The 24-angstrom structure of respiratory syncytial virus nucleocapsid protein-RNA decameric rings

Journal of Virology

Volumn 81, Issue 17, 2007, Pages 9519-9524

  MacLellan, Kirsty ^a,b   Loney, Colin ^a   Yeo, R Paul ^a,c   Bhella, David ^a  

^a INSTITUTE OF VIROLOGY   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c DURHAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY RNA; MONOMER; VIRUS RNA;

ARTICLE; BACULOVIRUS; COMPLEX FORMATION; CRYSTALLOGRAPHY; ELECTRON MICROSCOPY; GENE EXPRESSION; MONONEGAVIRALES; MORPHOLOGY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN STRUCTURE; RABIES VIRUS; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; STAINING; THREE DIMENSIONAL IMAGING; VESICULAR STOMATITIS VIRUS; VIRUS NUCLEOCAPSID;

IMAGE PROCESSING, COMPUTER-ASSISTED; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, MOLECULAR; NUCLEOCAPSID PROTEINS; RABIES VIRUS; RESPIRATORY SYNCYTIAL VIRUSES; RNA, VIRAL; VESICULAR STOMATITIS-INDIANA VIRUS;

HEXAPODA; MONONEGAVIRALES; RABIES VIRUS; RESPIRATORY SYNCYTIAL VIRUS; RICE STRIPE VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 34548161084     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00526-07     Document Type: Article

References (34)

1. Adrian, M., J. Dubochet, S. D. Fuller, and J. R. Harris. 1998. Cryo-negative staining. Micron 29:145-160.
2. Albertini, A. A., A. K. Wernimont, T. Muziol, R. B. Ravelli, C. R. Clapier, G. Schoehn, W. Weissenhorn, and R. W. Ruigrok. 2006. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313:360-363.
3. Bankamp, B., S. M. Horikami, P. D. Thompson, M. Huber, M. Billeter, and S. A. Moyer. 1996. Domains of the measles virus N protein required for binding to P protein and self-assembly. Virology 216:272-277.
4. Bhella, D., A. Ralph, L. B. Murphy, and R. P. Yeo. 2002. Significant differences in nucleocapsid morphology within the Paramyxoviridae. J. Gen. Virol. 83:1831-1839.
5. Bhella, D., A. Ralph, and R. P. Yeo. 2004. Conformational flexibility in recombinant measles virus nucleocapsids visualised by cryo-negative stain electron microscopy and real-space helical reconstruction. J. Mol. Biol. 340:319-331.
6. Bourhis, J. M., K. Johansson, V. Receveur-Brechot, C. J. Oldfield, K. A. Dunker, B. Canard, and S. Longhi. 2004. The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their physiological partner. Virus Res. 99:157-167.
7. Bourhis, J. M., V. Receveur-Brechot, M. Oglesbee, X. Zhang, M. Buccellato, H. Darbon, B. Canard, S. Finet, and S. Longhi. 2005. The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded. Protein Sci. 14:1975-1992.
8. Collins, P. L., and B. R. Murphy. 2001. Respiratory syncytial virus, p. 1443-1486. In B. N. Fields, D. M. Knipe, and P. M. Howley (ed.), Fields virology, 4th ed., vol. 1. Lippincott Williams & Wilkins, Philadelphia, PA.
9. Conway, J. F., and A. C. Steven. 1999. Methods for reconstructing density maps of "single" particles from cryoelectron micrographs to subnanometer resolution. J. Struct. Biol. 128:106-118.
10. Curran, J., J. B. Marq, and D. Kolakofsky. 1995. An N-terminal domain of the Sendai paramyxovirus P protein acts as a chaperone for the NP protein during the nascent chain assembly step of genome replication. J. Virol. 69:849-855.
11. Egelman, E. H., S. S. Wu, M. Amrein, A. Portner, and G. Murti. 1989. The Sendai virus nucleocapsid exists in at least four different helical states. J. Virol. 63:2233-2243.
12. Fooks, A. R., J. R. Stephenson, A. Warnes, A. B. Dowsett, B. K. Rima, and G. W. Wilkinson. 1993. Measles virus nucleocapsid protein expressed in insect cells assembles into nucleocapsid-like structures. J. Gen. Virol. 74:1439-1444.
13. Garcia-Barreno, B., T. Delgado, and J. A. Melero. 1996. Identification of protein regions involved in the interaction of human respiratory syncytial virus phosphoprotein and nucleoprotein: significance for nucleocapsid assembly and formation of cytoplasmic inclusions. J. Virol. 70:801-808.
14. Green, T. J., X. Zhang, G. W. Wertz, and M. Luo. 2006. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313:357-360.
15. Heymann, J. B. 2001. Bsoft: image and molecular processing in electron microscopy. J. Struct. Biol. 133:156-169.
16. Khattar, S. K., A. S. Yunus, P. L. Collins, and S. K. Samal. 2000. Mutational analysis of the bovine respiratory syncytial virus nucleocapsid protein using a minigenome system: mutations that affect encapsidation, RNA synthesis, and interaction with the phosphoprotein. Virology 270:215-228.
17. Kouznetzoff, A., M. Buckle, and N. Tordo. 1998. Identification of a region of the rabies virus N protein involved in direct binding to the viral RNA. J. Gen. Virol. 79:1005-1013.
18. Laine, D., M. C. Trescol-Biemont, S. Longhi, G. Libeau, J. C. Marie, P. O. Vidalain, O. Azocar, A. Diallo, B. Canard, C. Rabourdin-Combe, and H. Valentin. 2003. Measles virus (MV) nucleoprotein binds to a novel cell surface receptor distinct from FcγRII via its C-terminal domain: role in MV-induced immunosuppression. J. Virol. 77:11332-11346.
19. Li, X., P. Romero, M. Rani, A. K. Dunker, and Z. Obradovic. 1999. Predicting protein disorder for N-, C-, and internal regions. Genome Inform. Ser. Workshop Genome Inform. 10:30-40.
20. Longhi, S., V. Receveur-Brechot, D. Karlin, K. Johansson, H. Darbon, D. Bhella, R. Yeo, S. Finet, and B. Canard. 2003. The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J. Biol. Chem. 278:18638-18648.
21. Ludtke, S. J., P. R. Baldwin, and W. Chiu. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128:82-97.
22. Murray, J., C. Loney, L. B. Murphy, S. Graham, and R. P. Yeo. 2001. Characterization of monoclonal antibodies raised against recombinant respiratory syncytial virus nucleocapsid (N) protein: identification of a region in the carboxy terminus of N involved in the interaction with P protein. Virology 289:252-261.
23. Myers, T. M., S. Smallwood, and S. A. Moyer. 1999. Identification of nucleocapsid protein residues required for Sendai virus nucleocapsid formation and genome replication. J. Gen. Virol. 80:1383-1391.
24. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25:1605-1612.
25. Romero, P., Z. Obradovic, and A. K. Dunker. 2004. Natively disordered proteins: functions and predictions. Appl. Bioinformatics 3:105-113.
26. Romero, P., Z. Obradovic, X. Li, E. C. Garner, C. J. Brown, and A. K. Dunker. 2001. Sequence complexity of disordered protein. Proteins 42:38-48.
27. Schoehn, G., F. Iseni, M. Mavrakis, D. Blondel, and R. W. Ruigrok. 2001. Structure of recombinant rabies virus nucleoprotein-RNA complex and identification of the phosphoprotein binding site. J. Virol. 75:490-498.
28. Schoehn, G., M. Mavrakis, A. Albertini, R. Wade, A. Hoenger, and R. W. Ruigrok. 2004. The 12 Å structure of trypsin-treated measles virus N-RNA. J. Mol. Biol. 339:301-312.
29. Spehner, D., R. Drillien, and P. M. Howley. 1997. The assembly of the measles virus nucleoprotein into nucleocapsid-like particles is modulated by the phosphoprotein. Virology 232:260-268.
30. Spehner, D., A. Kirn, and R. Drillien. 1991. Assembly of nucleocapsidlike structures in animal cells infected with a vaccinia virus recombinant encoding the measles virus nucleoprotein. J. Virol. 65:6296-6300.
31. Tolley, K. P., A. C. Marriott, A. Simpson, D. J. Plows, D. A. Matthews, S. J. Longhurst, J. E. Evans, J. L. Johnson, P. A. Cane, V. B. Randolph, A. J. Easton, and C. R. Pringle. 1996. Identification of mutations contributing to the reduced virulence of a modified strain of respiratory syncytial virus. Vaccine 14:1637-1646.
32. Tran, T.-L., N. Castagne, D. Bhella, P. F. Varela, J. Bernard, S. Chilmonczyk, S. Berkenkamp, V. Benhamo, K. Grznarova, J. Grosclaude, C. Nespoulos, F. A. Rey, and J.-F. Eleouet. 2007. The nine C-terminal amino acids of the respiratory syncytial virus protein P are necessary and sufficient for binding to ribonucleoprotein complexes in which six ribonucleotides are contacted per N protein protomer. J. Gen. Virol. 88:196-206.
33. Wriggers, W., R. A. Milligan, and J. A. McCammon. 1999. Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J. Struct. Biol. 125:185-195.
34. Zhang, X., J. M. Bourhis, S. Longhi, T. Carsillo, M. Buccellato, B. Morin, B. Canard, and M. Oglesbee. 2005. Hsp72 recognizes a P binding motif in the measles virus N protein C terminus. Virology 337:162-174.