Abstract
Viperin, an evolutionarily highly conserved interferon-inducible multifunctional protein, has previously been reported to exhibit antiviral activity against a wide range of DNA and RNA viruses. Utilizing the complete nucleotide coding sequence data of fish viperin antiviral genes, and employing the maximum likelihood-based codon substitution models, the present study reports the pervasive role of positive selection in the evolution of viperin antiviral protein in fishes. The overall rate of nonsynonymous (dN) to synonymous (dS) substitutions (dN/dS) for the three functional domains of viperin (N-terminal, central domain and C-terminal) were 1.1, 0.12, and 0.24, respectively. Codon-by-codon substitution analyses have revealed that while most of the positively selected sites were located at the N-terminal amphipathic α-helix domain, few amino acid residues at the C-terminal domain were under positive selection. However, none of the sites in the central domain were under positive selection. These results indicate that, although viperin is evolutionarily highly conserved, the three functional domains experienced differential selection pressures. Taken together with the results of previous studies, the present study suggests that the persistent antagonistic nature of surrounding infectious viral pathogens might be the likely cause for such adaptive evolutionary changes of certain amino acids in fish viperin antiviral protein.
References
Chen D, Guo X, Nie P (2010) Phylogenetic studies of sinipercid fish (Perciformes: Sinipercidae) based on multiple genes, with first application of an immune-related gene, the virus-induced protein (viperin) gene. Mol Phylogenet Evol 55:1167–1176
Chen ZY, Lei XY, Zhang QY (2012) The antiviral defense mechanisms in mandarin fish induced by DNA vaccination against a rhabdovirus. Vet Microbiol 157:264–275
Chin KC, Cresswell P (2001) Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc Natl Acad Sci U S A 98:15125–15130
Dang W, Zhang M, Hu YH, Sun L (2010) Differential regulation of Sciaenops ocellatus viperin expression by intracellular and extracellular bacterial pathogens. Fish Shellfish Immunol 29:264–270
Emerman M, Malik HS (2010) Paleovirology—modern consequences of ancient viruses. PLoS Biol 8:e1000301
Fernandes JM, Ruangsri J, Kiron V (2010) Atlantic cod piscidin and its diversification through positive selection. PLoS One 5:e9501
Fitzgerald KA (2011) The interferon inducible gene: viperin. J Interferon Cytokine Res 31:131–135
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321
Hinson ER, Cresswell P (2009a) The antiviral protein, viperin, localizes to lipid droplets via its N-terminal amphipathic alpha-helix. Proc Natl Acad Sci U S A 106:20452–20457
Hinson ER, Cresswell P (2009b) The N-terminal amphipathic alpha-helix of viperin mediates localization to the cytosolic face of the endoplasmic reticulum and inhibits protein secretion. J Biol Chem 284:4705–4712
Hurley IA, Mueller RL, Dunn KA, Schmidt EJ, Friedman M, Ho RK, Prince VE, Yang Z, Thomas MG, Coates MI (2007) A new time-scale for ray-finned fish evolution. Proc Biol Sci 274:489–498
Jiang D, Guo H, Xu C, Chang J, Gu B, Wang L, Block TM, Guo JT (2008) Identification of three interferon-inducible cellular enzymes that inhibit the replication of hepatitis C virus. J Virol 82:1665–1678
Jiang D, Weidner JM, Qing M, Pan XB, Guo H, Xu C, Zhang X, Birk A, Chang J, Shi PY, Block TM, Guo JT (2010) Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections. J Virol 84:8332–8341
Jiggins FM, Kim KW (2007) A screen for immunity genes evolving under positive selection in Drosophila. J Evol Biol 20:965–970
Kimura M (1968) Evolutionary rate at the molecular level. Nature 217:624–626
King JL, Jukes TH (1969) Non-Darwinian evolution. Science 164:788–798
Lazzaro BP (2008) Natural selection on the Drosophila antimicrobial immune system. Curr Opin Microbiol 11:284–289
Levasseur A, Gouret P, Lesage-Meessen L, Asther M, Asther M, Record E, Pontarotti P (2006) Tracking the connection between evolutionary and functional shifts using the fungal lipase/feruloyl esterase A family. BMC Evol Biol 6:92
Levasseur A, Orlando L, Bailly X, Milinkovitch MC, Danchin EG, Pontarotti P (2007) Conceptual bases for quantifying the role of the environment on gene evolution: the participation of positive selection and neutral evolution. Biol Rev Camb Philos Soc 82:551–572
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lim ES, Wu LI, Malik HS, Emerman M (2012) The function and evolution of the restriction factor viperin in primates was not driven by lentiviruses. Retrovirology 9:55
Malik HS, Henikoff S (2005) Positive selection of iris, a retroviral envelope-derived host gene in Drosophila melanogaster. PLoS Genet 1:e44
Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P (2010) RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463
Patel MR, Emerman M, Malik HS (2011) Paleovirology—ghosts and gifts of viruses past. Curr Opin Virol 1:304–309
Patel MR, Loo YM, Horner SM, Gale M Jr, Malik HS (2012) Convergent evolution of escape from hepaciviral antagonism in primates. PLoS Biol 10:e1001282
Peng Z, He S, Wang J, Wang W, Diogo R (2006) Mitochondrial molecular clocks and the origin of the major Otocephalan clades (Pisces: Teleostei): a new insight. Gene 370:113–124
Purcell MK, Nichols KM, Winton JR, Kurath G, Thorgaard GH, Wheeler P, Hansen JD, Herwig RP, Park LK (2006) Comprehensive gene expression profiling following DNA vaccination of rainbow trout against infectious hematopoietic necrosis virus. Mol Immunol 43:2089–2106
Randall RE, Goodbourn S (2008) Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1–47
Rivieccio MA, Suh HS, Zhao Y, Zhao ML, Chin KC, Lee SC, Brosnan CF (2006) TLR3 ligation activates an antiviral response in human fetal astrocytes: a role for viperin/cig5. J Immunol 177:4735–4741
Rytkonen KT, Ryynanen HJ, Nikinmaa M, Primmer CR (2008) Variable patterns in the molecular evolution of the hypoxia-inducible factor-1 alpha (HIF-1alpha) gene in teleost fishes and mammals. Gene 420:1–10
Sackton TB, Lazzaro BP, Schlenke TA, Evans JD, Hultmark D, Clark AG (2007) Dynamic evolution of the innate immune system in Drosophila. Nat Genet 39:1461–1468
Sawyer SL, Emerman M, Malik HS (2007) Discordant evolution of the adjacent antiretroviral genes TRIM22 and TRIM5 in mammals. PLoS Pathog 3:e197
Schmitt P, Gueguen Y, Desmarais E, Bachere E, de Lorgeril J (2010) Molecular diversity of antimicrobial effectors in the oyster Crassostrea gigas. BMC Evol Biol 10:23
Seo JY, Yaneva R, Cresswell P (2011) Viperin: a multifunctional, interferon-inducible protein that regulates virus replication. Cell Host Microbe 10:534–539
Sun B, Skjaeveland I, Svingerud T, Zou J, Jorgensen J, Robertsen B (2011) Antiviral activity of salmonid gamma interferon against infectious pancreatic necrosis virus and salmonid alphavirus and its dependency on type I interferon. J Virol 85:9188–9198
Sun BJ, Nie P (2004) Molecular cloning of the viperin gene and its promoter region from the mandarin fish Siniperca chuatsi. Vet Immunol Immunopathol 101:161–170
Swanson WJ, Nielsen R, Yang Q (2003) Pervasive adaptive evolution in mammalian fertilization proteins. Mol Biol Evol 20:18–20
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tan KS, Olfat F, Phoon MC, Hsu JP, Howe JL, Seet JE, Chin KC, Chow VT (2012) In vivo and in vitro studies on the antiviral activities of viperin against influenza H1N1 virus infection. J Gen Virol 93:1269–1277
Verrier ER, Langevin C, Benmansour A, Boudinot P (2011) Early antiviral response and virus-induced genes in fish. Dev Comp Immunol 35:1204–1214
Wang S, Wu X, Pan T, Song W, Wang Y, Zhang F, Yuan Z (2012) Viperin inhibits hepatitis C virus replication by interfering with binding of NS5A to host protein hVAP-33. J Gen Virol 93:83–92
Wang X, Hinson ER, Cresswell P (2007) The interferon-inducible protein viperin inhibits influenza virus release by perturbing lipid rafts. Cell Host Microbe 2:96–105
Xu T, Sun Y, Shi G, Wang R (2012) Miiuy croaker hepcidin gene and comparative analyses reveal evidence for positive selection. PLoS One 7:e35449
Yang Z (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13:555–556
Yang Z, Nielsen R, Goldman N, Pedersen AM (2000) Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155:431–449
Yasuike M, Kondo H, Hirono I, Aoki T (2007) Difference in Japanese flounder, Paralichthys olivaceus gene expression profile following hirame rhabdovirus (HIRRV) G and N protein DNA vaccination. Fish Shellfish Immunol 23:531–541
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I thank Drs. Peggy Hill and B. Verghese and two anonymous reviewers for excellent comments which greatly improved the manuscript.
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Padhi, A. Positive selection drives rapid evolution of certain amino acid residues in an evolutionarily highly conserved interferon-inducible antiviral protein of fishes. Immunogenetics 65, 75–81 (2013). https://doi.org/10.1007/s00251-012-0655-8
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DOI: https://doi.org/10.1007/s00251-012-0655-8