Abstract
Interferon-γ plays a key role in the immune response against intracellular pathogens. Its gene is located inside a cluster of cytokines from the interleukin-10 family. A comparison of the coding sequences in the mammalian Glire lineage indicates a possible action of positive Darwinian selection promoting rapid amino-acid changes in the branch leading to murine rodents represented by Mus and Rattus. Looking at genomic diversity of this gene inside the genus Mus, we could propose that a recent selective sweep has affected M. m. domesticus, this subspecies harbouring predominantly a single Ifng haplotype that differs from that of the other subspecies by a unique amino-acid difference in a key position of the molecule. The sweep seems to have affected a region of at most 50 kb as recombinants could be found at flanking conserved non-coding sequences. Functional differences were clearly apparent in cis-regulation of Ifng transcription between the domesticus and the musculus-type haplotypes. As the presence of the musculus haplotype in a predominantly domesticus background seems to promote susceptibility to chronic infection by Theiler's virus, these findings open interesting avenues for documenting immune system gene co-evolution.
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References
Harr B, Voolstra C, Heinen T, Baines J, Rottscheidt R, Ihle S et al. A change of expression in the conserved signaling gene MKK7 is associated with a selective sweep in the western house mouse Mus musculus domesticus. J Evol Biol 2006; 19: 1486–1496.
Boyko AR, Williamson SH, Indap AR, Degenhardt JD, Hernandez RD, Lohmueller KE et al. Assessing the evolutionnary impact of amino acid mutations in the human genome. Plos Genet 2008; 4: 1–13.
Nielsen R . Molecular signatures of natural selection. Ann Rev Gen 2005; 39: 197–218.
Thornton K, Jensen J, Becquet C, Andolfatto P . Progress and prospects in mapping recent selection in the genome. Heredity 2007; 98: 340–348.
Guénet J-L . Assessing the genetic component of the susceptibility of mice to viral infections. Brief funct genomic proteomic 2005; 4: 225–240.
Levillayer F, Mas M, Levi-Acobas F, Brahic M, Bureau J-F . Interleukin 22 Is a Candidate Gene for Tmevp3, a Locus Controlling Theiler's Virus-Induced Neurological Diseases. Genetics 2007; 176: 1835–1844.
Pestka S, Krause C, Walter M . Interferons, interferon-like cytokines, and their receptors. Immunol Rev 2004; 202: 8–32.
Igawa D, Sakai M, Savan R . An unexpected discovery of two interferon gamma-like genes along with interleukin (IL)-22 and -26 from teleost: IL-22 and -26 genes have been described for the first time outside mammals. Mol Immunol 2006; 43: 999–1009.
Qi ZT, Nie P . Comparative study and expression analysis of the interferon gamma locus cytokines in Xenopus tropicalis. Immunogenetics 2008; 60: 699–710.
Schoenborn J, Dorschner M, Sekimata M, Santer D, Shnyreva M, Fitzpatrick D et al. Comprehensive epigenetic profiling identifies multiple distal regulatory elements dircting Ifng transcription. Nat Immunol 2007; 8: 732–742.
Dumoutier L, Van Roost E, Ameye G, Michaux L, Renauld J-C . IL-TIF/IL-22: genomic organization and mapping of the human and mouse genes. Genes Immun 2000; 1: 488–494.
Yang Z . Likelihood ratio tests for detecting positive selection and application to primate lyzozyme evolution. Mol Biol Evol 1998; 15: 568–573.
Yang Z, Nielsen R . Synonymous and nonsynonymous rate variation in nuclear genes of mammals. J Mol Evol 1998; 46: 409–418.
Nielsen R, Yang Z . Likelihood models for detecting positively selected amino acid sites and application to the HIV-1 envelope gene. Genetics 1998; 148: 929–936.
Yang Z, Nielsen R, Goldman N, Pederson A-M . Codon-substitution models for heterogeneous selection pressure at amino acid sites. Genetics 2000; 155: 431–449.
Yang Z, Nielsen R . Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol Biol Evol 2002; 19: 908–917.
Kosiol C, Vinar T, da Fonseca RR, Hubisz MJ, Bustamante CD, Nielsen R et al. Patterns of positive selection in six Mammalian genomes. Plos Genet 2008; 4: e1000144.
Vigneau S, Rohrlich P-S, Brahic M, Bureau J-F . TmevpgI, a candidate gene for the control of Theiler's virus persistence, could be implicated in the regulation of gamma interferon. J Virol 2003; 77: 5632–5638.
Zhao W, Valencia AZ, Melby PC . Biological activity of hamster interferon-gamma is modulated by the carboxyl-terminal tail. Cytokine 2006; 34: 243–251.
Bonhomme F, Rivals E, Orth A, Grant G, Jeffrey A, Bois P . Species-wide distribution of highly polymorphic minisatellite suggests past and present genetic exchanges among house mouse subspecies. Genome Biol 2007; 8: R80.
Salcedo T, Geraldes A, MW N . Nucleotide variation in wild and inbred mice. Genetics 2007; 177: 2277–2291.
Barrett JC, Fry B, Maller J, Daly MJ . Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005; 21: 263–265.
HapMap . A haplotype map of the human genome. Nature 2005; 437: 1299–1320.
Orth A, Belkhir K, Britton-Davidian J, Boursot P, Benazzou T, Bonhomme F . Natural hybridisation between two sympatric species of mice Mus musculus domesticus L. and Mus spretus Lataste. Comptes Rendus Biologies 2002; 325: 89–97.
Burgio G, Szatanik M, Guénet J, Arnau M, Panthier J, Montagutelli X . Interspecific recombinant congenic strains between C57BL/6 and mice of the Mus spretus species: a powerful tool to dissect genetic control of complex traits. Genetics 2007; 177: 2321–2333.
MacKay T-F . Quantitative trait loci in Drosophila. Nat Rev Genet 2001; 2: 11–20.
Landar A, Curry B, Parker M, DiGiacomo R, Indelicato S, Nagabhushan T et al. Design, characterization, and structure of a biologically active single-chain mutant of human IFN-γ. J Mol Biol 2000; 299: 169–179.
Walter M . Structural analysis of IL-10 and Type I interferon family members and their complexes with receptor. Adv protein chem 2004; 68: 171–223.
Mitchell-Olds T, Willis JH, Goldstein DB . Which evolutionary processes influence natural genetic variation for phenotypic trait? Nature Rev Genet 2007; 3: 845–856.
Li K . ClustalW-MPI: ClustalW analysis using distributed and parralel computing. Bioinformatics 2003; 19: 1585–1586.
Hall T . BioEdit a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 1999; 41: 95–98.
Guindon S, Lethiec F, Duroux P, Gascuel O . PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 2005; 33: W557–W559.
Yang Z . PAML4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 2007; 24: 1586–1591.
Goldman N, Yang Z . A codon-based model of nucleotide substitution for protein-coding DNA seqences. Mol Biol Evol 1994; 11: 725–736.
Muse S, Gaut B . A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol Biol Evol 1994; 11: 715–724.
Azoulay A, Brahic M, Bureau J-F . FVB mice transgenic for the H-2 Db gene become resistant to persistent infection by Theiler's virus. J Virol 1994; 68: 4049–4052.
McAllister A, Tangy F, Aubert C, Brahic M . Molecular cloning of the complete genome of Theiler's virus, strain DA, and production of infectious transcripts. Microb Pathog 1989; 7: 381–388.
Michiels T, Dejong V, Rodrigus R, Shaw-Jackson . Protein 2A is not required for Theiler's virus replication. J Virol 1997; 71: 9549–9556.
Huson DH, Bryant D . Application of Phylogenetic Networks in Evolutionary Studies. Mol Biol Evol 2006; 23: 254–267.
Acknowledgements
This work was initiated in Unité des Virus Lents directed by Michel Brahic. We are indebted to F Levillayer for technical help, K Chatziioannou for performing some of the DNA analyses, JJ Duquesne for taking care of the wild mice in Montpellier, Louis Jones for programming support, M Brahic, R Cheynier, M Delepierre, R Parker and S Wain-Hobson for helpful discussion. We also thank the anonymous referees for their fruitful comments. JFB and FB conceived the project. FL-A, LM, AA and JFB performed the experiments. LM, AA, JFB and FB analyzed the data. JFB and FB wrote the paper. This study was supported by the Institut Pasteur Fondation, Agence Nationale de la Recherche (MIME 2006), Centre National de la Recherche Scientifique. It is contribution ISEM 2009-019.
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Levi-Acobas, F., Mars, L., Orth, A. et al. Adaptive evolution of interferon-γ in Glire lineage and evidence for a recent selective sweep in Mus. m. domesticus. Genes Immun 10, 297–308 (2009). https://doi.org/10.1038/gene.2009.22
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DOI: https://doi.org/10.1038/gene.2009.22