Influenza virus assembly and lipid raft microdomains: A role for the cytoplasmic tails of the spike glycoproteins

Journal of Virology

Volumn 74, Issue 10, 2000, Pages 4634-4644

  Zhang, Jie ^a   Pekosz, Andrew ^a   Lamb, Robert A ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CEREBROSIDE; CHOLESTEROL; DETERGENT; GANGLIOSIDE; GLYCOPROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; ION CHANNEL; LACTOSYLCERAMIDE; LIPID; MATRIX PROTEIN; MEMBRANE PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; SPHINGOMYELIN; SULFATIDE; TRIACYLGLYCEROL; TRITON X 100; VIRUS SIALIDASE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOPLASM; HUMAN; HUMAN CELL; INFLUENZA VIRUS; LIPID COMPOSITION; NONHUMAN; PALMITOYLATION; PRIORITY JOURNAL; VIRION; VIRUS ASSEMBLY; VIRUS ENVELOPE;

ANIMALS; CELL LINE; CELL POLARITY; DETERGENTS; GLYCOLIPIDS; HELA CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS; INFLUENZAVIRUS C; MEMBRANE GLYCOPROTEINS; MEMBRANE LIPIDS; NEURAMINIDASE; SOLUBILITY; VIRAL MATRIX PROTEINS; VIRION; VIRUS ASSEMBLY;

EID: 0033995067     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.74.10.4634-4644.2000     Document Type: Article

References (71)

1. Avalos, R. T., Z. Yu, and D. P. Nayak. 1997. Association of influenza virus NP and M1 proteins with cellular cytoskeletal elements in influenza virus-infected cells. J. Virol. 71:2947-2958.
2. 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.
3. Brown, D. A., and E. London. 1998. Functions of lipid rafts in biological membranes. Annu. Rev. Cell Dev. Biol. 14:111-136.
4. 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.
5. Burnet, F. M. 1941. Growth of influenza virus in the allantoic cavity of the chick embryo. Aust. J. Exp. Biol. Med. Sci. 19:291-295.
6. Cheong, K. H., D. Zacchetti, E. E. Schneeberger, and K. Simons. 1999. VIP17/MAL, a lipid raft-associated protein, is involved in apical transport in MDCK cells. Proc. Natl. Acad. Sci. USA 96:6241-6248.
7. Colman, P. M. 1989. Neuraminidase: enzyme and antigen, p. 175-218. In R. M. Krug (ed.), The influenza viruses. Plenum Press, New York, N.Y.
8. Danielsen, E. M. 1995. Involvement of detergent-insoluble complexes in the intracellular transport of intestinal brush border enzymes. Biochemistry 34: 1596-1605.
9. Enami, M., and K. Enami. 1996. Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. J. Virol. 70:6653-6657.
10. Fiedler, K., T. Kobayashi, T. V. Kurzchalia, and K. Simons. 1993. Glycosphingolipid-enriched, detergent-insoluble complexes in protein sorting in epithelial cells. Biochemistry 32:6365-6373.
11. Fiedler, K., F. Lafont, R. G. Parton, and K. Simons. 1995. Annexin XIIIb: a novel epithelial specific annexin is implicated in vesicular traffic to the apical plasma membrane. J. Cell Biol. 128:1043-1053.
12. Friedrichson, T., and T. V. Kurzchalia. 1998. Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394:802-805.
13. Garcia-Sastre, A., and P. Palese. 1995. The cytoplasmic tail of the neuraminidase protein of influenza A virus does not play an important role in the packaging of this protein into viral envelopes. Virus Res. 37:37-47.
14. Goto, H., and Y. Kawaoka. 1998. A novel mechanism for the acquisition of virulence by a human influenza A virus. Proc. Natl. Acad. Sci. USA 95: 10224-10228.
15. Gregoriades, A., and B. Frangione. 1981. Insertion of influenza M protein into the viral lipid bilayer and localization of site of insertion. J. Virol. 40:323-328.
16. Gut, A., F. Kappeler, N. Hyka, M. S. Balda, H. P. Hauri, and K. Matter. 1998. Carbohydrate-mediated Golgi to cell surface transport and apical targeting of membrane proteins. EMBO J. 17:1919-1929.
17. Hay, A. J. 1974. Studies on the formation of the influenza virus envelope. Virology 60:398-418.
18. 2 protein. J. Virol. 69:1219-1225.
19. 2 protein is restricted to apical surfaces of polarized epithelial cells. J. Virol. 66:5542-5552.
20. Hunziker, W., C. Harter. K. Matter, and I. Mellman. 1991. Basolateral sorting in MDCK cells requires a distinct cytoplasmic domain determinant. Cell 66:907-920.
21. Jin, H., G. Leser, and R. A. Lamb. 1994. The influenza virus hemagglutinin cytoplasmic tail is not essential for virus assembly or infectivity. EMBO J. 13:5504-5515.
22. Jin, H., G. P. Leser, J. Zhang, and R. A. Lamb. 1997. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 16:1236-1247.
23. Jin, H., K. Subbarao, S. Bagai, G. P. Leser, B. R. Murphy, and R. A. Lamb. 1996. Palmitylation of the influenza virus hemagglutinin (H3) is not essential for virus assembly or infectivity. J. Virol. 70:1406-1414.
24. 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.
25. Keller, P., and K. Simons. 1998. Cholesterol is required for surface transport of influenza virus hemagglutinin. J. Cell Biol. 140:1357-1367.
26. Kretzschmar, E., M. Bui, and J. K. Rose. 1996. Membrane association of influenza virus matrix protein does not require specific Hydrophobic domains or the viral glycoproteins. Virology 220:37-45.
27. Kretzschmar, E., L. Buonocore, M. J. Schnell, and J. K. Rose. 1997. High-efficiency incorporation of functional influenza virus glycoproteins into recombinant vesicular stomatitis viruses. J. Virol. 71:5982-5989.
28. Kundu, A., R. T. Avalos, C. M. Sanderson, and D. P. Nayak. 1996. Transmembrane domain of influenza virus neuraminidase. a type II protein, possesses an apical sorting signal in polarized MDCK cells. J. Virol. 70:6508-6515.
29. Lafont, F., S. Lecat, P. Verkade, and K. Simons. 1998. Annexin XIIIb associates with lipid microdomains to function in apical delivery. J. Cell Biol. 142:1413-1427.
30. Lamb, R. A., P. R. Etkind, and P. W. Choppin. 1978. Evidence for a ninth influenza viral polypeptide. Virology 91:60-78.
31. 2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40:627-633.
32. Le Bivic, A., Y. Sambuy, K. Mostov, and E. Rodriguez-Boulan. 1990. Vectorial targeting of an endogenous apical membrane sialoglycoprotein and uvomorulin in MDCK cells. J. Cell Biol. 110:1533-1539.
33. Ledeen, R. W., R. K. Yu, and L. F. Eng. 1973. Gangliosides of human myelin: sialosylgalactosylceramide (G7) as a major component. J. Neurochem. 21: 829-839.
34. Lin, S., H. Y. Naim, A. C. Rodriguez, and M. G. Roth. 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.
35. 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.
36. Macala, L. J., R. K. Yu, and S. Ando. 1983. Analysis of brain lipids by high performance thin-layer chromatography and densitometry. J. Lipid Res. 24:1243-1250.
37. Martin, K., and A. Helenius. 1991. Nuclear transport of influenza virus ribonucleoproteins: the viral matrix protein (M1) promotes export and inhibits import. Cell 67:117-130.
38. Melkonian, K. A., A. G. Ostermeyer, J. Z. Chen, M. G. Roth, and D. A. Brown. 1999, Role of lipid modifications in targeting proteins to detergent-resistant membrane rafts. Many raft proteins are acylated, while few are prenylated. J. Biol. Chem. 274:3910-3917.
39. Millan, J., and M. A. Alonso. 1998. MAL, a novel integral membrane protein of human T lymphocytes, associates with glycosylphosphatidylinositol-anchored proteins and Src-like tyrosine kinases. Eur. J. lmmunol. 28:3675-3684.
40. Mitnaul, L. J., M. R. Castrucci, K. G. Murti, and Y. Kawaoka. 1996. The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J. Virol. 70:873-879.
41. Montixi, C., C. Langlet, A. M. Bernard, J. Thimonier, C. Dubois, M. A. Wurbel, J. P. Chauvin, M. Pierres, and H. T. He. 1998. Engagement of T cell receptor triggers its recruitment to low-density detergent-insoluble membrane domains. EMBO J. 17:5334-5348.
42. Moran, M., and M. C. Miceli. 1998. Engagement of GPI-linked CD48 contributes to TCR signals and cytoskeletal reorganization: a role for lipid rafts in T cell activation. Immunity 9:787-796.
43. Nobusawa, E., T. Aoyama, H. Kato, Y. Suzuki, Y. Tateno, and K. Nakajima. 1991. Comparison of complete amino acid sequences and receptor-binding properties among 13 serotypes of hemagglutinin of influenza A viruses. Virology 182:475-485.
44. O'Neill, R. E., J. Talon, and P. Palese. 1998. The influenza virus NEP (NS2 protein) mediates the nuclear export of viral ribonucleoproteins. EMBO J. 17:288-296.
45. Paterson, R. G., and R. A. Lamb. 1993. The molecular biology of influenza viruses and paramyxoviruses, p. 35-73. In A. Davidson and R. M. Elliott (ed.). Molecular virology: a practical approach. IRL Oxford University Press, Oxford, England.
46. Pekosz, A., and R. A. Lamb. 1999. Cell surface expression of biologically active influenza C virus HEF glycoprotein expressed from cDNA. J. Virol. 73:8808-8812.
47. Pekosz, A., and R. A. Lamb. 1997. The CM2 protein of influenza C virus is an oligomeric integral membrane glycoprotein structurally analogous to influenza A virus M2 and influenza B virus NB proteins. Virology 237:439-51.
48. Pimplikar, S. W., E. Ikonen, and K. Simons. 1994. Basolateral protein transport in streptolysin O-permeabilized MDCK cells. J. Cell Biol. 125: 1025-1035.
49. Puertollano, R., F. Martin-Belmonte, J. Millan, M. del Carmen de Marco, J. P. Albar, L. Kremer, and M. A. Alonso. 1999. The MAL proteolipid is necessary for normal apical transport and accurate sorting of the influenza virus hemagglutinin in Madin-Darby canine kidney cells. J. Cell Biol. 145: 141-151.
50. Rodriguez-Boulan, E., K. T. Paskiet, P. J. Salas, and E. Bard. 1984. Intracellular transport of influenza virus hemagglutinin to the apical surface of Madin-Darby canine kidney cell. J. Cell Biol. 98:308-319.
51. Romanoff, A. L. 1960. The avian embryo, p. 1039-1140. The Macmillan Company, New York, N.Y.
52. Scheiffele, P., J. Peranen, and K. Simons. 1995. N-glycans as apical sorting signals in epithelial cells. Nature 378:96-98.
53. Scheiffele, P., A. Rietveld, T. Wilk, and K. Simons. 1999. Influenza viruses select ordered lipid domains during budding from the plasma membrane. J. Biol. Chem. 274:2038-2044.
54. Scheiffele, P., M. G. Roth, and K. Simons. 1997. Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J. 16:5501-5508.
55. Schroeder, R., E. London, and D. Brown. 1994. Interactions between saturated acyl chains confer detergent resistance on lipids and glycosylphosphatidylinositol (GPI)-anchored proteins: GPI-anchored proteins in liposomes and cells show similar behavior. Proc. Natl. Acad. Sci. USA 91:12130-12134.
56. Simons, K., and E. Ikonen. 1997. Functional rafts in cell membranes. Nature 387:569-572.
57. Singer, S. J., and G. L. Nicolson. 1972. The fluid mosaic model of the structure of cell membranes. Science 175:720-731.
58. Skibbens, J. E., M. G. Roth, and K. S. Matlin. 1989. Differential extractability of influenza virus hemagglutinin during intracellular transport in polarized epithelial cells and nonpolar fibroblasts. J. Cell Biol. 108:821-832.
59. Sternberg, P. W., and S. L. Schmid. 1999. Caveolin, cholesterol and Ras signalling. Nat. Cell Biol. 1:E35-E37.
60. Sugawara, K., H. Nishimura, F. Kitame, and K. Nakamura. 1986. Antigenic variation among human strains of influenza C virus detected with monoclonal antibodies to gp88 glycoprotein. Virus Res. 6:27-32.
61. Varma, R., and S. Mayor. 1998. GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394:798-801.
62. Veit, M., G. Herrler, M. F. G. Schmidt, R. Rott, and H.-D. Klenk. 1990. The hemagglutinating glycoproteins of influenza B and C viruses are acylated with different fatty acids. Virology 177:807-811.
63. Velt, M., H.-D. Klenk, A. Kendal, and R. Rott. 1991. The M2 protein of influenza A virus is acylated. Virology 184:227-234.
64. Whittaker, G., I. Kemler, and A. Helenius. 1995. Hyperphosphorylation of mutant influenza virus matrix protein, M1, causes its retention in the nucleus. J. Virol. 69:439-445.
65. Xavier, R., T. Brennan, Q. Li, C. McCormack, and B. Seed. 1998. Membrane compartmentation is required for efficient T cell activation. Immunity 8:723-732.
66. Yeaman, C., A. H. Le Gall, A. N. Baldwin, L. Monlauzeur, A. Le Bivic, and E. Rodriguez-Boulan. 1997. The O-glycosylated stalk domain is required for apical sorting of neurotrophin receptors in polarized MDCK cells. J. Cell Biol. 139:929-940.
67. 2 in virions. J. Virol. 62:2762-2772.
68. Zhang, J., and R. A. Lamb. 1996. Characterization of the membrane association of the influenza virus matrix protein in living cells. Virology 225:255-266.
69. Zhang, J., G. P. Leser, A. Pekosz, and R. A. Lamb. The cytoplasmic tails of the influenza virus spike glycoproteins are required for normal genome packaging. Virology, in press.
70. Zhang, W., R. P. Trible, and L. E. Samelson. 1998. LAT palmitoylation: its essential role in membrane microdomain targeting and tyrosine phosphorylation during T cell activation. Immunity 9:239-246.
71. Zheng, X., D. Lu, and J. E. Sadler. 1999. Apical sorting of bovine enteropeptidase does not involve detergent-resistant association with sphingolipid-cholesterol rafts. J. Biol. Chem. 274:1596-1605.