Vaccinia virus lacking A17 induces complex membrane structures composed of open membrane sheets

Archives of Virology

Volumn 156, Issue 9, 2011, Pages 1647-1653

  Chlanda, Petr ^a   Carbajal, Maria Alejandra ^a   Kolovou, Androniki ^b   Hamasaki, Maho ^c   Cyrklaff, Marek ^b   Griffiths, Gareth ^d   Krijnse Locker, Jacomine ^b  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c OSAKA UNIVERSITY   (Japan)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

MATRIX PROTEIN; VIRUS ANTIBODY;

ARTICLE; ELECTRON TOMOGRAPHY; GENE EXPRESSION REGULATION; GENETICS; HELA CELL; HUMAN; METABOLISM; PHYSIOLOGY; VACCINIA VIRUS; VIRUS ASSEMBLY;

ANTIBODIES, VIRAL; ELECTRON MICROSCOPE TOMOGRAPHY; GENE EXPRESSION REGULATION, VIRAL; HELA CELLS; HUMANS; VACCINIA VIRUS; VIRAL MATRIX PROTEINS; VIRUS ASSEMBLY;

ALLIUM CEPA; VACCINIA VIRUS;

EID: 80052271264     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-011-1012-1     Document Type: Article

References (31)

1. Rodriguez D, Esteban M, Rodriguez JR (1995) Vaccinia virus A17L gene product is essential for an early step in virion morphogenesis. J Virol 69: 4640-4648.
2. Cyrklaff M, Risco C, Fernandez JJ, Jimenez MV, Esteban M, Baumeister W, Carrascosa JL (2005) Cryo-electron tomography of vaccinia virus. Proc Natl Acad Sci USA 102: 2772-2777.
3. Condit RC, Moussatche N, Traktman P (2006) In a nutshell: structure and assembly of the vaccinia virion. Adv Virus Res 66: 31-124.
4. Roberts KL, Smith GL (2008) Vaccinia virus morphogenesis and dissemination. Trends Microbiol 16: 472-479.
5. Sodeik B, Krijnse-Locker J (2002) Assembly of vaccinia virus revisited: de novo membrane synthesis or acquisition from the host? Trends Microbiol 10: 15-24.
6. Dales S, Mosbach EH (1968) Vaccinia as a model for membrane biogenesis. Virology 35: 564-583.
7. Chlanda P, Carbajal MA, Cyrklaff M, Griffiths G, Krijnse-Locker J (2009) Membrane rupture generates single open membrane sheets during vaccinia virus assembly. Cell Host Microbe 6: 81-90.
8. Heuser J (2005) Deep-etch EM reveals that the early poxvirus envelope is a single membrane bilayer stabilized by a geodetic "honeycomb" surface coat. J Cell Biol 169: 269-283.
9. Hollinshead M, Vanderplasschen A, Smith GL, Vaux DJ (1999) Vaccinia virus intracellular mature virions contain only one lipid membrane. J Virol 73: 1503-1517.
10. Husain M, Moss B (2003) Evidence against an essential role of COPII-mediated cargo transport to the endoplasmic reticulum-golgi intermediate compartment in the formation of the primary membrane of vaccinia virus. J Virol 77: 11754-11766.
11. Husain M, Weisberg AS, Moss B (2006) Existence of an operative pathway from the endoplasmic reticulum to the immature poxvirus membrane. Proc Natl Acad Sci USA 103: 19506-19511.
12. Rodriguez JR, Risco C, Carrascosa JL, Esteban M, Rodriguez D (1997) Characterization of early stages in vaccinia virus membrane biogenesis: implications of the 21-kilodalton protein and a newly identified 15-kilodalton envelope protein. J Virol 71: 1821-1833.
13. Sodeik B, Doms RW, Ericsson M, Hiller G, Machamer CE, van't Hof W, van Meer G, Moss B, Griffiths G (1993) Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the golgi stacks. J Cell Biol 121: 521-541.
14. Wolffe EJ, Moore DM, Peters PJ, Moss B (1996) Vaccinia virus A17L open reading frame encodes an essential component of nascent viral membranes that is required to initiate morphogenesis. J Virol 70: 2797-2808.
15. Lucic V, Forster F, Baumeister W (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74: 833-865.
16. Jensen ON, Houthaeve T, Shevchenko A, Cudmore S, Ashford T, Mann M, Griffiths G, Krijnse Locker J (1996) Identification of the major membrane and core proteins of vaccinia virus by two-dimensional electrophoresis. J Virol 70: 7485-7497.
17. Salmons T, Kuhn A, Wylie F, Schleich S, Rodriguez JR, Rodriguez D, Esteban M, Griffiths G, Locker JK (1997) Vaccinia virus membrane proteins p8 and p16 are cotranslationally inserted into the rough endoplasmic reticulum and retained in the intermediate compartment. J Virol 71: 7404-7420.
18. Sodeik B, Griffiths G, Ericsson M, Moss B, Doms RW (1994) Assembly of vaccinia virus: effects of rifampin on the intracellular distribution of viral protein p65. J Virol 68: 1103-1114.
19. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116: 71-76.
20. Rodriguez JR, Risco C, Carrascosa JL, Esteban M, Rodriguez D (1998) Vaccinia virus 15-kilodalton (A14L) protein is essential for assembly and attachment of viral crescents to virosomes. J Virol 72: 1287-1296.
21. Unger B, Traktman P (2004) Vaccinia virus morphogenesis: a13 phosphoprotein is required for assembly of mature virions. J Virol 78: 8885-8901.
22. Szajner P, Weisberg AS, Lebowitz J, Heuser J, Moss B (2005) External scaffold of spherical immature poxvirus particles is made of protein trimers, forming a honeycomb lattice. J Cell Biol 170: 971-981.
23. Bisht H, Weisberg AS, Szajner P, Moss B (2009) Assembly and disassembly of the capsid-like external scaffold of immature virions during vaccinia virus morphogenesis. J Virol 83: 9140-9150.
24. Hamai C, Cremer PS, Musser SM (2007) Single giant vesicle rupture events reveal multiple mechanisms of glass-supported bilayer formation. Biophys J 92: 1988-1999.
25. Betakova T, Moss B (2000) Disulfide bonds and membrane topology of the vaccinia virus A17L envelope protein. J Virol 74: 2438-2442.
26. Betakova T, Wolffe EJ, Moss B (1999) Membrane topology of the vaccinia virus A17L envelope protein. Virology 261: 347-356.
27. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, Zayas M, Bartenschlager R, Wakita T, Hijikata M, Shimotohno K (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nat Cell Biol 9: 1089-1097.
28. Samsa MM, Mondotte JA, Iglesias NG, Assuncao-Miranda I, Barbosa-Lima G, Da Poian AT, Bozza PT, Gamarnik AV (2009) Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog 5: e1000632.
29. Rodriguez D, Risco C, Rodriguez JR, Carrascosa JL, Esteban M (1996) Inducible expression of the vaccinia virus A17L gene provides a synchronized system to monitor sorting of viral proteins during morphogenesis. J Virol 70: 7641-7653.
30. Szajner P, Jaffe H, Weisberg AS, Moss B (2003) Vaccinia virus G7L protein Interacts with the A30L protein and is required for association of viral membranes with dense viroplasm to form immature virions. J Virol 77: 3418-3429.
31. Szajner P, Weisberg AS, Wolffe EJ, Moss B (2001) Vaccinia virus A30L protein is required for association of viral membranes with dense viroplasm to form immature virions. J Virol 75: 5752-5761.