Long-term balancing selection at the West Nile virus resistance gene, Oas1b, maintains transspecific polymorphisms in the house mouse

Molecular Biology and Evolution

Volumn 25, Issue 8, 2008, Pages 1609-1618

  Ferguson, William ^a,b   Dvora, Shira ^a   Gallo, Juliana ^a   Orth, Annie ^c   Boissinot, Stéphane ^a,b  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c CNRS   (France)

Author keywords

Balancing selection; Flavivirus; Mus musculus; Oas1b; West Nile virus

Indexed keywords

OLIGOADENYLATE SYNTHETASE 1B; SYNTHETASE;

ALLELE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GENETIC POLYMORPHISM; INTRASPECIFIC VARIATION; INTRON; MOUSE; MURIDAE; MUS MUSCULUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ANALYSIS; WEST NILE FLAVIVIRUS;

2',5'-OLIGOADENYLATE SYNTHETASE; AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; DNA PRIMERS; EVOLUTION, MOLECULAR; LIKELIHOOD FUNCTIONS; MICE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; POLYMORPHISM, GENETIC; SELECTION (GENETICS); SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

DENGUE VIRUS; FLAVIVIRUS; MAMMALIA; MUS MUSCULUS; WEST NILE VIRUS; YELLOW FEVER VIRUS;

EID: 47649126172     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msn106     Document Type: Article

References (46)

1. Bamshad MJ, Mummidi S, Gonzalez E, et al. (11 co-authors). 2002. A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc Natl Acad Sci USA. 99:10539-10544.
2. Baysal BE, Lawrence EC, Ferrell RE. 2007. Sequence variation in human succinate dehydrogenase genes: evidence for long-term balancing selection on SDHA. BMC Biol. 5:12.
3. Bergelson J, Kreitman M, Stahl EA, Tian D. 2001. Evolutionary dynamics of plant R-genes. Science. 292:2281-2285.
4. Bonhomme F, Rivals E, Orth A, Grant GR, Jeffreys AJ, Bois PR. 2007. Species-wide distribution of highly polymorphic minisatellite markers suggests past and present genetic exchanges among house mouse subspecies. Genome Biol. 8:R80.
5. Boursot P, Din W, Anand R, Darviche D, Dod B, Von Deimling F, Talwar GP, Bonhomme F. 1996. Origin and radiation of the house mouse: mitochondrial DNA phylogeny. J Evol Biol. 9:391-415.
6. Edwards SV, Chesnut K, Satta Y, Wakeland EK. 1997. Ancestral polymorphism of Mhc class II genes in mice: implications for balancing selection and the mammalian molecular clock. Genetics. 146:655-668.
7. Eskildsen S, Hartmann R, Kjeldgaard N, Justesen J. 2002. Gene structure of the murine 2′-5′-oligoadenylate synthetase family. Cell Mol Life Sci. 59:1212-1222.
8. Eyre-Walker A, Keightley PD, Smith NGC, Gaffney D. 2002. Quantifying the slightly deleterious mutation model of molecular evolution. Mol Biol Evol. 19:2142-2149.
9. Ferris SD, Sage RD, Huang CM, Nielsen JT, Ritte U, Wilson AC. 1983. Flow of mitochondrial DNA across a species boundary. Proc Natl Acad Sci USA. 80:2290-2294.
10. Figueroa F, Gunther E, Klein J. 1988. MHC polymorphism predating speciation. Nature. 335:265-267.
11. Garrigan D, Hedrick PW. 2003. Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution Int J Org Evolution. 57:1707-1722.
12. Gibbs RA, Weinstock GM, Metzker ML, et al. (228 co-authors). 2004. Genome sequence of the Brown Norway rat yields insights into mammalian evolution. Nature. 428:493-521.
13. Goodman GT, Koprowski H. 1962. Study of the mechanism of innate resistance to virus infection. J Cell Comp Physiol. 59:333-373.
14. Greene-Till R, Zhao Y, Hardies SC. 2000. Gene flow of unique sequences between Mus musculus domesticus and Mus spretus. Mamm Genome. 11:225-230.
15. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML Online - a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res. 33:W557-W559.
16. Gutierrez-Espeleta GA, Hedrick PW, Kalinowski ST, Garrigan D, Boyce WM. 2001. Is the decline of desert bighorn sheep from infectious disease the result of low MHC variation? Heredity. 86:439-450.
17. Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser. 41:95-98.
18. Hedrick P. 2004. Estimation of relative fitnesses from relative risk data and the predicted future of haemoglobin alleles S and C. J Evol Biol. 17:221-224.
19. Hedrick PW, Ginevan M, Ewing E. 1976. Genetic polymorphism in heterogeneous environment. Annu Rev Ecol Syst. 7:1-32.
20. Hedrick PW, Thomson G. 1983. Evidence for balancing selection at HLA. Genetics. 104:449-456.
21. Hovanessian AG, Justesen J. 2007. The human 2′-5′ oligoadenylate synthetase family: unique interferon-inducible enzymes catalyzing 2′-5′ instead of 3′-5′ phosphodiester bond formation. Biochimie. 89:779-788.
22. Hudson RR, Kreitman M, Aguade M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics. 116:153-159.
23. Kojima K. 1971. Is there a constant fitness for a given genotype? No!. Evolution. 25:281-285.
24. Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 5:150-163.
25. Mashimo T, Glaser P, Lucas M, Simon-Chazottes D, Ceccaldi PE, Montagutelli X, Despres P, Guenet JL. 2003. Structural and functional genomics and evolutionary relationships in the cluster of genes encoding murine 2′,5′-oligoadenylate synthetases. Genomics. 82:537-552.
26. Mashimo T, Lucas M, Simon-Chazottes D, Frenkiel MP, Montagutelli X, Ceccaldi PE, Deubel V, Guenet JL, Despres P. 2002. A nonsense mutation in the gene encoding 2′-5′-oligoadenylate synthetase/L1 isoform is associated with West Nile virus susceptibility in laboratory mice. Proc Natl Acad Sci USA. 99:11311-11316.
27. McDonald JH, Kreitman M. 1991. Adaptive protein evolution at the Adh locus in Drosophila. Nature. 351:652-654.
28. Nei M, Gojobori T. 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 3:418-426.
29. Newman RM, Hall L, Connole M, et al. 2006. Balancing selection and the evolution of functional polymorphism in Old World monkey TRIM5alpha. Proc Natl Acad Sci USA. 103:19134-19139 (11 co-authors).
30. Orth A, Adama T, Din W, Bonhomme F. 1998. Natural hybridization between two subspecies of the house mouse, Mus musculus domesticus and Mus musculus castaneus, near Lake Casitas, California. Genome. 41:104-110.
31. Orth A, Belkhir K, Britton-Davidian J, Boursot P, Benazzou T, Bonhomme F. 2002. Natural hybridization between two sympatric species of mice Mus musculus domesticus L. and Mus spretus Lataste. C R Biol. 325:89-97.
32. Perelygin AA, Scherbik SV, Zhulin IB, Stockman BM, Li Y, Brinton MA. 2002. Positional cloning of the murine flavivirus resistance gene. Proc Natl Acad Sci USA. 99:9322-9327.
33. Perelygin AA, Zharkikh AA, Scherbik SV, Brinton MA. 2006. The mammalian 2′-5′ oligoadenylate synthetase gene family: evidence for concerted evolution of paralogous Oas1 genes in Rodentia and Artiodactyla. J Mol Evol. 63:562-576.
34. Rogozin IB, Aravind L, Koonin EV. 2003. Differential action of natural selection on the N and C-terminal domains of 2′-5′ oligoadenylate synthetases and the potential nuclease function of the C-terminal domain. J Mol Biol. 326:1449-1461.
35. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 19:2496-2497.
36. Sabin AB. 1952. Genetic, hormonal and age factors in natural resistance to certain viruses. Ann N Y Acad Sci. 6:936-944.
37. Sangster MY, Heliams DB, MacKenzie JS, Shellam GR. 1993. Genetic studies of flavivirus resistance in inbred strains derived from wild mice: evidence for a new resistance allele at the flavivirus resistance locus (Flv). J Virol. 67:340-347.
38. Sangster MY, Mackenzie JS, Shellam GR. 1998. Genetically determined resistance to flavivirus infection in wild Mus musculus domesticus and other taxonomic groups in the genus Mus. Arch Virol. 143:697-715.
39. Sawyer SA. 1989. Statistical tests for detecting gene conversion. Mol Biol Evol. 6:526-538.
40. Scherbik SV, Paranjape JM, Stockman BM, Silverman RH, Brinton MA. 2006. RNase L plays a role in the antiviral response to West Nile virus. J Virol. 80:2987-2999.
41. Shyue SK, Hewett-Emmett D, Sperling HG, Hunt DM, Bowmaker JK, Mollon JD, Li WH. 1995. Adaptive evolution of color vision genes in higher primates. Science. 269:1265-1267.
42. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
43. Verrelli BC, McDonald JH, Argyropoulos G, Destro-Bisol G, Froment A, Drousiotou A, Lefranc G, Helal AN, Loiselet J, Tishkoff SA. 2002. Evidence for balancing selection from nucleotide sequence analyses of human G6PD. Am J Hum Genet. 71:1112-1128.
44. Woolhouse ME, Webster JP, Domingo E, Charlesworth B, Levin BR. 2002. Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nat Genet. 32:569-577.
45. Yonekawa H, Gotoh O, Tagashira Y, Matsushima Y, Shi LI, Cho WS, Miyashita N, Moriwaki K. 1986. A hybrid origin of Japanese mice "'Mus musculus molossinus"'. Curr Top Microbiol Immunol. 127:62-67.
46. Zhang J, Hunter KW, Gandolph M, Rowe WL, Finney RP, Kelley JM, Edmonson M, Buetow KH. 2005. A high-resolution multistrain haplotype analysis of laboratory mouse genome reveals three distinctive genetic variation patterns. Genome Res. 15:241-249.