The picobirnavirus crystal structure provides functional insights into virion assembly and cell entry

EMBO Journal

Volumn 28, Issue 11, 2009, Pages 1655-1665

  Duquerroy, Stéphane ^a,b   Da Costa, Bruno ^c   Henry, Céline ^d   Vigouroux, Armelle ^a,f   Libersou, Sonia ^e   Lepault, Jean ^e   Navaza, Jorge ^e,g   Delmas, Bernard ^c   Rey, Félix A ^a,h  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ PARIS SACLAY   (France)

^c INRA Institut National de la Recherche Agronomique   (France)

^d CEMAGREF   (France)

^e INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^f LABORATOIRE D ENZYMOLOGIE ET BIOCHIMIE STRUCTURALES   (France)

^g INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^h CNRS   (France)

Author keywords

Double stranded RNA viruses; Gastroenteritis viruses; Structural virology; Virus crystallography

Indexed keywords

COAT PROTEIN; NUCLEIC ACID; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CELL INVASION; CRYSTAL STRUCTURE; IN VITRO STUDY; NONHUMAN; PICOBIRNAVIRUS; PRIORITY JOURNAL; VIRION; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS PARTICLE;

AMINO ACID SEQUENCE; ANIMALS; CAPSID; CAPSID PROTEINS; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PICOBIRNAVIRUS; PROTEIN PROCESSING, POST-TRANSLATIONAL; VIRAL PROTEINS; VIRION; VIRUS INTERNALIZATION;

ANIMALIA; DSRNA VIRUSES; EUKARYOTA; MIRIDAE; PICOBIRNAVIRUS; RNA VIRUSES;

EID: 67349273766     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.109     Document Type: Article

References (59)

1. Agrawal DK, Johnson JE (1992) Sequence and analysis of the capsid protein of Nudaurelia capensis omega virus, an insect virus with T=4 icosahedral symmetry. Virology 190: 806-814
2. An W (2007) Histone acetylation and methylation: combinatorial players for transcriptional regulation. Subcell Biochem 41: 351-369
3. Bamford DH, Grimes JM, Stuart DI (2005) What does structure tell us about virus evolution? Curr Opin Struct Biol 15: 655-663
4. Bhattacharya R, Sahoo GC, Nayak MK, Rajendran K, Dutta P, Mitra U, Bhattacharya MK, Naik TN, Bhattacharya SK, Krishnana T
5. (2007) Detection of Genogroup I and II human picobirnaviruses showing small genomic RNA profile causing acute watery diarrhoea among children in Kolkata, India. Infect Genet Evol 7: 229-238
6. Brunger AT, Adams PD, Clore GM, Delano Wl, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice lM, Simonson T, Warren Gl (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr 54: 905-921
7. Caccio SM (2005) Molecular epidemiology of human cryptospor-idiosis. Parassitologia 47: 185-192
8. Carson M (1997) Ribbons. Methods Enzymol 277: 493-505
9. Caspar Dl, Klug A (1962) Physical principles in the construction of regular viruses. Cold Spring Harb Symp Quant Biol 27: 1-24
10. CCP4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr 50: 760-763
11. Chandra R (1997) Picobirnavirus, a novel group of undescribed viruses of mammals and birds: a minireview. Acta Virol 41: 59-62
12. Chevalier C, Galloux M, Pous J, Henry C, Denis J, Da Costa B, Navaza J, lepault J, Delmas B (2005) Structural peptides of a nonenveloped virus are involved in assembly and membrane translocation. J Virol 79: 12253-12263
13. Conway JF, Steven AC (1999) Methods for reconstructing density maps of 'single' particles from cryoelectron micrographs to sub-nanometer resolution. J Struct Biol 128: 106-118
14. Coulibaly F, Chevalier C, Gutsche I, Pous J, Navaza J, Bressanelli S, Delmas B, Rey FA (2005) The birnavirus crystal structure reveals structural relationships among icosahedral viruses. Cell 120: 761-772
15. Estes M, Kapikian A (2007) Rotaviruses. In Fields Virology, Knipe DM, Howley PM (eds), Vol. 2, 5 edn, pp 1917-1974. Philadelphia: lippincott Williams and Wilkins
16. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr 62: 72-82
17. Finkbeiner SR, Allred AF, Tarr PI, Klein EJ, Kirkwood CD, Wang D (2008) Metagenomic analysis of human diarrhea: viral detection and discovery. PloS Pathog 4: e1000011
18. Fujimura T, Esteban R, Wickner RB (1986) In vitro l-A double-stranded RNA synthesis in virus-like particles from Saccharomyces cerevisiae. Proc Natl Acad Sci USA 83: 4433-4437
19. Gallimore CI, Green J, Casemore DP, Brown DW (1995) Detection of a picobirnavirus associated with Cryptosporidium positive stools from humans. Arch Virol 140: 1275-1278
20. Galloux M, libersou S, Morellet N, Bouaziz S, Da Costa B, Ouldali M, lepault J, Delmas B (2007) Infectious bursal disease virus, a non-enveloped virus, possesses a capsid-associated peptide that deforms and perforates biological membranes. J Biol Chem 282: 20774-20784
21. Ghabrial S, Buck K, Hillman B, Milne R (2005) Partitiviridae. london: Elsevier/Academic Press
22. Giordano MO, Masachessi G, Martinez lC, Barril PA, Ferreyra lJ, Isa MB, Nates SV (2008) Two instances of large genome profile picobirnavirus occurrence in Argentinian infants with diarrhea over a 26-year period (1977-2002). J Infect 56: 371-375
23. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308
24. Green J, Gallimore CI, Clewley JP, Brown DW (1999) Genomic characterisation of the large segment of a rabbit picobirnavirus and comparison with the atypical picobirnavirus of Cryptosporidium parvum. Arch Virol 144: 2457-2465
25. Grimes JM, Burroughs JN, Gouet P, Diprose JM, Malby R, Zientara S, Mertens PP, Stuart DI (1998) The atomic structure of the bluetongue virus core. Nature 395: 470-478
26. Grohmann GS, Glass RI, Pereira HG, Monroe SS, Hightower AW, Weber R, Bryan RT (1993) Enteric viruses and diarrhea in HIV-infected patients. Enteric Opportunistic Infections Working Group. N Engl J Med 329: 14-20
27. Hosur MV, Schmidt T, Tucker RC, Johnson JE, Gallagher TM, Selling BH, Rueckert RR (1987) Structure of an insect virus at 3.0 A resolution. Proteins 2: 167-176
28. Huiskonen JT, de Haas F, Bubeck D, Bamford DH, Fuller SD, Butcher SJ (2006) Structure of the bacteriophage phi6 nucleo-capsid suggests a mechanism for sequential RNA packaging. Structure 14: 1039-1048
29. Ivanovic T, Agosto MA, Zhang l, Chandran K, Harrison SC, Nibert Ml (2008) Peptides released from reovirus outer capsid form membrane pores that recruit virus particles. EMBO J 27: 1289-1298
30. Jones TA (1992) A, yaap, asap, *? A set of averaging programs. In Molecular Replacement, EJ Dodson, S Gover and W Wolf (eds) pp 91-105. Warrington, England: SERC Daresbury laboratory
31. Jones TA, Zou JY, Cowan SW, Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr 47 (Pt 2): 110-119
32. Khramtsov NV, Upton SJ (2000) Association of RNA polymerase complexes of the parasitic protozoan Cryptosporidium parvum with virus-like particles: heterogeneous system. J Virol 74: 5788-5795
33. Krol MA, Olson NH, Tate J, Johnson JE, Baker TS, Ahlquist P (1999) RNA-controlled polymorphism in the in vivo assembly of 180-subunit and 120-subunit virions from a single capsid protein. Proc Natl Acad Sci USA 96: 13650-13655
34. Kuhn RJ, Zhang W, Rossmann MG, Pletnev SV, Corver J, lenches E, Jones CT, Mukhopadhyay S, Chipman PR, Strauss EG, Baker TS, Strauss JH (2002) Structure of dengue virus: implications for flavivirus organization, maturation, and fusion. Cell 108: 717-725
35. laskowski RA, Moss DS, Thornton JM (1993) Main-chain bond lengths and bond angles in protein structures. J Mol Biol 231: 1049-1067
36. lawton JA, Estes MK, Prasad BV (2000) Mechanism of genome transcription in segmented dsRNA viruses. Adv Virus Res 55: 185-229
37. leslie AG (2006) The integration of macromolecular diffraction data. Acta Crystallogr 62: 48-57
38. ludert JE, Hidalgo M, Gil F, liprandi F (1991) Identification in porcine faeces of a novel virus with a bisegmented double stranded RNA genome. Arch Virol 117: 97-107
39. ludtke SJ, Baldwin PR, Chiu W (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97
40. Masachessi G, Martinez lC, Giordano MO, Barril PA, Isa BM, Ferreyra l, Villareal D, Carello M, Asis C, Nates SV (2007) Picobirnavirus (PBV) natural hosts in captivity and virus excretion pattern in infected animals. Arch Virol 152: 989-998
41. McCabe PM, Pfeiffer P, Van Alfen NK (1999) The influence of dsRNA viruses on the biology of plant pathogenic fungi. Trends Microbiol 7: 377-381
42. Naitow H, Tang J, Canady M, Wickner RB, Johnson JE (2002) l-A virus at 3.4 A resolution reveals particle architecture and mRNA decapping mechanism. Nat Struct Biol 9: 725-728
43. Nakagawa A, Miyazaki N, Taka J, Naitow H, Ogawa A, Fujimoto Z, Mizuno H, Higashi T, Watanabe Y, Omura T, Cheng RH, Tsukihara T (2003) The atomic structure of rice dwarf virus reveals the self-assembly mechanism of component proteins. Structure 11: 1227-1238
44. Nandi P, Charpilienne A, Cohen J (1992) Interaction of rotavirus particles with liposomes. J Virol 66: 3363-3367
45. Navaza J (1994) AMoRe: an automated package for molecular replacement. Acta Crystallogr 50: 157-163
46. Ochoa WF, Havens WM, Sinkovits RS, Nibert Ml, Ghabrial SA, Baker TS (2008) Partitivirus structure reveals a 120-subunit, helix-rich capsid with distinctive surface arches formed by qua-sisymmetric coat-protein dimers. Structure 16: 776-786
47. Odegard Al, Chandran K, Zhang X, Parker JS, Baker TS, Nibert Ml (2004) Putative autocleavage of outer capsid protein μ1, allowing release of myristoylated peptide μ1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78: 8732-8745
48. Pesavento JB, Crawford SE, Estes MK, Prasad BV (2006) Rotavirus proteins: structure and assembly. Curr Top Microbiol Immunol 309: 189-219
49. Prasad BV, Hardy ME, Dokland T, Bella J, Rossmann MG, Estes MK (1999) X-ray crystallographic structure of the Norwalk virus capsid. Science (New York, NY) 286: 287-290
50. Qiao X, Sun Y, Qiao J, Mindich l (2008) Temporal control of message stability in the life cycle of ds. J Virol 83: 633-639
51. Reddy V, Schneemann A, Johnson JE (2003) Nodavirus endopeptidase. Handbook of Proteolytic Enzymes, 2nd edn 1-5
52. Reinisch KM, Nibert Ml, Harrison SC (2000) Structure of the reovirus core at 3.6 A resolution. Nature 404: 960-967
53. Roy P (2007) Orbiviruses. In Fields Virology, Knipe DM, Howley PM (eds), Vol. 1, 5 edn, 54, pp 1975-1998. Philadelphia: lippincott Williams and Wilkins
54. Schiff lA, Nibert M, Tyler K (2007) Orthoreoviruses and their replication. In Fields Virology, Knipe DM, Howley PM (eds), Vol. 1, 5 edn, pp 1853-1916. Philadelphia: lippincott Williams and Wilkins
55. van Heel M, Gowen B, Matadeen R, Orlova EV, Finn R, Pape T, Cohen D, Stark H, Schmidt R, Schatz M, Patwardhan A (2000) Single-particle electron cryo-microscopy: towards atomic resolution. Q Rev Biophys 33: 307-369
56. Wakuda M, Pongsuwanna Y, Taniguchi K (2005) Complete nucleotide sequences of two RNA segments of human picobirnavirus. J Virol Methods 126: 165-169
57. Wang Al, Wang CC (1991) Viruses of the protozoa. Annu Rev Microbiol 45: 251-263
58. Yu X, Jin l, Zhou ZH (2008) 3.88 A structure of cytoplasmic polyhedrosis virus by cryo-electron microscopy. Nature 453: 415-419
59. Zlotnick A, Aldrich R, Johnson JM, Ceres P, Young MJ (2000) Mechanism of capsid assembly for an icosahedral plant virus. Virology 277: 450-456