstract] [Full Text]
Simonsen, A., Pedersen, K. W., Nordeng, T. W., von der Lippe, A., Stang, E., Long, E. O., Bakke, O. (1999). Polarized Transport of MHC Class II Molecules in Madin-Darby Canine Kidney Cells Is Directed by a Leucine-Based Signal in the Cytoplasmic Tail of the {beta}-Chain. J. Immunol. 163: 2540-2548 [Abstract] [Full Text]
Simmen, T., Nobile, M., Bonifacino, J. S., Hunziker, W. (1999). Basolateral Sorting of Furin in MDCK Cells Requires a Phenylalanine-Isoleucine Motif Together with an Acidic Amino Acid Cluster. Mol. Cell. Biol. 19: 3136-3144 [Abstract] [Full Text]
Vijayakumar, S., Takito, J., Hikita, C., Al-Awqati, Q. (1999). Hensin Remodels the Apical Cytoskeleton and Induces Columnarization of Intercalated Epithelial Cells: Processes that Resemble Terminal Differentiation. JCB 144: 1057-1067 [Abstract] [Full Text]
Dannies, P. S. (1999). Protein Hormone Storage in Secretory Granules: Mechanisms for Concentration and Sorting. Endocr. Rev. 20: 3-21 [Abstract] [Full Text]
Kjer-Nielsen, L, van Vliet, C, Erlich, R, Toh, B., Gleeson, P. (1999). The Golgi-targeting sequence of the peripheral membrane protein p230. J. Cell Sci. 112: 1645-1654 [Abstract]
Nabi, I. (1999). The polarization of the motile cell. J. Cell Sci. 112: 1803-1811 [Abstract]
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]
Toomre, D, Keller, P, White, J, Olivo, J., Simons, K (1999). Dual-color visualization of trans-Golgi network to plasma membrane traffic along microtubules in living cells. J. Cell Sci. 112: 21-33 [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]
Zheng, P., Eastman, J., Vande Pol, S., Pimplikar, S. W. (1998). PAT1, a microtubule-interacting protein, recognizes the basolateral sorting signal of amyloid precursor protein. Proc. Natl. Acad. Sci. USA 95: 14745-14750 [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]
Al-Awqati, Q., Vijayakumar, S., Hikita, C., Chen, J., Takito, J. (1998). Phenotypic plasticity in the intercalated cell: the hensin pathway. Am. J. Physiol. Renal Physiol. 275: F183-F190 [Abstract] [Full Text]
Lin, S., Naim, H. Y., Chapin Rodriguez, A., Roth, M. G. (1998). Mutations in the Middle of the Transmembrane Domain Reverse the Polarity of Transport of the Influenza Virus Hemagglutinin in MDCK Epithelial Cells. JCB 142: 51-57 [Abstract] [Full Text]
Hunziker, W., Peters, P. J. (1998). Rab17 Localizes to Recycling Endosomes and Regulates Receptor-mediated Transcytosis in Epithelial Cells. J. Biol. Chem. 273: 15734-15741 [Abstract] [Full Text]
Harder, T., Scheiffele, P., Verkade, P., Simons, K. (1998). Lipid Domain Structure of the Plasma Membrane Revealed by Patching of Membrane Components. JCB 141: 929-942 [Abstract] [Full Text]
Keller, P., Simons, K. (1998). Cholesterol Is Required for Surface Transport of Influenza Virus Hemagglutinin. JCB 140: 1357-1367 [Abstract] [Full Text]
Zacchi, P., Stenmark, H., Parton, R. G., Orioli, D., Lim, F., Giner, A., Mellman, I., Zerial, M., Murphy, C. (1998). Rab17 Regulates Membrane Trafficking through Apical Recycling Endosomes in Polarized Epithelial Cells. JCB 140: 1039-1053 [Abstract] [Full Text]
de Vries, H., Schrage, C., Hoekstra, D. (1998). An Apical-Type Trafficking Pathway Is Present in Cultured Oligodendrocytes but the Sphingolipid-enriched Myelin Membrane Is the Target of a Basolateral-Type Pathway. Mol. Biol. Cell 9: 599-609 [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]
Scheiffele, P., Verkade, P., Fra, A.M., Virta, H., Simons, K., Ikonen, E. (1998). Caveolin-1 and -2 in the Exocytic Pathway of MDCK Cells. JCB 140: 795-806 [Abstract] [Full Text]
Lipardi, C., Mora, R., Colomer, V., Paladino, S., Nitsch, L., Rodriguez-Boulan, E., Zurzolo, C. (1998). Caveolin Transfection Results in Caveolae Formation but Not Apical Sorting of Glycosylphosphatidylinositol (GPI)-anchored Proteins in Epithelial Cells. JCB 140: 617-626 [Abstract] [Full Text]
Simon, J.-P., Shen, T.-H., Ivanov, I. E., Gravotta, D., Morimoto, T., Adesnik, M., Sabatini, D. D. (1998). Coatomer, but not P200/myosin II, is required for the in vitro formation of trans-Golgi network-derived vesicles containing the envelope glycoprotein of vesicular stomatitis�virus. Proc. Natl. Acad. Sci. USA 95: 1073-1078 [Abstract] [Full Text]
D'Souza, S., Garcia-Cabado, A., Yu, F., Teter, K., Lukacs, G., Skorecki, K., Moore, H.-P., Orlowski, J., Grinstein, S. (1998). The Epithelial Sodium-Hydrogen Antiporter Na+/H+ Exchanger 3�Accumulates and Is Functional in Recycling Endosomes. J. Biol. Chem. 273: 2035-2043 [Abstract] [Full Text]
Muniz, M., Martin, M. E., Hidalgo, J., Velasco, A. (1997). Protein kinase A activity is required for the budding of constitutive transport vesicles from the trans-Golgi�network. Proc. Natl. Acad. Sci. USA 94: 14461-14466 [Abstract] [Full Text]
Alonso, M. A., Fan, L., Alarcon, B. (1997). Multiple Sorting Signals Determine Apical Localization of a Nonglycosylated Integral Membrane Protein. J. Biol. Chem. 272: 30748-30752 [Abstract] [Full Text]
Musch, A., Cohen, D., Rodriguez-Boulan, E. (1997). Myosin II Is Involved in the Production of Constitutive Transport Vesicles from the TGN. JCB 138: 291-306 [Abstract] [Full Text]
Xu, H., Sweeney, D., Wang, R., Thinakaran, G., Lo, A. C.�Y., Sisodia, S. S., Greengard, P., Gandy, S. (1997). Generation of Alzheimer beta -amyloid protein in the trans-Golgi network in the apparent absence of vesicle�formation. Proc. Natl. Acad. Sci. USA 94: 3748-3752 [Abstract] [Full Text]
Wilson, J. M., Colton, T. L. (1997). Targeting of an Intestinal Apical Endosomal Protein to Endosomes in Nonpolarized Cells. JCB 136: 319-330 [Abstract] [Full Text]
Keller, P, Simons, K (1997). Post-Golgi biosynthetic trafficking. J. Cell Sci. 110: 3001-3009 [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]
Delgrossi, M., Breuza, L, Mirre, C, Chavrier, P, Le Bivic, A (1997). Human syntaxin 3 is localized apically in human intestinal cells. J. Cell Sci. 110: 2207-2214 [Abstract]
Bonilha, V., Marmorstein, A., Cohen-Gould, L, Rodriguez-Boulan, E (1997). Apical sorting of influenza hemagglutinin by transcytosis in retinal pigment epithelium. J. Cell Sci. 110: 1717-1727 [Abstract]
Simonsen, A, Stang, E, Bremnes, B, Roe, M, Prydz, K, Bakke, O (1997). Sorting of MHC class II molecules and the associated invariant chain (Ii) in polarized MDCK cells. J. Cell Sci. 110: 597-609 [Abstract]
Harsay, E., Schekman, R. (2002). A subset of yeast vacuolar protein sorting mutants is blocked in one branch of the exocytic pathway. JCB 156: 271-286 [Abstract] [Full Text]