Evolution of interferons and interferon receptors

Frontiers in Immunology

Volumn 8, Issue MAR, 2017, Pages

  Secombes, Chris J ^a   Zou, Jun ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Evolution; Fish; Gene duplication; Interferon; Interferon receptor; Retrotransposition; Vertebrate

Indexed keywords

BETA INTERFERON; FLAGELLIN; GAMMA INTERFERON RECEPTOR 1; INTERFERON; INTERFERON EPSILON; INTERFERON GAMMA RECEPTOR 17; INTERFERON RECEPTOR; INTERLEUKIN 22; JANUS KINASE 1; LIPOPOLYSACCHARIDE; MEMBRANE PROTEIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; PATTERN RECOGNITION RECEPTOR; STAT1 PROTEIN; STAT2 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 13; TOLL LIKE RECEPTOR 19 22; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ALTERNATIVE RNA SPLICING; FISH; GENE EXPRESSION; GENE SEQUENCE; GENE STRUCTURE; GNATHOSTOMA; INTRACELLULAR SIGNALING; NONHUMAN; PHYLOGENY; RECEPTOR BINDING; REVIEW;

EID: 85017242795     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2017.00209     Document Type: Review

References (63)

1. Nakatani Y, Takeda H, Kohara Y, Morishita S. Reconstruction of the vertebrate ancestral genome reveals dynamic genome reorganization in early vertebrates. Genome Res (2007) 17:1254-65. doi:10.1101/gr.6316407
2. Siupka P, Hamming OJ, Frétaud M, Luftalla G, Levraud JP, Hartmann R. The crystal structure of zebrafish IL-22 reveals an evolutionary, conserved structure highly similar to that of human IL-22. Genes Immun (2014) 15:293-302. doi:10.1038/gene.2014.18
3. Venkatesh B, Lee AP, Ravi V, Maurya AK, Lian MM, Swann JB, et al. Elephant shark genome provides unique insights into gnathostome evolution. Nature (2014) 505:174-9. doi:10.1038/nature12826
4. Boudinot P, Langevin C, Secombes CJ, Levraud JP. The peculiar characteristics of fish type I interferons. Viruses (2016) 8:298. doi:10.3390/v8110298
5. Robertsen B. The interferon system of teleost fish. Fish Shellfish Immunol (2006) 20:172-91. doi:10.1016/j.fsi.2005.01.010
6. Zhang YB, Gui JF. Molecular regulation of interferon antiviral response in fish. Dev Comp Immunol (2012) 38:193-202. doi:10.1016/j.dci.2012.06.003
7. Zou J, Secombes CJ. Teleost fish interferons and their role in immunity. Dev Comp Immunol (2011) 35:1376-87. doi:10.1016/j.dci.2011.07.001
8. Sepulcre MP, Alcaraz-Pérez F, López-Muñoz A, Roca FJ, Meseguer J, Cayuela ML, et al. Evolution of lipopolysaccharide (LPS) recognition and signaling: fish TLR4 does not recognize LPS and negatively regulates NF-kappaB activation. J Immunol (2009) 182:1836-45. doi:10.4049/jimmunol.0801755
9. Sullivan C, Charette J, Catchen J, Lage CR, Giasson G, Postlethwait JH, et al. The gene history of zebrafish tlr4a and tlr4b is predictive of their divergent functions. J Immunol (2009) 183:5896-908. doi:10.4049/jimmunol.0803285
10. Boudinot P, Zou J, Ota T, Buonocore F, Scapigliati G, Canapa A, et al. A tetrapod-like repertoire of innate immune receptors and effectors for coelacanths. J Exp Zool B Mol Dev Evol (2014) 322:415-37. doi:10.1002/jez.b.22559
11. Ishii A, Kawasaki M, Matsumoto M, Tochinai S, Seya T. Phylogenetic and expression analysis of amphibian Xenopus toll-like receptors. Immunogenetics (2007) 59:281-93. doi:10.1007/s00251-007-0193-y
12. Temperley ND, Berlin S, Paton IR, Griffin DK, Burt DW. Evolution of the chicken toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics (2008) 9:62. doi:10.1186/1471-2164-9-62
13. Brownlie R, Allan B. Avian toll-like receptors. Cell Tissue Res (2011) 343:121-30. doi:10.1007/s00441-010-1026-0
14. Roach JC, Glusman G, Rowen L, Kaur A, Purcell MK, Smith KD, et al. The evolution of vertebrate toll-like receptors. Proc Natl Acad Sci U S A (2005) 102:9577-82. doi:10.1073/pnas.0502272102
15. Wang T, Johansson P, Abós B, Holt A, Tafalla C, Jiang Y, et al. First in-depth analysis of the novel Th2-type cytokines in salmonid fish reveals distinct patterns of expression and modulation but overlapping bioactivities. Oncotarget (2016) 7:10917-46. doi:10.18632/oncotarget.7295
16. Lee PT, Zou J, Holland JW, Martin SA, Collet B, Kanellos T, et al. Identification and characterisation of TLR18-21 genes in Atlantic salmon (Salmo salar). Fish Shellfish Immunol (2014) 41:549-59. doi:10.1016/j.fsi.2014.10.006
17. Quiniou SM, Boudinot P, Bengtén E. Comprehensive survey and genomic characterization of toll-like receptors (TLRs) in channel catfish, Ictalurus punctatus: identification of novel fish TLRs. Immunogenetics (2013) 65:511-30. doi:10.1007/s00251-013-0694-9
18. Palti Y. Toll-like receptors in bony fish: from genomics to function. Dev Comp Immunol (2011) 35:1263-72. doi:10.1016/j.dci.2011.03.006
19. Broz P, Monack DM. Newly described pattern recognition receptors team up against intracellular pathogens. Nat Rev Immunol (2013) 13:551-65. doi:10.1038/nri3479
20. Zou J, Tafalla C, Truckle J, Secombes CJ. Identification of a second group of type I IFNs in fish sheds light on IFN evolution in vertebrates. J Immunol (2007) 179:3859-71. doi:10.4049/jimmunol.179.6.3859
21. Igawa D, Sakai M, Savan R. An unexpected discovery of two interferon gamma-like genes along with interleukin(IL)-22 and-26 from teleost: IL-22 and-26 genes have been described for the first time outside mammals. Mol Immunol (2006) 43:999-1009. doi:10.1016/j.molimm.2005.05.009
22. Hamming OJ, Lutfalla G, Levraud JP, Hartmann R. Crystal structure of zebrafish interferons I and II reveals conservation of type I interferon structure in vertebrates. J Virol (2011) 85:8181-7. doi:10.1128/JVI.00521-11
23. Chen SN, Zhang XW, Li L, Ruan BY, Huang B, Huang WS, et al. Evolution of IFN-lambda in tetrapod vertebrates and its functional characterization in green anole lizard (Anolis carolinensis). Dev Comp Immunol (2016) 61:208-24. doi:10.1016/j.dci.2016.04.004
24. Karpala AJ, Morris KR, Broadway MM, McWaters PGD, O'Neil TE, Goossens KE, et al. Molecular cloning, expression, and characterization of chicken IFN-lambda. J Interferon Cytokine Res (2008) 28:341-50. doi:10.1089/jir.2007.0117
25. Qi Z, 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) 84:5038-46. doi:10.4049/jimmunol.0903374
26. Stein C, Caccamo M, Laird G, Leptin M. Conservation and divergence of gene families encoding components of innate immune response systems in zebrafish. Genome Biol (2007) 8:R251. doi:10.1186/gb-2007-8-11-r251
27. Sun B, Greiner-Tollersrud L, Koop BF, Robertsen B. Atlantic salmon possesses two clusters of type I interferon receptor genes on different chromosomes, which allows for a larger repertoire of interferon receptors than in zebrafish and mammals. Dev Comp Immunol (2014) 47:275-86. doi:10.1016/j.dci.2014.08.007
28. Aggad D, Mazel M, Boudinot P, Mogensen KE, Hamming OJ, Hartmann R, et al. The two groups of zebrafish virus-induced interferons signal via distinct receptors with specific and shared chains. J Immunol (2009) 183:3924-31. doi:10.4049/jimmunol.0901495
29. Chang M-X, Zou J, Nie P, Huang B, Yu Z, Collet B, et al. Intracellular interferons in fish: a unique means to combat viral infection. PLoS Pathog (2013) 9:e1003736. doi:10.1371/journal.ppat.1003736
30. Thomas C, Moraga I, Levin D, Krutzik PO, Podoplelova Y, Trejo A, et al. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell (2011) 146:621-32. doi:10.1016/j.cell.2011.06.048
31. Agaisse H, Perrimon N. The roles of JAK/STAT signaling in Drosophila immune responses. Immunol Rev (2004) 198:72-82. doi:10.1111/j.0105-2896.2004.0133.x
32. Arbouzova NI, Zeidler MP. JAK/STAT signalling in Drosophila: insights into conserved regulatory and cellular functions. Development (2006) 133:2605-16. doi:10.1242/dev.02411
33. Barillas-Mury C, Han YS, Seeley D, Kafatos FC. Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. EMBO J (1999) 18:959-67. doi:10.1093/emboj/18.4.959
34. Lin CC, Chou CM, Hsu YL, Lien JC, Wang YM, Chen ST, et al. Characterization of two mosquito STATs, AaSTAT and CtSTAT. Differential regulation of tyrosine phosphorylation and DNA binding activity by lipopolysaccharide treatment and by Japanese encephalitis virus infection. J Biol Chem (2004) 279:3308-17. doi:10.1074/jbc.M309749200
35. Gan Z, Chen SN, Huang B, Hou J, Nie P. 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. Dev Comp Immunol (2016) 67:166-76. doi:10.1016/j.dci.2016.10.007
36. Sang Y, Liu Q, Lee J, Ma W, McVey DS, Blecha F. Expansion of amphibian intronless interferons revises the paradigm for interferon evolution and functional diversity. Sci Rep (2016) 6:29072. doi:10.1038/srep29072
37. Krause CD. Intron loss in interferon genes follows a distinct set of stages, and may confer an evolutionary advantage. Cytokine (2016) 83:193-205. doi:10.1016/j.cyto.2016.04.018
38. Krause CD, Pestka S. Cut, copy, move, delete: the study of human interferon genes reveal multiple mechanisms underlying their evolution in amniotes. Cytokine (2015) 76:480-95. doi:10.1016/j.cyto.2015.07.019
39. Krause CD. Intron loss in interferon genes follows a distinct set of stages, and may confer an evolutionary advantage. Cytokine (2016) 83:193-205. doi:10.1016/j.cyto.2016.04.018
40. Zou J, Gorgoglione B, Taylor NG, Summathed T, Lee PT, Panigrahi A, et al. Salmonids have an extraordinary complex type I IFN system: characterization of the IFN locus in rainbow trout Oncorhynchus mykiss reveals two novel IFN subgroups. J Immunol (2014) 193:2273-86. doi:10.4049/jimmunol.1301796
41. Long S, Wilson M, Bengten E, Bryan L, Clem LW, Miller NW, et al. Identification of a cDNA encoding channel catfish interferon. Dev Comp Immunol (2004) 28:97-111. doi:10.1016/S0145-305X(03)00122-8
42. Purcell MK, Laing KJ, Woodson JC, Thorgaard GH, Hansen JD. Characterization of the interferon genes in homozygous rainbow trout reveals two novel genes, alternate splicing and differential regulation of duplicated genes. Fish Shellfish Immunol (2009) 26:293-304. doi:10.1016/j.fsi.2008.11.012
43. Ding Y, Ao J, Huang X, Chen X. Identification of two subgroups of type I IFNs in perciforme fish large yellow croaker Larimichthys crocea provides novel insights into function and regulation of fish type I IFNs. Front Immunol (2016) 7:343. doi:10.3389/fimmu.2016.00343
44. Chen YM, Kuo CE, Chen GR, Kao YT, Zou J, Secombes CJ, et al. Functional analysis of an orange-spotted grouper (Epinephelus coioides) interferon gene and characterisation of its expression in response to nodavirus infection. Dev Comp Immunol (2014) 46:117-28. doi:10.1016/j.dci.2014.04.004
45. Maekawa S, Chiang YA, Hikima J, Sakai M, Lo CF, Wang HC, et al. Expression and biological activity of two types of interferon genes in medaka (Oryzias latipes). Fish Shellfish Immunol (2016) 48:20-9. doi:10.1016/j.fsi.2015.11.036
46. Yabu T, Toda H, Shibasaki Y, Araki K, Yamashita M, Anzai H, et al. Antiviral protection mechanisms mediated by ginbuna crucian carp interferon gamma isoforms 1 and 2 through two distinct interferon gamma-receptors. J Biochem (2011) 150:635-48. doi:10.1093/jb/mvr108
47. Wang T, Husain M, Hong S, Holland JW. Differential expression, modulation and bioactivity of distinct fish IL-12 isoforms: implication towards the evolution of Th1-like immune responses. Eur J Immunol (2014) 44:1541-51. doi:10.1002/eji.201344273
48. Belmonte R, Wang T, Duncan GJ, Skaar I, Mélida H, Bulone V, et al. Role of pathogen-derived cell wall carbohydrates and prostaglandin E2 in immune response and suppression of fish immunity by the oomycete Saprolegnia parasitica. Infect Immun (2014) 82:4518-29. doi:10.1128/IAI.02196-14
49. Araki K, Takizawa F, Yamasaki M, Esumi M, Moritomo T, Ototake M, et al. Expression profiles of interferon gamma genes in response to immunostimulants and alloantigen in ginbuna crucian carp Carassius auratus langsdorfii. Fish Sci (2013) 79:213-20. doi:10.1007/s12562-012-0590-5
50. Shibasaki Y, Hatanaka C, Matsuura Y, Miyazawa R, Yabu T, Moritomo T, et al. Effects of IFN? administration on allograft rejection in ginbuna crucian carp. Dev Comp Immunol (2016) 62:108-15. doi:10.1016/j.dci.2016.04.021
51. Chen WQ, Xu QQ, Chang MX, Zou J, Secombes CJ, Peng KM, et al. Molecular characterization and expression analysis of the IFN-gamma related gene (IFN-γrel) in grass carp Ctenopharyngodon idella. Vet Immunol Immunopathol (2010) 134:199-207. doi:10.1016/j.vetimm.2009.09.007
52. Swain B, Basu M, Lenka SS, Das S, Jayasankar P, Samanta M. Characterization and inductive expression analysis of interferon gamma-related gene in the Indian major carp, Rohu (Labeo rohita). DNA Cell Biol (2015) 34:367-78. doi:10.1089/dna.2014.2656
53. Savan R, Ravichandran S, Collins JR, Sakai M, Young HA. Structural conservation of interferon gamma among vertebrates. Cytokine Growth Factor Rev (2009) 20:115-24. doi:10.1016/j.cytogfr.2009.02.006
54. Zou J, Carrington A, Collet B, Dijkstra JM, Bols N, Secombes CJ. Identification and bioactivities of interferon gamma in rainbow trout Oncorhynchus mykiss: the first Th1 type cytokine characterised functionally in fish. J Immunol (2005) 175:2484-94. doi:10.4049/jimmunol.175.4.2484
55. Shibasaki Y, Yabu T, Araki K, Mano N, Shiba H, Moritomo T, et al. Peculiar monomeric interferon gammas, IFN?rel 1 and IFN?rel 2, in ginbuna crucian carp. FEBS J (2014) 281:1046-56. doi:10.1111/febs.12666
56. Yoon S, Alnabulsi A, Wang T-Y, Lee PT, Chen T-Y, Bird S, et al. Analysis of interferon gamma protein expression in zebrafish (Danio rerio). Fish Shellfish Immunol (2016) 57:79-86. doi:10.1016/j.fsi.2016.08.023
57. Grayfer L, Garcia EG, Belosevic M. Comparison of macrophage antimicrobial responses induced by type II interferons in the goldfish (Carassius auratus L.). J Biol Chem (2010) 285:23537-47. doi:10.1074/jbc.M109.096925
58. Peng W, Lu DQ, Li GF, Zhang X, Yao M, Zhang Y, et al. Two distinct interferon-γ genes in Tetraodon nigroviridis: functional analysis during Vibrio parahaemolyticus infection. Mol Immunol (2016) 70:34-46. doi:10.1016/j.molimm.2015.12.004
59. Biswas G, Nagamine R, Hikima JI, Sakai M, Kono T. Inductive immune responses in the Japanese pufferfish (Takifugu rubripes) treated with recombinant IFN-γ, IFN-γrel, IL-4/13A and IL-4/13B. Int Immunopharmacol (2016) 31:50-6. doi:10.1016/j.intimp.2015.12.005
60. Gao Q, Nie P, Thompson KD, Adams A, Wang T, Secombes CJ, et al. The search for the IFN-gamma receptor in fish: functional and expression analysis of putative binding and signalling chains in rainbow trout Oncorhynchus mykiss. Dev Comp Immunol (2009) 33:920-31. doi:10.1016/j.dci.2009.03.001
61. Grayfer L, Belosevic M. Molecular characterization of novel interferon gamma receptor 1 isoforms in zebrafish (Danio rerio) and goldfish (Carassius auratus L.). Mol Immunol (2009) 46:3050-9. doi:10.1016/j.molimm.2009.06.004
62. Aggad D, Stein C, Sieger D, Mazel M, Boudinot P, Herbomel P, et al. In vivo analysis of Ifn-γ1 and Ifn-γ2 signaling in zebrafish. J Immunol (2010) 185:677467-82. doi:10.4049/jimmunol.1000549
63. Lu DQ, Leng TT, Ding X, Peng W, Yao M, Li SS, et al. Two IFNGR1 homologues in Tetraodon nigroviridis: origin, expression analysis and ligand-binding preference. Dev Comp Immunol (2014) 44:270-9. doi:10.1016/j.dci.2014.01.001