Chapter 16 : Origin and Evolution of the Proteome

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This chapter briefly reviews our current understanding of the origin and evolutionary dynamic of the picornavirus proteome. There is a large body of literature on protein evolution recorded during picornavirus outbreaks and on picornavirus passaging in cells and animals in the absence or presence of a selective factor, e.g., a drug. Before discussing picornavirus proteins, it is useful to recall that they were originally named without regard to evolutionary considerations, which is a common framework in contemporary studies. Two processes, mutation and homologous recombination, have been shown to be involved in generating these changes in the most conserved proteins. Special cases of nonhomologous recombination are gene duplication and loss in progeny of a single parent. In the case of gene duplication, a genetic locus is repeatedly copied, while gene loss is a result of skipping a genetic locus from copying; both are considered to be aberrations of template-mediated replication in picornaviruses. The origin of the N-terminal amphipathic helix of 2C is another case open to different evolutionary interpretations. Gene loss along with repeated introduction of a protein variety may be invoked for explaining phylogenetic discontinuity of the presence of the protein variety in picornaviruses.

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16
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Image of Figure 1.
Figure 1.

Phylogenetic tree of the family. A phylogeny of 28 picornaviruses representing species diversity is shown. The maximum-likelihood tree is based on a multiple alignment of RdRps and was compiled using the PhyML program under the WAG amino acid substitution matrix and rate heterogeneity among sites (gamma distribution with four categories) ( ). A Bayesian reconstruction utilizing the BEAST software resulted in an identical topology. Numbers at branching points indicate bootstrap support values from 1,000 replicates. The scale of evolution in average number of amino acid substitutions per position is shown by the bar. The tree was rooted according to a separate phylogenetic analysis using nidovirus RdRps as an outgroup (data not shown). Picornavirus genera are indicated to the right of the phylogeny. For picornavirus species the presence of L and 2A proteins in polyproteins is depicted using rectangles of different shades. The widths of the rectangles are scaled proportionally to the size of L and 2A proteins. Homologous proteins are coded as described for Fig. 2 , below. The viruses included are: HAV, avian encephalomyelitis virus (AvEMV), HPeV, LjV, DuHV AP, SealPV, porcine teschovirus (PTeV), FMDV SAT 2, ERAV, Theiler’s-like virus of rats (TheiloV), encephalomyocarditis virus (EMCV), Seneca Valley virus (SVV), EERBV1, Aichi virus (AiV), bovine kobuvirus (BKoV), avian sapelovirus (DuPV), porcine sapelovirus (PEV-A), simian picornavirus 1 (SiPV), bovine enterovirus (BEV), simian enterovirus A (SiEV), HRV 30 (HRV-A), HRV-C, HRV-B, HEV-C, HEV-D, HEV 71 (HEV-A), HEV-B, and porcine enterovirus B (PEV-B).

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16
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Image of Figure 2.
Figure 2.

Polyprotein layout characteristics of genera or species of the family. Genomic organizations for 17 picornaviruses of 13 genera are shown, describing all variants of the polyprotein domain architecture found for the by 2009. The organizations were aligned at the 2B-2C border and are ranked in order of descending genome size. Mature proteins are depicted as different shaded rectangles (with the exception of 2A3 and 2A4 [NPGP] in cardioviruses, which are released as a fused product from the polyprotein), and UTRs are shown as solid horizontal lines. The identity of proteins can be determined using the legend at the bottom. Borders of proteins were identified using protein annotations for the most-well-characterized viruses, which were then applied to a family-wide polyprotein alignment, generated by using Muscle and curated manually with support of the Viralis software platform (Gorbalenya, unpublished). For the sake of this comparison, a region between a leader protein (where it is present) or the initiator codon (leaderless viruses) and 1B (VP2) was considered as 1A (VP4) in all viruses, although it is not produced in some viruses. For a discussion of the complexities of VP4 evolution, see the text. For TMEV two reading frames are shown (from top to bottom: 0 and + 1 with respect to the start of the most upstream open reading frame), as it encodes an additional protein (L*) in the + 1 frame.

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16
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Image of Figure 3.
Figure 3.

Polyprotein conservation of the family. A plot of the conservation along the polyprotein alignment of 13 picornaviruses representing genus diversity is shown. The normalized similarity measure was compiled using the Bio3d package in R under the Blosum62 substitution matrix and a sliding window size of 10 amino acid positions ( ). The mean similarity of the polyprotein is indicated by the dashed horizontal line. On top, the positions of single protein alignments are highlighted by black rectangles and names with the same nomenclature as used for Fig. 2 . For L and 2A proteins the positions of alignments for the different protein families (see also Table 1 ) are shown by grey vertical lines. The grey inserts represent separate conservation plots for the different L and 2A proteins that are expressed by at least two virus species. The following conserved sequence motifs are indicated at peaks of the similarity measure: NPGP cleavage motif in 2A4; 2C helicase motifs A, B, and C; 3B conserved Tyr (Y) nucleotidylated during priming in RNA synthesis; 3C protease catalytic His (H) and Cys (C), noncatalytic Asp/Glu (D/E) residues, and a substrate-binding motif (SB); 3D polymerase motifs A, B, C, E, F, and G.

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16
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Image of Figure 4.
Figure 4.

Protein conservation in the family. For each of the different picornavirus proteins the mean normalized similarity (see Fig. 3 and text) is plotted against the length deviation, where the latter was compiled as the standard deviation divided by the mean length. For the main figure (in black), lengths of protein regions L, 1A, 1B, 1C, 1D, 2A, 2B, 2C, 3A, 3B, 3C, and 3D were used (allowing lengths of 0 in cases of absent proteins), whereas lengths in the inset plot (grey) are based on mature proteins (absent proteins were not counted). The same data set used for Fig. 3 was used here.

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16
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Image of Figure 5.
Figure 5.

Conservation and diversity of genetic plans of the order Genomic organizations for seven viruses are shown (similar to Fig. 2 ) and represent polyprotein layouts of families of the Different shapes and shades were used to highlight protein families found in all or several virus families. Borders of proteins were identified using the GenBank annotation where available. Otherwise, positions were estimated utilizing homology searches (HMMer) against profiles of the picornavirus proteins ( ). The viruses included are Strawberry latent ringspot virus (Sadwavirus), Maize chlorotic dwarf virus (Sequivirus), Patchouli mild mosaic virus (Comovirus), Deformed wing virus (Iflavirus), Kashmir bee virus (Dicistrovirus), Heterosigma akashiwo RNA virus (Marnavirus), and encephalomyocarditis virus (Picornavirus). For Sadwavirus and Comovirus the two RNA segments are shown.

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16
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1. Adams, P.,, E. Kandiah,, G. Effantin,, A. C. Steven, and, E. Ehrenfeld. 2009. Poliovirus 2C protein forms homo-oligomeric structures required for ATPase activity. J. Biol. Chem. 284: 2201222021.
2. Agol, V. I. 2002. Picornavirus genetics: an overview, p. 269–284. In B. Semler and, E. Wimmer (ed.), Molecular Biology of Picornaviruses. American Society for Microbiology, Washington, DC.
3. Agol, V. I. 2002. Picornavirus genome: an overview, p. 127–148. In B. Semler and, E. Wimmer (ed.), Molecular Biology of Picornaviruses. American Society for Microbiology, Washington, DC.
4. Agol, V. I.,, A. V. Paul, and, E. Wimmer. 1999. Paradoxes of the replication of picornaviral genomes. Virus Res. 62: 129147.
5. Allaire, M.,, M. M. Chernaia,, B. A. Malcolm, and, M. N. G. James. 1994. Picornaviral 3C cysteine proteinases have a fold similar to chymotrypsin-like serine proteinases. Nature 369: 7276.
6. Aminev, A. G.,, S. P. Amineva, and, A. C. Palmenberg. 2003. Encephalomyocarditis virus (EMCV) proteins 2A and 3BCD localize to nuclei and inhibit cellular mRNA transcription but not rRNA transcription. Virus Res. 95: 5973.
7. Anantharaman, V., and, L. Aravind. 2003. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol. 4: R11.
8. Andino, R.,, G. E. Rieckhof, and, D. Baltimore. 1990. A functional ribonucleoprotein complex forms around the 5′ end of poliovirus RNA. Cell 63: 369380.
9. Andino, R.,, D. Silvera,, S. D. Suggett,, P. L. Achacoso,, C. J. Miller,, D. Baltimore, and, M. B. Feinberg. 1994. Engineering poliovirus as a vaccine vector for the expression of diverse antigens. Science 265: 14481451.
10. Argos, P.,, G. Kamer,, M. J. H. Nicklin, and, E. Wimmer. 1984. Similarity in gene organization and homology between proteins of animal picornaviruses and a plant comovirus suggest common ancestry of these virus families. Nucleic Acids Res. 12: 72517267.
11. Baranowski, E.,, C. M. Ruiz-Jarabo,, N. Pariente,, N. Verdaguer, and, E. Domingo. 2003. Evolution of cell recognition by viruses: a source of biological novelty with medical implications. Adv. Virus Res. 62: 19111.
12. Bazan, J. F., and, R. J. Fletterick. 1988. Viral cysteine proteases are homologous to the trypsin-like family of serine proteases: structural and functional implications. Proc. Natl. Acad. Sci. USA 85: 78727876.
13. Belshaw, R.,, O. G. Pybus, and, A. Rambaut. 2007. The evolution of genome compression and genomic novelty in RNA viruses. Genome Res. 17: 14961504.
14. Bennett, S. P.,, L. Lu, and, D. L. Brutlag. 2003. 3MATRIX and 3MOTIF: a protein structure visualization system for conserved sequence motifs. Nucleic Acids Res. 31: 33283332.
15. Blinov, V. M.,, A. P. Donchenko, and, A. E. Gorbalenia. 1985. Internal homology in the primary structure of poliovirus polyprotein: the possible existence of 2 virus-specific proteinases. Dokl. Akad. Nauk. SSSR 281: 984987. (In Russian.)
16. Blinov, V. M.,, A. E. Gorbalenia, and, A. P. Donchenko. 1984. The structural similarity between poliovirus cysteine protein-ase P3-7C and cellular serine proteinase of trypsin. Dokl. Akad. Nauk. SSSR 279: 502505. (In Russian.)
17. Boonyakiat, Y.,, P. J. Hughes,, F. Ghazi, and, G. Stanway. 2001. Arginine-glycine-aspartic acid motif is critical for human parechovirus 1 entry. J. Virol. 75: 1000010004.
18. Brown, B.,, M. S. Oberste,, K. Maher, and, M. A. Pallansch. 2003. Complete genomic sequencing shows that polioviruses and members of human enterovirus species C are closely related in the noncapsid coding region. J. Virol. 77: 89738984.
19. Bruenn, J. A. 2003. A structural and primary sequence comparison of the viral RNA-dependent RNA polymerases. Nucleic Acids Res. 31: 18211829.
20. Carrillo, C.,, E. R. Tulman,, G. Delhon,, Z. Lu,, A. Carreno,, A. Vagnozzi,, G. F. Kutish, and, D. L. Rock. 2005. Comparative genomics of foot-and-mouth disease virus. J. Virol. 79: 64876504.
21. Charini, W. A.,, S. Todd,, G. A. Gutman, and, B. L. Semler. 1994. Transduction of a human RNA sequence by poliovirus. J. Virol. 68: 65476552.
22. Chen, H. H.,, W. P. Kong, and, R. P. Roos. 1995. The leader peptide of Theiler’s murine encephalomyelitis virus is a zinc-binding protein. J. Virol. 69: 80768078.
23. Chen, H. H.,, W. P. Kong,, L. Zhang,, P. L. Ward, and, R. P. Roos. 1995. A picornaviral protein synthesized out of frame with the polyprotein plays a key role in a virus-induced immune-mediated demyelinating disease. Nat. Med. 1: 927931.
24. Chow, M.,, J. F. E. Newman,, D. Filman,, J. M. Hogle,, D. J. Rowlands, and, F. Brown. 1987. Myristoylation of picornavirus capsid protein Vp4 and its structural significance. Nature 327: 482486.
25. Cohen, J. I.,, B. Rosenblum,, J. R. Ticehurst,, R. J. Daemer,, S. M. Feinstone, and, R. H. Purcell. 1987. Complete nucleotide sequence of an attenuated hepatitis A virus: comparison with wild-type virus. Proc. Natl. Acad. Sci. USA 84: 24972501.
26. Coutard, B.,, A. E. Gorbalenya,, E. J. Snijder,, A. M. Leontovich,, A. Poupon,, X. de Lamballerie,, R. Charrel,, E. A. Gould,, S. Gunther,, H. Norder,, B. Klempa,, H. Bourhy,, J. Rohayem,, E. L’hermite,, P. Nordlund,, D. I. Stuart,, R. J. Owens,, J. M. Grimes,, P. A. Tucker,, M. Bolognesi,, A. Mattevi,, M. Coll,, T. A. Jones,, J. Aqvist,, T. Unge,, R. Hilgenfeld,, G. Bricogne,, J. Neyts,, P. La Colla,, G. Puerstinger,, J. P. Gonzalez,, E. Leroy,, C. Cambillau,, J. L. Romette, and, B. Canard. 2008. The VIZIER project: preparedness against pathogenic RNA viruses. Antiviral Res. 78: 3746.
27. Cuff, A. L.,, I. Sillitoe,, T. Lewis,, O. C. Redfern,, R. Garratt,, J. Thornton, and, C. A. Orengo. 2009. The CATH classification revisited: architectures reviewed and new ways to characterize structural divergence in superfamilies. Nucleic Acids Res. 37: D310D314.
28. de Jong, A. S.,, E. Wessels,, H. B. P. M. Dijkman,, J. M. D. Galama,, W. J. G. Melchers,, P. H. G. M. Willems, and, F. J. M. van Kuppeveld. 2003. Determinants for membrane association and permeabilization of the coxsackievirus 2B protein and the identification of the Golgi complex as the target organelle. J. Biol. Chem. 278: 10121021.
29. Ding, C. Y., and, D. B. Zhang. 2007. Molecular analysis of duck hepatitis virus type 1. Virology 361: 917.
30. Doherty, M.,, D. Todd,, N. McFerran, and, E. M. Hoey. 1999. Sequence analysis of a porcine enterovirus serotype 1 isolate: relationships with other picornaviruses. J. Gen. Virol. 80: 19291941.
31. Domingo, E. 2007. Virus evolution, p. 389–421. In D. M. Knipe,, P. M. Howley,, D. E. Griffin,, R. A. Lamb,, M. A. Martin,, B. Roizman, and, S. E. Straus (ed.), Fields Virology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, PA.
32. Domingo, E.,, E. Baranowski,, C. Escarmis,, F. Sobrino, and, J. J. Holland. 2002. Error frequencies of picornavirus RNA polymerases: evolutionary implications for virus populations, p. 285–298. In B. Semler and, E. Wimmer (ed.), Molecular Biology of Picornaviruses. American Society for Microbiology, Washington, DC.
33. Donnelly, M. L.,, D. Gani,, M. Flint,, S. Monaghan, and, M. D. Ryan. 1997. The cleavage activities of aphthovirus and cardio-virus 2A proteins. J. Gen. Virol. 78: 1321.
34. Doronina, V. A.,, C. Wu,, P. de Felipe,, M. S. Sachs,, M. D. Ryan, and, J. D. Brown. 2008. Site-specific release of nascent chains from ribosomes at a sense codon. Mol. Cell. Biol. 28: 42274239.
35. Eddy, S. R. 1998. Profile hidden Markov models. Bioinformatics 14: 755763.
36. Erzberger, J. P., and, J. M. Berger. 2006. Evolutionary relationships and structural mechanisms of AAA plus proteins. Annu. Rev. Biophys. Biomol. Struct. 35: 93114.
37. Falk, M. M.,, F. Sobrino, and, E. Beck. 1992. Vpg gene amplification correlates with infective particle formation in foot-and-mouth disease virus. J. Virol. 66: 22512260.
38. Ferrer-Orta, C.,, A. Arias,, C. Escarmis, and, N. Verdaguer. 2006. A comparison of viral RNA-dependent RNA polymerases. Curr. Opin. Struct. Biol. 16: 2734.
39. Ferrer-Orta, C., and, N. Verdaguer. 2009. RNA virus polymerases, p. 383–401. In C. E. Cameron,, M. Gotte, and, K. D. Raney (ed.), Viral Genome Replication. Springer, New York, NY.
40. Franssen, H.,, J. Leunissen,, R. Goldbach,, G. Lomonossoff, and, D. Zimmern. 1984. Homologous sequences in non-structural proteins from cowpea mosaic virus and picornaviruses. EMBO J. 3: 855861.
41. Ghosh, R. C.,, B. V. Ball,, M. M. Willcocks, and, M. J. Carter. 1999. The nucleotide sequence of sacbrood virus of the honey bee: an insect picorna-like virus. J. Gen. Virol. 80: 15411549.
42. Goldbach, R. 1987. Genome similarities between plant and animal RNA viruses. Microbiol. Sci. 4: 197201.
43. Goodfellow, I. G.,, D. Kerrigan, and, D. J. Evans. 2003. Structure and function analysis of the poliovirus cis-acting replication element (CRE). RNA 9: 124137.
44. Gorbalenya, A. E. 1992. Host-related sequences in RNA virus genomes. Semin. Virol. 3: 359371.
45. Gorbalenya, A. E. 1995. Origin of RNA viral genomes: approaching the problem by comparative sequence analysis, p. 49–66. In A. J. Gibbs,, C. H. Calisher, and, F. Garcia-Arenal (ed.), Molecular Basis of Virus Evolution. Cambridge University Press, Cambridge, United Kingdom.
46. Gorbalenya, A. E. 2000. Papain-like fold, acyl-enzyme intermediate and a complex evolution history are predicted for 2A proteins of several picornaviruses from bioinformatics anaylsis of their distant relationships. J13. Abstr. XIth Meet. Eur. Study Group Mol. Biol. Picornaviruses, 2000. Baia delle Zagare, 23 May 2000.
47. Gorbalenya, A. E.,, K. M. Chumakov, and, V. I. Agol. 1978. RNA-binding properties of nonstructural polypeptide G of encephalomyocarditis virus. Virology 88: 183185.
48. Gorbalenya, A. E.,, A. P. Donchenko, and, V. M. Blinov. 1986. A possible common origin of poliovirus proteins with different functions. Mol. Gen. Mikrobiol. Virusol. 1986: 3641. (In Russian.)
49. Gorbalenya, A. E.,, A. P. Donchenko,, V. M. Blinov, and, E. V. Koonin. 1989. Cysteine proteases of positive strand RNA viruses and chymotrypsin-like serine proteases: a distinct protein superfamily with a common structural fold. FEBS Lett. 243: 103114.
50. Gorbalenya, A. E., and, E. V. Koonin. 1993. Comparative analysis of the amino acid sequences of the key enzymes of the replication and expression of positive-strand RNA viruses. Validity of the approach and functional and evolutionary implications. Sov. Sci. Rev. D Physicochem. Biol. 11: 184.
51. Gorbalenya, A. E.,, E. V. Koonin, and, M. M. C. Lai. 1991. Putative papain-related thiol proteases of positive-strand RNA viruses. FEBS Lett. 288: 201205.
52. Gorbalenya, A. E.,, E. V. Koonin, and, Y. A. Wolf. 1990. A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett. 262: 145148.
53. Gorbalenya, A. E.,, F. M. Pringle,, J. L. Zeddam,, B. T. Luke,, C. E. Cameron,, J. Kalmakoff,, T. N. Hanzlik,, K. H. Gordon, and, V. K. Ward. 2002. The palm subdomain-based active site is internally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J. Mol. Biol. 324: 4762.
54. Gorbalenya, A. E., and, E. J. Snijder. 1996. Viral cysteine proteinases. Perspect. Drug Discov. Design 6: 6486.
55. Gorbalenya, A. E.,, Y. V. Svitkin,, Y. A. Kazachkov, and, V. I. Agol. 1979. Encephalomyocarditis virus-specific polypeptide p22 is involved in the processing of the viral precursor polypeptides. FEBS Lett. 108: 15.
56. Grant, B. J.,, A. P. C. Rodrigues,, K. M. Elsawy,, J. A. McCammon, and, L. S. D. Caves. 2006. Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics 22: 26952696.
57. Green, K. Y.,, T. Ando,, M. S. Balayan,, T. Berke,, I. N. Clarke,, M. K. Estes,, D. O. Matson,, S. Nakata,, J. D. Neill,, M. J. Studdert, and, H. J. Thiel. 2000. Taxonomy of the caliciviruses. J. Infect. Dis. 181: S322S330.
58. Gromeier, M.,, E. Wimmer, and, A. E. Gorbalenya. 1999. Genetics, pathogenesis and evolution of picornaviruses, p. 287–343. In E. Domingo,, R. G. Webster, and, J. J. Holland (ed.), Origin and Evolution of Viruses. Academic Press, San Diego, CA.
59. Guarne, A.,, J. Tormo,, R. Kirchweger,, D. Pfistermueller,, I. Fita, and, T. Skern. 1998. Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition. EMBO J. 17: 74697479.
60. Guindon, S., and, O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52: 696704.
61. Hales, L. M.,, N. J. Knowles,, P. S. Reddy,, L. Xu,, C. Hay, and, P. L. Hallenbeck. 2008. Complete genome sequence analysis of Seneca Valley virus-001, a novel oncolytic picornavirus. J. Gen. Virol. 89: 12651275.
62. Hansen, J. L.,, A. M. Long, and, S. C. Schultz. 1997. Structure of the RNA-dependent RNA polymerase of poliovirus. Structure 5: 11091122.
63. Hellen, C. U. T., and, S. de Breyne. 2007. A distinct group of hepacivirus/pestivirus-like internal ribosomal entry sites in members of diverse Picornavirus genera: evidence for modular exchange of functional noncoding RNA elements by recombination. J. Virol. 81: 58505863.
64. Hendry, E.,, H. Hatanaka,, E. Fry,, M. Smyth,, J. Tate,, G. Stanway,, J. Santti,, M. Maaronen,, T. Hyypia, and, D. Stuart. 1999. The crystal structure of coxsackievirus A9: new insights into the un-coating mechanisms of enteroviruses. Structure 7: 15271538.
65. Hogle, J. M.,, M. Chow, and, D. J. Filman. 1985. 3-Dimensional structure of poliovirus at 2.9 Å resolution. Science 229: 13581365.
66. Hughes, A. L. 2004. Phylogeny of the Picornaviridae and differential evolutionary divergence of picornavirus proteins. Infect. Genet. Evol. 4: 143152.
67. Hughes, P. J., and, G. Stanway. 2000. 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: 201207.
68. Hulo, N.,, A. Bairoch,, V. Bulliard,, L. Cerutti,, B. A. Cuche,, E. de Castro,, C. Lachaize,, P. S. Langendijk-Genevaux, and, C. J. Sigrist. 2008. The 20 years of PROSITE. Nucleic Acids Res. 36: D245D249.
69. Isawa, H.,, S. Asano,, K. Sahara,, T. Iizuka, and, H. Bando. 1998. Analysis of genetic information of an insect picorna-like virus, infectious flacherie virus of silkworm: evidence for evolutionary relationships among insect, mammalian and plant picorna(-like) viruses. Arch. Virol. 143: 127143.
70. Jiang, P.,, J. A. J. Faase,, H. Toyoda,, A. Paul,, E. Wimmer, and, A. E. Gorbalenya. 2007. Evidence for emergence of diverse polioviruses from C-cluster coxsackie A viruses and implications for global poliovirus eradication. Proc. Natl. Acad. Sci. USA 104: 94579462.
71. Johansson, S.,, B. Niklasson,, J. Maizel,, A. E. Gorbalenya, and, A. M. Lindberg. 2002. 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: 89208930.
72. Kamer, G., and, P. Argos. 1984. Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial-viruses. Nucleic Acids Res. 12: 72697282.
73. Kapoor, A.,, J. Victoria,, P. Simmonds,, E. Slikas,, T. Chieochansin,, A. Naeem,, S. Shaukat,, S. Sharif,, M. M. Alam,, M. Angez,, C. L. Wang,, R. W. Shafer,, S. Zaidi, and, E. Delwart. 2008. A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc. Natl. Acad. Sci. USA 105: 2048220487.
74. Kapoor, A.,, J. Victoria,, P. Simmonds,, C. Wang,, R. W. Shafer,, R. Nims,, O. Nielsen, and, E. Delwart. 2008. A highly divergent picornavirus in a marine mammal. J. Virol. 82: 311320.
75. Keese, P. K., and, A. Gibbs. 1992. Origins of genes: Big Bang or continuous creation. Proc. Natl. Acad. Sci. USA 89: 94899493.
76. Kim, M. C.,, Y. K. Kwon,, S. J. Joh,, A. M. Lindberg,, J. H. Kwon,, J. H. Kim, and, S. J. Kim. 2006. Molecular analysis of duck hepatitis virus type 1 reveals a novel lineage close to the genus Parechovirus in the family Picornaviridae. J. Gen. Virol. 87: 33073316.
77. King, A. M.,, Q. F. Brown,, P. Christian,, T. Hovi,, T. Hyypiä,, N. J. Knowles,, S. M. Lemon,, P. D. Minor,, A. C. Palmenberg,, T. Skern, and, G. Stanway. 2000. Picornaviridae, p. 657–678. In M. H. V. van Regenmortel,, C. M. Fauquet,, D. H. L. Bishop,, E. B. Carstens,, M. K. Estes,, S. M. Lemon,, J. Maniloff,, M. A. Mayo,, D. J. McGeoch,, C. R. Pringle, and, R. B. Wickner (ed.), Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, New York, NY.
78. Kong, W. P.,, G. D. Ghadge, and, R. P. Roos. 1994. Involvement of cardiovirus leader in host cell-restricted virus expression. Proc. Natl. Acad. Sci. USA 91: 17961800.
79. Kong, W. P., and, R. P. Roos. 1991. Alternative translation initiation site in the DA strain of Theiler’s murine encephalomyelitis virus. J. Virol. 65: 33953399.
80. Koonin, E. V. 1991. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 72: 21972206.
81. Koonin, E. V., and, A. E. Gorbalenya. 1992. An insect picorna-virus may have genome organization similar to that of caliciviruses. FEBS Lett. 297: 8186.
82. Koonin, E. V.,, Y. I. Wolf,, K. Nagasaki, and, V. V. Dolja. 2008. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol. 6: 925939.
83. Krumbholz, A.,, M. Dauber,, A. Henke,, E. Birch-Hirschfeld,, N. J. Knowles,, A. Stelzner, and, R. Zell. 2002. Sequencing of porcine enterovirus groups II and III reveals unique features of both virus groups. J. Virol. 76: 58135821.
84. Lang, A. S.,, A. I. Culley, and, C. A. Suttle. 2004. Genome sequence and characterization of a virus (HaRNAV) related to picorna-like viruses that infects the marine toxic bloom-forming alga Heterosigma akashiwo. Virology 320: 206217.
85. Lanzi, G.,, J. R. de Miranda,, M. B. Boniotti,, C. E. Cameron,, A. Lavazza,, L. Capucci,, S. M. Camazine, and, C. Rossi. 2006. Molecular and biological characterization of deformed wing virus of honeybees ( Apis mellifera L.). J. Virol. 80: 49985009.
86. Le Gall, O.,, P. Christian,, C. M. Fauquet,, A. M. Q. King,, N. J. Knowles,, N. Nakashima,, G. Stanway, and, A. E. Gorbalenya. 2008. Picornavirales, a proposed order of positive-sense single-stranded RNA viruses with a pseudo-T=3 virion architecture. Arch. Virol. 153: 715727.
87. Li, J. P., and, D. Baltimore. 1988. Isolation of poliovirus 2C mutants defective in viral RNA synthesis. J. Virol. 62: 40164021.
88. Li, J. P., and, D. Baltimore. 1990. An intragenic revertant of a poliovirus-2C mutant has an uncoating defect. J. Virol. 64: 11021107.
89. Liljas, L.,, J. Tate,, T. Lin,, P. Christian, and, J. E. Johnson. 2002. Evolutionary and taxonomic implications of conserved structural motifs between picornaviruses and insect picorna-like viruses. Arch. Virol. 147: 5984.
90. Luke, G. A.,, P. de Felipe,, A. Lukashev,, S. E. Kallioinen,, E. A. Bruno, and, M. D. Ryan. 2008. Occurrence, function and evolutionary origins of ‘2A-like’ sequences in virus genomes. J. Gen. Virol. 89: 10361042.
91. Marc, D.,, G. Drugeon,, A. L. Haenni,, M. Girard, and, S. Vanderwerf. 1989. Role of myristoylation of poliovirus capsid protein Vp4 as determined by site-directed mutagenesis of its N-terminal sequence. EMBO J. 8: 26612668.
92. Martin-Belmonte, F.,, J. A. Lopez-Guerrero,, L. Carrasco, and, M. A. Alonso. 2000. The amino-terminal nine amino acid sequence of poliovirus capsid VP4 protein is sufficient to confer N-myristoylation and targeting to detergent-insoluble membranes. Biochemistry 39: 10831090.
93. Marvil, P.,, N. J. Knowles,, A. P. Mockett,, P. Britton,, T. D. Brown, and, D. Cavanagh. 1999. Avian encephalomyelitis virus is a picornavirus and is most closely related to hepatitis A virus. J. Gen. Virol. 80: 653662.
94. Mason, P. W.,, E. Rieder, and, B. Baxt. 1994. RGD sequence of foot-and-mouth-disease virus is essential for infecting cells via the natural receptor but can be bypassed by an antibody-dependent enhancement pathway. Proc. Natl. Acad. Sci. USA 91: 19321936.
95. Mitra, T.,, S. V. Sosnovtsev, and, K. Y. Green. 2004. Mutagenesis of tyrosine 24 in the VPg protein is lethal for feline calicivirus. J. Virol. 78: 49314935.
96. Morace, G.,, Y. Kusov,, G. Dzagurov,, F. Beneduce, and, V. Gauss-Muller. 2008. The unique role of domain 2A of the hepatitis A virus precursor polypeptide P1-2A in viral morphogenesis. BMB Rep. 41: 678683.
97. Nakashima, N., and, N. Shibuya. 2006. Multiple coding sequences for the genome-linked virus protein (VPg) in dicistroviruses. J. Invertebr. Pathol. 92: 100104.
98. Oberste, M. S.,, K. Maher, and, M. A. Pallansch. 2003. Genomic evidence that simian virus 2 and six other simian picornaviruses represent a new genus in Picornaviridae. Virology 314: 283293.
99. Ongus, J. R.,, D. Peters,, J. M. Bonmatin,, E. Bengsch,, J. M. Vlak, and, M. M. van Oers. 2004. Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. J. Gen. Virol. 85: 37473755.
100. Palmenberg, A. C. 1989. Sequence alignments of picornaviral capsid proteins, p. 211–241. In B. Semler and, E. Ehrenfeld (ed.), Molecular Aspects of Picornavirus Infection and Detection. American Society for Microbiology, Washington, DC.
101. Palmenberg, A. C.,, M. A. Pallansch, and, R. R. Rueckert. 1979. Protease required for processing picornaviral coat protein resides in the viral replicase gene. J. Virol. 32: 770778.
102. Palmenberg, A. C.,, G. D. Parks,, D. J. Hall,, R. H. Ingraham,, T. W. Seng, and, P. V. Pallai. 1992. Proteolytic processing of the cardioviral P2 region: primary 2A/2B cleavage in clone-derived precursors. Virology 190: 754762.
103. Palmenberg, A. C., and, J. Y. Sgro. 2002. Alignments and comparative profiles of picornavirus genera, p. 149–155. In B. Semler and, E. Wimmer (ed.), Molecular Biology of Picornaviruses. American Society for Microbiology, Washington, DC.
104. Palmenberg, A. C.,, D. Spiro,, R. Kuzmickas,, S. Wang,, A. Djikeng,, J. A. Rathe,, C. M. Fraser-Liggett, and, S. B. Liggett. 2009. Sequencing and analyses of all known human rhino-virus genomes reveal structure and evolution. Science 324: 5559.
105. Paul, A. V.,, A. Molla, and, E. Wimmer. 1994. Studies of a putative amphipathic helix in the N-terminus of poliovirus protein 2C. Virology 199: 188199.
106. Paul, A. V.,, A. Schultz,, S. E. Pincus,, S. Oroszlan, and, E. Wimmer. 1987. Capsid protein Vp4 of poliovirus is N-myristoylated. Proc. Natl. Acad. Sci. USA 84: 78277831.
107. Paul, A. V.,, J. H. van Boom,, D. Filippov, and, E. Wimmer. 1998. Protein-primed RNA synthesis by purified poliovirus RNA polymerase. Nature 393: 280284.
108. Pestova, T. V.,, C. U. T. Hellen, and, E. Wimmer. 1994. A conserved AUG triplet in the 5′ nontranslated region of poliovirus can function as an initiation codon in-vitro and in-vivo. Virology 204: 729737.
109. Petersen, J. F. W.,, M. M. Cherney,, H. D. Liebig,, T. Skern,, E. Kuechler, and, M. N. G. James. 1999. The structure of the 2A proteinase from a common cold virus: a proteinase responsible for the shut-off of host-cell protein synthesis. EMBO J. 18: 54635475.
110. Pfister, T.,, K. W. Jones, and, E. Wimmer. 2000. A cysteine-rich motif in poliovirus protein 2C ATPase is involved in RNA replication and binds zinc in vitro. J. Virol. 74: 334343.
111. Piccone, M. E.,, H. H. Chen,, R. P. Roos, and, M. J. Grubman. 1996. Construction of a chimeric Theiler’s murine encephalomyelitis virus containing the leader gene of foot-and-mouth disease virus. Virology 226: 135139.
112. Piccone, M. E.,, E. Rieder,, P. W. Mason, and, M. J. Grubman. 1995. The foot-and-mouth disease virus leader proteinase gene is not required for viral replication. J. Virol. 69: 53765382.
113. Poch, O.,, I. Sauvaget,, M. Delarue, and, N. Tordo. 1989. Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J. 8: 38673874.
114. Porter, F. W., and, A. C. Palmenberg. 2009. Leader-induced phosphorylation of nucleoporins correlates with nuclear trafficking inhibition by cardioviruses. J. Virol. 83: 19411951.
115. Racaniello, V. 2007. Picornaviridae: the viruses and their replication, p. 795–838. In D. M. Knipe,, P. M. Howley,, D. E. Griffin,, R. A. Lamb,, M. A. Martin,, B. Roizman, and, S. E. Straus (ed.), Fields Virology, 5th ed. Lippincott, Williams and Wilkins, Philadelphia, PA.
116. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing. http://www.R-project.org.
117. Reavy, B.,, M. A. Mayo,, A. D. Turnbullross, and, A. F. Mu-rant. 1993. Parsnip yellow fleck and Rice tungro spherical viruses resemble picornaviruses and represent 2 genera in a proposed new plant Picornavirus family ( Sequiviridae). Arch. Virol. 131: 441446.
118. Reddick, B. B.,, L. F. Habera, and, M. D. Law. 1997. Nucleotide sequence and taxonomy of maize chlorotic dwarf virus within the family Sequiviridae. J. Gen. Virol. 78: 11651174.
119. Reuter, G.,, A. Boldizsar, and, P. Pankovics. 2009. Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae. Arch. Virol. 154: 101108.
120. Ricour, C.,, F. Borghese,, F. Sorgeloos,, S. V. Hato,, F. J. M. van Kuppeveld, and, T. Michiels. 2009. Random mutagenesis defines a domain of Theiler’s virus leader protein that is essential for antagonism of nucleocytoplasmic trafficking and cytokine gene expression. J. Virol. 83: 1122311232.
121. Rodriguez, P. L., and, L. Carrasco. 1993. Poliovirus protein 2C has ATPase and GTPase activities. J. Biol. Chem. 268: 81058110.
122. Romanova, L. I.,, P. V. Lidsky,, M. S. Kolesnikova,, K. V. Fominykh,, A. P. Gmyl,, E. V. Sheval,, S. V. Hato,, F. J. M. van Kuppeveld, and, V. I. Agol. 2009. Antiapoptotic activity of the cardiovirus leader protein, a viral “security” protein. J. Virol. 83: 72737284.
123. Rossmann, M. G.,, E. Arnold,, J. W. Erickson,, E. A. Frankenberger,, J. P. Griffith,, H.-J. Hecht,, J. E. Johnson,, G. Kamer,, M. Luo,, A. G. Mosser,, R. R. Rueckert,, B. Sherry, and, G. Vriend. 1985. Structure of human cold virus and functional relationship to other picornaviruses. Nature (London) 317: 145153.
124. Rossmann, M. G., and, J. E. Johnson. 1989. Icosahedral RNA virus structure. Annu. Rev. Biochem. 58: 533573.
125. Rueckert, R. R., and, E. Wimmer. 1984. Systematic nomenclature of picornavirus proteins. J. Virol. 50: 957959.
126. Rux, J. J., and, R. M. Burnett. 1998. Spherical viruses. Curr. Opin. Struct. Biol. 8: 142149.
127. Ryabov, E. V. 2007. A novel virus isolated from the aphid Brevicoryne brassicae with similarity to Hymenoptera picorna-like viruses. J. Gen. Virol. 88: 25902595.
128. Ryan, M. D., and, M. Flint. 1997. Virus-encoded proteinases of the picornavirus super-group. J. Gen. Virol. 78: 699723.
129. Schein, C. H.,, N. Oezguen,, D. E. Volk,, R. Garimella,, A. Paul, and, W. Braun. 2006. NMR structure of the viral peptide linked to the genome (VPg) of poliovirus. Peptides 27: 16761684.
130. Siew, N.,, Y. Azaria, and, D. Fischer. 2004. The ORFanage: an ORFan database. Nucleic Acids Res. 32: D281D283.
131. Skern, T.,, B. Hampoelz,, A. Guarne,, I. Fita,, E. Bergmann,, J. Petersen, and, M. N. G. James. 2002. Structure and function of picornavirus proteinases, p. 199–212. In B. L. Semler and, E. Wimmer (eds.), Molecular Biology of Picornaviruses. American Society for Microbiology, Washington, DC.
132. Stanway, G., and, T. Hyypia. 1999. Parechoviruses. J. Virol. 73: 52495254.
133. Summers, D. F.,, J. V. Maizel, and, J. E. Darnell. 1965. Evidence for virus-specific noncapsid proteins in poliovirus-infected HeLa cells. Proc. Natl. Acad. Sci. USA 54: 505513.
134. Tate, J.,, L. Liljas,, P. Scotti,, P. Christian,, T. W. Lin, and, J. E. Johnson. 1999. The crystal structure of cricket paralysis virus: the first view of a new virus family. Nat. Struct. Biol. 6: 765774.
135. Teterina, N. L.,, A. E. Gorbalenya,, D. Egger,, K. Bienz, and, E. Ehrenfeld. 1997. Poliovirus 2C protein determinants of membrane binding and rearrangements in mammalian cells. J. Virol. 71: 89628972.
136. Teterina, N. L.,, A. E. Gorbalenya,, D. Egger,, K. Bienz,, M. S. Rinaudo, and, E. Ehrenfeld. 2006. Testing the modularity of the N-terminal amphipathic helix conserved in picornavirus 2C proteins and hepatitis C NS5A protein. Virology 344: 453467.
137. Thompson, A. A., and, O. B. Peersen. 2004. Structural basis for proteolysis-dependent activation of the poliovirus RNA-dependent RNA polymerase. EMBO J. 23: 34623471.
138. Tolskaya, E. A.,, L. I. Romanova,, M. S. Kolesnikova,, A. P. Gmyl,, A. E. Gorbalenya, and, V. I. Agol. 1994. Genetic studies on the poliovirus 2C protein, an NTPase. A plausible mechanism of guanidine effect on the 2C function and evidence for the importance of 2C oligomerization. J. Mol. Biol. 236: 13101323.
139. Toyoda, H.,, M. J. H. Nicklin,, M. G. Murray,, C. W. Anderson,, J. J. Dunn,, F. W. Studier, and, E. Wimmer. 1986. A 2Nd virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein. Cell 45: 761770.
140. Tseng, C. H.,, N. J. Knowles, and, H. J. Tsai. 2007. Molecular analysis of duck hepatitis virus type 1 indicates that it should be assigned to a new genus. Virus Res. 123: 190203.
141. Tseng, C. H., and, H. J. Tsai. 2007. Sequence analysis of a duck picornavirus isolate indicates that it together with porcine enterovirus type 8 and simian picornavirus type 2 should be assigned to a new picornavirus genus. Virus Res. 129: 104114.
142. Venkataraman, S.,, S. P. Reddy,, J. Loo,, N. Idamakanti,, P. L. Hallenbeck, and, V. S. Reddy. 2008. Structure of Seneca Valley virus-001: an oncolytic picornavirus representing a new genus. Structure 16: 15551561.
143. Victoria, J. G.,, A. Kapoor,, K. Dupuis,, D. P. Schnurr, and, E. L. Delwart. 2008. Rapid identification of known and new RNA viruses from animal tissues. Plos Pathog. 4: e1000163.
144. Wessels, E.,, R. A. Notebaart,, D. Duijsings,, K. Lanke,, B. Vergeer,, W. J. G. Melchers, and, F. J. M. van Kuppeveld. 2006. Structure-function analysis of the coxsackievirus protein 3A. Identification of residues important for dimerization, viral RNA replication, and transport inhibition. J. Biol. Chem. 281: 2823228243.
145. Whelan, S., and, N. Goldman. 2001. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18: 691699.
146. Williams, C. H.,, T. Kajander,, T. Hyypia,, T. Jackson,, D. Sheppard, and, G. Stanway. 2004. Integrin α vβ 6 is an RGD-dependent receptor for coxsackievirus A9. J. Virol. 78: 69676973.
147. Wimmer, E.,, C. U. T. Hellen, and, X. Cao. 1993. Genetics of poliovirus. Annu. Rev. Genet. 27: 353436.
148. Wutz, G.,, H. Auer,, N. Nowotny,, B. Grosse,, T. Skern, and, E. Kuechler. 1996. Equine rhinovirus serotypes 1 and 2: relationship to each other and to aphthoviruses and cardioviruses. J. Gen. Virol. 77: 17191730.
149. Yang, Y.,, M. K. Yi,, D. J. Evans,, P. Simmonds, and, S. M. Lemon. 2008. Identification of a conserved RNA replication element (cre) within the 3D pol-coding sequence of hepatoviruses. J. Virol. 82: 1011810128.
150. Yu, S. F., and, R. E. Lloyd. 1992. Characterization of the roles of conserved cysteine and histidine residues in poliovirus 2A protease. Virology 186: 725735.
151. Zhang, L.,, S. Sato,, J. I. Kim, and, R. P. Roos. 1995. Theiler’s virus as a vector for foreign gene delivery. J. Virol. 69: 31713175.
152. Zhao, W. D.,, E. Wimmer, and, F. C. Lahser. 1999. Poliovirus/hepatitis C virus (internal ribosomal entry site-core) chimeric viruses: improved growth properties through modification of a proteolytic cleavage site and requirement for core RNA sequences but not for core-related polypeptides. J. Virol. 73: 15461554.
153. Zimmern, D. 1988. Evolution of RNA viruses, p. 211–240. In E. Domingo,, J. J. Holland, and, P. Ahlquist (ed.), RNA Genetics. CRC Press, Boca Raton, FL.


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Table 1.

The picornavirus proteome: function, structure, and evolution

Citation: Gorbalenya A, Lauber C. 2010. Origin and Evolution of the Proteome, p 253-270. In Ehrenfeld E, Domingo E, Roos R (ed), The Picornaviruses. ASM Press, Washington, DC. doi: 10.1128/9781555816698.ch16

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