Abstract
Our understanding of the viral world changed just after the first structures of icosahedral viral particles were unveiled. The structural similarities between capsid proteins of distant viral groups were not anticipated, and the findings suggested the existence of common ancestors for viruses with different host range, genomic structure and multiplication strategies. This way, diverse viruses with icosahedral particles can now be grouped based on the structural homology between their capsid proteins. In the last years, the presence of conserved folds between viral proteins in non-icosahedral viruses has also emerged. Viral particles with radically different morphologies, ranging from naked and filamentous to enveloped and pleomorphic, have shown structural homology between the nucleoproteins that bind directly to their genomes. This chapter overviews recent findings regarding the similar structure found between nucleoproteins of eukaryotic ssRNA viruses. The structural homology includes the coat proteins from all known families of flexible filamentous plant viruses, a group with monopartite (+)ssRNA genomes. Their coat proteins share a core domain with nucleoproteins of previously unrelated families of enveloped viruses that have segmented (−)ssRNA genomes. This last group consists of mostly animals viruses, including influenza virus.
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References
Abad-Zapatero C, Abdel-Meguid SS, Johnson JE, Leslie AG, Rayment I, Rossmann MG, Suck D, Tsukihara T (1980) Structure of southern bean mosaic virus at 2.8 A resolution. Nature 286(5768):33–39
Abrescia NG, Bamford DH, Grimes JM, Stuart DI (2012) Structure unifies the viral universe. Annu Rev Biochem 81:795–822. https://doi.org/10.1146/annurev-biochem-060910-095130
Adams MJ, Lefkowitz EJ, King AMQ, Harrach B, Harrison RL, Knowles NJ, Kropinski AM, Krupovic M, Kuhn JH, Mushegian AR, Nibert M, Sabanadzovic S, Sanfacon H, Siddell SG, Simmonds P, Varsani A, Zerbini FM, Gorbalenya AE, Davison AJ (2017) Changes to taxonomy and the international code of virus classification and nomenclature ratified by the international committee on taxonomy of viruses (2017). Arch Virol 162:2505. https://doi.org/10.1007/s00705-017-3358-5
Agirrezabala X, Mendez-Lopez E, Lasso G, Sanchez-Pina MA, Aranda M, Valle M (2015) The near-atomic cryoEM structure of a flexible filamentous plant virus shows homology of its coat protein with nucleoproteins of animal viruses. Elife 4:e11795. https://doi.org/10.7554/eLife.11795
Aiewsakun P, Katzourakis A (2015) Endogenous viruses: connecting recent and ancient viral evolution. Virology 479-480:26–37. https://doi.org/10.1016/j.virol.2015.02.011
Ariza A, Tanner SJ, Walter CT, Dent KC, Shepherd DA, Wu W, Matthews SV, Hiscox JA, Green TJ, Luo M, Elliott RM, Fooks AR, Ashcroft AE, Stonehouse NJ, Ranson NA, Barr JN, Edwards TA (2013) Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization. Nucleic Acids Res 41(11):5912–5926. https://doi.org/10.1093/nar/gkt268
Arranz R, Coloma R, Chichon FJ, Conesa JJ, Carrascosa JL, Valpuesta JM, Ortin J, Martin-Benito J (2012) The structure of native influenza virion ribonucleoproteins. Science 338(6114):1634–1637. https://doi.org/10.1126/science.1228172
Ballinger MJ, Bruenn JA, Kotov AA, Taylor DJ (2013) Selectively maintained paleoviruses in Holarctic water fleas reveal an ancient origin for phleboviruses. Virology 446(1–2):276–282. https://doi.org/10.1016/j.virol.2013.07.032
Baltimore D (1971) Expression of animal virus genomes. Bacteriol Rev 35(3):235–241
Buchmann JP, Holmes EC (2015) Cell walls and the convergent evolution of the viral envelope. Microbiol Mol Biol Rev 79(4):403–418. https://doi.org/10.1128/MMBR.00017-15
Chenavas S, Estrozi LF, Slama-Schwok A, Delmas B, Di Primo C, Baudin F, Li X, Crepin T, Ruigrok RW (2013) Monomeric nucleoprotein of influenza A virus. PLoS Pathog 9(3):e1003275. https://doi.org/10.1371/journal.ppat.1003275
Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logo generator. Genome Res 14(6):1188–1190. https://doi.org/10.1101/gr.849004
DiMaio F, Chen CC, Yu X, Frenz B, Hsu YH, Lin NS, Egelman EH (2015) The molecular basis for flexibility in the flexible filamentous plant viruses. Nat Struct Mol Biol 22(8):642–644. https://doi.org/10.1038/nsmb.3054
Dolja VV, Boyko VP, Agranovsky AA, Koonin EV (1991) Phylogeny of capsid proteins of rod-shaped and filamentous RNA plant viruses: two families with distinct patterns of sequence and probably structure conservation. Virology 184(1):79–86
Dong H, Li P, Bottcher B, Elliott RM, Dong C (2013) Crystal structure of Schmallenberg orthobunyavirus nucleoprotein-RNA complex reveals a novel RNA sequestration mechanism. RNA 19(8):1129–1136. https://doi.org/10.1261/rna.039057.113
Freiberg AN, Sherman MB, Morais MC, Holbrook MR, Watowich SJ (2008) Three-dimensional organization of Rift Valley fever virus revealed by cryoelectron tomography. J Virol 82(21):10341–10348. https://doi.org/10.1128/JVI.01191-08
Geoghegan JL, Duchene S, Holmes EC (2017) Comparative analysis estimates the relative frequencies of co-divergence and cross-species transmission within viral families. PLoS Pathog 13(2):e1006215. https://doi.org/10.1371/journal.ppat.1006215
Gough J (2005) Convergent evolution of domain architectures (is rare). Bioinformatics 21(8):1464–1471. https://doi.org/10.1093/bioinformatics/bti204
Harrison SC, Olson AJ, Schutt CE, Winkler FK, Bricogne G (1978) Tomato bushy stunt virus at 2.9 A resolution. Nature 276(5686):368–373
Hastie KM, Kimberlin CR, Zandonatti MA, MacRae IJ, Saphire EO (2011) Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3′ to 5′ exonuclease activity essential for immune suppression. Proc Natl Acad Sci U S A 108(6):2396–2401. https://doi.org/10.1073/pnas.1016404108
Hong JS, Ju HJ (2017) The plant cellular systems for plant virus movement. Plant Pathol J 33(3):213–228. https://doi.org/10.5423/PPJ.RW.09.2016.0198
Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P (1987) Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc Natl Acad Sci U S A 84(22):8140–8144
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. J Virol 83(8):3762–3769. https://doi.org/10.1128/JVI.02483-08
Illergard K, Ardell DH, Elofsson A (2009) Structure is three to ten times more conserved than sequence--a study of structural response in protein cores. Proteins 77(3):499–508. https://doi.org/10.1002/prot.22458
Katzourakis A, Gifford RJ (2010) Endogenous viral elements in animal genomes. PLoS Genet 6(11):e1001191. https://doi.org/10.1371/journal.pgen.1001191
Kawabata T (2003) MATRAS: A program for protein 3D structure comparison. Nucleic Acids Res 31(13):3367–3369
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. J Virol 82(19):9546–9554. https://doi.org/10.1128/JVI.00895-08
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(1):173–178. https://doi.org/10.1016/j.virol.2012.11.008
Komoda K, Narita M, Yamashita K, Tanaka I, Yao M (n.d.) Tomato spotted wilt tospovirus nucleocapsid protein-ssRNA complex. pdb code 5IP2
Koonin EV (1991) The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J Gen Virol 72(Pt 9):2197–2206. https://doi.org/10.1099/0022-1317-72-9-2197
Koonin EV, Dolja VV (1993) Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit Rev Biochem Mol Biol 28(5):375–430. https://doi.org/10.3109/10409239309078440
Koonin EV, Dolja VV, Krupovic M (2015) Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479-480C:2–25. https://doi.org/10.1016/j.virol.2015.02.039
Kormelink R, Garcia ML, Goodin M, Sasaya T, Haenni AL (2011) Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res 162(1–2):184–202. https://doi.org/10.1016/j.virusres.2011.09.028
Li CX, Shi M, Tian JH, Lin XD, Kang YJ, Chen LJ, Qin XC, Xu J, Holmes EC, Zhang YZ (2015) Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 4:e05378. https://doi.org/10.7554/eLife.05378
Lyles DS (2013) Assembly and budding of negative-strand RNA viruses. Adv Virus Res 85:57–90. https://doi.org/10.1016/B978-0-12-408116-1.00003-3
Nagy PD, Pogany J (2011) The dependence of viral RNA replication on co-opted host factors. Nat Rev Microbiol 10(2):137–149. https://doi.org/10.1038/nrmicro2692
Namba K, Stubbs G (1986) Structure of tobacco mosaic virus at 3.6 A resolution: implications for assembly. Science 231(4744):1401–1406
Nasir A, Caetano-Anolles G (2017) Identification of capsid/coat related protein folds and their utility for virus classification. Front Microbiol 8:380. https://doi.org/10.3389/fmicb.2017.00380
Niu F, Shaw N, Wang YE, Jiao L, Ding W, Li X, Zhu P, Upur H, Ouyang S, Cheng G, Liu ZJ (2013) Structure of the Leanyer orthobunyavirus nucleoprotein-RNA complex reveals unique architecture for RNA encapsidation. Proc Natl Acad Sci U S A 110(22):9054–9059. https://doi.org/10.1073/pnas.1300035110
Qi X, Lan S, Wang W, Schelde LM, Dong H, Wallat GD, Ly H, Liang Y, Dong C (2010) Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468(7325):779–783. https://doi.org/10.1038/nature09605
Raju R, Kolakofsky D (1989) The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired. J Virol 63(1):122–128
Raymond DD, Piper ME, Gerrard SR, Skiniotis G, Smith JL (2012) Phleboviruses encapsidate their genomes by sequestering RNA bases. Proc Natl Acad Sci U S A 109(47):19208–19213. https://doi.org/10.1073/pnas.1213553109
Reguera J, Malet H, Weber F, Cusack S (2013) Structural basis for encapsidation of genomic RNA by La Crosse Orthobunyavirus nucleoprotein. Proc Natl Acad Sci U S A 110(18):7246–7251. https://doi.org/10.1073/pnas.1302298110
Reguera J, Cusack S, Kolakofsky D (2014) Segmented negative strand RNA virus nucleoprotein structure. Curr Opin Virol 5:7–15. https://doi.org/10.1016/j.coviro.2014.01.003
Rossmann MG, Abad-Zapatero C, Murthy MR, Liljas L, Jones TA, Strandberg B (1983) Structural comparisons of some small spherical plant viruses. J Mol Biol 165(4):711–736
Ruigrok RW, Crepin T, Kolakofsky D (2011) Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr Opin Microbiol 14(4):504–510. https://doi.org/10.1016/j.mib.2011.07.011
Sherman MB, Freiberg AN, Holbrook MR, Watowich SJ (2009) Single-particle cryo-electron microscopy of Rift Valley fever virus. Virology 387(1):11–15. https://doi.org/10.1016/j.virol.2009.02.038
Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ (2016) Redefining the invertebrate RNA virosphere. Nature 540:539. https://doi.org/10.1038/nature20167
Tanne E, Sela I (2005) Occurrence of a DNA sequence of a non-retro RNA virus in a host plant genome and its expression: evidence for recombination between viral and host RNAs. Virology 332(2):614–622. https://doi.org/10.1016/j.virol.2004.11.007
Theze J, Leclercq S, Moumen B, Cordaux R, Gilbert C (2014) Remarkable diversity of endogenous viruses in a crustacean genome. Genome Biol Evol 6(8):2129–2140. https://doi.org/10.1093/gbe/evu163
Yang S, Wang T, Bohon J, Gagne ME, Bolduc M, Leclerc D, Li H (2012) Crystal structure of the coat protein of the flexible filamentous papaya mosaic virus. J Mol Biol 422(2):263–273. https://doi.org/10.1016/j.jmb.2012.05.032
Ye Q, Krug RM, Tao YJ (2006) The mechanism by which influenza a virus nucleoprotein forms oligomers and binds RNA. Nature 444(7122):1078–1082. https://doi.org/10.1038/nature05379
Zamora M, Mendez-Lopez E, Agirrezabala X, Cuesta R, Lavin JL, Sanchez-Pina MA, Aranda M, Valle M (2017) Potyvirus virion structure shows conserved protein fold and RNA binding site in ssRNA viruses. Sci Adv 3(9):eaao2182. https://doi.org/10.1126/sciadv.aao2182
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 Microbiol 21(9):475–484. https://doi.org/10.1016/j.tim.2013.07.006
Acknowledgments
This work was supported by grant BFU2015-66326-P from the Spanish Ministry of Economy and Competitiveness (MINECO). Also the Severo Ochoa Excellence Accreditation (SEV-2016-0644) by MINECO is acknowledged.
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Valle, M. (2018). Structural Homology Between Nucleoproteins of ssRNA Viruses. In: Harris, J., Bhella, D. (eds) Virus Protein and Nucleoprotein Complexes. Subcellular Biochemistry, vol 88. Springer, Singapore. https://doi.org/10.1007/978-981-10-8456-0_6
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