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

Journal of Virology

Volumn 70, Issue 9, 1996, Pages 6508-6515

  Kundu, A ^a   Avalos, R T ^a   Sanderson, C M ^a   Nayak, D P ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS SIALIDASE;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL MEMBRANE TRANSPORT; CONTROLLED STUDY; DOG; INFLUENZA VIRUS; INTRACELLULAR TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TRANSPORT; VIRUS CELL INTERACTION;

EID: 0029839393     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.9.6508-6515.1996     Document Type: Article

References (62)

1. Apodaca, G., L. A. Katz, and K. E. Mostov. 1994. Receptor-mediated transcytosis of IgA in MDCK cells is via apical recycling endosomes. J. Cell Biol. 125:67-86.
2. 2 terminal hydrophobic region of influenza virus neuraminidase provides the signal function in translocation. Proc. Natl. Acad. Sci. USA 81:2327-2331.
3. Brewer, C. B., and M. G. Roth. 1991. A single amino acid change in the cytoplasmic domain alters the polarized delivery of influenza virus hemagglutinin. J. Cell Biol. 114:413-421.
4. Brown, D. A., B. Crise, and J. K. Rose. 1989. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science 245:1499-1501.
5. Brown, D. A., and J. K. Rose. 1992. Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68:533-544.
6. +-ATPase, an endogenous component of MDCK cell basolateral plasma membranes. Cell 46:623-631.
7. Casanova, J. E., G. Apodaca, and K. E. Mostov. 1991. An autonomous signal for basolateral sorting in the cytoplasmic domain of the polymeric immunoglobulin receptor. Cell 65:65-75.
8. Compton, T., I. E. Ivanov, T. Gottlieb, M. Rindler, M. Adesnik, and D. D. Sabatini. 1989. A sorting signal for the basolateral delivery of the vesicular stomatitis virus (VSV) G protein lies in its luminal domain: analysis of the targeting of VSV G-influenza hemagglutinin chimeras. Proc. Natl. Acad. Sci. USA 86:4112-4116.
9. Geffen, I., C. Fuhrer, B. Leitinger, M. Weiss, K. Huggerl, G. Griffiths, and M. Speiss. 1993. Related signals for endocytosis and basolateral sorting of the asialoglycoprotein receptor. J. Biol. Chem. 268:20772-20777.
10. Gottardi, C. J., and M. J. Capian. 1993. An ion transporting ATPase encodes multiple apical localization signals. J. Cell Biol. 121:283-293.
11. Hogue, B., and D. P. Nayak. 1992. Synthesis and processing of the influenza virus neuraminidase, a type II transmembrane glycoprotein. Virology 188:510-517.
12. Hughey, P. G., R. W. Compans, S. I. Zebedee, and R. A. Lamb. 1992. Expression of the influenza A virus M2 protein is restricted to apical surfaces of polarized epithelial cells. J. Virol. 66:5542-5552.
13. Hunziker, W., C. Harter, K. Matter, and I. Mellman. 1991. Basal lateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 66:907-920.
14. Hunziker, W., and I. Mellman. 1989. Expression of macrophage-lymphocyte Fc receptors in Madin-Darby canine kidney cells: polarity and transcytosis differ for isoforms with or without coated pit localization domains. J. Cell Biol. 109:3291-3302.
15. Jing, S., T. Spencer, K. Miller, C. Hopkins, and I. S. Trowbridge. 1990. The role of human transferrin receptor cytoplasmic domain in endocytosis: localization of a specific signal sequence for internalization. J. Cell Biol. 110:283-294.
16. Jones, L. V., R. W. Compans, A. R. Davis, T. J. Bos, and D. P. Nayak. 1985. Surface expression of influenza virus neuraminidase, an amino-terminally anchored viral membrane glycoprotein. in polarized epithelial cells. Mol. Cell. Biol. 5:2181-2189.
17. Kilpatrick, D. P., R. V. Srinivas, and R. W. Compans. 1988. Expression of the spleen focus-forming virus envelope gene in polarized epithelial cells. Virology 164:547-550.
18. Kristakis, N. T., D. Thomas, and M. G. Roth. 1990. Characteristics of the tyrosine recognition signals for internalization of transmembrane surface glycoproteins. J. Cell Biol. 111:1393-1407.
19. Kundu, A., M. Abdul Jabbar, and D. P. Nayak. 1991. Cell surface transport, oligomerization, and endocytosis of chimeric type II glycoproteins: role of cytoplasmic and anchor domains. Mol. Cell. Biol. 11:2675-2685.
20. Kundu, A., and D. P. Nayak. 1994. Analysis of the signals for polarized transport of influenza virus (A/WSN/33) neuraminidase and human transferrin receptor, type II transmembrane proteins. J. Virol. 68:1812-1818.
21. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227:680-685.
22. Lazarovits, J., and M. Roth. 1988. A single amino acid change in the cytoplasmic domain allows the influenza virus hemagglutinin to be endocytosed through coated pits. Cell 53:743-752.
23. Le Bivic, A., Y. Sambuy, A. Patzak, N. Patil, M. Chao, and E. Rodriguez-Boulan. 1991. An internal deletion in the cytoplasmic tail reverses the apical localization of human NGF receptor in transfected MDCK cells. J. Cell Biol. 115:607-618.
24. Lisanti, M. P., I. W. Caras, M. A. Davitz, and E. Rodriguez-Boulan. 1989. A glycophospholipid membrane anchor acts as an apical targeting signal in polarized epithelial cells. J. Cell Biol. 109:2145-2156.
25. Lisanti, M. P., A. Le Bivic, M. Sargiacomo, and E. Rodriguez-Boulan. 1989. Steady state distribution and biogenesis of endogenous MDCK glycoproteins: evidence for intracellular sorting and polarization surface delivery. J. Cell Biol. 109:2117-2128.
26. Lisanti, M. P., M. Sargiacomo, L. Graeve, A. R. Saltiel, and E. Rodriguez-Boulan. 1988. Polarized apical distribution of glycophosphatidylinositol-anchored proteins in a renal epithelial cell line. Proc. Natl. Acad. Sci. USA 85:9557-9561.
27. Lobigs, M., Z. Hongxing, and H. Garoff. 1990. Function of Semliki Forest virus E3 peptide in virus assembly: replacement of E3 with an artificial signal peptide abolishes spike heterodimerization and surface expression of E1. J. Virol. 64:4346-4355.
28. Matlin, K. S. 1986. The sorting of proteins to the plasma membrane in epithelial cells. J. Cell Biol. 103:2565-2568.
29. Matter, K., W. Hunziker, and I. Mellman. 1992. Basolateral sorting of LDL receptor in MDCK cells: the cytoplasmic domain contains two tyrosine-dependent targeting determinants. Cell 71:741-753.
30. Matter, K., J. A. Whitney, E. M. Yamamoto, and I. Mellman. 1993. Common signals control low density lipoprotein receptor sorting in endosomes and the Golgi complex of MDCK cells. Cell 74:1053-1064.
31. 2-terminus or the COOH-terminus of G protein of vesicular stomatitis virus is defective in transport to the cell surface. Proc. Natl. Acad. Sci. USA 81:395-399.
32. McQueen, N. L., D. P. Nayak, E. B. Stephens, and R. W. Compans. 1986. Polarized expression of a chimeric protein in which the transmembrane and cytoplasmic domains of the influenza virus hemagglutinin have been replaced by those of the vesicular stomatitis virus G protein. Proc. Natl. Acad. Sci. USA 83:9318-9322.
33. McQueen, N. L., D. P. Nayak, E. B. Stephens, and R. W. Compans. 1987. Basolateral expression of a chimeric protein in which the transmembrane and cytoplasmic domains of vesicular stomatitis virus G protein have been replaced by those of the influenza virus hemagglutinin. J. Biol. Chem. 262:16233-16240.
34. Morrison, T. G., and L. J. McGinnes. 1985. Cytochlasin D accelerates the release of Newcastle disease virus from infected cells. Virus Res. 4:93-106.
35. Mostov, K. E., A. de Bruyn Kops, and D. L. Deitcher. 1986. Deletion of the cytoplasmic domain of the polymeric immunoglobulin receptor prevents basolateral localization and endocytosis. Cell 47:359-364.
36. Nayak, D. P., K. Tobita, J. M. Janda, A. R. Davis, and B. K. De. 1978. Homologous interference mediated by defective interfering influenza virus derived from a tempenitive-sensitive mutant of influenza virus. J. Virol. 28:375-386.
37. Neame, S. J., and C. M. Isacke. 1993. The cytoplasmic tail of CD44 is required for basolateral localization in epithelial MDCK cells but does not mediate association with the detergent insoluble cytoskeleton of fibroblasts. J. Cell Biol. 121:1299-1310.
38. Powell, S. K., B. A. Cunningham, G. M. Edelman, and E. Rodriguez-Boulan. 1991. Targeting transmembrane and GPI-anchored forms of N-CAM to opposite domains of a polarized epithelial cell. Nature (London) 353:76-77.
39. Prill, V., L. Lehmann, K. von Figura, and C. Peters. 1993. The cytoplasmic tail of lysosomal acid phosphatase contains overlapping but distinct signals for basolateral sorting and rapid internalization in polarized MDCK cells. EMBO J. 12:2181-2193.
40. Puddington, L., C. Woodgett, and J. K. Rose. 1987. Replacement of the cytoplasmic domain alters sorting of a viral glycoprotein in polarized cells. Proc. Natl. Acad. Sci. USA 84:2756-2760.
41. Rodriguez-Boulan, E., and M. Pendergast. 1980. Polarized distribution of viral envelope proteins in the plasma membrane of infected epithelial cells. Cell 20:45-54.
42. Rodriguez-Boulan, E., P. J. Salas, M. Sargiacomo, M. Lisanti, A. Le Bivic, Y. Sambuy, D. Vega-Salas, and L. Graeve. 1989. Methods to estimate the polarized distribution of surface antigens in cultured epithelial cells. Methods Cell Biol. 32:37-110.
43. Rodriguez-Boulan, E. J., and D. D. Sabatini. 1978. Asymmetric budding of viruses in epithelial monolayers: a model for the study of epithelial polarity. Proc. Natl. Acad. Sci. USA 75:5071-5075.
44. Roman, L. M., and H. Garoff. 1986. Alteration of the cytoplasmic domain of the membrane spanning glycoprotein p62 of Semliki Forest virus does not affect its polar distribution in established lines of Madin-Darby canine kidney cells. J. Cell Biol. 103:2607-2618.
45. Roth, M. G., R. W. Compans, L. Giusti, A. R. Davis, D. P. Nayak, M. J. Gething, and J. Sambrook. 1983. Influenza virus hemagglutinin expression is polarized in cells infected with recombinant SV 40 viruses carrying cloned hemagglutinin DNA. Cell 33:435-443.
46. Roth, M. G., C. Doyle, J. Sambrook, and M.-J. Gething. 1986. Heterologous transmembrane and cytoplasmic domains direct functional chimeric influenza virus hemagglutinins into the endocytic pathway. J. Cell Biol. 102:1271-1283.
47. Roth, M. G., D. Gunderson, N. Patil, and E. Rodriguez-Boulan. 1987. The large external domain is sufficient for the correct sorting of secreted or chimeric influenza virus hemagglutinin in polarized monkey kidney cells. J. Cell Biol. 104:769-782.
48. Roth, M. G., R. V. Srinivas, and R. W. Compans. 1983. Basolateral maturation of retroviruses in polarized epithelial cells. J. Virol. 45:1065-1073.
49. Sanderson, C. M., R. Avalos, A. Kundu, and D. P. Nayak. 1995. Interaction of Sendai viral F, HN and M proteins with host cytoskeletal and lipid components in Sendai virus-infected BHK cells. Virology 209:701-707.
50. Sanderson, C. M., H.-H. Wu, and D. P. Nayak. 1994. Sendai virus M protein hinds independently to either the F or the HN glycoprotein in vivo. J. Virol. 68:69-76.
51. Scheiffele, P., J. Peränen, and K. Simons. 1995. N-glycans as apical sorting signals in epithelial cells. Nature (London) 378:96-98.
52. Simons, K., and G. van Meer. 1988. Lipid sorting in epithelial cells. Biochemistry 27:6197-6202.
53. Simons, K., and A. Wandinger-Ness. 1990. Polarized sorting in epithelia. Cell 62:207-210.
54. Skibbens, J. E., M. G. Roth, and K. S. Matlin. 1989. Differential extractibility of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J. Cell Biol. 108:821-832.
55. Tashiro, M., J. T. Seto, H.-D. Klenk, and R. Rott. 1993. Possible involvement of microtubule disruption in bipolar budding of a Sendai virus mutant, F1-R, in epithelial MDCK cells. J. Virol. 67:5902-5910.
56. Tashiro, M., M. Yamakawa, K. Tobita, H. D. Klenk, R. Rott, and J. T. Seto. 1990. Altered budding site of pantropic mutant of Sendai virus, F1-R, in polarized epithelial cells. J. Virol. 64:4672-4677.
57. Thomas, D. C., C. B. Brewer, and M. G. Roth. 1993. Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon a tyrosine. J. Biol. Chem. 268:3313-3320.
58. Thomas, D. C., and M. G. Roth. 1994. The basolateral targeting signal in the cytoplasmic domain of glycoprotein G from vesicular stomatitis virus resembles a variety of intracellular targeting motifs related by primary sequence but having diverse targeting activities. J. Biol. Chem. 269:15732-15739.
59. vanMeer, G., and K. Simons. 1982. Viruses budding from either the apical or the basolateral plasma membrane domain of MDCK cells have unique phospholipid compositions. EMBO J. 1:847-852.
60. Vogel, L. K., O. Noren, and H. Sjostram. 1995. Transcytosis of aminopepti-dase N in Caco-2 cells is mediated by a non-cytoplasmic signal. J. Biol. Chem. 270:22933-22938.
61. Yokode, M., R. K. Pathak, R. E. Hammer, M. S. Brown, J. L. Goldstein, and R. G. W. Anderson. 1992. Cytoplasmic sequence required for basolateral targeting of LDL receptor in livers of transgenic mice. J. Cell Biol. 117:39-46.
62. Zurzolo, C., W. van't Hof, G. van Meer, and E. Rodriguez-Boulan. 1994. VIP21/caveolin, glycosphingolipid clusters and the sorting of glycosylphosphatidylinositol-anchored proteins in epithelial cells. EMBO J. 13:42-53.