Intronless and intron-containing type I IFN genes coexist in amphibian Xenopus tropicalis: Insights into the origin and evolution of type I IFNs in vertebrates

Developmental and Comparative Immunology

Volumn 67, Issue , 2017, Pages 166-176

  Gan, Zhen ^a,b   Chen, Shan Nan ^a   Huang, Bei ^c   Hou, Jing ^a,b   Nie, Pin ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c JIMEI UNIVERSITY   (China)

Author keywords

Intron containing type I IFN; Intronless type I IFN; Retroposition event; Type I IFN; Xenopus tropicalis

Indexed keywords

ARTICLE; CONTROLLED STUDY; GENE; GENE EXPRESSION PROFILING; IFN5 GENE; IFNI1.2 GENE; IFNI2.1 GENE; IFNI3.1 GENE; INTRON; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SYNTENY; XENOPUS TROPICALIS; ANIMAL; BIOLOGICAL MODEL; EVOLUTION; GENETIC RECOMBINATION; GENETICS; IMMUNOLOGY; RETROPOSON; XENOPUS;

AMPHIBIAN PROTEIN; INTERFERON; TRANSCRIPTOME;

AMPHIBIAN PROTEINS; ANIMALS; BIOLOGICAL EVOLUTION; EVOLUTION, MOLECULAR; INTERFERON TYPE I; INTRONS; MODELS, BIOLOGICAL; PHYLOGENY; RECOMBINATION, GENETIC; RETROELEMENTS; TRANSCRIPTOME; XENOPUS;

EID: 84998631726     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2016.10.007     Document Type: Article

References (38)

1. Abascal, F., Zardoya, R., Posada, D., ProtTest: selection of best-fit models of protein evolution. Bioinformatics 21 (2005), 2104–2105.
2. Chaves-Pozo, E., Zou, J., Secombes, C.J., Cuesta, A., Tafalla, C., The rainbow trout (Oncorhynchus mykiss) interferon response in the ovary. Mol. Immunol. 47 (2010), 1757–1764.
3. Chen, Q., Ma, J., Fan, Y., Meng, Y., Xu, J., Zhou, Y., Liu, W., Zeng, X., Zeng, L., Identification of type I IFN in Chinese giant salamander (Andrias davidianus) and the response to an iridovirus infection. Mol. Immunol. 65 (2015), 350–359.
4. Chen, S.N., Zhang, X.W., Li, L., Ruan, B.Y., Huang, B., Huang, W.S., Zou, P.F., Fu, J.P., Zhao, L.J., Li, N., Nie, P., Evolution of IFN-λ in tetrapod vertebrates and its functional characterization in green anole lizard (Anolis carolinensis). Dev. Comp. Immunol. 61 (2016), 208–224.
5. Fung, K.Y., Mangan, N.E., Cumming, H., Horvat, J.C., Mayall, J.R., Stifter, S.A., De Weerd, N., Roisman, L.C., Rossjohn, J., Robertson, S.A., Schjenken, J.E., Parker, B., Gargett, C.E., Nguyen, H.P., Carr, D.J., Hansbro, P.M., Hertzog, P.J., Interferon-epsilon protects the female reproductive tract from viral and bacterial infection. Science 339 (2013), 1088–1092.
6. Goossens, K.E., Ward, A.C., Lowenthal, J.W., Bean, A.G., Chicken interferons, their receptors and interferon-stimulated genes. Dev. Comp. Immunol. 41 (2013), 370–376.
7. Grayfer, L., De Jesus Andino, F., Robert, J., The amphibian (Xenopus laevis) type I interferon response to frog virus 3: new insight into ranavirus pathogenicity. J. Virol. 88 (2014), 5766–5777.
8. Hellsten, U., Harland, R.M., Gilchrist, M.J., Hendrix, D., Jurka, J., Kapitonov, V., Ovcharenko, I., Putnam, N.H., Shu, S., Taher, L., Blitz, I.L., Blumberg, B., Dichmann, D.S., Dubchak, I., Amaya, E., Detter, J.C., Fletcher, R., Gerhard, D.S., Goodstein, D., Graves, T., Grigoriev, I.V., Grimwood, J., Kawashima, T., Lindquist, E., Lucas, S.M., Mead, P.E., Mitros, T., Ogino, H., Ohta, Y., Poliakov, A.V., Pollet, N., Robert, J., Salamov, A., Sater, A.K., Schmutz, J., Terry, A., Vize, P.D., Warren, W.C., Wells, D., Wills, A., Wilson, R.K., Zimmerman, L.B., Zorn, A.M., Grainger, R., Grammer, T., Khokha, M.K., Richardson, P.M., Rokhsar, D.S., The genome of the Western clawed frog Xenopus tropicalis. Science 328 (2010), 633–636.
9. Kaessmann, H., Origins, evolution, and phenotypic impact of new genes. Genome Res. 20 (2010), 1313–1326.
10. Karpusas, M., Nolte, M., Benton, C.B., Meier, W., Lipscomb, W.N., Goelz, S., The crystal structure of human interferon beta at 2.2-A resolution. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 11813–11818.
11. Karpusas, M., Whitty, A., Runkel, L., Hochman, P., The structure of human interferon-beta: implications for activity. Cell Mol. Life Sci. 54 (1998), 1203–1216.
12. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., Thompson, J.D., Gibson, T.J., Higgins, D.G., Clustal W and clustal X version 2.0. Bioinformatics 23 (2007), 2947–2948.
13. Lazear, H.M., Nice, T.J., Diamond, M.S., Interferon-lambda: immune functions at barrier surfaces and beyond. Immunity 43 (2015), 15–28.
14. −ΔΔCt method. Methods 25 (2001), 402–408.
15. Marie, I., Durbin, J.E., Levy, D.E., Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17 (1998), 6660–6669.
16. O'Shea, J.J., Plenge, R., JAK and STAT signaling molecules in immunoregulation and immune-mediated disease. Immunity 36 (2012), 542–550.
17. Pestka, S., Krause, C.D., Walter, M.R., Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 202 (2004), 8–32.
18. Platanias, L.C., Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5 (2005), 375–386.
19. Qi, Z., Nie, P., Secombes, C.J., Zou, J., Intron-containing type I and type III IFN coexist in amphibians: refuting the concept that a retroposition event gave rise to type I IFNs. J. Immunol. 184 (2010), 5038–5046.
20. Radhakrishnan, R., Walter, L.J., Hruza, A., Reichert, P., Trotta, P.P., Nagabhushan, T.L., Walter, M.R., Zinc mediated dimer of human interferon-alpha 2b revealed by X-ray crystallography. Structure 4 (1996), 1453–1463.
21. Roelants, K., Gower, D.J., Wilkinson, M., Loader, S.P., Biju, S.D., Guillaume, K., Moriau, L., Bossuyt, F., Global patterns of diversification in the history of modern amphibians. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 887–892.
22. Ronquist, F., Huelsenbeck, J.P., MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003), 1572–1574.
23. Sadler, A.J., Williams, B.R., Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8 (2008), 559–568.
24. Sang, Y., Bergkamp, J., Blecha, F., Molecular evolution of the porcine type I interferon family: subtype-specific expression and antiviral activity. PLoS One, 9, 2014, e112378.
25. Sang, Y., Liu, Q., Lee, J., Ma, W., McVey, D.S., Blecha, F., Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity. Sci. Rep., 6, 2016, 29072, 10.1038/srep29072.
26. Sato, M., Suemori, H., Hata, N., Asagiri, M., Ogasawara, K., Nakao, K., Nakaya, T., Katsuki, M., Noguchi, S., Tanaka, N., Taniguchi, T., Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13 (2000), 539–548.
27. Schindler, C., Levy, D.E., Decker, T., JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282 (2007), 20059–20063.
28. Schoenborn, J.R., Wilson, C.B., Regulation of interferon-gamma during innate and adaptive immune responses. Adv. Immunol. 96 (2007), 41–101.
29. Schoggins, J.W., Wilson, S.J., Panis, M., Murphy, M.Y., Jones, C.T., Bieniasz, P., Rice, C.M., A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472 (2011), 481–485.
30. Stark, G.R., Darnell, J.E. Jr., The JAK-STAT pathway at twenty. Immunity 36 (2012), 503–514.
31. 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.
32. Teijaro, J.R., Type I interferons in viral control and immune regulation. Curr. Opin. Virol. 16 (2016), 31–40.
33. Valero, Y., Morcillo, P., Meseguer, J., Buonocore, F., Esteban, M.A., Chaves-Pozo, E., Cuesta, A., Characterization of the IFN pathway in the teleost fish gonad against vertically transmitted viral nervous necrosis virus. J. Gen. Virol. 96 (2015), 2176–2187.
34. Voss, S.R., Kump, D.K., Putta, S., Pauly, N., Reynolds, A., Henry, R.J., Basa, S., Walker, J.A., Smith, J.J., Origin of amphibian and avian chromosomes by fission, fusion, and retention of ancestral chromosomes. Genome Res. 21 (2011), 1306–1312.
35. Wetzel, R., Assignment of the disulphide bonds of leukocyte interferon. Nature 289 (1981), 606–607.
36. Xu, L., Yang, L., Liu, W., Distinct evolution process among type I interferon in mammals. Protein Cell 4 (2013), 383–392.
37. Zou, J., Secombes, C.J., Teleost fish interferons and their role in immunity. Dev. Comp. Immunol. 35 (2011), 1376–1387.
38. Zou, J., Tafalla, C., Truckle, J., Secombes, C.J., Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J. Immunol. 179 (2007), 3859–3871.