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Immunogenetics

, Volume 67, Issue 9, pp 487–499 | Cite as

Contrasted patterns of variation and evolutionary convergence at the antiviral OAS1 gene in old world primates

  • Ian Fish
  • Stéphane BoissinotEmail author
Original Article

Abstract

The oligoadenylate synthetase 1 (OAS1) enzyme acts as an innate sensor of viral infection and plays a major role in the defense against a wide diversity of viruses. Polymorphisms at OAS1 have been shown to correlate with differential susceptibility to several infections of great public health significance, including hepatitis C virus, SARS coronavirus, and West Nile virus. Population genetics analyses in hominoids have revealed interesting evolutionary patterns. In Central African chimpanzee, OAS1 has evolved under long-term balancing selection, resulting in the persistence of polymorphisms since the origin of hominoids, whereas human populations have acquired and retained OAS1 alleles from Neanderthal and Denisovan origin. We decided to further investigate the evolution of OAS1 in primates by characterizing intra-specific variation in four species commonly used as models in infectious disease research: the rhesus macaque, the cynomolgus macaque, the olive baboon, and the Guinea baboon. In baboons, OAS1 harbors a very low level of variation. In contrast, OAS1 in macaques exhibits a level of polymorphism far greater than the genomic average, which is consistent with the action of balancing selection. The region of the enzyme that directly interacts with viral RNA, the RNA-binding domain, contains a number of polymorphisms likely to affect the RNA-binding affinity of OAS1. This strongly suggests that pathogen-driven balancing selection acting on the RNA-binding domain of OAS1 is maintaining variation at this locus. Interestingly, we found that a number of polymorphisms involved in RNA-binding were shared between macaques and chimpanzees. This represents an unusual case of convergent polymorphism.

Keywords

OAS1 Polymorphism Balancing selection Macaque Baboon 

Notes

Acknowledgments

The work was conducted in part with equipment from the Core Facilities for Imaging, Cellular and Molecular Biology at Queens College. This research was supported by the Professional Staff Congress-City University of New York grant 66642–00 44 to S.B. This investigation used resources that were supported by the Southwest National Primate Research Center grant P51 RR013986 from the National Center for Research Resources, National Institutes of Health, and that are currently supported by the Office of Research Infrastructure Programs through P51 OD011133.

References

  1. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, Kondrashov AS, Sunyaev SR (2010) A method and server for predicting damaging missense mutations. Nat Methods 7:248–249PubMedCentralCrossRefPubMedGoogle Scholar
  2. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98:10037–10041PubMedCentralCrossRefPubMedGoogle Scholar
  3. Bamshad MJ, Mummidi S, Gonzalez E, Ahuja SS, Dunn DM, Watkins WS, Wooding S, Stone AC, Jorde LB, Weiss RB, Ahuja SK (2002) A strong signature of balancing selection in the 5′ cis-regulatory region of CCR5. Proc Natl Acad Sci U S A 99:10539–10544PubMedCentralCrossRefPubMedGoogle Scholar
  4. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48CrossRefPubMedGoogle Scholar
  5. Bigham AW, Buckingham KJ, Husain S, Emond MJ, Bofferding KM, Gildersleeve H, Rutherford A, Astakhova NM, Perelygin AA, Busch MP, Murray KO, Sejvar JJ, Green S, Kriesel J, Brinton MA, Bamshad M (2011) Host genetic risk factors for West Nile virus infection and disease progression. PLoS One 6:e24745PubMedCentralCrossRefPubMedGoogle Scholar
  6. Boissinot S, Alvarez L, Giraldo-Ramirez J, Tollis M (2014) Neutral nuclear variation in Baboons (genus Papio) provides insights into their evolutionary and demographic histories. Am J Phys Anthropol 155:621–634CrossRefPubMedGoogle Scholar
  7. Cagliani R, Sironi M (2013) Pathogen-driven selection in the human genome. Int J Evol Biol 2013:204240PubMedCentralCrossRefPubMedGoogle Scholar
  8. Cagliani R, Fumagalli M, Biasin M, Piacentini L, Riva S, Pozzoli U, Bonaglia MC, Bresolin N, Clerici M, Sironi M (2010) Long-term balancing selection maintains trans-specific polymorphisms in the human TRIM5 gene. Hum Genet 128:577–588CrossRefPubMedGoogle Scholar
  9. Cai Y, Chen Q, Zhou W, Chu C, Ji W, Ding Y, Xu J, Ji Z, You H, Wang J (2014) Association analysis of polymorphisms in OAS1 with susceptibility and severity of hand, foot and mouth disease. Int J Immunogene 41:384–392CrossRefGoogle Scholar
  10. Charlesworth D (2006) Balancing selection and its effects on sequences in nearby genome regions. PLoS Genet 2:e64PubMedCentralCrossRefPubMedGoogle Scholar
  11. Deo S, Patel TR, Dzananovic E, Booy EP, Zeid K, McEleney K, Harding SE, McKenna SA (2014) Activation of 2′ 5′-oligoadenylate synthetase by stem loops at the 5′-end of the West Nile virus genome. PLoS One 9:e92545PubMedCentralCrossRefPubMedGoogle Scholar
  12. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA (2004) PDB2PQR: an automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32:W665–W667PubMedCentralCrossRefPubMedGoogle Scholar
  13. Donovan J, Dufner M, Korennykh A (2013) Structural basis for cytosolic double-stranded RNA surveillance by human oligoadenylate synthetase 1. Proc Natl Acad Sci U S A 110:1652–1657PubMedCentralCrossRefPubMedGoogle Scholar
  14. Egea R, Casillas S, Barbadilla A (2008) Standard and generalized McDonald-Kreitman test: a website to detect selection by comparing different classes of DNA sites. Nucleic Acids Res 36:W157–W162PubMedCentralCrossRefPubMedGoogle Scholar
  15. Eisenberg D, Luthy R, Bowie JU (1997) VERIFY3D: assessment of protein models with three-dimensional profiles. Methods Enzymol 277:396–404CrossRefPubMedGoogle Scholar
  16. Ferguson B, Street SL, Wright H, Pearson C, Jia Y, Thompson SL, Allibone P, Dubay CJ, Spindel E, Norgren RB Jr (2007) Single nucleotide polymorphisms (SNPs) distinguish Indian-origin and Chinese-origin rhesus macaques (Macaca mulatta). BMC Genomics 8:43PubMedCentralCrossRefPubMedGoogle Scholar
  17. Ferguson W, Dvora S, Gallo J, Orth A, Boissinot S (2008) Long-term balancing selection at the West Nile virus resistance gene, Oas1b, maintains transspecific polymorphisms in the house mouse. Mol Biol Evol 25:1609–1618PubMedCentralCrossRefPubMedGoogle Scholar
  18. Ferguson W, Dvora S, Fikes RW, Stone AC, Boissinot S (2012) Long-term balancing selection at the antiviral gene OAS1 in Central African chimpanzees. Mol Biol Evol 29:1093–1103PubMedCentralCrossRefPubMedGoogle Scholar
  19. Ferrer-Admetlla A, Bosch E, Sikora M, Marques-Bonet T, Ramirez-Soriano A, Muntasell A, Navarro A, Lazarus R, Calafell F, Bertranpetit J, Casals F (2008) Balancing selection is the main force shaping the evolution of innate immunity genes. J Immunol 181:1315–1322CrossRefPubMedGoogle Scholar
  20. Fischer MC, Foll M, Heckel G, Excoffier L (2014) Continental-scale footprint of balancing and positive selection in a small rodent (Microtus arvalis). PLoS One 9:e112332PubMedCentralCrossRefPubMedGoogle Scholar
  21. Fumagalli M, Sironi M (2014) Human genome variability, natural selection and infectious diseases. Curr Opin Immunol 30:9–16CrossRefPubMedGoogle Scholar
  22. Garrigan D, Hedrick PW (2003) Perspective: detecting adaptive molecular polymorphism: lessons from the MHC. Evolution 57:1707–1722CrossRefPubMedGoogle Scholar
  23. Goodbourn S, Didcock L, Randall RE (2000) Interferons: cell signalling, immune modulation, antiviral response and virus countermeasures. J Gen Virol 81:2341–2364PubMedGoogle Scholar
  24. Hamano E, Hijikata M, Itoyama S, Quy T, Phi NC, Long HT, Ha LD, Ban VV, Matsushita I, Yanai H, Kirikae F, Kirikae T, Kuratsuji T, Sasazuki T, Keicho N (2005) Polymorphisms of interferon-inducible genes OAS-1 and MxA associated with SARS in the Vietnamese population. Biochem Biophys Res Commun 329:1234–1239CrossRefPubMedGoogle Scholar
  25. Hartmann R, Norby PL, Martensen PM, Jorgensen P, James MC, Jacobsen C, Moestrup SK, Clemens MJ, Justesen J (1998) Activation of 2′-5′ oligoadenylate synthetase by single-stranded and double-stranded RNA aptamers. J Biol Chem 273:3236–3246CrossRefPubMedGoogle Scholar
  26. Hartmann R, Justesen J, Sarkar SN, Sen GC, Yee VC (2003) Crystal structure of the 2′-specific and double-stranded RNA-activated interferon-induced antiviral protein 2′-5′-oligoadenylate synthetase. Mol Cell 12:1173–1185CrossRefPubMedGoogle Scholar
  27. He J, Feng D, de Vlas SJ, Wang H, Fontanet A, Zhang P, Plancoulaine S, Tang F, Zhan L, Yang H, Wang T, Richardus JH, Habbema JD, Cao W (2006) Association of SARS susceptibility with single nucleic acid polymorphisms of OAS1 and MxA genes: a case–control study. BMC Infect Dis 6:106PubMedCentralCrossRefPubMedGoogle Scholar
  28. Hedrick PW (2010) Genetics of populations, 4th edn. Jones and Bartlett, BostonGoogle Scholar
  29. Hernandez RD, Hubisz MJ, Wheeler DA, Smith DG, Ferguson B, Rogers J, Nazareth L, Indap A, Bourquin T, McPherson J, Muzny D, Gibbs R, Nielsen R, Bustamante CD (2007) Demographic histories and patterns of linkage disequilibrium in Chinese and Indian rhesus macaques. Science 316:240–243CrossRefPubMedGoogle Scholar
  30. Hovanessian AG (2007) On the discovery of interferon-inducible, double-stranded RNA activated enzymes: the 2′-5′oligoadenylate synthetases and the protein kinase PKR. Cytokine Growth Factor Rev 18:351–361CrossRefPubMedGoogle Scholar
  31. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164PubMedCentralPubMedGoogle Scholar
  32. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159PubMedCentralPubMedGoogle Scholar
  33. Justesen J, Hartmann R, Kjeldgaard NO (2000) Gene structure and function of the 2′-5′-oligoadenylate synthetase family. Cell Mol Life Sci 57:1593–1612CrossRefPubMedGoogle Scholar
  34. Key FM, Teixeira JC, de Filippo C, Andres AM (2014) Advantageous diversity maintained by balancing selection in humans. Curr Opin Genet Dev 29:45–51CrossRefPubMedGoogle Scholar
  35. Klein J, Satta Y, O’HUigin C, Takahata N (1993) The molecular descent of the major histocompatibility complex. Annu Rev Immunol 11:269–295CrossRefPubMedGoogle Scholar
  36. Knapp S, Yee LJ, Frodsham AJ, Hennig BJ, Hellier S, Zhang L, Wright M, Chiaramonte M, Graves M, Thomas HC, Hill AV, Thursz MR (2003) Polymorphisms in interferon-induced genes and the outcome of hepatitis C virus infection: roles of MxA, OAS-1 and PKR. Genes Immun 4:411–419CrossRefPubMedGoogle Scholar
  37. Kodym R, Kodym E, Story MD (2009) 2′-5′-Oligoadenylate synthetase is activated by a specific RNA sequence motif. Biochem Biophys Res Commun 388:317–322CrossRefPubMedGoogle Scholar
  38. Kumar S, Mitnik C, Valente G, Floyd-Smith G (2000) Expansion and molecular evolution of the interferon-induced 2′-5′ oligoadenylate synthetase gene family. Mol Biol Evol 17:738–750CrossRefPubMedGoogle Scholar
  39. Lawlor DA, Ward FE, Ennis PD, Jackson AP, Parham P (1988) HLA-A and B polymorphisms predate the divergence of humans and chimpanzees. Nature 335:268–271CrossRefPubMedGoogle Scholar
  40. Leffler EM, Gao Z, Pfeifer S, Segurel L, Auton A, Venn O, Bowden R, Bontrop R, Wall JD, Sella G, Donnelly P, McVean G, Przeworski M (2013) Multiple instances of ancient balancing selection shared between humans and chimpanzees. Science 339:1578–1582PubMedCentralCrossRefPubMedGoogle Scholar
  41. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefPubMedGoogle Scholar
  42. Lim JK, Lisco A, McDermott DH, Huynh L, Ward JM, Johnson B, Johnson H, Pape J, Foster GA, Krysztof D, Follmann D, Stramer SL, Margolis LB, Murphy PM (2009) Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man. PLoS Pathog 5:e1000321PubMedCentralCrossRefPubMedGoogle Scholar
  43. Mayer WE, Jonker M, Klein D, Ivanyi P, van Seventer G, Klein J (1988) Nucleotide sequences of chimpanzee MHC class I alleles: evidence for trans-species mode of evolution. EMBO J 7:2765–2774PubMedCentralPubMedGoogle Scholar
  44. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654CrossRefPubMedGoogle Scholar
  45. Mendez FL, Watkins JC, Hammer MF (2012) Global genetic variation at OAS1 provides evidence of archaic admixture in Melanesian populations. Mol Biol Evol 29:1513–1520CrossRefPubMedGoogle Scholar
  46. Mendez FL, Watkins JC, Hammer MF (2013) Neandertal origin of genetic variation at the cluster of OAS immunity genes. Mol Biol Evol 30:798–801CrossRefPubMedGoogle Scholar
  47. Misra A, Thippeshappa R, Kimata JT (2013) Macaques as model hosts for studies of HIV-1 infection. Front Microbiol 4:176PubMedCentralPubMedGoogle Scholar
  48. Mozzi A, Pontremoli C, Forni D, Clerici M, Pozzoli U, Bresolin N, Cagliani R, Sironi M (2015) OASes and STING: adaptive evolution in concert. Genome Biol EvolGoogle Scholar
  49. Osada N, Hashimoto K, Kameoka Y, Hirata M, Tanuma R, Uno Y, Inoue I, Hida M, Suzuki Y, Sugano S, Terao K, Kusuda J, Takahashi I (2008) Large-scale analysis of Macaca fascicularis transcripts and inference of genetic divergence between M. fascicularis and M. mulatta. BMC Genomics 9:90PubMedCentralCrossRefPubMedGoogle Scholar
  50. Osada N, Uno Y, Mineta K, Kameoka Y, Takahashi I, Terao K (2010) Ancient genome-wide admixture extends beyond the current hybrid zone between Macaca fascicularis and M. mulatta. Mol Ecol 19:2884–2895CrossRefPubMedGoogle Scholar
  51. Palermo RE, Tisoncik-Go J, Korth MJ, Katze MG (2013) Old world monkeys and new age science: the evolution of nonhuman primate systems virology. ILAR J 54:166–180PubMedCentralCrossRefPubMedGoogle Scholar
  52. Rand DM, Kann LM (1996) Excess amino acid polymorphism in mitochondrial DNA: contrasts among genes from Drosophila, mice, and humans. Mol Biol Evol 13:735–748CrossRefPubMedGoogle Scholar
  53. Rebouillat D, Hovanessian AG (1999) The human 2′,5′-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. J Interferon Cytokine Res 19:295–308CrossRefPubMedGoogle Scholar
  54. Silverman RH (2007) Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J Virol 81:12720–12729PubMedCentralCrossRefPubMedGoogle Scholar
  55. Sippl MJ (1993) Recognition of errors in three-dimensional structures of proteins. Proteins 17:355–362CrossRefPubMedGoogle Scholar
  56. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing-data imputation. Am J Hum Genet 76:449–462PubMedCentralCrossRefPubMedGoogle Scholar
  57. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989PubMedCentralCrossRefPubMedGoogle Scholar
  58. Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedCentralPubMedGoogle Scholar
  59. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralCrossRefPubMedGoogle Scholar
  60. Vachon VK, Calderon BM, Conn GL (2015) A novel RNA molecular signature for activation of 2′-5′ oligoadenylate synthetase-1. Nucleic Acids Res 43:544–552PubMedCentralCrossRefPubMedGoogle Scholar
  61. Valdes I, Gil L, Castro J, Odoyo D, Hitler R, Munene E, Romero Y, Ochola L, Cosme K, Kariuki T, Guillen G, Hermida L (2013) Olive baboons: a non-human primate model for testing dengue virus type 2 replication. Int J Infect Dis 17:e1176–e1181CrossRefPubMedGoogle Scholar
  62. Wiederstein M, Sippl MJ (2007) ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res 35:W407–W410PubMedCentralCrossRefPubMedGoogle Scholar
  63. Wolf RF, Papin JF, Hines-Boykin R, Chavez-Suarez M, White GL, Sakalian M, Dittmer DP (2006) Baboon model for West Nile virus infection and vaccine evaluation. Virology 355:44–51CrossRefPubMedGoogle Scholar
  64. Zhao Y, Kang H, Ji Y, Chen X (2013) Evaluate the relationship between polymorphisms of OAS1 gene and susceptibility to chronic hepatitis C with high resolution melting analysis. Clin Exp Med 13:171–176CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  1. 1.Biology Department, Queens Collegethe City University of New YorkFlushingUSA
  2. 2.Graduate Centerthe City University of New YorkNew YorkUSA
  3. 3.New York University Abu DhabiAbu DhabiUAE

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