Functional evolution of the OAS1 viral sensor: Insights from old world primates

Infection, Genetics and Evolution

Volumn 44, Issue , 2016, Pages 341-350

  Fish, Ian ^a,b   Boissinot, Stéphane ^c  

^a CITY UNIVERSITY OF NEW YORK   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

^c NEW YORK UNIVERSITY ABU DHABI   (United Arab Emirates)

Author keywords

Cercopithecidae; dsRNA sensor; Immune system evolution; Innate immunity; OAS1; Positive selection

Indexed keywords

DOUBLE STRANDED RNA; OLIGOADENYLATE SYNTHETASE 1; RIBONUCLEASE L; SYNTHETASE; UNCLASSIFIED DRUG; 2',5' OLIGOADENYLATE SYNTHETASE;

ADAPTIVE IMMUNITY; ARTICLE; BETA SHEET; CERCOPITHECIDAE; CODON; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVE SITE; GENE; GENE EXPRESSION REGULATION; GENETIC SELECTION; GENETIC VARIATION; IMMUNE EVASION; INNATE IMMUNITY; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OAS1 GENE; PHYLOGENETIC TREE; POSITIVE SELECTION; PRIMATE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; PURIFYING SELECTION; RNA BINDING DOMAIN; RNA DEGRADATION; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION; UPREGULATION; VIRAL ANTAGONISM; VIRAL PHENOMENA AND FUNCTIONS; VIRUS CELL INTERACTION; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; DISEASE RESISTANCE; DNA SEQUENCE; EVOLUTION; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MOLECULAR MODEL; PHYLOGENY; PROTEIN CONFORMATION; RNA-BINDING DOMAIN; VIROLOGY; VIRUS INFECTION;

2',5'-OLIGOADENYLATE SYNTHETASE; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; BIOLOGICAL EVOLUTION; CATALYTIC DOMAIN; CERCOPITHECIDAE; DISEASE RESISTANCE; EVOLUTION, MOLECULAR; GENETIC VARIATION; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; MODELS, MOLECULAR; PHYLOGENY; PROTEIN CONFORMATION; RNA, DOUBLE-STRANDED; RNA-BINDING MOTIFS; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; VIRUS DISEASES;

EID: 84980361811     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2016.07.005     Document Type: Article

References (61)

1. Adzhubei, I.A., Schmidt, S., Peshkin, L., Ramensky, V.E., Gerasimova, A., Bork, P., Kondrashov, A.S., Sunyaev, S.R., A method and server for predicting damaging missense mutations. Nat. Methods 7 (2010), 248–249, 10.1038/nmeth0410-248.
2. Alagarasu, K., Honap, T., Damle, I.M., Mulay, A.P., Shah, P.S., Cecilia, D., Polymorphisms in the oligoadenylate synthetase gene cluster and its association with clinical outcomes of dengue virus infection. Infect. Genet. Evol. 14 (2013), 390–395, 10.1016/j.meegid.2012.12.021.
3. Arnold, K., Bordoli, L., Kopp, J., Schwede, T., The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 (2006), 195–201, 10.1093/bioinformatics/bti770.
4. Behera, A.K., Kumar, M., Lockey, R.F., Mohapatra, S.S., 2′-5′ Oligoadenylate synthetase plays a critical role in interferon-gamma inhibition of respiratory syncytial virus infection of human epithelial cells. J. Biol. Chem. 277 (2002), 25601–25608, 10.1074/jbc.M200211200.
5. Bonnevie-Nielsen, V., Field, L.L., Lu, S., Zheng, D.J., Li, M., Martensen, P.M., Nielsen, T.B., Beck-Nielsen, H., Lau, Y.L., Pociot, F., Variation in antiviral 2′,5′-oligoadenylate synthetase (2′5′AS) enzyme activity is controlled by a single-nucleotide polymorphism at a splice-acceptor site in the OAS1 gene. Am. J. Hum. Genet. 76 (2005), 623–633, 10.1086/429391.
6. Bordoli, L., Kiefer, F., Arnold, K., Benkert, P., Battey, J., Schwede, T., Protein structure homology modeling using SWISS-MODEL workspace. Nat. Protoc. 4 (2009), 1–13, 10.1038/nprot.2008.197.
7. Cai, Y., Chen, Q., Zhou, W., Chu, C., Ji, W., Ding, Y., Xu, J., Ji, Z., You, H., Wang, J., Association analysis of polymorphisms in OAS1 with susceptibility and severity of hand, foot and mouth disease. Int. J. Immunogenet. 41 (2014), 384–392, 10.1111/iji.12134.
8. Daugherty, M.D., Malik, H.S., Rules of engagement: molecular insights from host-virus arms races. Annu. Rev. Genet. 46 (2012), 677–700, 10.1146/annurev-genet-110711-155522.
9. Delport, W., Scheffler, K., Seoighe, C., Frequent toggling between alternative amino acids is driven by selection in HIV-1. PLoS Pathog., 4, 2008, e1000242, 10.1371/journal.ppat.1000242.
10. Delport, W., Poon, A.F., Frost, S.D., Kosakovsky Pond, S.L., Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 26 (2010), 2455–2457, 10.1093/bioinformatics/btq429.
11. Delport, W., Scheffler, K., Botha, G., Gravenor, M.B., Muse, S.V., Kosakovsky Pond, S.L., CodonTest: modeling amino acid substitution preferences in coding sequences. PLoS Comput. Biol., 6, 2010, 10.1371/journal.pcbi.1000885.
12. Donovan, J., Dufner, M., Korennykh, A., Structural basis for cytosolic double-stranded RNA surveillance by human oligoadenylate synthetase 1. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 1652–1657, 10.1073/pnas.1218528110.
13. Donovan, J., Whitney, G., Rath, S., Korennykh, A., Structural mechanism of sensing long dsRNA via a noncatalytic domain in human oligoadenylate synthetase 3. Proc. Natl. Acad. Sci. U. S. A. 112 (2015), 3949–3954, 10.1073/pnas.1419409112.
14. Doron-Faigenboim, A., Pupko, T., A combined empirical and mechanistic codon model. Mol. Biol. Evol. 24 (2007), 388–397, 10.1093/molbev/msl175.
15. Doron-Faigenboim, A., Stern, A., Mayrose, I., Bacharach, E., Pupko, T., Selecton: a server for detecting evolutionary forces at a single amino-acid site. Bioinformatics 21 (2005), 2101–2103, 10.1093/bioinformatics/bti259.
16. Drappier, M., Michiels, T., Inhibition of the OAS/RNase L pathway by viruses. Curr. Opin. Virol. 15 (2015), 19–26, 10.1016/j.coviro.2015.07.002.
17. Ferguson, W., Dvora, S., Gallo, J., Orth, A., Boissinot, S., Long-term balancing selection at the west Nile virus resistance gene, Oas1b, maintains transspecific polymorphisms in the house mouse. Mol. Biol. Evol. 25 (2008), 1609–1618, 10.1093/molbev/msn106.
18. Ferguson, W., Dvora, S., Fikes, R.W., Stone, A.C., Boissinot, S., Long-term balancing selection at the antiviral gene OAS1 in Central African chimpanzees. Mol. Biol. Evol. 29 (2012), 1093–1103, 10.1093/molbev/msr247.
19. Fish, I., Boissinot, S., Contrasted patterns of variation and evolutionary convergence at the antiviral OAS1 gene in old world primates. Immunogenetics 67 (2015), 487–499, 10.1007/s00251-015-0855-0.
20. Ghosh, A., Sarkar, S.N., Guo, W., Bandyopadhyay, S., Sen, G.C., Enzymatic activity of 2′-5′-oligoadenylate synthetase is impaired by specific mutations that affect oligomerization of the protein. J. Biol. Chem. 272 (1997), 33220–33226.
21. Gokhale, N.S., Vazquez, C., Horner, S.M., Hepatitis C Virus. Strategies to evade antiviral responses. Futur. Virol. 9 (2014), 1061–1075, 10.2217/fvl.14.89.
22. Han, Y., Whitney, G., Donovan, J., Korennykh, A., Innate immune messenger 2-5A tethers human RNase L into active high-order complexes. Cell Rep. 2 (2012), 902–913, 10.1016/j.celrep.2012.09.004.
23. Hancks, D.C., Hartley, M.K., Hagan, C., Clark, N.L., Elde, N.C., Overlapping patterns of rapid evolution in the nucleic acid sensors cGAS and OAS1 suggest a common mechanism of pathogen antagonism and escape. PLoS Genet., 11, 2015, e1005203, 10.1371/journal.pgen.1005203.
24. Hartmann, R., Justesen, J., Sarkar, S.N., Sen, G.C., Yee, V.C., Crystal structure of the 2′-specific and double-stranded RNA-activated interferon-induced antiviral protein 2′-5′-oligoadenylate synthetase. Mol. Cell 12 (2003), 1173–1185.
25. Hasegawa, M., Kishino, H., Yano, T., Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22 (1985), 160–174.
26. Huang, H., Zeqiraj, E., Dong, B., Jha, B.K., Duffy, N.M., Orlicky, S., Thevakumaran, N., Talukdar, M., Pillon, M.C., Ceccarelli, D.F., Wan, L.C., Juang, Y.C., Mao, D.Y., Gaughan, C., Brinton, M.A., Perelygin, A.A., Kourinov, I., Guarne, A., Silverman, R.H., Sicheri, F., Dimeric structure of pseudokinase RNase L bound to 2-5A reveals a basis for interferon-induced antiviral activity. Mol. Cell 53 (2014), 221–234, 10.1016/j.molcel.2013.12.025.
27. Ibsen, M.S., Gad, H.H., Thavachelvam, K., Boesen, T., Despres, P., Hartmann, R., The 2′-5′-oligoadenylate synthetase 3 enzyme potently synthesizes the 2′-5′-oligoadenylates required for RNase L activation. J. Virol. 88 (2014), 14222–14231, 10.1128/JVI.01763-14.
28. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., Drummond, A., Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28 (2012), 1647–1649, 10.1093/bioinformatics/bts199.
29. Kodym, R., Kodym, E., Story, M.D., 2′-5′-Oligoadenylate synthetase is activated by a specific RNA sequence motif. Biochem. Biophys. Res. Commun. 388 (2009), 317–322, 10.1016/j.bbrc.2009.07.167.
30. Kosakovsky Pond, S.L., Frost, S.D., Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 22 (2005), 1208–1222, 10.1093/molbev/msi105.
31. Krieger, E., Joo, K., Lee, J., Lee, J., Raman, S., Thompson, J., Tyka, M., Baker, D., Karplus, K., Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 77:Suppl. 9 (2009), 114–122, 10.1002/prot.22570.
32. Lim, J.K., Lisco, A., McDermott, D.H., Huynh, L., Ward, J.M., Johnson, B., Johnson, H., Pape, J., Foster, G.A., Krysztof, D., Follmann, D., Stramer, S.L., Margolis, L.B., Murphy, P.M., Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man. PLoS Pathog., 5, 2009, e1000321, 10.1371/journal.ppat.1000321.
33. Lohofener, J., Steinke, N., Kay-Fedorov, P., Baruch, P., Nikulin, A., Tishchenko, S., Manstein, D.J., Fedorov, R., The activation mechanism of 2′-5′-oligoadenylate synthetase gives new insights into OAS/cGAS triggers of innate immunity. Structure 23 (2015), 851–862, 10.1016/j.str.2015.03.012.
34. Marie, I., Blanco, J., Rebouillat, D., Hovanessian, A.G., 69-kDa and 100-kDa isoforms of interferon-induced (2′-5′)oligoadenylate synthetase exhibit differential catalytic parameters. Eur. J. Biochem. 248 (1997), 558–566.
35. Mashimo, T., Lucas, M., Simon-Chazottes, D., Frenkiel, M.P., Montagutelli, X., Ceccaldi, P.E., Deubel, V., Guenet, J.L., Despres, P., 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. U. S. A. 99 (2002), 11311–11316, 10.1073/pnas.172195399.
36. Maurer-Stroh, S., Eisenhaber, F., Refinement and prediction of protein prenylation motifs. Genome Biol., 6, 2005, R55, 10.1186/gb-2005-6-6-r55.
37. Mendez, F.L., Watkins, J.C., Hammer, M.F., Global genetic variation at OAS1 provides evidence of archaic admixture in Melanesian populations. Mol. Biol. Evol. 29 (2012), 1513–1520, 10.1093/molbev/msr301.
38. Mendez, F.L., Watkins, J.C., Hammer, M.F., Neandertal origin of genetic variation at the cluster of OAS immunity genes. Mol. Biol. Evol. 30 (2013), 798–801, 10.1093/molbev/mst004.
39. Minin, V.N., Dorman, K.S., Fang, F., Suchard, M.A., Dual multiple change-point model leads to more accurate recombination detection. Bioinformatics 21 (2005), 3034–3042, 10.1093/bioinformatics/bti459.
40. Morin, B., Rabah, N., Boretto-Soler, J., Tolou, H., Alvarez, K., Canard, B., High yield synthesis, purification and characterisation of the RNase L activators 5′-triphosphate 2′-5′-oligoadenylates. Antivir. Res. 87 (2010), 345–352, 10.1016/j.antiviral.2010.06.003.
41. Mozzi, A., Pontremoli, C., Forni, D., Clerici, M., Pozzoli, U., Bresolin, N., Cagliani, R., Sironi, M., OASes and STING: adaptive evolution in concert. Genome Biol. Evol., 2015, 10.1093/gbe/evv046.
42. Murrell, B., Wertheim, J.O., Moola, S., Weighill, T., Scheffler, K., Kosakovsky Pond, S.L., Detecting individual sites subject to episodic diversifying selection. PLoS Genet., 8, 2012, e1002764, 10.1371/journal.pgen.1002764.
43. Perelman, P., Johnson, W.E., Roos, C., Seuanez, H.N., Horvath, J.E., Moreira, M.A., Kessing, B., Pontius, J., Roelke, M., Rumpler, Y., Schneider, M.P., Silva, A., O'Brien, S.J., Pecon-Slattery, J., A molecular phylogeny of living primates. PLoS Genet., 7, 2011, e1001342, 10.1371/journal.pgen.1001342.
44. Perelygin, A.A., Zharkikh, A.A., Scherbik, S.V., Brinton, M.A., The mammalian 2′-5′ oligoadenylate synthetase gene family: evidence for concerted evolution of paralogous Oas1 genes in Rodentia and Artiodactyla. J. Mol. Evol. 63 (2006), 562–576, 10.1007/s00239-006-0073-3.
45. Pond, S.L., Frost, S.D., Muse, S.V., HyPhy: hypothesis testing using phylogenies. Bioinformatics 21 (2005), 676–679, 10.1093/bioinformatics/bti079.
46. Pupko, T., Pe'er, I., Shamir, R., Graur, D., A fast algorithm for joint reconstruction of ancestral amino acid sequences. Mol. Biol. Evol. 17 (2000), 890–896.
47. Quintana-Murci, L., Alcais, A., Abel, L., Casanova, J.L., Immunology in natura: clinical, epidemiological and evolutionary genetics of infectious diseases. Nat. Immunol. 8 (2007), 1165–1171, 10.1038/ni1535.
48. Rausell, A., Telenti, A., Genomics of host-pathogen interactions. Curr. Opin. Immunol. 30 (2014), 32–38, 10.1016/j.coi.2014.06.001.
49. Rebouillat, D., Hovnanian, A., Marie, I., Hovanessian, A.G., The 100-kDa 2′,5′-oligoadenylate synthetase catalyzing preferentially the synthesis of dimeric pppA2′p5′A molecules is composed of three homologous domains. J. Biol. Chem. 274 (1999), 1557–1565.
50. Sanchez, R., Mohr, I., Inhibition of cellular 2′-5′ oligoadenylate synthetase by the herpes simplex virus type 1 Us11 protein. J. Virol. 81 (2007), 3455–3464, 10.1128/JVI.02520-06.
51. Sharp, T.V., Moonan, F., Romashko, A., Joshi, B., Barber, G.N., Jagus, R., The vaccinia virus E3L gene product interacts with both the regulatory and the substrate binding regions of PKR: implications for PKR autoregulation. Virology 250 (1998), 302–315, 10.1006/viro.1998.9365.
52. Silverman, R.H., Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81 (2007), 12720–12729, 10.1128/JVI.01471-07.
53. Sippl, M.J., Recognition of errors in three-dimensional structures of proteins. Proteins 17 (1993), 355–362, 10.1002/prot.340170404.
54. Stern, A., Doron-Faigenboim, A., Erez, E., Martz, E., Bacharach, E., Pupko, T., Selecton 2007: advanced models for detecting positive and purifying selection using a Bayesian inference approach. Nucleic Acids Res. 35 (2007), W506–W511, 10.1093/nar/gkm382.
55. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., Kumar, S., MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28 (2011), 2731–2739, 10.1093/molbev/msr121.
56. The PyMOL Molecular Graphics System, Version 1.5.0.4: Schrödinger, LLC. 2010.
57. Torshin, I.Y., Three-dimensional models of human 2′-5′ oligoadenylate synthetases: a new computational method for reconstructing an enzyme assembly. Med. Sci. Monit. 11 (2005), BR235–BR247.
58. Whelan, S., Goldman, N., A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 18 (2001), 691–699.
59. Wiederstein, M., Sippl, M.J., ProSA-web: interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 35 (2007), W407–W410, 10.1093/nar/gkm290.
60. Yang, Z., Kumar, S., Nei, M., A new method of inference of ancestral nucleotide and amino acid sequences. Genetics 141 (1995), 1641–1650.
61. Zinzula, L., Tramontano, E., Strategies of highly pathogenic RNA viruses to block dsRNA detection by RIG-I-like receptors: hide, mask, hit. Antivir. Res. 100 (2013), 615–635, 10.1016/j.antiviral.2013.10.002.