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. 2013 Apr 30;4(5):383–392. doi: 10.1007/s13238-013-3021-1

Distinct evolution process among type I interferon in mammals

Lei Xu 13021,23021, Limin Yang 13021,✉, Wenjun Liu 13021,23021,33021,✉
PMCID: PMC4875548  PMID: 23636688

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, 13genomes 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, IFNɛ, and IFNκ formed a clade separate from 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 selection pressure upon type I IFNs during their evolution.

Keywords: type I IFN, evolutionary history, vertebrate, gene cluster

Contributor Information

Limin Yang, Email: lmyang@im.ac.cn.

Wenjun Liu, Email: liuwj@im.ac.cn.

References

  1. Altmann SM, Mellon MT, Distel DL, Kim CH. Molecular and functional analysis of an interferon gene from the zebrafish, Danio rerio. J Virol. 2003;77:1992–2002. doi: 10.1128/JVI.77.3.1992-2002.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bazer FW, Spencer TE, Ott TL. Interferon tau: A novel pregnancy eecognition signal. Am J Reprod Immunol. 1997;37:412–420. doi: 10.1111/j.1600-0897.1997.tb00253.x. [DOI] [PubMed] [Google Scholar]
  3. Buhler JD, Lancaster JM, Jacob AC, Chamberlain RD. In Reconfigurable Systems Summer Institute. Oxford: Oxford University Press; 2007. Mercury BLASTN: Faster DNA sequence comparison using a streaming hardware architecture; pp. 1–8. [Google Scholar]
  4. Chelmońskasoyta A. Interferon tau and its immunobiological role in ruminant reproduction. Arch Immunol Ther Exp. 2002;50:47–52. [PubMed] [Google Scholar]
  5. Cochet M, Vaiman D, Lefèvre F. 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. 2009;433:88–99. doi: 10.1016/j.gene.2008.11.026. [DOI] [PubMed] [Google Scholar]
  6. David M. Biotechniques (Suppl) 2002. Signal tr ansduction by type I interferons; pp. 58–65. [PubMed] [Google Scholar]
  7. Hardy MP, Owczarek CM, Jermiin LS, Ejdebäck M, Hertzog PJ. Characterization of the type I interferon locus and identification of novel genes. Genomics. 2004;84:331–345. doi: 10.1016/j.ygeno.2004.03.003. [DOI] [PubMed] [Google Scholar]
  8. Harley ITW, Niewold TB, Stormont RM, Kaufman KM, Glenn SB, Franek BS, Kelly JA, Johnson GA, Stewart MD, Gray CA, Choi Y, Burghardt RC, Yu-Lee LY, Bazer FW, Spencer TE. Effects of the estrous cycle, pregnancy, and interferon tau on 2′,5′-oligoadenylate synthetase expression in the ovine uterus. Biol Repr. 2001;64:1392–1399. doi: 10.1095/biolreprod64.5.1392. [DOI] [PubMed] [Google Scholar]
  9. Henco K, Brosius J, Fujisawa A, Fujisawa JI, Haynes JR, Hochstadt J, Kovacic T, Pasek M, Schambock A, Schmid J, et al. Structural relationship of human interferon alpha genes and pseudogenes. J Mol Biol. 1985;185:227–260. doi: 10.1016/0022-2836(85)90401-2. [DOI] [PubMed] [Google Scholar]
  10. Kilpatrick JR, Hutchings D, Divers J, et al. The role of genetic variation near interferon-kappa in systemic lupus erythematosus. J Biomed Biotechnol. 2010;2010:1–11. doi: 10.1155/2010/706825. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Isaacs A, Lindenmann J. Virus interference. I. The interferon. Proc Roy Soc B: Biol Sci. 1957;147:258–267. doi: 10.1098/rspb.1957.0048. [DOI] [PubMed] [Google Scholar]
  12. Lavoie TB, Kalie E, Crisafulli-Cabatu S, Abramovich R, DiGioia G, Moolchan K, Pestka S, Schreiber G. Binding and activity of all human alpha interferon subtypes. Cytokine. 2011;56:282–289. doi: 10.1016/j.cyto.2011.07.019. [DOI] [PubMed] [Google Scholar]
  13. Lefèvre F, Boulay V. A novel and atypical type one interferon gene expressed by trophoblast during early pregnancy. J Biol Chem. 1993;268:19760–19768. [PubMed] [Google Scholar]
  14. Oritani K, Medina KL, Tomiyama Y, Ishikawa J, Okajima Y, Ogawa M, Yokota T, Aoyama K, Takahashi I, Kincade PW, et al. Limitin: An interferon-like cytokine that preferentially influences B-lymphocyte precursors. Nat Med. 2000;6:659–666. doi: 10.1038/76233. [DOI] [PubMed] [Google Scholar]
  15. Pestka S, Krause CD, Walter M R. Interferons, interferon-like cytokines, and their receptors. Immunol Rev. 2004;202:8–32. doi: 10.1111/j.0105-2896.2004.00204.x. [DOI] [PubMed] [Google Scholar]
  16. Qi ZT, Nie P, Secombes CJ, 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. 2010;184:5038–5046. doi: 10.4049/jimmunol.0903374. [DOI] [PubMed] [Google Scholar]
  17. Qu H, Yang L, Meng S, Xu L, Bi Y, Jia X, Li J, Sun L, Liu W. The differential antiviral activities of chicken interferon α (ChIFN-α) and ChIFN-β are related to distinct interferon-stimulated gene expression. PLoS ONE. 2013;8:e59307. doi: 10.1371/journal.pone.0059307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Roberts RM, Liu L, Guo QT, Leaman D, Bixby J. The evolution of the type I interferons. J Interferon Cytokine Res. 1998;18:805–816. doi: 10.1089/jir.1998.18.805. [DOI] [PubMed] [Google Scholar]
  19. Roberts RM. Interferon-tau, a type 1 i nterferon involved in maternal recognition of pregnancy. Cytokine Growth Factor Rev. 2007;18:403–408. doi: 10.1016/j.cytogfr.2007.06.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Robertsen B, Bergan V, Røkenes T, Larsen R, Albuquerque A. Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res. 2003;23:601–612. doi: 10.1089/107999003322485107. [DOI] [PubMed] [Google Scholar]
  21. Sang Y, Rowland RR, Hesse RA, Blecha F. Differential expression and activity of the porcine type I interferon family. Physiol Genomics. 2010;42:248–258. doi: 10.1152/physiolgenomics.00198.2009. [DOI] [PubMed] [Google Scholar]
  22. Schwartz S, Elnitski L, Li M, Weirauch M, Riemer C, Smit A, Program NCS, Green ED, Hardison RC, Miller W. MultiPipMaker and supporting tools: alignments and analysis of multiple genomic DNA sequences. Nucleic Acids Res. 2003;31:3518–3524. doi: 10.1093/nar/gkg579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, Kuestner R, Garrigues U, Birks C, Roraback J, et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol. 2003;4:63–68. doi: 10.1038/ni873. [DOI] [PubMed] [Google Scholar]
  24. Sick C, Schultz U, Münster U, Meier J, Kaspers B, Staeheli P. Promoter structures and differential responses to viral and nonviral inducers of chicken type I interferon genes. J Biol Chem. 1998;273:9749–9754. doi: 10.1074/jbc.273.16.9749. [DOI] [PubMed] [Google Scholar]
  25. Sick C, Schultz U, Staeheli P. A family of genes coding for two serologically distinct chicken interferons. J Biol Chem. 1996;271:7635–7639. doi: 10.1074/jbc.271.13.7635. [DOI] [PubMed] [Google Scholar]
  26. Stancato LF, Sakatsume M, David M, Dent P, Dong F, Petricoin EF, Krolewski JJ, Silvennoinen O, Saharinen P, et al. Beta interferon and oncostatin M activate Raf-1 and mitogen-activated protein kinase through a JAK1-dependent pathway. Mol Cell Biol. 1997;17:3833–3840. doi: 10.1128/MCB.17.7.3833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stark GR, Kerr IM, Williams BRG, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227–264. doi: 10.1146/annurev.biochem.67.1.227. [DOI] [PubMed] [Google Scholar]
  28. Sun BJ, Robertsen B, Wang ZQ, Liu B. I dentification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev Comp Immunol. 2009;33:547–558. doi: 10.1016/j.dci.2008.10.001. [DOI] [PubMed] [Google Scholar]
  29. Svingerud T, Solstad T, Sun BJ, Nyrud MLJ, Kileng, Greiner-Tollersrud L, Robertsen B. 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. 2012;189:5912–5923. doi: 10.4049/jimmunol.1201188. [DOI] [PubMed] [Google Scholar]
  30. 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. 2011;28:2731–2739. doi: 10.1093/molbev/msr121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thomas C, Moraga I, Levin D, Krutzik PO, Podoplelova Y, Trejo A, Lee C, Yarden G, Vleck SE, Glenn JS, et al. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell. 2011;146:621–632. doi: 10.1016/j.cell.2011.06.048. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Thompson JD, Gibson TJ, Higgins DG. Multiple sequence alignment using ClustalW and ClustalX. 2002. [DOI] [PubMed] [Google Scholar]
  33. Vassileva G, Chen SC, Zeng M, Abbondanzo S, Jensen K, Gorman D, Baroudy BM, Jiang Y, Murgolo N, Lira SA. Expression of a novel murine type I IFN in the pancreatic islets induces diabetes in mice. J Immunol. 2003;170:5748–5755. doi: 10.4049/jimmunol.170.11.5748. [DOI] [PubMed] [Google Scholar]
  34. Whaley AE, Meka CS, Harbison LA, Hunt JS, Imakawa K. Identification and cellular localization of unique interferon mRNA from human placenta. J Biol Chem. 1994;269:10864–10868. [PubMed] [Google Scholar]
  35. Woelk CH, Frost SDW, Richman DD, Higley PE, Kosakovsky Pond SL. Evolution of the interferon alpha gene family in eutherian mammals. Gene. 2007;397:38–50. doi: 10.1016/j.gene.2007.03.018. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Xi Y, Day SL, Jackson RJ, Ranasinghe C. Role of novel type I interferon epsilon in viral infection and mucosal immunity. Mucosal Immunol. 2012;5:610–622. doi: 10.1038/mi.2012.35. [DOI] [PMC free article] [PubMed] [Google Scholar]

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