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J. Virol., 09 1996, 6508-6515, Vol 70, No. 9
Copyright © 1996, American Society for Microbiology

Transmembrane domain of influenza virus neuraminidase, a type II protein, possesses an apical sorting signal in polarized MDCK cells

A Kundu, RT Avalos, CM Sanderson and DP Nayak
Jonsson Comprehensive Cancer Center, Department of Microbiology and Immunology, University of California at Los Angeles 90095-1747, USA.

The influenza virus neuraminidase (NA), a type II transmembrane protein, is directly transported to the apical plasma membrane in polarized MDCK cells. By using deletion mutants and chimeric constructs of influenza virus NA with the human transferrin receptor, a type II basolateral transmembrane protein, we investigated the location of the apical sorting signal of influenza virus NA. When these mutant and chimeric proteins were expressed in stably transfected polarized MDCK cells, the transmembrane domain of NA, and not the cytoplasmic tail, provided a determinant for apical targeting in polarized MDCK cells and this transmembrane signal was sufficient for sorting and transport of the ectodomain of a reporter protein (transferrin receptor) directly to the apical plasma membrane of polarized MDCK cells. In addition, by using differential detergent extraction, we demonstrated that influenza virus NA and the chimeras which were transported to the apical plasma membrane also became insoluble in Triton X-100 but soluble in octylglucoside after extraction from MDCK cells during exocytic transport. These data indicate that the transmembrane domain of NA provides the determinant(s) both for apical transport and for association with Triton X-100-insoluble lipids.

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• Quinones, B, Riento, K, Olkkonen, V., Hardy, S, Bennett, M. (1999). Syntaxin 2 splice variants exhibit differential expression patterns, biochemical properties and subcellular localizations. J. Cell Sci. 112: 4291-4304 [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]  
• 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]  
• Gut, A., Balda, M. S., Matter, K. (1998). The Cytoplasmic Domains of a beta 1 Integrin Mediate Polarization in Madin-Darby Canine Kidney Cells by Selective Basolateral Stabilization. J. Biol. Chem. 273: 29381-29388 [Abstract] [Full Text]  
• Roush, D. L., Gottardi, C. J., Naim, H. Y., Roth, M. G., Caplan, M. J. (1998). Tyrosine-based Membrane Protein Sorting Signals Are Differentially Interpreted by Polarized Madin-Darby Canine Kidney and LLC-PK1 Epithelial Cells. J. Biol. Chem. 273: 26862-26869 [Abstract] [Full Text]  
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• Tugizov, S., Maidji, E., Xiao, J., Zheng, Z., Pereira, L. (1998). Human Cytomegalovirus Glycoprotein B Contains Autonomous Determinants for Vectorial Targeting to Apical Membranes of Polarized Epithelial Cells. J. Virol. 72: 7374-7386 [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. J. Cell Biol. 142: 51-57 [Abstract] [Full Text]  
• Keller, P., Simons, K. (1998). Cholesterol Is Required for Surface Transport of Influenza Virus Hemagglutinin. J. Cell Biol. 140: 1357-1367 [Abstract] [Full Text]  
• Walsh, E., Falsey, A., Sullender, W. (1998). Monoclonal antibody neutralization escape mutants of respiratory syncytial virus with unique alterations in the attachment (G) protein. J. Gen. Virol. 79: 479-487 [Abstract]  
• 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. J. Cell Biol. 140: 617-626 [Abstract] [Full Text]  
• Matter, K, Balda, M. (1998). Biogenesis of tight junctions: the C-terminal domain of occludin mediates basolateral targeting. J. Cell Sci. 111: 511-519 [Abstract]  
• Fiedler, K., Rothman, J. E. (1997). Sorting Determinants in the Transmembrane Domain of p24 Proteins. J. Biol. Chem. 272: 24739-24742 [Abstract] [Full Text]  
• Keller, P, Simons, K (1997). Post-Golgi biosynthetic trafficking. J. Cell Sci. 110: 3001-3009 [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]  
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• Nadler, L. S., Kumar, G., Nathanson, N. M. (2001). Identification of a Basolateral Sorting Signal for the M3 Muscarinic Acetylcholine Receptor in Madin-Darby Canine Kidney Cells. J. Biol. Chem. 276: 10539-10547 [Abstract] [Full Text]  
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