Evolution of IFN-λ in tetrapod vertebrates and its functional characterization in green anole lizard (Anolis carolinensis)

Developmental and Comparative Immunology

Volumn 61, Issue , 2016, Pages 208-224

  Chen, Shan Nan ^a,b   Zhang, Xiao Wen ^a,b   Li, Li ^a,b   Ruan, Bai Ye ^a,b   Huang, Bei ^c   Huang, Wen Shu ^c   Zou, Peng Fei ^c   Fu, Jian Ping ^a   Zhao, Li Juan ^a   Li, Nan ^a   Nie, Pin ^a  

^a INSTITUTE OF HYDROBIOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c JIMEI UNIVERSITY   (China)

Author keywords

Evolution; IFN ; IFNL; IFNLR1; IL10RB; Lizard

Indexed keywords

INTERFERON; INTERFERON REGULATORY FACTOR 3; LAMBDA INTERFERON; UNCLASSIFIED DRUG; IFNL4 PROTEIN, HUMAN; INTERFERON RECEPTOR; INTERLEUKIN DERIVATIVE; POLYINOSINIC POLYCYTIDYLIC ACID;

ANIMAL CELL; ANOLIS CAROLINENSIS; ARTICLE; BIOINFORMATICS; CELLULAR DISTRIBUTION; COMPUTER MODEL; CONTROLLED STUDY; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC CONSERVATION; GENETIC DATABASE; GENETIC TRANSFECTION; GENOMIC ORGANIZATION; IFNL GENE; IFNLR1 GENE; IL10RB GENE; IRF3 GENE; MOLECULAR CLONING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENETIC TREE; POPULATION GENETIC PARAMETERS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN FUNCTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; SYNTENY; TETRAPOD; UPREGULATION; ANIMAL; CELL LINE; CROCODILIAN; EVOLUTION; GENETICS; HUMAN; IMMUNOLOGY; LIZARD; METABOLISM; PHYLOGENY; TURTLE; XENOPUS;

ALLIGATORS AND CROCODILES; ANIMALS; BIOLOGICAL EVOLUTION; CELL LINE; HUMANS; INTERFERON REGULATORY FACTOR-3; INTERLEUKINS; LIZARDS; PHYLOGENY; POLY I-C; PROMOTER REGIONS, GENETIC; RECEPTORS, INTERFERON; SIGNAL TRANSDUCTION; TURTLES; XENOPUS;

EID: 84962820634     PISSN: 0145305X     EISSN: 18790089     Source Type: Journal    
DOI: 10.1016/j.dci.2016.04.004     Document Type: Article

References (62)

1. Abascal F., Zardoya R., Posada D. ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
2. Abushahba W., Balan M., Castaneda I., Yuan Y., Reuhl K., Raveche E., de la Torre A., Lasfar A., Kotenko S.V. Antitumor activity of Type I and Type III interferons in BNL hepatoma model. Cancer Immunol. Immun. 2010, 59:1059-1071.
3. Akdis M., Burgler S., Crameri R., Eiwegger T., Fujita H., Gomez E., Klunker S., Meyer N., O'Mahony L., Palomares O., Rhyner C., Quaked N., Schaffartzik A., Van De Veen W., Zeller S., Zimmermann M., Akdis C.A. Interleukins, from 1 to 37, and interferon-gamma: receptors, functions, and roles in diseases. J. Allergy Clin. Immun. 2011, 127:701-721.
4. Alföldi J., Di Palma F., Grabherr M., Williams C., Kong L.S., Mauceli E., Russell P., Lowe C.B., Glor R.E., Jaffe J.D., Ray D.A., Boissinot S., Shedlock A.M., Botka C., Castoe T.A., Colbourne J.K., Fujita M.K., Moreno R.G., ten Hallers B.F., Haussler D., Heger A., Heiman D., Janes D.E., Johnson J., de Jong P.J., Koriabine M.Y., Lara M., Novick P.A., Organ C.L., Peach S.E., Poe S., Pollock D.D., de Queiroz K., Sanger T., Searle S., Smith J.D., Smith Z., Swofford R., Turner-Maier J., Wade J., Young S., Zadissa A., Edwards S.V., Glenn T.C., Schneider C.J., Losos J.B., Lander E.S., Breen M., Ponting C.P., Lindblad-Toh K. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 2011, 477:587-591.
5. Almeida G.M., de Oliveira D.B., Magalhaes C.L., Bonjardim C.A., Ferreira P.C., Kroon E.G. Antiviral activity of type I interferons and interleukins 29 and 28a (type III interferons) against Apeu virus. Antivir. Res. 2008, 80:302-308.
6. Amemiya C.T., Alföldi J., Lee A.P., Fan S.H., Philippe H., MacCallum I., Braasch I., Manousaki T., Schneider I., Rohner N., Organ C., Chalopin D., Smith J.J., Robinson M., Dorrington R.A., Gerdol M., Aken B., Biscotti M.A., Barucca M., Baurain D., Berlin A.M., Blatch G.L., Buonocore F., Burmester T., Campbell M.S., Canapa A., Cannon J.P., Christoffels A., De Moro G., Edkins A.L., Fan L., Fausto A.M., Feiner N., Forconi M., Gamieldien J., Gnerre S., Gnirke A., Goldstone J.V., Haerty W., Hahn M.E., Hesse U., Hoffmann S., Johnson J., Karchner S.I., Kuraku S., Lara M., Levin J.Z., Litman G.W., Mauceli E., Miyake T., Mueller M.G., Nelson D.R., Nitsche A., Olmo E., Ota T., Pallavicini A., Panji S., Picone B., Ponting C.P., Prohaska S.J., Przybylski D., Saha N.R., Ravi V., Ribeiro F.J., Sauka-Spengler T., Scapigliati G., Searle S.M.J., Sharpe T., Simakov O., Stadler P.F., Stegeman J.J., Sumiyama K., Tabbaa D., Tafer H., Turner-Maier J., van Heusden P., White S., Williams L., Yandell M., Brinkmann H., Volff J.N., Tabin C.J., Shubin N., Schartl M., Jaffe D.B., Postlethwait J.H., Venkatesh B., Di Palma F., Lander E.S., Meyer A., Lindblad-Toh K. The African coelacanth genome provides insights into tetrapod evolution. Nature 2013, 496:311-316.
7. Anisimova M., Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst. Biol. 2006, 55:539-552.
8. Baker M.L., Schountz T., Wang L.F. Antiviral immune responses of bats: a review. Zoonoses Public Health 2013, 60:104-116.
9. Bartlett N.W., Buttigieg K., Kotenko S.V., Smith G.L. Murine interferon lambdas (type III interferons) exhibit potent antiviral activity in vivo in a poxvirus infection model. J. Gen. Virol. 2005, 86:1589-1596.
10. Chang M.X., Collet B., Nie P., Lester K., Campbell S., Secombes C.J., Zou J. Expression and functional characterization of the RIG-I-like receptors MDA5 and LGP2 in rainbow Trout (Oncorhynchus mykiss). J. Virol. 2011, 85:8403-8412.
11. Commins S., Steinke J.W., Borish L. The extended IL-10 superfamily: IL-10, IL-19, IL-20, IL-22, IL-24, IL-26, IL-28, and IL-29. J. Allergy Clin. Immun. 2008, 121:1108-1111.
12. Dai J.H., Megjugorac N.J., Gallagher G.E., Yu R.Y.L., Gallagher G. IFN-lambda 1 (IL-29) inhibits GATA3 expression and suppresses Th2 responses in human naive and memory T cells. Blood 2009, 113:5829-5838.
13. Diaz-San Segundo F., Weiss M., Perez-Martin E., Koster M.J., Zhu J., Grubman M.J., de los Santos T. Antiviral activity of bovine type III interferon against foot-and-mouth disease virus. Virology 2011, 413:283-292.
14. Donnelly R.P., Dickensheets H., O'Brien T.R. Interferon-lambda and therapy for chronic hepatitis C virus infection. Trends Immunol. 2011, 32:443-450.
15. Dumoutier L., Tounsi A., Michiels T., Sommereyns C., Kotenko S.V., Renauld J.C. Role of the interleukin (IL)-28 receptor tyrosine residues for antiviral and antiproliferative activity of IL-29/interferon-lambda 1-Similarities with type I interferon signaling. J. Biol. Chem. 2004, 279:32269-32274.
16. Fox B.A., Sheppard P.O., O'Hara P.J. The role of genomic data in the discovery, annotation and evolutionary interpretation of the interferon-lambda family. PLoS One 2009, 4:e4933.
17. Fu J.P., Chen S.N., Zou P.F., Huang B., Guo Z., Zeng L.B., Qin Q.W., Nie P. IFN-gamma in turtle: conservation in sequence and signalling and role in inhibiting iridovirus replication in Chinese soft-shelled turtle Pelodiscus sinensis. Dev. Comp. Immunol. 2014, 43:87-95.
18. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
19. Hamming O.J., Lutfalla G., Levraud J.P., Hartmann R. Crystal structure of zebrafish interferons I and II reveals conservation of Type I interferon structure in vertebrates. J. Virol. 2011, 85:8181-8187.
20. Hamming O.J., Terczynska-Dyla E., Vieyres G., Dijkman R., Jorgensen S.E., Akhtar H., Siupka P., Pietschmann T., Thiel V., Hartmann R. Interferon lambda 4 signals via the IFN lambda receptor to regulate antiviral activity against HCV and coronaviruses. EMBO J. 2013, 32:3055-3065.
21. Hou W., Wang X., Ye L., Zhou L., Yang Z.Q., Riedel E., Ho W.Z. Lambda interferon inhibits human immunodeficiency virus type 1 infection of macrophages. J. Virol. 2009, 83:3834-3842.
22. Huang B., Qi Z.T., Xu Z., Nie P. Global characterization of interferon regulatory factor (IRF) genes in vertebrates: glimpse of the diversification in evolution. BMC Immunol. 2010, 11:22.
23. Huang Y.H., Li Y.R., Burt D.W., Chen H.L., Zhang Y., Qian W.B., Kim H., Gan S.Q., Zhao Y.Q., Li J.W., Yi K., Feng H.P., Zhu P.Y., Li B., Liu Q.Y., Fairley S., Magor K.E., Du Z.L., Hu X.X., Goodman L., Tafer H., Vignal A., Lee T., Kim K.W., Sheng Z.Y., An Y., Searle S., Herrero J., Groenen M.A.M., Crooijmans R.P.M.A., Faraut T., Cai Q.L., Webster R.G., Aldridge J.R., Warren W.C., Bartschat S., Kehr S., Marz M., Stadler P.F., Smith J., Kraus R.H.S., Zhao Y.F., Ren L.M., Fei J., Morisson M., Kaiser P., Griffin D.K., Rao M., Pitel F., Wang J., Li N. The duck genome and transcriptome provide insight into an avian influenza virus reservoir species. Nat. Genet. 2013, 45:776-783.
24. Iversen M.B., Ank N., Melchjorsen J., Paludan S.R. Expression of type III interferon (IFN) in the vaginal mucosa is mediated primarily by dendritic cells and displays stronger dependence on NF-kappaB than type I IFNs. J. Virol. 2010, 84:4579-4586.
25. Jewell N.A., Cline T., Mertz S.E., Smirnov S.V., Flano E., Schindler C., Grieves J.L., Durbin R.K., Kotenko S.V., Durbin J.E. Lambda interferon is the predominant interferon induced by influenza A virus infection in vivo. J. Virol. 2010, 84:11515-11522.
26. Jordan W.J., Eskdale J., Srinivas S., Pekarek V., Kelner D., Rodia M., Gallagher G. Human interferon lambda-1 (IFN-lambda 1/IL-29) modulates the Th1/Th2 response. Genes Immun. 2007, 8:254-261.
27. Karpala A.J., Morris K.R., Broadway M.M., McWaters P.G.D., O'Neil T.E., Goossens K.E., Lowenthal J.W., Bean A.G.D. Molecular cloning, expression, and characterization of chicken IFN-lambda. J. Interf. Cytok. Res. 2008, 28:341-350.
28. Kotenko S.V. IFN-λs. Curr. Opin. Immunol. 2011, 23:583-590.
29. Kotenko S.V., Gallagher G., Baurin V.V., Lewis-Antes A., Shen M.L., Shah N.K., Langer J.A., Sheikh F., Dickensheets H., Donnelly R.P. IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 2003, 4:69-77.
30. Krause C.D., Pestka S. Evolution of the Class 2 cytokines and receptors, and discovery of new friends and relatives. Pharmacol. Ther. 2005, 106:299-346.
31. 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 2007, 23:2947-2948.
32. Lasfar A., Lewis-Antes A., Smirnov S.V., Anantha S., Abushahba W., Tian B., Reuhl K., Dickensheets H., Sheikh F., Donnelly R.P., Raveche E., Kotenko S.V. Characterization of the mouse IFN-lambda ligand-receptor system: IFN-lambda s exhibit antitumor activity against B16 melanoma. Cancer Res. 2006, 66:4468-4477.
33. Levraud J.P., Boudinot P., Colin I., Benmansour A., Peyrieras N., Herbomel P., Lutfalla G. Identification of the zebrafish IFN receptor: implications for the origin of the vertebrate IFN system. J. Immunol. 2007, 178:4385-4394.
34. Li M.L., Xu W.W., Gao Y.D., Guo Y., Wang W.J., Wang C., Jiang S.Y., Willden A., Huang J.F., Zhang H.T. Interferon-λ3 (IFN-λ3) and its cognate receptor subunits in tree shrews (Tupaia belangeri): genomic sequence retrieval, molecular identification and expression analysis. PLoS One 2013, 8:e60048.
35. Ma D., Jiang D., Qing M., Weidner J.M., Qu X., Guo H., Chang J., Gu B., Shi P.Y., Block T.M., Guo J.T. Antiviral effect of interferon lambda against West Nile virus. Antivir. Res. 2009, 83:53-60.
36. Meager A., Visvalingam K., Dilger P., Bryan D., Wadhwa M. Biological activity of interleukins-28 and-29: comparison with type I interferons. Cytokine 2005, 31:109-118.
37. Mennechet F.J.D., Uze G. Interferon-lambda-treated dendritic cells specifically induce proliferation of FOXP3-expressing suppressor T cells. Blood 2006, 107:4417-4423.
38. Miknis Z.J., Magracheva E., Li W., Zdanov A., Kotenko S.V., Wlodawer A. Crystal structure of human interferon-λ1 in complex with its high-affinity receptor interferon-lambda R1. J. Mol. Biol. 2010, 404:650-664.
39. Mouchaty S.K., Gullberg A., Janke A., Arnason U. The phylogenetic position of the Talpidae within eutheria based on analysis of complete mitochondrial sequences. Mol. Biol. Evol. 2000, 17:60-67.
40. Onoguchi K., Yoneyama M., Takemura A., Akira S., Taniguchi T., Namiki H., Fujita T. Viral infections activate types I and III interferon genes through a common mechanism. J. Biol. Chem. 2007, 282:7576-7581.
41. Osterlund P.I., Pietilae T.E., Veckman V., Kotenko S.V., Julkunen I. IFN regulatory factor family members differentially regulate the expression of type III IFN (IFN-lambda) genes. J. Immunol. 2007, 179:3434-3442.
42. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
43. Pott J., Mahlakoiv T., Mordstein M., Duerr C.U., Michiels T., Stockinger S., Staeheli P., Hornef M.W. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7944-7949.
44. Prokunina-Olsson L., Muchmore B., Tang W., Pfeiffer R.M., Park H., Dickensheets H., Hergott D., Porter-Gill P., Mumy A., Kohaar I., Chen S., Brand N., Tarway M., Liu L.Y., Sheikh F., Astemborski J., Bonkovsky H.L., Edlin B.R., Howell C.D., Morgan T.R., Thomas D.L., Rehermann B., Donnelly R.P., O'Brien T.R. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat. Genet. 2013, 45:164-171.
45. Qi Z.T., Nie P. Comparative study and expression analysis of the interferon gamma gene locus cytokines in Xenopus tropicalis. Immunogenetics 2008, 60:699-710.
46. Qi Z.T., 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. 2010, 184:5038-5046.
47. Reuter A., Soubies S., Hartle S., Schusser B., Kaspers B., Staeheli P., Rubbenstroth D. Antiviral activity of lambda interferon in chickens. J. Virol. 2014, 88:2835-2843.
48. Robek M.D., Boyd B.S., Chisari F.V. Lambda interferon inhibits hepatitis B and C virus replication. J. Virol. 2005, 79:3851-3854.
49. Ronquist F., Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19:1572-1574.
50. Sheppard P., Kindsvogel W., Xu W.F., Henderson K., Schlutsmeyer S., Whitmore T.E., Kuestner R., Garrigues U., Birks C., Roraback J., Ostrander C., Dong D., Shin J., Presnell S., Fox B., Haldeman B., Cooper E., Taft D., Gilbert T., Grant F.J., Tackett M., Krivan W., McKnight G., Clegg C., Foster D., Klucher K.M. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 2003, 4:63-68.
51. Smith J.L.B. The living coelacanthid fish from South Africa. Nature 1939, 143:748-750.
52. Sommereyns C., Paul S., Staeheli P., Michiels T. IFN-lambda (IFN-λ) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 2008, 4:e1000017.
53. Sugiyama M., Tanaka Y., Wakita T., Nakanishi M., Mizokami M. Genetic variation of the IL-28B promoter affecting gene expression. PLoS One 2011, 6:e26620.
54. Sun B.J., Robertsen B., Wang Z.Q., Bin L. Identification of an Atlantic salmon IFN multigene cluster encoding three IFN subtypes with very different expression properties. Dev. Comp. Immunol. 2009, 33:547-558.
55. Tamura K., Dudley J., Nei M., Kumar S. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 2007, 24:1596-1599.
56. Wang D., Fang L.R., Zhao F.W., Luo R., Chen H.C., Xiao S.B. Molecular cloning, expression and antiviral activity of porcine interleukin-29 (poIL-29). Dev. Comp. Immunol. 2011, 35:378-384.
57. Warren W.C., Hillier L.W., Graves J.A.M., Birney E., Ponting C.P., Grutzner F., Belov K., Miller W., Clarke L., Chinwalla A.T., Yang S.P., Heger A., Locke D.P., Miethke P., Waters P.D., Veyrunes F., Fulton L., Fulton B., Graves T., Wallis J., Puente X.S., Lopez-Otin C., Ordonez G.R., Eichler E.E., Chen L., Cheng Z., Deakin J.E., Alsop A., Thompson K., Kirby P., Papenfuss A.T., Wakefield M.J., Olender T., Lancet D., Huttley G.A., Smit A.F.A., Pask A., Temple-Smith P., Batzer M.A., Walker J.A., Konkel M.K., Harris R.S., Whittington C.M., Wong E.S.W., Gemmell N.J., Buschiazzo E., Jentzsch I.M.V., Merkel A., Schmitz J., Zemann A., Churakov G., Kriegs J.O., Brosius J., Murchison E.P., Sachidanandam R., Smith C., Hannon G.J., Tsend-Ayush E., McMillan D., Attenborough R., Rens W., Ferguson-Smith M., Lefevre C.M., Sharp J.A., Nicholas K.R., Ray D.A., Kube M., Reinhardt R., Pringle T.H., Taylor J., Jones R.C., Nixon B., Dacheux J.L., Niwa H., Sekita Y., Huang X.Q., Stark A., Kheradpour P., Kellis M., Flicek P., Chen Y., Webber C., Hardison R., Nelson J., Hallsworth-Pepin K., Delehaunty K., Markovic C., Minx P., Feng Y.C., Kremitzki C., Mitreva M., Glasscock J., Wylie T., Wohldmann P., Thiru P., Nhan M.N., Pohl C.S., Smith S.M., Hou S.F., Renfree M.B., Mardis E.R., Wilson R.K. Genome analysis of the platypus reveals unique signatures of evolution. Nature 2008, 453:175-183.
58. Zhou H., Chen S., Wang M.S., Cheng A.C. Interferons and their receptors in birds: a comparison of gene structure, phylogenetic analysis, and cross modulation. Int. J. Mol. Sci. 2014, 15:21045-21068.
59. Zhou P., Cowled C., Marsh G.A., Shi Z.L., Wang L.F., Baker M.L. Type III IFN receptor expression and functional characterisation in the pteropid bat, Pteropus alecto. PLoS One 2011, 6:e25385.
60. Zhou P., Cowled C., Todd S., Crameri G., Virtue E.R., Marsh G.A., Klein R., Shi Z.L., Wang L.F., Baker M.L. Type III IFNs in pteropid bats: differential expression patterns provide evidence for distinct roles in antiviral immunity. J. Immunol. 2011, 186:3138-3147.
61. Zitzmann K., Brand S., Baehs S., Goke B., Meinecke J., Spottl G., Meyer H., Auernhammer C.J. Novel interferon-λs induce antiproliferative effects in neuroendocrine tumor cells. Biochem. Biophys.. Res. Commun. 2006, 344:1334-1341.
62. 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. 2007, 179:3859-3871.