IFN-λ4: The paradoxical new member of the interferon lambda family

Journal of Interferon and Cytokine Research

Volumn 34, Issue 11, 2014, Pages 829-838

  O'Brien, Thomas R ^a   Prokunina Olsson, Ludmila ^a   Donnelly, Raymond P ^b  

^a NATIONAL CANCER INSTITUTE   (United States)

^b CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; HOST FACTOR; INTERFERON; INTERFERON LAMBDA3; INTERFERON LAMBDA4; JANUS KINASE; STAT PROTEIN; UNCLASSIFIED DRUG; IFNL4 PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; VIRUS RNA;

AFRICAN; ALLELE; ANTIVIRAL ACTIVITY; ARTICLE; ASIAN; CYTOKINE RELEASE; GENETIC SELECTION; HEPATITIS C; HUMAN; IMMUNE RESPONSE; JAK-STAT SIGNALING; NONHUMAN; PRIORITY JOURNAL; ANIMAL; BLACK PERSON; CHEMISTRY; GENETIC PREDISPOSITION; GENETICS; HEPACIVIRUS; IMMUNOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VIRUS LOAD;

AFRICAN CONTINENTAL ANCESTRY GROUP; ALLELES; ANIMALS; GENETIC PREDISPOSITION TO DISEASE; HEPACIVIRUS; HEPATITIS C; HUMANS; INTERLEUKINS; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, VIRAL; SIGNAL TRANSDUCTION; VIRAL LOAD;

EID: 84908124655     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2013.0136     Document Type: Article

References (60)

1. Aka PV, Kuniholm MH, Pfeiffer RM, Wang AS, Tang W, Chen S, Astemborski J, Plankey M, Villacres MC, Peters MG, Desai S, Seaberg EC, Edlin BR, Strickler HD, Thomas DL, Prokunina-Olsson L, Sharp GB, O'Brien TR. 2014. Association of the IFNL4-DG allele with impaired spontaneous clearance of hepatitis C virus. J Infect Dis 209(3):350-354.
2. Amanzada A, Kopp W, Spengler U, Ramadori G, Mihm S. 2013. Interferon-l4 (IFNL4) transcript expression in human liver tissue samples. PLoS One 8(12):e84026.
3. Bibert S, Roger T, Calandra T, Bochud M, Cerny A, Semmo N, Duong FHT, Gerlach T, Malinverni R, Moradpour D, Negro F, Müllhaupt B, Bochud P-Y; the Swiss Hepatitis C Cohort Study. 2013. IL28B expression depends on a novel TT/-G polymorphism which improves HCV clearance prediction. J Exp Med 210(6):1109-1116.
4. Buontempo PJ, Jubin RG, Buontempo CA, Wagner NE, Reyes GR, Baroudy BM. 2006. Antiviral activity of transiently expressed IFN-kappa is cell-associated. J Interferon Cytokine Res 26(1):40-52.
5. de Castellarnau M, Aparicio E, Parera M, Franco S, Tural C, Clotet B, Martínez MA. 2012. Deciphering the interleukin 28B variants that better predict response to pegylated interferon-a and ribavirin therapy in HCV/HIV-1 coinfected patients. PLoS One 7(2):e31016.
6. de Weerd NA, Nguyen T. 2012. The interferons and their receptors-distribution and regulation. Immunol Cell Biol 90(5):483-491.
7. Dellgren C, Gad HH, Hamming OJ, Melchjorsen J, Hartmann R. 2009. Human interferon-lambda3 is a potent member of the type III interferon family. Genes Immun 10(2):125-131.
8. Dickensheets H, Sheikh F, Park O, Gao B, Donnelly RP. 2013. Interferon-lambda (IFN-lambda) induces signal transduction and gene expression in human hepatocytes, but not in lymphocytes or monocytes. J Leukoc Biol 93(3):377-385.
9. Diegelmann J, Beigel F, Zitzmann K, Kaul A, Göke B, Auernhammer CJ, Bartenschlager R, Diepolder HM, Brand S. 2010. Comparative analysis of the lambda-interferons IL-28A and IL-29 regarding their transcriptome and their antiviral properties against hepatitis C virus. PLoS One 5(12): e15200.
10. Donnelly RP, Kotenko SV. 2010. Interferon-lambda: a new addition to an old family. J Interferon Cytokine Res 30(8): 555-564.
11. Doyle SE, Schreckhise H, Khuu-Duong K, Henderson K, Rosler R, Storey H, Yao L, Liu H, Barahmand-Pour F, Sivakumar P, Chan C, Birks C, Foster D, Clegg CH, Wietzke-Braun P, Mihm S, Klucher KM. 2006. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44(4):896-906.
12. Duong FHT, Trincucci G, Boldanova T, Calabrese D, Campana B, Krol I, Durand SC, Heydmann L, Zeisel MB, Baumert TF, Heim MH. Hepatic IFN-l receptor 1 expression is induced in chronic hepatitis C and correlates with IFN-l3 minor alleles and with non-response to IFN-a therapies. J Exp Med(In press).
13. Fox BA, Sheppard PO, O'Hara PJ. 2009. The role of genomic data in the discovery, annotation and evolutionary interpretation of the interferon-lambda family. PLoS One 4(3):e4933.
14. Franco S, Aparicio E, Parera M, Clotet B, Tural C, Martinez MA. 2014. IFNL4 ss469415590 variant is a better predictor than rs12979860 of pegylated interferon-alpha/ribavirin therapy failure in hepatitis C virus/HIV-1 coinfected patients. AIDS 28(1):133-136.
15. Francois-Newton V, Magno de Freitas Almeida G, Payelle-Brogard B, Monneron D, Pichard-Garcia L, Piehler J, Pel-legrini S, Uze G. 2011. USP18-based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon alpha response. PLoS One 6(7):e22200.
16. Fukuhara T, Taketomi A, Motomura T, Okano S, Ninomiya A, Abe T, Uchiyama H, Soejima Y, Shirabe K, Matsuura Y, Maehara Y. 2010. Variants in IL28B in liver recipients and donors correlate with response to peg-interferon and ribavirin therapy for recurrent hepatitis C. Gastroenterology 139(5): 1577-1585, 1585.e1571-e1573.
17. Gad HH, Dellgren C, Hamming OJ, Vends S, Paludan SR, Hartmann R. 2009. Interferon-l is functionally an interferon but structurally related to the interleukin-10 family. J Biol Chem 284(31):20869-20875.
18. Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ, Sulkowski M, McHutchison JG, Goldstein DB. 2009. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461(7262):399-401.
19. Griffiths SJ, Koegl M, Boutell C, Zenner HL, Crump CM, Pica F, Gonzalez O, Friedel CC, Barry G, Martin K, Craigon MH, Chen R, Kaza LN, Fossum E, Fazakerley JK, Efstathiou S, Volpi A, Zimmer R, Ghazal P, Haas J. 2013. A systematic analysis of host factors reveals a Med23-interferon-l regulatory axis against herpes simplex virus type 1 replication. PLoS Pathog 9(8):e1003514.
20. Hamming OJ, Terczynska-Dyla E, Vieyres G, Dijkman R, Jørgensen SE, Akhtar H, Siupka P, Pietschmann T, Thiel V, Hartmann R. 2013. Interferon lambda 4 signals via the IFNl receptor to regulate antiviral activity against HCV and coronaviruses. EMBO J 32(23):3055-3065.
21. Honda M, Sakai A, Yamashita T, Nakamoto Y, Mizukoshi E, Sakai Y, Yamashita T, Nakamura M, Shirasaki T, Horimoto K, Tanaka Y, Tokunaga K, Mizokami M, Kaneko S. 2010. Hepatic ISG expression is associated with genetic variation in IL28B and the outcome of IFN therapy for chronic hepatitis C. Gastroenterology 139(2):499-509.
22. Honda M, Shirasaki T, Shimakami T, Sakai A, Horii R, Arai K, Yamashita T, Sakai Y, Yamashita T, Okada H, Murai K, Nakamura M, Mizukoshi E, Kaneko S. 2014. Hepatic interferon-stimulated genes are differentially regulated in the liver of chronic hepatitis C patients with different interleukin-28B genotypes. Hepatology 59(3):828-838.
23. Horner SM, Gale M, Jr. 2013. Regulation of hepatic innate immunity by hepatitis C virus. Nat Med 19(7):879-888.
24. Jewell NA, Cline T, Mertz SE, Smirnov SV, Flaño E, Schindler C, Grieves JL, Durbin RK, Kotenko SV, Durbin JE. 2010. Lambda interferon is the predominant interferon induced by influenza A virus infection in vivo. Journal of Virology 84(21):11515-11522.
25. Jilg N, Chung RT. 2013. One more piece in the interleukin 28B gene puzzle? The case of hepatitis B. Hepatology 57(3):870-872.
26. Kamatani Y, Wattanapokayakit S, Ochi H, Kawaguchi T, Taka-hashi A, Hosono N, Kubo M, Tsunoda T, Kamatani N, Kumada H, Puseenam A, Sura T, Daigo Y, Chayama K, Chantratita W, Nakamura Y, Matsuda K. 2009. A genome-wide association study identifies variants in the HLA-DP locus associated with chronic hepatitis B in Asians. Nat Genet 41(5):591-595.
27. Konishi H, Motomura T, Matsumoto Y, Harimoto N, Ikegami T, Yoshizumi T, Soejima Y, Shirabe K, Fukuhara T, Maehara Y. 2013. Interferon-lambda4 genetic polymorphism is associated with the therapy response for hepatitis C virus recurrence after a living donor liver transplant. J Viral Hepat [Epub ahead of print]; DOI: 10.1111/jvh.12154.
28. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP. 2003. IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4(1):69-77.
29. Kroczynska B, Joshi S, Eklund EA, Verma A, Kotenko SV, Fish EN, Platanias LC. 2011. Regulatory effects of ribosomal S6 kinase 1 (RSK1) in IFNlambda signaling. J Biol Chem 286(2):1147-1156.
30. Lancet. 2014. Only just the beginning of the end of hepatitis C. Lancet 383(9914):281.
31. Lawitz E, Poordad FF, Pang PS, Hyland RH, Ding X, Mo H, Symonds WT, McHutchison JG, Membreno FE. 2014. Sofosbuvir and ledipasvir fixed-dose combination with and without ribavirin in treatment-naive and previously treated patients with genotype 1 hepatitis C virus infection (LONE-STAR): an open-label, randomised, phase 2 trial. Lancet 383(9916):515-523.
32. Makowska Z, Duong FHT, Trincucci G, Tough DF, Heim MH. 2011. Interferon-b and interferon-l signaling is not affected by interferon-induced refractoriness to interferon-a in vivo. Hepatology 53(4):1171-1180.
33. Malhotra S, Morcillo-Suarez C, Brassat D, Goertsches R, Lechner-Scott J, Urcelay E, Fernandez O, Drulovic J, Garcia-Merino A, Martinelli Boneschi F, Chan A, Vandenbroeck K, Navarro A, Bustamante MF, Rio J, Akkad DA, Giacalone G, Sanchez AJ, Leyva L, Alvarez-Lafuente R, Zettl UK, Oksen-berg J, Montalban X, Comabella M. 2011. IL28B polymorphisms are not associated with the response to interferon-beta in multiple sclerosis. J Neuroimmunol 239(1-2):101-104.
34. Manry J, Laval G, Patin E, Fornarino S, Itan Y, Fumagalli M, Sironi M, Tichit M, Bouchier C, Casanova JL, Barreiro LB, Quintana-Murci L. 2011. Evolutionary genetic dissection of human interferons. J Exp Med 208(13):2747-2759.
35. Marcello T, Grakoui A, Barba-Spaeth G, Machlin ES, Kotenko SV, MacDonald MR, Rice CM. 2006. Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 131(6):1887-1898.
36. Martin, Maureen P, Qi Y, James Goedert J, Shehnaz Hussain K, Gregory Kirk D, Hoots KW, Buchbinder S, Carrington M, Thio CL. 2010. IL28B polymorphism does not determine outcomes of hepatitis B Virus or HIV infection. J Infect Dis 202(11):1749-1753.
37. McFarland AP, Horner SM, Jarret A, Joslyn RC, Bindewald E, Shapiro BA, Delker DA, Hagedorn CH, Carrington M, Gale M, Jr., Savan R. 2014. The favorable IFNL3 genotype escapes mRNA decay mediated by AU-rich elements and hepatitis C virus-induced microRNAs. Nat Immunol 15(1):72-79.
38. Meager A, Visvalingam K, Dilger P, Bryan D, Wadhwa M. 2005. Biological activity of interleukins-28 and - 29: comparison with type I interferons. Cytokine 31(2):109-118.
39. Meissner EG, Bon D, Prokunina-Olsson L, Tang W, Masur H, O'Brien TR, Herrmann E, Kottilil S, Osinusi A. 2014. IFNL4-DeltaG genotype is associated with slower viral clearance in hepatitis C, genotype-1 patients treated with sofosbuvir and ribavirin. J Infect Dis [Epub ahead of print]. DOI: 10.1093/infdis/jit.827.
40. Miknis ZJ, Magracheva E, Li W, Zdanov A, Kotenko SV, Wlodawer A. 2010. Crystal structure of human interferon-lambda1 in complex with its high-affinity receptor interferon-lambdaR1. J Mol Biol 404(4):650-664.
41. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Fal-cone V, Sorgeloos F, Ehl S, Mayer D, Kochs G, Schwemmle M, Gunther S, Drosten C, Michiels T, Staeheli P. 2010. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J Virol 84(11):5670-5677.
42. Muchmore B, Tang W, Porter-Gill P, Kohaar I, Liu L, Brand N, Park H, Dickensheets H, Sheikh F, Rehermann B, Donnelly RP, O'Brien TR, Prokunina-Olsson L. 2013. Identification and characterization of interferon-l4 (IFN-l4), a novel class-2 cytokine which impairs clearance of hepatitis C virus (Abstract 182). Cytokine 63(3):286.
43. Muir AJ, Shiffman ML, Zaman A, Yoffe B, de la Torre A, Flamm S, Gordon SC, Marotta P, Vierling JM, Lopez-Talavera JC, Byrnes-Blake K, Fontana D, Freeman J, Gray T, Hausman D, Hunder NN, Lawitz E. 2010. Phase 1b study of pegylated interferon lambda 1 with or without ribavirin in patients with chronic genotype 1 hepatitis C virus infection. Hepatology 52(3):822-832.
44. Pacanowski M, Amur S, Zineh I. 2012. New genetic discoveries and treatment for hepatitis C. JAMA 307(18):1921-1922.
45. Pedergnana V, Abdel-Hamid M, Guergnon J, Mohsen A, Le Fouler L, Theodorou I, Mohamed MK, Fontanet A, Plan-coulaine S, Abel L. 2012. Analysis of IL28B variants in an egyptian population defines the 20 kilobases minimal region involved in spontaneous clearance of hepatitis C virus. PLoS One 7(6):e38578.
46. Pott J, Mahlakõiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, Staeheli P, Hornef MW. 2011. IFN-l determines the intestinal epithelial antiviral host defense. Proc Nat Acad Sci USA 108(19):7944-7949.
47. Prokunina-Olsson L, Muchmore B, Tang W, Pfeiffer RM, Park H, Dickensheets H, Hergott D, Porter-Gill P, Mumy A, Kohaar I, Chen S, Brand N, Tarway M, Liu L, Sheikh F, Astemborski J, Bonkovsky HL, Edlin BR, Howell CD, Morgan TR, Thomas DL, Rehermann B, Donnelly RP, O'Brien TR. 2013. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat Genet 45(2):164-171.
48. Rauch A, Kutalik Z, Descombes P, Cai T, Di Iulio J, Mueller T, Bochud M, Battegay M, Bernasconi E, Borovicka J, Colombo S, Cerny A, Dufour J-F, Furrer H, Günthard HF, Heim M, Hirschel B, Malinverni R, Moradpour D, Müllhaupt B, Wit-teck A, Beckmann JS, Berg T, Bergmann S, Negro F, Telenti A, Bochud P-Y. 2010. Genetic variation in IL28B Is associated with chronic hepatitis C and treatment failure: a genome-wide association study. Gastroenterology 138(4):1338-1345.
49. Sheahan T, Imanaka N, Marukian S, Dorner M, Liu P, Ploss A, Rice CM. 2014. Interferon lambda alleles predict innate antiviral immune responses and hepatitis C virus permissiveness. Cell Host Microbe 15(2):190-202.
50. Shepard CW, Finelli L, Alter MJ. 2005. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 5(9):558-567.
51. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S, Whitmore TE, Kuestner R, Garrigues U, Birks C, Rora-back J, Ostrander C, Dong D, Shin J, Presnell S, Fox B, Haldeman B, Cooper E, Taft D, Gilbert T, Grant FJ, Tackett M, Krivan W, McKnight G, Clegg C, Foster D, Klucher KM. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol 4(1):63-68.
52. Sommereyns C, Paul S, Staeheli P, Michiels T. 2008. IFNlambda (IFN-l) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog 4(3):e1000017.
53. Suppiah V, Moldovan M, Ahlenstiel G, Berg T, Weltman M, Abate ML, Bassendine M, Spengler U, Dore GJ, Powell E, Riordan S, Sheridan D, Smedile A, Fragomeli V, Muller T, Bahlo M, Stewart GJ, Booth DR, George J. 2009. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat Genet 41(10):1100-1104.
54. Tanaka Y, Nishida N, Sugiyama M, Kurosaki M, Matsuura K, Sakamoto N, Nakagawa M, Korenaga M, Hino K, Hige S, Ito Y, Mita E, Tanaka E, Mochida S, Murawaki Y, Honda M, Sakai A, Hiasa Y, Nishiguchi S, Koike A, Sakaida I, Imamura M, Ito K, Yano K, Masaki N, Sugauchi F, Izumi N, Tokunaga K, Mizokami M. 2009. Genome-wide association of IL28B with response to pegylated interferon-[alpha] and ribavirin therapy for chronic hepatitis C. Nat Genet 41(10):1105-1109.
55. Tang W, Dennis M, Prokunina-Olsson L. 2013. Comparative analysis of biological activity of 11 mammalian paralogs of the novel human interferon IFNl-4 (IFNL4) associated with viral clearance. Presented at the 63rd Annual Meeting of The American Society of Human Genetics, October 2013, Boston, MA
56. Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, Kidd J, Kidd K, Khakoo SI, Alexander G, Goedert JJ, Kirk GD, Donfield SM, Rosen HR, Tobler LH, Busch MP, McHutchison JG, Goldstein DB, Carrington M. 2009. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461(7265):798-801.
57. Thompson AJ, Muir AJ, Sulkowski MS, Ge D, Fellay J, Shianna KV, Urban T, Afdhal NH, Jacobson IM, Esteban R, Poordad F, Lawitz EJ, McCone J, Shiffman ML, Galler GW, Lee WM, Reindollar R, King JW, Kwo PY, Ghalib RH, Freilich B, Nyberg LM, Zeuzem S, Poynard T, Vock DM, Pieper KS, Patel K, Tillmann HL, Noviello S, Koury K, Pedicone LD, Brass CA, Albrecht JK, Goldstein DB, McHutchison JG. 2010. Interleukin-28B polymorphism improves viral kinetics and is the strongest pretreatment predictor of sustained virologic response in hepatitis C virus-1 patients. Gastroenterology 139(1):120-129.
58. Urban TJ, Thompson AJ, Bradrick SS, Fellay J, Schuppan D, Cronin KD, Hong L, McKenzie A, Patel K, Shianna KV, McHutchison JG, Goldstein DB, Afdhal N. 2010. IL28B genotype is associated with differential expression of intrahepatic interferon-stimulated genes in patients with chronic hepatitis C. Hepatology 52(6):1888-1896.
59. Zeuzem S, Soriano V, Asselah T, Bronowicki J-P, Lohse AW, Mullhaupt B, Schuchmann M, Bourliere M, Buti M, Roberts SK, Gane EJ, Stern JO, Vinisko R, Kukolj G, Gallivan J-P, Bocher W-O, Mensa FJ. 2013. Faldaprevir and deleobuvir for HCV genotype 1 infection. N Engl J Med 369(7):630-639.
60. Zhou Z, Hamming OJ, Ank N, Paludan SR, Nielsen AL, Hartmann R. 2007. Type III interferon (IFN) induces a type I IFN-like response in a restricted subset of cells through signaling pathways involving both the Jak-STAT pathway and the mitogen-activated protein kinases. J Virol 81(14):7749-7758.