Architecture of respiratory syncytial virus revealed by electron cryotomography

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 27, 2013, Pages 11133-11138

  Liljeroos, Lassi ^a   Krzyzaniak, Magdalena Anna ^b   Helenius, Ari ^b   Butcher, Sarah Jane ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b ETH ZURICH   (Switzerland)

Author keywords

Cryo ET; Paramyxovirus; Virus structure

Indexed keywords

MATRIX PROTEIN; NUCLEOCAPSID PROTEIN; VIRUS GLYCOPROTEIN;

ARTICLE; CELL CULTURE; CONTROLLED STUDY; ELECTRON CRYOTOMOGRAPHY; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; TOMOGRAPHY; VIRION; VIRUS MORPHOLOGY; VIRUS NUCLEOCAPSID; VIRUS PARTICLE;

CRYO-ET; PARAMYXOVIRUS; VIRUS STRUCTURE;

CELL LINE; CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; HUMANS; PROTEIN CONFORMATION; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; RIBONUCLEOPROTEINS; VIRAL FUSION PROTEINS;

HUMAN RESPIRATORY SYNCYTIAL VIRUS; PARAMYXOVIRIDAE; PARAMYXOVIRINAE; PNEUMOVIRINAE; RESPIRATORY SYNCYTIAL VIRUS;

EID: 84879707555     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1309070110     Document Type: Article

References (36)

1. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE (2005) Respiratory syncytial virus infection in elderly and high-risk adults. N Engl J Med 352(17):1749-1759. (Pubitemid 40570923)
2. Nair H, et al. (2010) Global burden of acute lower respiratory infections due to respiratory syncytial virus in young children: A systematic review and meta-analysis. Lancet 375(9725):1545-1555.
3. Group TI-RS (1998) Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. The IMpact-RSV Study Group. Pediatrics 102(3 Pt 1):531-537.
4. Battisti AJ, et al. (2012) Structure and assembly of a paramyxovirus matrix protein. Proc Natl Acad Sci USA 109(35):13996-14000.
5. Liljeroos L, Huiskonen JT, Ora A, Susi P, Butcher SJ (2011) Electron cryotomography of measles virus reveals how matrix protein coats the ribonucleocapsid within intact virions. Proc Natl Acad Sci USA 108(44):18085-18090.
6. Loney C, Mottet-Osman G, Roux L, Bhella D (2009) Paramyxovirus ultrastructure and genome packaging: Cryo-electron tomography of Sendai virus. J Virol 83(16):8191-8197.
7. Liljeroos L, Butcher SJ (2013) Matrix proteins as centralized organizers of negativesense RNA virions. Front Biosci 18:696-715.
8. Collins PL, Wertz GW (1985) The envelope-associated 22K protein of human respiratory syncytial virus: Nucleotide sequence of the mRNA and a related polytranscript. J Virol 54(1):65-71. (Pubitemid 15136846)
9. Huang YT, Collins PL, Wertz GW (1985) Characterization of the 10 proteins of human respiratory syncytial virus: Identification of a fourth envelope-associated protein. Virus Res 2(2):157-173. (Pubitemid 15148065)
10. Li D, et al. (2008) Association of respiratory syncytial virus M protein with viral nucleocapsids is mediated by the M2-1 protein. J Virol 82(17):8863-8870.
11. Fearns R, Collins PL (1999) Role of the M2-1 transcription antitermination protein of respiratory syncytial virus in sequential transcription. J Virol 73(7):5852-5864. (Pubitemid 29274872)
12. Radhakrishnan A, et al. (2010) Protein analysis of purified respiratory syncytial virus particles reveals an important role for heat shock protein 90 in virus particle assembly. Mol Cell Proteomics 9(9):1829-1848.
13. Tawar RG, et al. (2009) Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326(5957):1279-1283.
14. McLellan JS, Yang Y, Graham BS, Kwong PD (2011) Structure of respiratory syncytial virus fusion glycoprotein in the postfusion conformation reveals preservation of neutralizing epitopes. J Virol 85(15):7788-7796.
15. Bächi T, Howe C (1973) Morphogenesis and ultrastructure of respiratory syncytial virus. J Virol 12(5):1173-1180.
16. Mitra R, Baviskar P, Duncan-Decocq RR, Patel D, Oomens AG (2012) The human respiratory syncytial virus matrix protein is required for maturation of viral filaments. J Virol 86(8):4432-4443.
17. McPhee HK, et al. (2011) Influence of lipids on the interfacial disposition of respiratory syncytical virus matrix protein. Langmuir 27(1):304-311.
18. Bharat TA, et al. (2011) Cryo-electron tomography of Marburg virus particles and their morphogenesis within infected cells. PLoS Biol 9(11):e1001196.
19. Calder LJ, Wasilewski S, Berriman JA, Rosenthal PB (2010) Structural organization of a filamentous influenza A virus. Proc Natl Acad Sci USA 107(23):10685-10690.
20. Pietilä MK, et al. (2012) Virion architecture unifies globally distributed pleolipoviruses infecting halophilic archaea. J Virol 86(9):5067-5079.
21. Welch BD, et al. (2012) Structure of the cleavage-activated prefusion form of the parainfluenza virus 5 fusion protein. Proc Natl Acad Sci USA 109(41):16672-16677.
22. Krzyzaniak MA, Zumstein MT, Gerez JA, Picotti P, Helenius A (2013) Host cell entry of respiratory syncytial virus involves macropinocytosis followed by proteolytic activation of the f protein. PLoS Pathog 9(4):e1003309.
23. Schoehn G, et al. (2004) The 12 A structure of trypsin-treated measles virus N-RNA. J Mol Biol 339(2):301-312. (Pubitemid 38596950)
24. Kuzyk A, et al. (2012) DNA-based self-assembly of chiral plasmonic nanostructures with tailored optical response. Nature 483(7389):311-314.
25. Techaarpornkul S, Barretto N, Peeples ME (2001) Functional analysis of recombinant respiratory syncytial virus deletion mutants lacking the small hydrophobic and/or attachment glycoprotein gene. J Virol 75(15):6825-6834. (Pubitemid 32641568)
26. Zimmer G, Budz L, Herrler G (2001) Proteolytic activation of respiratory syncytial virus fusion protein. Cleavage at two furin consensus sequences. J Biol Chem 276(34):31642-31650.
27. Ludwig K, et al. (2008) Electron cryomicroscopy reveals different F1+F2 protein States in intact parainfluenza virions. J Virol 82(7):3775-3781. (Pubitemid 351429952)
28. Shaikh FY, et al. (2012) A critical phenylalanine residue in the respiratory syncytial virus fusion protein cytoplasmic tail mediates assembly of internal viral proteins into viral filaments and particles. MBio 3(1):e00270-11.
29. Fleming EH, Kolokoltsov AA, Davey RA, Nichols JE, Roberts NJ, Jr. (2006) Respiratory syncytial virus F envelope protein associates with lipid rafts without a requirement for other virus proteins. J Virol 80(24):12160-12170. (Pubitemid 44904367)
30. Saarikangas J, et al. (2009) Molecular mechanisms of membrane deformation by I-BAR domain proteins. Curr Biol 19(2):95-107.
31. Ghildyal R, et al. (2005) Interaction between the respiratory syncytial virus G glycoprotein cytoplasmic domain and the matrix protein. J Gen Virol 86(Pt 7):1879-1884. (Pubitemid 40916370)
32. Heumann JM, Hoenger A, Mastronarde DN (2011) Clustering and variance maps for cryo-electron tomography using wedge-masked differences. J Struct Biol 175(3):288-299.
33. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of threedimensional image data using IMOD. J Struct Biol 116(1):71-76. (Pubitemid 26093126)
34. Nicastro D, et al. (2006) The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313(5789):944-948. (Pubitemid 44267380)
35. Heymann JB, Belnap DM (2007) Bsoft: Image processing and molecular modeling for electron microscopy. J Struct Biol 157(1):3-18. (Pubitemid 44880789)
36. Bakker SE, et al. (2013) The Respiratory Syncytial Virus nucleoprotein-RNA complex forms a left-handed helical nucleocapsid. J Gen Virol, 10.1099/vir.0.053025-0.