Chordopoxvirus protein F12 implicated in enveloped virion morphogenesis is an inactivated DNA polymerase
Tóm tắt
Through the course of their evolution, viruses with large genomes have acquired numerous host genes, most of which perform function in virus reproduction in a manner that is related to their original activities in the cells, but some are exapted for new roles. Here we report the unexpected finding that protein F12, which is conserved among the chordopoxviruses and is implicated in the morphogenesis of enveloped intracellular virions, is a derived DNA polymerase, possibly of bacteriophage origin, in which the polymerase domain and probably the exonuclease domain have been inactivated. Thus, F12 appears to present a rare example of a drastic, exaptive functional change in virus evolution. Reviewers: This article was reviewed by Frank Eisenhaber and Juergen Brosius. For complete reviews, go the Reviewers’ Reports section.
Tài liệu tham khảo
Koonin EV, Senkevich TG, Dolja VV: The ancient Virus World and evolution of cells. Biol Direct. 2006, 1: 29-10.1186/1745-6150-1-29.
Yutin N, Wolf YI, Koonin EV: Origin of giant viruses from smaller DNA viruses not from a fourth domain of cellular life. Virology. 2014, 466-467: 38-52.
Filee J: Route of NCLDV evolution: the genomic accordion. Curr Opin Virol. 2013, 3 (5): 595-599. 10.1016/j.coviro.2013.07.003.
Senkevich TG, Koonin EV, Bugert JJ, Darai G, Moss B: The genome of molluscum contagiosum virus: analysis and comparison with other poxviruses. Virology. 1997, 233 (1): 19-42. 10.1006/viro.1997.8607.
Moss B, Shisler JL, Xiang Y, Senkevich TG: Immune-defense molecules of molluscum contagiosum virus, a human poxvirus. Trends Microbiol. 2000, 8 (10): 473-477. 10.1016/S0966-842X(00)01838-2.
Moss B: Poxviridae: The Viruses and their Replication. Fields Virology, vol. 2. Edited by: Fields BN, Knipe DM, Howley PM, Griffin DE. 2001, Philadelphia: Lippincott, Williams & Wilkins, 2849-2884. 4
Smith GL, Benfield CT, Maluquer de Motes C, Mazzon M, Ember SW, Ferguson BJ, Sumner RP: Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J Gen Virol. 2013, 94 (Pt 11): 2367-2392.
Gould SJ: The exaptive excellence of spandrels as a term and prototype. Proc Natl Acad Sci U S A. 1997, 94 (20): 10750-10755. 10.1073/pnas.94.20.10750.
Stanitsa ES, Arps L, Traktman P: Vaccinia virus uracil DNA glycosylase interacts with the A20 protein to form a heterodimeric processivity factor for the viral DNA polymerase. J Biol Chem. 2006, 281 (6): 3439-3451. 10.1074/jbc.M511239200.
Senkevich TG, Koonin EV, Moss B: Vaccinia virus F16 protein, a predicted catalytically inactive member of the prokaryotic serine recombinase superfamily, is targeted to nucleoli. Virology. 2011, 417 (2): 334-342. 10.1016/j.virol.2011.06.017.
Dodding MP, Newsome TP, Collinson LM, Edwards C, Way M: An E2-F12 complex is required for intracellular enveloped virus morphogenesis during vaccinia infection. Cell Microbiol. 2009, 11 (5): 808-824. 10.1111/j.1462-5822.2009.01296.x.
Johnston SC, Ward BM: Vaccinia virus protein F12 associates with intracellular enveloped virions through an interaction with A36. J Virol. 2009, 83 (4): 1708-1717. 10.1128/JVI.01364-08.
Morgan GW, Hollinshead M, Ferguson BJ, Murphy BJ, Carpentier DC, Smith GL: Vaccinia protein F12 has structural similarity to kinesin light chain and contains a motor binding motif required for virion export. PLoS Pathog. 2010, 6 (2): e1000785-10.1371/journal.ppat.1000785.
Braithwaite DK, Ito J: Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res. 1993, 21 (4): 787-802. 10.1093/nar/21.4.787.
Tahirov TH, Makarova KS, Rogozin IB, Pavlov YI, Koonin EV: Evolution of DNA polymerases: an inactivated polymerase-exonuclease module in Pol epsilon and a chimeric origin of eukaryotic polymerases from two classes of archaeal ancestors. Biol Direct. 2009, 4: 11-10.1186/1745-6150-4-11.
Senkevich TG, Wyatt LS, Weisberg AS, Koonin EV, Moss B: A conserved poxvirus NlpC/P60 superfamily protein contributes to vaccinia virus virulence in mice but not to replication in cell culture. Virology. 2008, 374 (2): 506-514. 10.1016/j.virol.2008.01.009.
Rogozin IB, Makarova KS, Pavlov YI, Koonin EV: A highly conserved family of inactivated archaeal B family DNA polymerases. Biol Direct. 2008, 3: 32-10.1186/1745-6150-3-32.
Makarova KS, Krupovic M, Koonin EV: Evolution of replicative DNA polymerases in archaea and their contributions to the eukaryotic replication machinery. Frontiers Microbiol. 2014, doi:10.3389/fmicb.2014.00354
Kazlauskas D, Venclovas C: Herpesviral helicase-primase subunit UL8 is inactivated B-family polymerase. Bioinformatics. 2014, 30 (15): 2093-2097. 10.1093/bioinformatics/btu204.
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25 (17): 3389-3402. 10.1093/nar/25.17.3389.
Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32 (5): 1792-1797. 10.1093/nar/gkh340.
Yutin N, Makarova KS, Mekhedov SL, Wolf YI, Koonin EV: The deep archaeal roots of eukaryotes. Mol Biol Evol. 2008, 25 (8): 1619-1630. 10.1093/molbev/msn108.
Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ: Jalview Version 2–a multiple sequence alignment editor and analysis workbench. Bioinformatics. 2009, 25 (9): 1189-1191. 10.1093/bioinformatics/btp033.
Thompson JD, Gibson TJ, Higgins DG: Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. 2002, Chapter 2: Unit 2 3-
Soding J: Protein homology detection by HMM-HMM comparison. Bioinformatics. 2005, 21 (7): 951-960. 10.1093/bioinformatics/bti125.
Kelley LA, Sternberg MJ: Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc. 2009, 4 (3): 363-371. 10.1038/nprot.2009.2.
Price MN, Dehal PS, Arkin AP: FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE. 2010, 5 (3): e9490-10.1371/journal.pone.0009490.
Karpenahalli MR, Lupas AN, Soding J: TPRpred: a tool for prediction of TPR-, PPR- and SEL1-like repeats from protein sequences. BMC Bioinformatics. 2007, 8: 2-10.1186/1471-2105-8-2.