Lipid domain association of influenza virus proteins detected by dynamic fluorescence microscopy techniques

Cellular Microbiology

Volumn 15, Issue 2, 2013, Pages 179-189

  Veit, Michael ^a   Engel, Stephanie ^a   Thaa, Bastian ^a   Scolari, Silvia ^b   Herrmann, Andreas ^b  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

LIPID; PROTEIN M2; VIRUS HEMAGGLUTININ; VIRUS PROTEIN; VIRUS SIALIDASE;

CELL SURFACE; FLUORESCENCE MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC TRANSFECTION; INFLUENZA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; VIRUS ASSEMBLY; VIRUS RELEASE; VIRUS REPLICATION;

ANIMALS; CHO CELLS; CRICETINAE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; MEMBRANE MICRODOMAINS; MICROSCOPY, FLUORESCENCE; ORTHOMYXOVIRIDAE; TRANSFECTION; VIRAL MATRIX PROTEINS; VIRUS ASSEMBLY; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE;

EID: 84872609131     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12045     Document Type: Review

References (60)

1. Anderson, R.G., and Jacobson, K. (2002) A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296: 1821-1825.
2. Brown, D.A., and Rose, J.K. (1992) Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface. Cell 68: 533-544.
3. Castrucci, M.R., Hughes, M., Calzoletti, L., Donatelli, I., Wells, K., Takada, A., and Kawaoka, Y. (1997) The cysteine residues of the M2 protein are not required for influenza A virus replication. Virology 238: 128-134.
4. Chen, B.J., and Lamb, R.A. (2008) Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology 372: 221-232.
5. Chen, B.J., Takeda, M., and Lamb, R.A. (2005) Influenza virus hemagglutinin (H3 subtype) requires palmitoylation of its cytoplasmic tail for assembly: M1 proteins of two subtypes differ in their ability to support assembly. J Virol 79: 13673-13684.
6. Chen, B.J., Leser, G.P., Morita, E., and Lamb, R.A. (2007) Influenza virus hemagglutinin and neuraminidase, but not the matrix protein, are required for assembly and budding of plasmid-derived virus-like particles. J Virol 81: 7111-7123.
7. Chen, B.J., Leser, G.P., Jackson, D., and Lamb, R.A. (2008) The influenza virus M2 protein cytoplasmic tail interacts with the M1 protein and influences virus assembly at the site of virus budding. J Virol 82: 10059-10070.
8. Engel, S., Scolari, S., Thaa, B., Krebs, N., Korte, T., Herrmann, A., and Veit, M. (2010) FLIM-FRET and FRAP reveal association of influenza virus haemagglutinin with membrane rafts. Biochem J 425: 567-573.
9. Engel, S., de Vries, M., Herrmann, A., and Veit, M. (2012) Mutation of a raft-targeting signal in the transmembrane region retards transport of influenza virus hemagglutinin through the Golgi. FEBS Lett 586: 277-282.
10. Ge, M., and Freed, J.H. (2011) Two conserved residues are important for inducing highly ordered membrane domains by the transmembrane domain of influenza hemagglutinin. Biophys J 100: 90-97.
11. Gerl, M.J., Sampaio, J.L., Urban, S., Kalvodova, L., Verbavatz, J.M., Binnington, B., etal. (2012) Quantitative analysis of the lipidomes of the influenza virus envelope and MDCK cell apical membrane. J Cell Biol 196: 213-221.
12. Gowrishankar, K., Ghosh, S., Saha, S., Rumamol, C., Mayor, S., and Rao, M. (2012) Active remodeling of cortical actin regulates spatiotemporal organization of cell surface molecules. Cell 149: 1353-1367.
13. Grantham, M.L., Wu, W.H., Lalime, E.N., Lorenzo, M.E., Klein, S.L., and Pekosz, A. (2009) Palmitoylation of the influenza A virus M2 protein is not required for virus replication in vitro but contributes to virus virulence. J Virol 83: 8655-8661.
14. Gunewardene, M.S., Subach, F.V., Gould, T.J., Penoncello, G.P., Gudheti, M.V., Verkhusha, V.V., and Hess, S.T. (2011) Superresolution imaging of multiple fluorescent proteins with highly overlapping emission spectra in living cells. Biophys J 101: 1522-1528.
15. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. (1998) Lipid domain structure of the plasma membrane revealed by patching of membrane components. J Cell Biol 141: 929-942.
16. Hess, S.T., Kumar, M., Verma, A., Farrington, J., Kenworthy, A., and Zimmerberg, J. (2005) Quantitative electron microscopy and fluorescence spectroscopy of the membrane distribution of influenza hemagglutinin. J Cell Biol 169: 965-976.
17. Hess, S.T., Gould, T.J., Gudheti, M.V., Maas, S.A., Mills, K.D., and Zimmerberg, J. (2007) Dynamic clustered distribution of hemagglutinin resolved at 40nm in living cell membranes discriminates between raft theories. Proc Natl Acad Sci USA 104: 17370-17375.
18. Itano, M.S., Neumann, A.K., Liu, P., Zhang, F., Gratton, E., Parak, W.J., etal. (2011) DC-SIGN and influenza hemagglutinin dynamics in plasma membrane microdomains are markedly different. Biophys J 100: 2662-2670.
19. Ivanchenko, S., Godinez, W.J., Lampe, M., Krausslich, H.G., Eils, R., Rohr, K., etal. (2009) Dynamics of HIV-1 assembly and release. PLoS Pathog 5: e1000652.
20. Jouvenet, N., Bieniasz, P.D., and Simon, S.M. (2008) Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454: 236-240.
21. Kenworthy, A.K. (2008) Have we become overly reliant on lipid rafts? Talking Point on the involvement of lipid rafts in T-cell activation. EMBO Rep 9: 531-535.
22. Kenworthy, A.K., Nichols, B.J., Remmert, C.L., Hendrix, G.M., Kumar, M., Zimmerberg, J., and Lippincott-Schwartz, J. (2004) Dynamics of putative raft-associated proteins at the cell surface. J Cell Biol 165: 735-746.
23. Kordyukova, L.V., Serebryakova, M.V., Baratova, L.A., and Veit, M. (2008) S acylation of the hemagglutinin of influenza viruses: mass spectrometry reveals site-specific attachment of stearic acid to a transmembrane cysteine. J Virol 82: 9288-9292.
24. Kusumi, A., Koyama-Honda, I., and Suzuki, K. (2004) Molecular dynamics and interactions for creation of stimulation-induced stabilized rafts from small unstable steady-state rafts. Traffic 5: 213-230.
25. Kusumi, A., Suzuki, K.G., Kasai, R.S., Ritchie, K., and Fujiwara, T.K. (2011) Hierarchical mesoscale domain organization of the plasma membrane. Trends Biochem Sci 36: 604-615.
26. Leser, G.P., and Lamb, R.A. (2005) Influenza virus assembly and budding in raft-derived microdomains: a quantitative analysis of the surface distribution of HA, NA and M2 proteins. Virology 342: 215-227.
27. Levental, I., Grzybek, M., and Simons, K. (2010) Greasing their way: lipid modifications determine protein association with membrane rafts. Biochemistry 49: 6305-6316.
28. Melkonian, K.A., Ostermeyer, A.G., Chen, J.Z., Roth, M.G., and Brown, D.A. (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.
29. Munro, S. (2003) Lipid rafts: elusive or illusive? Cell 115: 377-388.
30. Nayak, D.P., Hui, E.K., and Barman, S. (2004) Assembly and budding of influenza virus. Virus Res 106: 147-165.
31. Nayak, D.P., Balogun, R.A., Yamada, H., Zhou, Z.H., and Barman, S. (2009) Influenza virus morphogenesis and budding. Virus Res 143: 147-161.
32. Patterson, G.H., Hirschberg, K., Polishchuk, R.S., Gerlich, D., Phair, R.D., and Lippincott-Schwartz, J. (2008) Transport through the Golgi apparatus by rapid partitioning within a two-phase membrane system. Cell 133: 1055-1067.
33. Rossman, J.S., and Lamb, R.A. (2011) Influenza virus assembly and budding. Virology 411: 229-236.
34. Rossman, J.S., Jing, X., Leser, G.P., Balannik, V., Pinto, L.H., and Lamb, R.A. (2010a) Influenza virus m2 ion channel protein is necessary for filamentous virion formation. J Virol 84: 5078-5088.
35. Rossman, J.S., Jing, X., Leser, G.P., and Lamb, R.A. (2010b) Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142: 902-913.
36. Scheiffele, P., Roth, M.G., and Simons, K. (1997) Interaction of influenza virus haemagglutinin with sphingolipid-cholesterol membrane domains via its transmembrane domain. EMBO J 16: 5501-5508.
37. Schroeder, C. (2010) Cholesterol-binding viral proteins in virus entry and morphogenesis. Subcell Biochem 51: 77-108.
38. Schroeder, C., Heider, H., Möncke-Buchner, E., and Lin, T.I. (2005) The influenza virus ion channel and maturation cofactor M2 is a cholesterol-binding protein. Eur Biophys J 34: 52-66.
39. Scolari, S., Engel, S., Krebs, N., Plazzo, A.P., De Almeida, R.F., Prieto, M., etal. (2009) Lateral distribution of the transmembrane domain of influenza virus hemagglutinin revealed by time-resolved fluorescence imaging. J Biol Chem 284: 15708-15716.
40. Sharma, P., Varma, R., Sarasij, R.C., Ira, Gousset, K., Krishnamoorthy, G., etal. (2004) Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116: 577-589.
41. Shaw, M.L., Stone, K.L., Colangelo, C.M., Gulcicek, E.E., and Palese, P. (2008) Cellular proteins in influenza virus particles. PLoS Pathog 4: e1000085.
42. Shvartsman, D.E., Kotler, M., Tall, R.D., Roth, M.G., and Henis, Y.I. (2003) Differently anchored influenza hemagglutinin mutants display distinct interaction dynamics with mutual rafts. J Cell Biol 163: 879-888.
43. Simons, K., and Gerl, M.J. (2010) Revitalizing membrane rafts: new tools and insights. Nat Rev Mol Cell Biol 11: 688-699.
44. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387: 569-572.
45. Simons, K., and Vaz, W.L. (2004) Model systems, lipid rafts, and cell membranes. Annu Rev Biophys Biomol Struct 33: 269-295.
46. Simpson-Holley, M., Ellis, D., Fisher, D., Elton, D., McCauley, J., and Digard, P. (2002) A functional link between the actin cytoskeleton and lipid rafts during budding of filamentous influenza virions. Virology 301: 212-225.
47. Stewart, S.M., and Pekosz, A. (2011) Mutations in the membrane-proximal region of the influenza A virus M2 protein cytoplasmic tail have modest effects on virus replication. J Virol 85: 12179-12187.
48. Stewart, S.M., Wu, W.H., Lalime, E.N., and Pekosz, A. (2010) The cholesterol recognition/interaction amino acid consensus motif of the influenza A virus M2 protein is not required for virus replication but contributes to virulence. Virology 405: 530-538.
49. Sugrue, R.J., Belshe, R.B., and Hay, A.J. (1990) Palmitoylation of the influenza A virus M2 protein. Virology 179: 51-56.
50. Takeda, M., Leser, G.P., Russell, C.J., and Lamb, R.A. (2003) Influenza virus hemagglutinin concentrates in lipid raft microdomains for efficient viral fusion. Proc Natl Acad Sci USA 100: 14610-14617.
51. Thaa, B., Herrmann, A., and Veit, M. (2010) Intrinsic cytoskeleton-dependent clustering of influenza virus M2 protein with hemagglutinin assessed by FLIM-FRET. J Virol 84: 12445-12449.
52. Thaa, B., Levental, I., Herrmann, A., and Veit, M. (2011) Intrinsic membrane association of the cytoplasmic tail of influenza virus M2 protein and lateral membrane sorting regulated by cholesterol binding and palmitoylation. Biochem J 437: 389-397.
53. Thaa, B., Tielesch, C., Möller, L., Schmitt, A.O., Wolff, T., Bannert, N., etal. (2012) Growth of influenza A virus is not impeded by simultaneous removal of the cholesterol-binding and acylation sites in the M2 protein. J Gen Virol 93: 282-292.
54. Veit, M. (2012) Palmitoylation of virus proteins. Biol Cell 104: 493-515.
55. Veit, M., and Thaa, B. (2011) Association of influenza virus proteins with membrane rafts. Adv Virol 2011: 370606.
56. Veit, M., Klenk, H.D., Kendal, A., and Rott, R. (1991) The M2 protein of influenza A virus is acylated. J Gen Virol 72 (Pt 6): 1461-1465.
57. Vogel, A., Reuther, G., Weise, K., Triola, G., Nikolaus, J., Tan, K.T., etal. (2009) The lipid modifications of Ras that sense membrane environments and induce local enrichment. Angew Chem Int Ed Engl 48: 8784-8787.
58. Wagner, R., Herwig, A., Azzouz, N., and Klenk, H.D. (2005) Acylation-mediated membrane anchoring of avian influenza virus hemagglutinin is essential for fusion pore formation and virus infectivity. J Virol 79: 6449-6458.
59. Zacharias, D.A., Violin, J.D., Newton, A.C., and Tsien, R.Y. (2002) Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells. Science 296: 913-916.
60. Zhang, J., Pekosz, A., and Lamb, R.A. (2000) Influenza virus assembly and lipid raft microdomains: a role for the cytoplasmic tails of the spike glycoproteins. J Virol 74: 4634-4644.