Structural analysis of the roles of influenza A virus membrane-associated proteins in assembly and morphology

Journal of Virology

Volumn 89, Issue 17, 2015, Pages 8957-8966

  Chlanda, Petr ^a,c   Schraidt, Oliver ^a   Kummer, Susann ^b   Riches, James ^a,d   Oberwinkler, Heike ^b,e   Prinz, Simone ^a,f   Kräusslich, Hans Georg ^b   Briggs, John A G ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f MAX PLANCK INSTITUTE OF BIOPHYSICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; M PROTEIN; VIRUS PROTEIN; INFLUENZA VIRUS HEMAGGLUTININ; M1 PROTEIN, INFLUENZA A VIRUS; M2 PROTEIN, INFLUENZA A VIRUS; MATRIX PROTEIN; SIALIDASE;

ARTICLE; BIOCHEMICAL ANALYSIS; CELL MEMBRANE; CLUSTER ANALYSIS; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; HUMAN; HUMAN CELL; INFLUENZA VIRUS A; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; VIRUS MORPHOLOGY; VIRUS PARTICLE; VIRUS RELEASE; BIOSYNTHESIS; CELL LINE; CRYOELECTRON MICROSCOPY; GENETICS; HEK293 CELL LINE; INFLUENZA A VIRUS (H2N2); INFLUENZA A VIRUS (H3N2); METABOLISM; VIRUS ASSEMBLY;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

CELL LINE; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; HEK293 CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H2N2 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; NEURAMINIDASE; VIRAL MATRIX PROTEINS; VIRUS ASSEMBLY; VIRUS RELEASE;

EID: 84938912620     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00592-15     Document Type: Article

References (38)

1. Lamb RA, Zebedee SL, Richardson CD. 1985. Influenza virus M2 protein is an integral membrane protein expressed on the infected-cell surface. Cell 40:627-633. http://dx.doi.org/10.1016/0092-8674(85)90211-9.
2. Calder LJ, Wasilewski S, Berriman JA, Rosenthal PB. 2010. Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci U S A 107:10685-10690. http://dx.doi.org/10.1073/pnas.1002123107.
3. Palese P, Shaw ML. 2007. Orthomyxoviridae: the viruses and their replication, p 1647-1689. In Knipe DM, Howley PM, Griffin DE, Lamb RA, Martin MA, Roizman B, Straus SE (ed), Fields virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
4. Rossman JS, Lamb RA. 2011. Influenza virus assembly and budding. Virology 411:229-236. http://dx.doi.org/10.1016/j.virol.2010.12.003.
5. Rossman JS, Jing X, Leser GP, Lamb RA. 2010. Influenza virus M2 protein mediates ESCRT-independent membrane scission. Cell 142:902-913. http://dx.doi.org/10.1016/j.cell.2010.08.029.
6. Murti KG, Webster RG. 1986. Distribution of hemagglutinin and neuraminidase on influenza virions as revealed by immunoelectron microscopy. Virology 149:36-43. http://dx.doi.org/10.1016/0042-6822(86)90084-X.
7. Mosley VM, Wyckoff RW. 1946. Election micrography of the virus of influenza. Nature 157:263.
8. Seladi-Schulman J, Steel J, Lowen AC. 2013. Spherical influenza viruses have a fitness advantage in embryonated eggs, while filament-producing strains are selected in vivo. J Virol 87:13343-13353. http://dx.doi.org/10.1128/JVI.02004-13.
9. Booy FP, Ruigrok RW, van Bruggen EF. 1985. Electron microscopy of influenza virus. A comparison of negatively stained and ice-embedded particles. J Mol Biol 184:667-676.
10. Burnet FM, Lind PE. 1957. Studies on filamentary forms of influenza virus with special reference to the use of dark-ground-microscopy. Arch Gesamte Virusforsch 7:413-428. http://dx.doi.org/10.1007/BF01241959.
11. Chu CM, Dawson IM, Elford WJ. 1949. Filamentous forms associated with newly isolated influenza virus. Lancet i:602.
12. Donald HB, Isaacs A. 1954. Some properties of influenza virus filaments shown by electron microscopic particle counts. J Gen Microbiol 11:325-331. http://dx.doi.org/10.1099/00221287-11-2-325.
13. Neumann G, Noda T, Kawaoka Y. 2009. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature 459:931-939. http://dx.doi.org/10.1038/nature08157.
14. Roberts PC, Compans RW. 1998. Host cell dependence of viral morphology. Proc Natl Acad Sci U S A 95:5746-5751. http://dx.doi.org/10.1073/pnas.95.10.5746.
15. Chen BJ, Leser GP, Morita E, Lamb RA. 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. http://dx.doi.org/10.1128/JVI.00361-07.
16. Yondola MA, Fernandes F, Belicha-Villanueva A, Uccelini M, Gao Q, Carter C, Palese P. 2011. Budding capability of the influenza virus neuraminidase can be modulated by tetherin. J Virol 85:2480-2491. http://dx.doi.org/10.1128/JVI.02188-10.
17. Wang D, Harmon A, Jin J, Francis DH, Christopher-Hennings J, Nelson E, Montelaro RC, Li F. 2010. The lack of an inherent membrane targeting signal is responsible for the failure of the matrix (M1) protein of influenza A virus to bud into virus-like particles. J Virol 84:4673-4681. http://dx.doi.org/10.1128/JVI.02306-09.
18. Gomez-Puertas P, Albo C, Perez-Pastrana E, Vivo A, Portela A. 2000. Influenza virus matrix protein is the major driving force in virus budding. J Virol 74:11538-11547. http://dx.doi.org/10.1128/JVI.74.24.11538-11547.2000.
19. Ali A, Avalos RT, Ponimaskin E, Nayak DP. 2000. Influenza virus assembly: effect of influenza virus glycoproteins on the membrane association of M1 protein. J Virol 74:8709-8719. http://dx.doi.org/10.1128/JVI.74.18.8709-8719.2000.
20. Enami M, Enami K. 1996. Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. J Virol 70:6653-6657.
21. Bourmakina SV, Garcia-Sastre A. 2003. Reverse genetics studies on the filamentous morphology of influenza A virus. J Gen Virol 84:517-527. http://dx.doi.org/10.1099/vir.0.18803-0.
22. Burleigh LM, Calder LJ, Skehel JJ, Steinhauer DA. 2005. Influenza A viruses with mutations in theM1helix six domain display a wide variety of morphological phenotypes. J Virol 79:1262-1270. http://dx.doi.org/10.1128/JVI.79.2.1262-1270.2005.
23. Elleman CJ, Barclay WS. 2004. The M1 matrix protein controls the filamentous phenotype of influenza A virus. Virology 321:144-153. http://dx.doi.org/10.1016/j.virol.2003.12.009.
24. Iwatsuki-Horimoto K, Horimoto T, Noda T, Kiso M, Maeda J, Watanabe S, Muramoto Y, Fujii K, Kawaoka Y. 2006. The cytoplasmic tail of the influenza A virus M2 protein plays a role in viral assembly. J Virol 80:5233-5240. http://dx.doi.org/10.1128/JVI.00049-06.
25. McCown MF, Pekosz A. 2006. Distinct domains of the influenza A virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J Virol 80:8178-8189. http://dx.doi.org/10.1128/JVI.00627-06.
26. Roberts KL, Leser GP, Ma C, Lamb RA. 2013. The amphipathic helix of influenza A virus M2 protein is required for filamentous bud formation and scission of filamentous and spherical particles. J Virol 87:9973-9982. http://dx.doi.org/10.1128/JVI.01363-13.
27. Roberts PC, Lamb RA, Compans RW. 1998. The M1 and M2 proteins of influenza A virus are important determinants in filamentous particle formation. Virology 240:127-137. http://dx.doi.org/10.1006/viro.1997.8916.
28. Rossman JS, Jing X, Leser GP, Balannik V, Pinto LH, Lamb RA. 2010. Influenza virus M2 ion channel protein is necessary for filamentous virion formation. J Virol 84:5078-5088. http://dx.doi.org/10.1128/JVI.00119-10.
29. Niwa H, Yamamura K, Miyazaki J. 1991. Efficient selection for highexpression transfectants with a novel eukaryotic vector. Gene 108:193-199. http://dx.doi.org/10.1016/0378-1119(91)90434-D.
30. Yewdell JW, Frank E, Gerhard W. 1981. Expression of influenza A virus internal antigens on the surface of infected P815 cells. J Immunol 126: 1814-1819.
31. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A. 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676-682. http://dx.doi.org/10.1038/nmeth.2019.
32. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-76. http://dx.doi.org/10.1006/jsbi.1996.0013.
33. Jackson D, Lamb RA. 2008. The influenza A virus spliced messenger RNA M mRNA3 is not required for viral replication in tissue culture. J Gen Virol 89:3097-3101. http://dx.doi.org/10.1099/vir.0.2008/004739-0.
34. Inglis SC, Brown CM. 1981. Spliced and unspliced RNAs encoded by virion RNA segment 7 of influenza virus. Nucleic Acids Res 9:2727-2740. http://dx.doi.org/10.1093/nar/9.12.2727.
35. Shih SR, Nemeroff ME, Krug RM. 1995. The choice of alternative 5= splice sites in influenza virus M1 mRNA is regulated by the viral polymerase complex. Proc Natl Acad Sci U S A 92:6324-6328. http://dx.doi.org/10.1073/pnas.92.14.6324.
36. Lai JC, Chan WW, Kien F, Nicholls JM, Peiris JS, Garcia JM. 2010. Formation of virus-like particles from human cell lines exclusively expressing influenza neuraminidase. J Gen Virol 91:2322-2330. http://dx.doi.org/10.1099/vir.0.019935-0.
37. Vijayakrishnan S, Loney C, Jackson D, Suphamungmee W, Rixon FJ, Bhella D. 2013. Cryotomography of budding influenza A virus reveals filaments with diverse morphologies that mostly do not bear a genome at their distal end. PLoS Pathog 9:e1003413. http://dx.doi.org/10.1371/journal.ppat.1003413.
38. Harris A, Cardone G, Winkler DC, Heymann JB, Brecher M, White JM, Steven AC. 2006. Influenza virus pleiomorphy characterized by cryoelectron tomography. Proc Natl Acad Sci U S A 103:19123-19127. http://dx.doi.org/10.1073/pnas.0607614103.