Distinct evolution process among type I interferon in mammals

Abstract

Interferon (IFN) is thought to play an important role in the vertebrate immune system, but systemic knowledge of IFN evolution has yet to be elucidated. To evaluate the phylogenic distribution and evolutionary history of type I IFNs, 13gen omes were searched using BLASTn program, and a phylogenetic tree of vertebrate type I IFNs was constructed. In the present study, an IFNδ-like gene in the human genome was identified, refuting the concept that humans have no IFNδ genes, and other mammalian IFN genes were also identified. In the phylogenetic tree, the mammalian IFNβ, IFN?, and IFNκ formed a clad e sepa rate f rom the other mammalian type I IFNs, while piscine and avian IFNs formed distinct clades. Based on this phylogenetic analysis and the various characteristics of type I IFNs, the evolutionary history of type I IFNs was further evaluated. Our data indicate that an ancestral IFNα-like gene forms a core from which new IFNs divided during vertebrate evolution. In addition, the data suggest how the other type I IFNs evolved from IFNα and shaped the complex type I IFN system. The promoters of type I IFNs were conserved among different mammals, as well as their genic regions. However, the intergenic regions of type I IFN clusters were not conserved among different mammals, demonstrating a high selec tion pressure upon type I IFNs during their evolution.

Keywords

type I IFN / evolutionary history / vertebrate / gene cluster

References

[1] Altmann, S.M., Mellon, M.T., Distel, D.L., and Kim, C.H. (2003). Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol 77, 1992-2002 .10.1128/JVI.77.3.1992-2002.2003
[2] Bazer, F.W., Spencer, T.E., and Ott, T.L. (1997). Interferon tau: A novel pregnancy eecognition signal. Am J Reprod Immunol 37, 412-420 .10.1111/j.1600-0897.1997.tb00253.x
[3] Buhler, J.D., Lancaster, J.M., Jacob, A.C., and Chamberlain, R.D. (2007). Mercury BLASTN: Faster DNA sequence comparison using a streaming hardware architecture. In Reconfigurable Systems Summer Institute, Oxford University Press, Oxford , 1-8 .
[4] Chelmońskasoyta, A. (2002). Interferon tau and its immunobiological role in ruminant reproduction. Arch Immunol Ther Exp 50, 47-52 .
[5] Cochet, M., Vaiman, D., and Lefèvre, F. (2009). Novel interferon delta genes in mammals: Cloning of one gene from the sheep, two genes expressed by the horse conceptus and discovery of related sequences in several taxa by genomic database screening. Gene 433, 88-99 .10.1016/j.gene.2008.11.026
[6] David, M. (2002). Signal tr ansduction by type I interferons. Biotechniques (Suppl) , 58-65 .
[7] Hardy, M.P., Owczarek, C.M., Jermiin, L.S., Ejdeb?ck, M., and Hertzog, P.J. (2004). Characterization of the type I interferon locus and identification of novel genes. Genomics 84, 331-345 .10.1016/j.ygeno.2004.03.003
[8] Harley, I.T.W., Niewold, T.B., Stormont, R.M., Kaufman, K.M., Glenn, S.B., Franek, B.S., Kelly, J.A., Johnson, G.A., Stewart, M.D., Gray, C.A., Choi, Y., Burghardt, R.C., Yu-Lee, L.Y., Bazer, F.W., and Spencer, T.E. (2001). Effects of the estrous cycle, pregnancy, and interferon tau on 2’5’-oligoadenylate synthetase expression in the ovine uterus. Biol Repr 64, 1392-1399 .10.1095/biolreprod64.5.1392
[9] Henco, K., Brosius, J., Fujisawa, A., Fujisawa, J.I., Haynes, J.R., Hochstadt, J., Kovacic, T., Pasek, M., Schambock, A., Schmid, J., . (1985). Structural relationship of human interferon alpha genes and pseudogenes. J Mol Biol 185, 227-260 .10.1016/0022-2836(85)90401-2
[10] Kilpatrick, J.R., Hutchings, D., Divers, J., . (2010). The role of genetic variation near interferon-kappa in systemic lupus erythematosus. J Biomed Biotechnol 2010, 1-11 .
[11] Isaacs, A., and Lindenmann, J. (1957). Virus interference. I. The interferon. Proc Roy Soc B: Biol Sci 147, 258-267 .10.1098/rspb.1957.0048
[12] Lavoie, T.B., Kalie, E., Crisafulli-Cabatu, S., Abramovich, R., DiGioia, G., Moolchan, K., Pestka, S., and Schreiber, G. (2011). Binding and activity of all human alpha interferon subtypes. Cytokine 56, 282-289 .10.1016/j.cyto.2011.07.019
[13] Lefèvre, F., and Boulay, V. (1993). A novel and atypical type one interferon gene expressed by trophoblast during early pregnancy. J Biol Chem 268, 19760-19768 .
[14] Oritani, K., Medina, K.L., Tomiyama, Y. , Ishikawa, J., Okajima, Y., Ogawa, M., Yokota, T., Aoyama, K., Takahashi, I., Kincade, P.W., . (2000). Limitin: An interferon-like cytokine that preferentially infl uences B-lymphocyte precursors. Nat Med 6, 659-666 .10.1038/76233
[15] Pestka, S., Krause, C.D., and Walter, M. R. (2004). Interferons, interferon- like cytokines, and their receptors. Immunol Rev 202, 8-32 .10.1111/j.0105-2896.2004.00204.x
[16] Qi, Z.T., Nie, P., Secombes, C.J., and Zou, J. (2010). 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, 5038-5046 .10.4049/jimmunol.0903374
[17] Qu, H., Yang, L., Meng, S., Xu, L., Bi, Y., Jia, X., Li, J., Sun, L., and Liu, W. (2013). The differential antiviral activities of chicken interferon α (ChIFN-α) and ChIFN-β are related to distinct interferon-stimulated gene expression. PLoS ONE 8, e59307.10.1371/journal.pone.0059307
[18] Roberts, R.M., Liu, L., Guo, Q.T., Leaman, D., and Bixby, J. (1998). The evolution of the type I interferons. J Interferon Cytokine Res 18, 805-816 .10.1089/jir.1998.18.805
[19] Roberts, R.M. (2007). Interferon-tau, a type 1 i nterferon involved in maternal recognition of pregnancy. Cytokine Growth Factor Rev 18, 403-408 .10.1016/j.cytogfr.2007.06.010
[20] Robertsen, B., Bergan, V., R?kenes, T., Larsen, R., and Albuquerque, A. (2003). Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res 23, 601-612 .10.1089/107999003322485107
[21] Sang, Y., Rowland, R.R., Hesse, R.A., and Blecha, F. (2010). Differential expression and activity of the porcine type I interferon family. Physiol Genomics 42, 248-258 .10.1152/physiolgenomics.00198.2009
[22] Schwartz, S., Elnitski, L., Li, M., Weirauch, M., Riemer, C., Smit, A., Program, N.C.S., Green, E.D., Hardison, R.C., and Miller, W. (2003). MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res 31, 3518-3524 .10.1093/nar/gkg579
[23] Sheppard, P., Kindsvogel, W., Xu, W., Henderson, K., Schlutsmeyer, S., Whitmore, T.E., Kuestner, R., Garrigues, U., Birks, C., Roraback, J., . (2003). IL-28, IL-29 and their class II cytokine receptor IL- 28R. Nat Immunol 4, 63-68 .10.1038/ni873
[24] Sick, C., Schultz, U., Münster, U., Meier, J., Kaspers , B., and Staeheli, P. (1998). Promoter structures and differential responses to viral and nonviral inducers of chicken type I interferon genes. J Biol Chem 273, 9749-9754 .10.1074/jbc.273.16.9749
[25] Sick, C., Schultz, U., and Staeheli, P. (1996). A family of genes coding for two serologically distinct chicken interferons. J Biol Chem 271, 7635-7639 .10.1074/jbc.271.13.7635
[26] Stancato, L.F., Sakatsume, M., David, M., Dent, P., Dong, F., Petricoin, E.F., Krolewski, J.J., Silvennoinen, O., Saharinen, P., . (1997). Beta interferon and oncostatin M activate Raf-1 and mitogen-activated protein kinase through a JAK1-dependent pathway. Mol Cell Biol 17, 3833-3840 .
[27] Stark, G.R., Kerr, I.M., Williams, B.R.G., Silverman, R.H. , and Schreiber, R.D. (1998). How cells respond to interferons. Annu Rev Biochem 67, 227-264 .10.1146/annurev.biochem.67.1.227
[28] Sun, B.J., Robertsen, B., Wang, Z.Q., and Liu, B. (2009). I dentification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev Comp Immunol 33, 547-558 .10.1016/j.dci.2008.10.001
[29] Svingerud, T., Solstad, T., Sun, B.J., Nyrud, M.L.J., Kileng , ?., Greiner-Tollersrud, L., and Robertsen, B. (2012). Atlantic salmon type I IFN subtypes show differences in antiviral activity and cell-dependent expression: Evidence for high IFNb/IFNc-producing cells in fish lymphoid tissues. J Immunol 189, 5912-5923 .10.4049/jimmunol.1201188
[30] Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011). MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739 .10.1093/molbev/msr121
[31] Thomas, C., Moraga, I., Levin, D., Krutzik, P.O., Podoplelova, Y., Trejo, A., Lee, C., Yarden, G., Vleck, S.E., Glenn, J.S., et al. (2011). Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 146, 621-632 .10.1016/j.cell.2011.06.048
[32] Thompson, J.D., Gibson, T.J., and Higgins, D.G. (2002). Multiple sequence alignment using ClustalW and ClustalX. In Current Protocols in Bioinformatics , John Wiley & Sons, Inc.10.1002/0471250953.bi0203s00
[33] Vassileva, G., Chen, S.C., Zeng, M., Abbondanzo, S., Jensen, K., Gorman, D., Baroudy, B.M., Jiang, Y., Murgolo, N., and Lira, S.A. (2003). Expression of a novel murine type I IFN in the pancreatic islets induces diabetes in mice. J Immunol 170, 5748-5755 .
[34] Whaley, A.E., Meka, C.S., Harbison, L.A., Hunt, J.S., and Imakawa , K. (1994). Identification and cellular localization of unique interferon mRNA from human placenta. J Biol Chem 269, 10864-10868 .
[35] Woelk, C.H., Frost, S.D.W., Richman, D.D., Higley, P.E., and Kosak ovsky Pond, S.L. (2007). Evolution of the interferon alpha gene family in eutherian mammals. Gene 397, 38-50 .10.1016/j.gene.2007.03.018
[36] Xi, Y., Day, S.L., Jackson, R.J., and Ranasinghe, C. (2012). Role o fnovel type I interferon epsilon in viral infection and mucosal immunity. Mucosal Immunol 5, 610-622 .10.1038/mi.2012.35