Structure of Ljungan virus provides insight into genome packaging of this picornavirus

Nature Communications

Volumn 6, Issue , 2015, Pages

  Zhu, Ling ^a,b   Wang, Xiangxi ^c   Ren, Jingshan ^a   Porta, Claudine ^a,b   Wenham, Hannah ^b   Ekström, Jens Ola ^d   Panjwani, Anusha ^b   Knowles, Nick J ^b   Kotecha, Abhay ^a   Siebert, C Alistair ^a   Lindberg, A Michael ^d   Fry, Elizabeth E ^a   Rao, Zihe ^c,e   Tuthill, Tobias J ^b   Stuart, David I ^f  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^c INSTITUTE OF BIOPHYSICS   (China)

^d LINNAEUS UNIVERSITY   (Sweden)

^e Tsinghua University ^*  (China)

^f DIAMOND LIGHT SOURCE LTD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; PROTEIN VP1; PROTEIN VP3; VIRUS RNA; COMPLEMENTARY DNA;

DIABETES; ELECTRON MICROSCOPY; GENOME; PROTEIN; RNA; VIRUS;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYOELECTRON MICROSCOPY; DIABETES MELLITUS; DNA PACKAGING; HEPATITIS A VIRUS; LJUNGAN VIRUS; NONHUMAN; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN RNA BINDING; VIRUS CHARACTERIZATION; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS MYOCARDITIS; ANIMAL; CELL LINE; CHEMISTRY; CONFORMATION; PARECHOVIRUS; PHYSIOLOGY;

ANIMALIA; LJUNGAN VIRUS; PARECHOVIRUS; PICORNAVIRIDAE;

ANIMALS; CELL LINE; CRYOELECTRON MICROSCOPY; DNA, COMPLEMENTARY; NUCLEIC ACID CONFORMATION; PARECHOVIRUS; RNA, VIRAL;

EID: 84943631507     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9316     Document Type: Article

References (59)

1. Rao, A. L. Genome packaging by spherical plant RNA viruses. Annu. Rev. Phytopathol. 44, 61-87 (2006).
2. Ni, P. & Cheng Kao, C. Non-encapsidation activities of the capsid proteins of positive-strand RNA viruses. Virology 446, 123-132 (2013).
3. Casjens, S. R. The DNA-packaging nanomotor of tailed bacteriophages. Nat. Rev. Microbiol. 9, 647-657 (2011).
4. Ford, R. J. et al. Sequence-specific, RNA-protein interactions overcome electrostatic barriers preventing assembly of satellite tobacco necrosis virus coat protein. J. Mol. Biol. 425, 1050-1064 (2013).
5. Whitton, J. L., Cornell, C. T. & Feuer, R. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3, 765-776 (2005).
6. Jiang, P., Liu, Y., Ma, H. C., Paul, A. V. & Wimmer, E. Picornavirus morphogenesis. Microbiol. Mol. Biol. Rev. 78, 418-437 (2014).
7. Liu, Y. et al. Direct interaction between two viral proteins, the nonstructural protein 2C and the capsid protein VP3, is required for enterovirus morphogenesis. PLoS Pathog. 6, e1001066 (2010).
8. 0-end sequence of the genome of Aichi virus, a picornavirus, contains an element critical for viral RNA encapsidation. J. Virol. 77, 3542-3548 (2003).
9. Niklasson, B. Current views on Ljungan virus and its relationship to human diabetes. J. Med. Virol. 83, 1673 (2011).
10. Tolf, C. et al. Molecular characterization of a novel Ljungan virus (Parechovirus; Picornaviridae) reveals a fourth genotype and indicates ancestral recombination. J. Gen. Virol. 90, 843-853 (2009).
11. Lindberg, A. M. & Johansson, S. Phylogenetic analysis of Ljungan virus and A-2 plaque virus, new members of the Picornaviridae. Virus Res. 85, 61-70 (2002).
12. Johansson, E. S. et al. Cell culture propagation and biochemical analysis of the Ljungan virus prototype strain. Biochem. Biophys. Res. Commun. 317, 1023-1029 (2004).
13. Johansson, S., Niklasson, B., Maizel, J., Gorbalenya, A. E. & Lindberg, A. M. Molecular analysis of three Ljungan virus isolates reveals a new, close-to-root lineage of the Picornaviridae with a cluster of two unrelated 2A proteins. J. Virol. 76, 8920-8930 (2002).
14. Stanway, G. & Hyypia, T. Parechoviruses. J. Virol. 73, 5249-5254 (1999).
15. Seitsonen, J. et al. Interaction of alpha Vbeta3 and alpha Vbeta6 integrins with human parechovirus 1. J. Virol. 84, 8509-8519 (2010).
16. Hughes, P. J. & Stanway, G. The 2A proteins of three diverse picornaviruses are related to each other and to the H-rev107 family of proteins involved in the control of cell proliferation. J. Gen. Virol. 81, 201-207 (2000).
17. Panjwani, A. et al. Capsid protein VP4 of human rhinovirus induces membrane permeability by the formation of a size-selective multimeric pore. PLoS Pathog. 10, e1004294 (2014).
18. Chow, M. et al. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327, 482-486 (1987).
19. Pulli, T., Koivunen, E. & Hyypia, T. Cell-surface interactions of echovirus 22. J. Biol. Chem. 272, 21176-21180 (1997).
20. Triantafilou, K., Triantafilou, M., Takada, Y. & Fernandez, N. Human parechovirus 1 utilizes integrins alphavbeta3 and alphavbeta1 as receptors. J. Virol. 74, 5856-5862 (2000).
21. Wang, X. et al. Hepatitis A virus and the origins of picornaviruses. Nature 517, 85-88 (2015).
22. Ekstrom, J.-O. Doctoral Dissertation (University of Kalmar, 2007).
23. Levy, H. C., Bostina, M., Filman, D. J. & Hogle, J. M. Catching a virus in the act of RNA release: a novel poliovirus uncoating intermediate characterized by cryo-electron microscopy. J. Virol. 84, 4426-4441 (2010).
24. Ekstrom, J. O., Tolf, C., Edman, K. A. & Lindberg, A. M. Physicochemical properties of the Ljungan virus prototype virion in different environments: inactivated by heat but resistant to acidic pH, detergents and non-physiological environments such as Virkon-containing solutions. Microbiol. Immunol. 51, 841-850 (2007).
25. 0-end, infectious cDNA clones and host cell response to viral infections. Virus Res. 130, 129-139 (2007).
26. Walter, T. S. et al. A plate-based high-throughput assay for virus stability and vaccine formulation. J. Virol. Methods 185, 166-170 (2012).
27. Tang, G. et al. EMAN2: an extensible image processing suite for electron microscopy. J. Struct. Biol. 157, 38-46 (2007).
28. Scheres, S. H. W. RELION: Implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519-530 (2012).
29. Guo, F. & Jiang, W. Single particle cryo-electron microscopy and 3-D reconstruction of viruses. Methods Mol. Biol. 1117, 401-443 (2014).
30. Henderson, R. et al. Outcome of the first electron microscopy validation task force meeting. Structure 20, 205-214 (2012).
31. Scheres, S. H. W. & Chen, S. X. Prevention of overfitting in cryo-EM structure determination. Nat. Methods 9, 853-854 (2012).
32. Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D Biol. Crystallogr. 68, 352-367 (2012).
33. Rossmann, M. G. et al. Structure of a human common cold virus and functional relationship to other picornaviruses. Nature 317, 145-153 (1985).
34. Hogle, J. M., Chow, M. & Filman, D. J. Three-dimensional structure of poliovirus at 2.9 A resolution. Science 229, 1358-1365 (1985).
35. Wang, X. et al. A sensor-adaptor mechanism for enterovirus uncoating from structures of EV71. Nat. Struct. Mol. Biol. 19, 424-429 (2012).
36. Tate, J. et al. The crystal structure of cricket paralysis virus: the first view of a new virus family. Nat. Struct. Biol. 6, 765-774 (1999).
37. Dang, M. et al. Molecular mechanism of SCARB2-mediated attachment and uncoating of EV71. Protein Cell 5, 692-703 (2014).
38. Tolf, C. et al. Characterization of polyclonal antibodies against the capsid proteins of Ljungan virus. J. Virol. Methods 150, 34-40 (2008).
39. Squires, G. et al. Structure of the Triatoma virus capsid. Acta Crystallogr. D Biol. Crystallogr. 69, 1026-1037 (2013).
40. Tolf, C., Gullberg, M., Ekstrom, J. O., Jonsson, N. & Michael Lindberg, A. Identification of amino acid residues of Ljungan virus VP0 and VP1 associated with cytolytic replication in cultured cells. Arch. Virol. 154, 1271-1284 (2009).
41. Larson, S. B., Lucas, R. W., Greenwood, A. & McPherson, A. The RNA of turnip yellow mosaic virus exhibits icosahedral order. Virology 334, 245-254 (2005).
42. Seal, L. A. & Jamison, R. M. Evidence for secondary structure within the virion RNA of echovirus 22. J. Virol. 50, 641-644 (1984).
43. Hogle, J. M., Maeda, A. & Harrison, S. C. Structure and assembly of turnip crinkle virus. I. X-ray crystallographic structure analysis at 3.2A resolution. J. Mol. Biol. 191, 625-638 (1986).
44. Sorger, P. K., Stockley, P. G. & Harrison, S. C. Structure and assembly of turnip crinkle virus. II. Mechanism of reassembly in vitro. J. Mol. Biol. 191, 639-658 (1986).
45. Larson, S. B. et al. Double-helical RNA in satellite tobacco mosaic virus. Nature 361, 179-182 (1993).
46. Tang, L. et al. The structure of pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat. Struct. Biol. 8, 77-83 (2001).
47. Fisher, A. J. & Johnson, J. E. Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature 361, 176-179 (1993).
48. Toropova, K., Basnak, G., Twarock, R., Stockley, P. G. & Ranson, N. A. The three-dimensional structure of genomic RNA in bacteriophage MS2: implications for assembly. J. Mol. Biol. 375, 824-836 (2008).
49. Sangita, V. et al. T=1 capsid structures of Sesbania mosaic virus coat protein mutants: determinants of T=3 and T=1 capsid assembly. J. Mol. Biol. 342, 987-999 (2004).
50. Dong, X. F., Natarajan, P., Tihova, M., Johnson, J. E. & Schneemann, A. Particle polymorphism caused by deletion of a peptide molecular switch in a quasiequivalent icosahedral virus. J. Virol. 72, 6024-6033 (1998).
51. Stockley, P. G. et al. Packaging signals in single-stranded RNA viruses: nature's alternative to a purely electrostatic assembly mechanism. J. Biol. Phys. 39, 277-287 (2013).
52. Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36-51 (2005).
53. Li, X. et al. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nat. Methods 10, 584-590 (2013).
54. Kivioja, T., Ravantti, J., Verkhovsky, A., Ukkonen, E. & Bamford, D. Local average intensity-based method for identifying spherical particles in electron micrographs. J. Struct. Biol. 131, 126-134 (2000).
55. Ludtke, S. J., Baldwin, P. R. & Chiu, W. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128, 82-97 (1999).
56. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
57. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
58. Chen, V. B. et al. Mol Probity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
59. Yamashita, T. et al. Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. J. Virol. 72, 8408-8412 (1998).