The near-atomic cryoEM structure of a flexible filamentous plant virus shows homology of its coat protein with nucleoproteins of animal viruses

eLife

Volumn 4, Issue DECEMBER2015, 2015, Pages

  Agirrezabala, Xabier ^a   Méndez López, Eduardo ^b,c   Lasso, Gorka ^d   Sánchez Pina, M Amelia ^b,c   Aranda, Miguel ^b,c   Valle, Mikel ^a  

^a CIC BIOGUNE   (Spain)

^b RESEARCH GROUP ON QUALITY   (Spain)

^c CSIC   (Spain)

^d Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COAT PROTEIN; NUCLEOPROTEIN; PLASMID VECTOR; RIBONUCLEOTIDE; VIRUS RNA; CAPSID PROTEIN; PROTEIN BINDING;

AGROBACTERIUM TUMEFACIENS; ALPHA HELIX; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; GENE TRANSFER; HORIZONTAL GENE TRANSFER; INOCULATION; NICOTIANA BENTHAMIANA; NONHUMAN; PEPINO MOSAIC VIRUS; PHLEBOVIRUS; POTEXVIRUS; PROTEIN RNA BINDING; PROTEIN STRUCTURE; PROTEIN-FRAGMENT COMPLEMENTATION ASSAY; RIFT VALLEY FEVER VIRUS; STRUCTURAL HOMOLOGY; TOSCANA VIRUS; WESTERN BLOTTING; METABOLISM; MOLECULAR MODEL; PROTEIN FOLDING; ULTRASTRUCTURE;

CAPSID PROTEINS; CRYOELECTRON MICROSCOPY; MODELS, MOLECULAR; POTEXVIRUS; PROTEIN BINDING; PROTEIN FOLDING; RNA, VIRAL;

EID: 84986002755     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.11795     Document Type: Article

References (34)

1. AbouHaidar MG, Xu H, Hefferon KL. 1998. Potexvirus isolation and RNA extraction. Methods in Molecular Biology 81:131-143. doi: 10.1385/0-89603-385-6:131
2. Aguilar JM, Hernández-Gallardo MD, Cenis JL, Lacasa A, Aranda MA. 2002. Complete sequence of the pepino mosaic virus RNA genome. Archives of Virology 147:2009-2015. doi: 10.1007/s00705-002-0848-9
3. Chen VB, Arendall WB, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC. 2010. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallographica Section D Biological Crystallography 66:12-21 doi: 10.1107/S0907444909042073. doi: 10.1107/S0907444909042073
4. Chou F-C, Sripakdeevong P, Dibrov SM, Hermann T, Das R. 2013. Correcting pervasive errors in RNA crystallography through enumerative structure prediction. Nature Methods 10:74-76. doi: 10.1038/nmeth.2262
5. Desfosses A, Ciuffa R, Gutsche I, Sachse C. 2014. SPRING - an image processing package for single-particle based helical reconstruction from electron cryomicrographs. Journal of Structural Biology 185:15-26. doi: 10.1016/j.jsb.2013.11.003
6. DiMaio F, Chen C-C, Yu X, Frenz B, Hsu Y-H, Lin N-S, Egelman EH. 2015. The molecular basis for flexibility in the flexible filamentous plant viruses. Nature Structural & Molecular Biology 22:642-644. doi: 10.1038/nsmb.3054
7. Emsley P, Lohkamp B, Scott WG, Cowtan K. 2010. Features and development of coot. Acta Crystallographica Section D Biological Crystallography 66:486-501. doi: 10.1107/S0907444910007493
8. Freiberg AN, Sherman MB, Morais MC, Holbrook MR, Watowich SJ. 2008. Three-dimensional organization of rift valley fever virus revealed by cryoelectron tomography. Journal of Virology 82:10341-10348. doi: 10.1128/JVI.01191-08
9. Hanssen IM, Thomma BPHJ. 2010. Pepino mosaic virus: a successful pathogen that rapidly evolved from emerging to endemic in tomato crops. Molecular Plant Pathology 11:179-189. doi: 10.1111/j.1364-3703.2009.00600.x
10. Holm L, Rosenstrom P. 2010. Dali server: conservation mapping in 3D. Nucleic Acids Research 38:W545-W549. doi: 10.1093/nar/gkq366
11. Huiskonen JT, Overby AK, Weber F, Grunewald K. 2009. Electron cryo-microscopy and single-particle averaging of rift valley fever virus: evidence for GN-GC glycoprotein heterodimers. Journal of Virology 83:3762-3769. doi: 10.1128/JVI.02483-08
12. Jones RAC, Koenig R, Lesemann DE. 1980. Pepino mosaic virus, a new potexvirus from pepino (solanum muricatum). Annals of Applied Biology 94:61-68. doi: 10.1111/j.1744-7348.1980.tb03896.x
13. Kendall A, McDonald M, Bian W, Bowles T, Baumgarten SC, Shi J, Stewart PL, Bullitt E, Gore D, Irving TC, Havens WM, Ghabrial SA, Wall JS, Stubbs G. 2008. Structure of flexible filamentous plant viruses. Journal of Virology 82:9546-9554. doi: 10.1128/JVI.00895-08
14. Kendall A, Bian W, Maris A, Azzo C, Groom J, Williams D, Shi J, Stewart PL, Wall JS, Stubbs G. 2013. A common structure for the potexviruses. Virology 436:173-178. doi: 10.1016/j.virol.2012.11.008
15. Koonin EV, Dolja VV, Krupovic M. 2015. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479-480:2-25. doi: 10.1016/j.virol.2015.02.039
16. Kucukelbir A, Sigworth FJ, Tagare HD. 2014. Quantifying the local resolution of cryo-EM density maps. Nature Methods 11:63-65. doi: 10.1038/nmeth.2727
17. Li L, Li C, Sarkar S, Zhang J, Witham S, Zhang Z, Wang L, Smith N, Petukh M, Alexov E. 2012. DelPhi: a comprehensive suite for DelPhi software and associated resources. BMC Biophysics 5:9. doi: 10.1186/2046-1682-5-9
18. Li X, Mooney P, Zheng S, Booth CR, Braunfeld MB, Gubbens S, Agard DA, Cheng Y. 2013. Electron counting and beam-induced motion correction enable near-atomic-resolution single-particle cryo-EM. Nature Methods 10:584-590. doi: 10.1038/nmeth.2472
19. Lough TJ, Netzler NE, Emerson SJ, Sutherland P, Carr F, Beck DL, Lucas WJ, Forster RLS. 2000. Cell-to-cell movement of potexviruses: evidence for a ribonucleoprotein complex involving the coat protein and first triple gene block protein. Molecular Plant-Microbe Interactions 13:962-974. doi: 10.1094/MPMI.2000.13.9.962
20. Mackerell AD, Feig M, Brooks CL. 2004. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. Journal of Computational Chemistry 25:1400-1415. doi: 10.1002/jcc.20065
21. Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in electron microscopy. Journal of Structural Biology 142:334-347. doi: 10.1016/S1047-8477(03)00069-8
22. Murshudov GN, Vagin AA, Lebedev A, Wilson KS, Dodson EJ. 1999. Efficient anisotropic refinement of macromolecular structures using FFT. Acta Crystallographica Section D Biological Crystallography 55:247-255. doi: 10.1107/S090744499801405X
23. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF chimera - a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25:1605-1612. doi: 10.1002/jcc.20084
24. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, Villa E, Chipot C, Skeel RD, Kalé L, Schulten K. 2005. Scalable molecular dynamics with NAMD. Journal of Computational Chemistry 26:1781-1802. doi: 10.1002/jcc.20289
25. Raymond DD, Piper ME, Gerrard SR, Skiniotis G, Smith JL. 2012. Phleboviruses encapsidate their genomes by sequestering RNA bases. Proceedings of the National Academy of Sciences of the United States of America 109:19208-19213. doi: 10.1073/pnas.1213553109
26. Revers F, García JA. 2015. Molecular biology of potyviruses. Advances in Virus Research 92:101-199. doi: 10.1016/bs.aivir.2014.11.006
27. Sambrook J, Russell DW. 2001. Molecular cloning. A Laboratory Manual.
28. Sempere RN, Gómez P, Truniger V, Aranda MA. 2011. Development of expression vectors based on pepino mosaic virus. Plant Methods 7:6. doi: 10.1186/1746-4811-7-6
29. Tang G, Peng L, Baldwin PR, Mann DS, Jiang W, Rees I, Ludtke SJ. 2007. EMAN2: an extensible image processing suite for electron microscopy. Journal of Structural Biology 157:38-46. doi: 10.1016/j.jsb.2006.05.009
30. Trabuco LG, Villa E, Mitra K, Frank J, Schulten K. 2008. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16:673-683. doi: 10.1016/j.str.2008.03.005
31. Yang S, Wang T, Bohon J, Gagné Marie-Éve Laliberté, Bolduc M, Leclerc D, Li H. 2012. Crystal structure of the coat protein of the flexible filamentous papaya mosaic virus. Journal of Molecular Biology 422:263-273. doi: 10.1016/j.jmb.2012.05.032
32. Zhang Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40. doi: 10.1186/1471-2105-9-40
33. Zhang Y, Skolnick J. 2005. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Research 33:2302-2309. doi: 10.1093/nar/gki524
34. Zhou H, Sun Y, Guo Y, Lou Z. 2013. Structural perspective on the formation of ribonucleoprotein complex in negative-sense single-stranded RNA viruses. Trends in Microbiology 21:475-484. doi: 10.1016/j.tim.2013.07.006