Shared and Distinct Functions of Type I and Type III Interferons

Immunity

Volumn 50, Issue 4, 2019, Pages 907-923

  Lazear, Helen M ^a   Schoggins, John W ^b   Diamond, Michael S ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; TYPE III INTERFERON; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; INTERFERON TYPE III; TRANSCRIPTOME;

ANTINEOPLASTIC ACTIVITY; ANTIVIRAL ACTIVITY; AUTOIMMUNITY; HUMAN; IMMUNOMODULATION; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; ADAPTIVE IMMUNITY; ANIMAL; ANTIBODY SPECIFICITY; AUTOIMMUNE DISEASE; COMPARATIVE STUDY; EPITHELIUM CELL; FEMALE; FETOMATERNAL TRANSFUSION; GENETIC TRANSCRIPTION; IMMUNOLOGY; MALE; MOUSE; NEOPLASM; PREGNANCY; VIRUS INFECTION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIVIRAL AGENTS; AUTOIMMUNE DISEASES; EPITHELIAL CELLS; FEMALE; HUMANS; INTERFERON TYPE I; INTERFERONS; MALE; MATERNAL-FETAL EXCHANGE; MICE; NEOPLASMS; ORGAN SPECIFICITY; PREGNANCY; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TRANSCRIPTOME; VIRUS DISEASES;

EID: 85063796827     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2019.03.025     Document Type: Review

References (223)

1. Aboulnasr, F., Hazari, S., Nayak, S., Chandra, P.K., Panigrahi, R., Ferraris, P., Chava, S., Kurt, R., Song, K., Dash, A., et al. IFN-λ inhibits MiR-122 transcription through a Stat3-HNF4α inflammatory feedback loop in an IFN-α resistant HCV cell culture system. PLoS ONE, 10, 2015, e0141655.
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. Immunother. 59 (2010), 1059–1071.
3. Alspach, E., Lussier, D.M., Schreiber, R.D., Interferon γ and its important roles in promoting and inhibiting spontaneous and therapeutic cancer immunity. Cold Spring Harb. Perspect. Biol., 11, 2018, a028480.
4. Ander, S.E., Diamond, M.S., Coyne, C.B., Immune responses at the maternal-fetal interface. Sci. Immunol., 4, 2019, eaat6114.
5. Andrade, D., Kim, M., Blanco, L.P., Karumanchi, S.A., Koo, G.C., Redecha, P., Kirou, K., Alvarez, A.M., Mulla, M.J., Crow, M.K., et al. Interferon-α and angiogenic dysregulation in pregnant lupus patients who develop preeclampsia. Arthritis Rheumatol. 67 (2015), 977–987.
6. Ank, N., Iversen, M.B., Bartholdy, C., Staeheli, P., Hartmann, R., Jensen, U.B., Dagnaes-Hansen, F., Thomsen, A.R., Chen, Z., Haugen, H., et al. An important role for type III interferon (IFN-lambda/IL-28) in TLR-induced antiviral activity. J. Immunol. 180 (2008), 2474–2485.
7. Baldridge, M.T., Nice, T.J., McCune, B.T., Yokoyama, C.C., Kambal, A., Wheadon, M., Diamond, M.S., Ivanova, Y., Artyomov, M., Virgin, H.W., Commensal microbes and interferon-λ determine persistence of enteric murine norovirus infection. Science 347 (2015), 266–269.
8. Baldridge, M.T., Lee, S., Brown, J.J., McAllister, N., Urbanek, K., Dermody, T.S., Nice, T.J., Virgin, H.W., Expression of Ifnlr1 on intestinal epithelial cells is critical to the antiviral effects of interferon lambda against norovirus and reovirus. J. Virol., 91, 2017 e02079-16.
9. Bamford, C.G.G., Aranday-Cortes, E., Filipe, I.C., Sukumar, S., Mair, D., Filipe, A.D.S., Mendoza, J.L., Garcia, K.C., Fan, S., Tishkoff, S.A., McLauchlan, J., A polymorphic residue that attenuates the antiviral potential of interferon lambda 4 in hominid lineages. PLoS Pathog., 14, 2018, e1007307.
10. Bayas, A., Gold, R., Lessons from 10 years of interferon beta-1b (Betaferon/Betaseron) treatment. J. Neurol. 250:Suppl 4 (2003), IV3–IV8.
11. Bayer, A., Lennemann, N.J., Ouyang, Y., Bramley, J.C., Morosky, S., Marques, E.T. Jr., Cherry, S., Sadovsky, Y., Coyne, C.B., Type III interferons produced by human placental trophoblasts confer protection against Zika virus infection. Cell Host Microbe 19 (2016), 705–712.
12. Belloni, L., Allweiss, L., Guerrieri, F., Pediconi, N., Volz, T., Pollicino, T., Petersen, J., Raimondo, G., Dandri, M., Levrero, M., IFN-α inhibits HBV transcription and replication in cell culture and in humanized mice by targeting the epigenetic regulation of the nuclear cccDNA minichromosome. J. Clin. Invest. 122 (2012), 529–537.
13. Bierne, H., Travier, L., Mahlakõiv, T., Tailleux, L., Subtil, A., Lebreton, A., Paliwal, A., Gicquel, B., Staeheli, P., Lecuit, M., Cossart, P., Activation of type III interferon genes by pathogenic bacteria in infected epithelial cells and mouse placenta. PLoS ONE, 7, 2012, e39080.
14. Blazek, K., Eames, H.L., Weiss, M., Byrne, A.J., Perocheau, D., Pease, J.E., Doyle, S., McCann, F., Williams, R.O., Udalova, I.A., IFN-λ resolves inflammation via suppression of neutrophil infiltration and IL-1β production. J. Exp. Med. 212 (2015), 845–853.
15. Bolen, C.R., Ding, S., Robek, M.D., Kleinstein, S.H., Dynamic expression profiling of type I and type III interferon-stimulated hepatocytes reveals a stable hierarchy of gene expression. Hepatology 59 (2014), 1262–1272.
16. Booy, S., Hofland, L., van Eijck, C., Potentials of interferon therapy in the treatment of pancreatic cancer. J. Interferon Cytokine Res. 35 (2015), 327–339.
17. Borden, E.C., Interferons α and β in cancer: therapeutic opportunities from new insights. Nat. Rev. Drug Discov. 18 (2019), 219–234.
18. Boxx, G.M., Cheng, G., The roles of type I interferon in bacterial infection. Cell Host Microbe 19 (2016), 760–769.
19. Broggi, A., Tan, Y., Granucci, F., Zanoni, I., IFN-λ suppresses intestinal inflammation by non-translational regulation of neutrophil function. Nat. Immunol. 18 (2017), 1084–1093.
20. Budhwani, M., Mazzieri, R., Dolcetti, R., Plasticity of type I interferon-mediated responses in cancer therapy: from anti-tumor immunity to resistance. Front. Oncol., 8, 2018, 322.
21. Burkart, C., Arimoto, K., Tang, T., Cong, X., Xiao, N., Liu, Y.C., Kotenko, S.V., Ellies, L.G., Zhang, D.E., Usp18 deficient mammary epithelial cells create an antitumour environment driven by hypersensitivity to IFN-λ and elevated secretion of Cxcl10. EMBO Mol. Med. 5 (2013), 1035–1050.
22. Caine, E.A., Scheaffer, S.M., Arora, N., Zaitsev, K., Artyomov, M.N., Coyne, C.B., Moley, K.H., Diamond, M.S., Interferon lambda protects the female reproductive tract against Zika virus infection. Nat. Commun., 10, 2019, 280.
23. Cascinelli, N., Belli, F., MacKie, R.M., Santinami, M., Bufalino, R., Morabito, A., Effect of long-term adjuvant therapy with interferon alpha-2a in patients with regional node metastases from cutaneous melanoma: a randomised trial. Lancet 358 (2001), 866–869.
24. Cohen, T.S., Prince, A.S., Bacterial pathogens activate a common inflammatory pathway through IFNλ regulation of PDCD4. PLoS Pathog., 9, 2013, e1003682.
25. Cooksley, W.G., Piratvisuth, T., Lee, S.D., Mahachai, V., Chao, Y.C., Tanwandee, T., Chutaputti, A., Chang, W.Y., Zahm, F.E., Pluck, N., Peginterferon alpha-2a (40 kDa): an advance in the treatment of hepatitis B e antigen-positive chronic hepatitis B. J. Viral Hepat. 10 (2003), 298–305.
26. Corry, J., Arora, N., Good, C.A., Sadovsky, Y., Coyne, C.B., Organotypic models of type III interferon-mediated protection from Zika virus infections at the maternal-fetal interface. Proc. Natl. Acad. Sci. USA 114 (2017), 9433–9438.
27. Crotta, S., Davidson, S., Mahlakoiv, T., Desmet, C.J., Buckwalter, M.R., Albert, M.L., Staeheli, P., Wack, A., Type I and type III interferons drive redundant amplification loops to induce a transcriptional signature in influenza-infected airway epithelia. PLoS Pathog., 9, 2013, e1003773.
28. Crouse, J., Kalinke, U., Oxenius, A., Regulation of antiviral T cell responses by type I interferons. Nat. Rev. Immunol. 15 (2015), 231–242.
29. Crow, Y.J., Manel, N., Aicardi-Goutières syndrome and the type I interferonopathies. Nat. Rev. Immunol. 15 (2015), 429–440.
30. Daffis, S., Szretter, K.J., Schriewer, J., Li, J., Youn, S., Errett, J., Lin, T.Y., Schneller, S., Zust, R., Dong, H., et al. 2′-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468 (2010), 452–456.
31. Dai, J., Megjugorac, N.J., Gallagher, G.E., Yu, R.Y., Gallagher, G., IFN-lambda1 (IL-29) inhibits GATA3 expression and suppresses Th2 responses in human naive and memory T cells. Blood 113 (2009), 5829–5838.
32. Daniels, B.P., Holman, D.W., Cruz-Orengo, L., Jujjavarapu, H., Durrant, D.M., Klein, R.S., Viral pathogen-associated molecular patterns regulate blood-brain barrier integrity via competing innate cytokine signals. MBio, 5, 2014 e01476–e14.
33. Daniels, B.P., Jujjavarapu, H., Durrant, D.M., Williams, J.L., Green, R.R., White, J.P., Lazear, H.M., Gale, M. Jr., Diamond, M.S., Klein, R.S., Regional astrocyte IFN signaling restricts pathogenesis during neurotropic viral infection. J. Clin. Invest. 127 (2017), 843–856.
34. Davis, G.L., Balart, L.A., Schiff, E.R., Lindsay, K., Bodenheimer, H.C. Jr., Perrillo, R.P., Carey, W., Jacobson, I.M., Payne, J., Dienstag, J.L., Hepatitis Interventional Therapy Group. Treatment of chronic hepatitis C with recombinant interferon alfa. A multicenter randomized, controlled trial. N. Engl. J. Med. 321 (1989), 1501–1506.
35. de Groen, R.A., Groothuismink, Z.M., Liu, B.S., Boonstra, A., IFN-λ is able to augment TLR-mediated activation and subsequent function of primary human B cells. J. Leukoc. Biol. 98 (2015), 623–630.
36. de Weerd, N.A., Vivian, J.P., Nguyen, T.K., Mangan, N.E., Gould, J.A., Braniff, S.J., Zaker-Tabrizi, L., Fung, K.Y., Forster, S.C., Beddoe, T., et al. Structural basis of a unique interferon-β signaling axis mediated via the receptor IFNAR1. Nat. Immunol. 14 (2013), 901–907.
37. de Weerd, N.A., Matthews, A.Y., Pattie, P.R., Bourke, N.M., Lim, S.S., Vivian, J.P., Rossjohn, J., Hertzog, P.J., A hot spot on interferon α/β receptor subunit 1 (IFNAR1) underpins its interaction with interferon-β and dictates signaling. J. Biol. Chem. 292 (2017), 7554–7565.
38. Delhaye, S., Paul, S., Blakqori, G., Minet, M., Weber, F., Staeheli, P., Michiels, T., Neurons produce type I interferon during viral encephalitis. Proc. Natl. Acad. Sci. USA 103 (2006), 7835–7840.
39. Dhib-Jalbut, S., Marks, S., Interferon-beta mechanisms of action in multiple sclerosis. Neurology 74:Suppl 1 (2010), S17–S24.
40. Di Bisceglie, A.M., Martin, P., Kassianides, C., Lisker-Melman, M., Murray, L., Waggoner, J., Goodman, Z., Banks, S.M., Hoofnagle, J.H., Recombinant interferon alfa therapy for chronic hepatitis C. A randomized, double-blind, placebo-controlled trial. N. Engl. J. Med. 321 (1989), 1506–1510.
41. Di Trolio, R., Simeone, E., Di Lorenzo, G., Buonerba, C., Ascierto, P.A., The use of interferon in melanoma patients: a systematic review. Cytokine Growth Factor Rev. 26 (2015), 203–212.
42. Ding, Q., Gaska, J.M., Douam, F., Wei, L., Kim, D., Balev, M., Heller, B., Ploss, A., Species-specific disruption of STING-dependent antiviral cellular defenses by the Zika virus NS2B3 protease. Proc. Natl. Acad. Sci. USA 115 (2018), E6310–E6318.
43. Douam, F., Soto Albrecht, Y.E., Hrebikova, G., Sadimin, E., Davidson, C., Kotenko, S.V., Ploss, A., Type III interferon-mediated signaling is critical for controlling live attenuated yellow fever virus infection in vivo. MBio, 8, 2017 e00819-17.
44. Doyle, S.E., Schreckhise, H., Khuu-Duong, K., Henderson, K., Rosler, R., Storey, H., Yao, L., Liu, H., Barahmand-pour, F., Sivakumar, P., et al. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44 (2006), 896–906.
45. Drokhlyansky, E., Göz Aytürk, D., Soh, T.K., Chrenek, R., O'Loughlin, E., Madore, C., Butovsky, O., Cepko, C.L., The brain parenchyma has a type I interferon response that can limit virus spread. Proc. Natl. Acad. Sci. USA 114 (2017), E95–E104.
46. Duncan, C.J., Mohamad, S.M., Young, D.F., Skelton, A.J., Leahy, T.R., Munday, D.C., Butler, K.M., Morfopoulou, S., Brown, J.R., Hubank, M., et al. Human IFNAR2 deficiency: Lessons for antiviral immunity. Sci. Transl. Med., 7, 2015, 307ra154.
47. Eggermont, A.M., Suciu, S., Santinami, M., Testori, A., Kruit, W.H., Marsden, J., Punt, C.J., Salès, F., Gore, M., Mackie, R., et al., EORTC Melanoma Group. Adjuvant therapy with pegylated interferon alfa-2b versus observation alone in resected stage III melanoma: final results of EORTC 18991, a randomised phase III trial. Lancet 372 (2008), 117–126.
48. Egli, A., Santer, D.M., O'Shea, D., Barakat, K., Syedbasha, M., Vollmer, M., Baluch, A., Bhat, R., Groenendyk, J., Joyce, M.A., et al. IL-28B is a key regulator of B- and T-cell vaccine responses against influenza. PLoS Pathog., 10, 2014, e1004556.
49. Espinosa, V., Dutta, O., McElrath, C., Du, P., Chang, Y.J., Cicciarelli, B., Pitler, A., Whitehead, I., Obar, J.J., Durbin, J.E., et al. Type III interferon is a critical regulator of innate antifungal immunity. Sci. Immunol., 2, 2017, eaan5357.
50. Fallet, B., Narr, K., Ertuna, Y.I., Remy, M., Sommerstein, R., Cornille, K., Kreutzfeldt, M., Page, N., Zimmer, G., Geier, F., et al. Interferon-driven deletion of antiviral B cells at the onset of chronic infection. Sci. Immunol., 1, 2016, eaah6817.
51. 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, 4, 2009, e4933.
52. Fox, J.M., Crabtree, J.M., Sage, L.K., Tompkins, S.M., Tripp, R.A., Interferon lambda upregulates IDO1 expression in respiratory epithelial cells after influenza virus infection. J. Interferon Cytokine Res. 35 (2015), 554–562.
53. François-Newton, V., Magno de Freitas Almeida, G., Payelle-Brogard, B., Monneron, D., Pichard-Garcia, L., Piehler, J., Pellegrini, S., Uzé, G., USP18-based negative feedback control is induced by type I and type III interferons and specifically inactivates interferon α response. PLoS ONE, 6, 2011, e22200.
54. Fung, K.Y., Mangan, N.E., Cumming, H., Horvat, J.C., Mayall, J.R., Stifter, S.A., De Weerd, N., Roisman, L.C., Rossjohn, J., Robertson, S.A., et al. Interferon-ε protects the female reproductive tract from viral and bacterial infection. Science 339 (2013), 1088–1092.
55. Galani, I.E., Triantafyllia, V., Eleminiadou, E.E., Koltsida, O., Stavropoulos, A., Manioudaki, M., Thanos, D., Doyle, S.E., Kotenko, S.V., Thanopoulou, K., Andreakos, E., Interferon-λ mediates non-redundant front-line antiviral protection against influenza virus infection without compromising host fitness. Immunity 46 (2017), 875–890.e6.
56. García-Sastre, A., Ten strategies of interferon evasion by viruses. Cell Host Microbe 22 (2017), 176–184.
57. Gizzi, A.S., Grove, T.L., Arnold, J.J., Jose, J., Jangra, R.K., Garforth, S.J., Du, Q., Cahill, S.M., Dulyaninova, N.G., Love, J.D., et al. A naturally occurring antiviral ribonucleotide encoded by the human genome. Nature 558 (2018), 610–614.
58. Good, C., Wells, A.I., Coyne, C.B., Type III interferon signaling restricts enterovirus 71 infection of goblet cells. Sci. Adv., 5, 2019, u4255.
59. Goodin, D.S., Ebers, G.C., Cutter, G., Cook, S.D., O'Donnell, T., Reder, A.T., Kremenchutzky, M., Oger, J., Rametta, M., Beckmann, K., Knappertz, V., Cause of death in MS: long-term follow-up of a randomised cohort, 21 years after the start of the pivotal IFNβ-1b study. BMJ Open, 2, 2012, e001972.
60. Goritzka, M., Durant, L.R., Pereira, C., Salek-Ardakani, S., Openshaw, P.J., Johansson, C., Alpha/beta interferon receptor signaling amplifies early proinflammatory cytokine production in the lung during respiratory syncytial virus infection. J. Virol. 88 (2014), 6128–6136.
61. Goritzka, M., Makris, S., Kausar, F., Durant, L.R., Pereira, C., Kumagai, Y., Culley, F.J., Mack, M., Akira, S., Johansson, C., Alveolar macrophage-derived type I interferons orchestrate innate immunity to RSV through recruitment of antiviral monocytes. J. Exp. Med. 212 (2015), 699–714.
62. Gorman, M.J., Caine, E.A., Zaitsev, K., Begley, M.C., Weger-Lucarelli, J., Uccellini, M.B., Tripathi, S., Morrison, J., Yount, B.L., Dinnon, K.H. 3rd, et al. An immunocompetent mouse model of Zika virus infection. Cell Host Microbe 23 (2018), 672–685.e6.
63. Grant, A., Ponia, S.S., Tripathi, S., Balasubramaniam, V., Miorin, L., Sourisseau, M., Schwarz, M.C., Sánchez-Seco, M.P., Evans, M.J., Best, S.M., García-Sastre, A., Zika virus targets human STAT2 to inhibit type I interferon signaling. Cell Host Microbe 19 (2016), 882–890.
64. Greenberg, H.B., Pollard, R.B., Lutwick, L.I., Gregory, P.B., Robinson, W.S., Merigan, T.C., Effect of human leukocyte interferon on hepatitis B virus infection in patients with chronic active hepatitis. N. Engl. J. Med. 295 (1976), 517–522.
65. Griffiths, S.J., Dunnigan, C.M., Russell, C.D., Haas, J.G., The role of interferon-λ locus polymorphisms in hepatitis C and other infectious diseases. J. Innate Immun. 7 (2015), 231–242.
66. Grine, L., Dejager, L., Libert, C., Vandenbroucke, R.E., An inflammatory triangle in psoriasis: TNF, type I IFNs and IL-17. Cytokine Growth Factor Rev. 26 (2015), 25–33.
67. Haller, O., Staeheli, P., Schwemmle, M., Kochs, G., Mx GTPases: dynamin-like antiviral machines of innate immunity. Trends Microbiol. 23 (2015), 154–163.
68. Hamming, O.J., Terczyńska-Dyla, E., Vieyres, G., Dijkman, R., Jørgensen, S.E., Akhtar, H., Siupka, P., Pietschmann, T., Thiel, V., Hartmann, R., Interferon lambda 4 signals via the IFNλ receptor to regulate antiviral activity against HCV and coronaviruses. EMBO J. 32 (2013), 3055–3065.
69. Hansson, J., Aamdal, S., Bastholt, L., Brandberg, Y., Hernberg, M., Nilsson, B., Stierner, U., von der Maase, H., Nordic Melanoma Cooperative Group. Two different durations of adjuvant therapy with intermediate-dose interferon alfa-2b in patients with high-risk melanoma (Nordic IFN trial): a randomised phase 3 trial. Lancet Oncol. 12 (2011), 144–152.
70. Harris, B.D., Schreiter, J., Chevrier, M., Jordan, J.L., Walter, M.R., Human interferon-ε and interferon-κ exhibit low potency and low affinity for cell-surface IFNAR and the poxvirus antagonist B18R. J. Biol. Chem. 293 (2018), 16057–16068.
71. Hauser, S.L., Bar-Or, A., Comi, G., Giovannoni, G., Hartung, H.P., Hemmer, B., Lublin, F., Montalban, X., Rammohan, K.W., Selmaj, K., et al., OPERA I and OPERA II Clinical Investigators. Ocrelizumab versus Interferon Beta-1a in Relapsing Multiple Sclerosis. N. Engl. J. Med. 376 (2017), 221–234.
72. Heim, M.H., 25 years of interferon-based treatment of chronic hepatitis C: an epoch coming to an end. Nat. Rev. Immunol. 13 (2013), 535–542.
73. Hendricks, M.R., Lashua, L.P., Fischer, D.K., Flitter, B.A., Eichinger, K.M., Durbin, J.E., Sarkar, S.N., Coyne, C.B., Empey, K.M., Bomberger, J.M., Respiratory syncytial virus infection enhances Pseudomonas aeruginosa biofilm growth through dysregulation of nutritional immunity. Proc. Natl. Acad. Sci. USA 113 (2016), 1642–1647.
74. Hermant, P., Francius, C., Clotman, F., Michiels, T., IFN-ε is constitutively expressed by cells of the reproductive tract and is inefficiently secreted by fibroblasts and cell lines. PLoS ONE, 8, 2013, e71320.
75. Ho, H.H., Ivashkiv, L.B., Role of STAT3 in type I interferon responses. Negative regulation of STAT1-dependent inflammatory gene activation. J. Biol. Chem. 281 (2006), 14111–14118.
76. Hoffmann, H.H., Schneider, W.M., Rice, C.M., Interferons and viruses: an evolutionary arms race of molecular interactions. Trends Immunol. 36 (2015), 124–138.
77. Honda, K., Yanai, H., Negishi, H., Asagiri, M., Sato, M., Mizutani, T., Shimada, N., Ohba, Y., Takaoka, A., Yoshida, N., Taniguchi, T., IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 434 (2005), 772–777.
78. Honda, K., Takaoka, A., Taniguchi, T., Type I interferon [corrected] gene induction by the interferon regulatory factor family of transcription factors. Immunity 25 (2006), 349–360.
79. Hornung, V., Hartmann, R., Ablasser, A., Hopfner, K.P., OAS proteins and cGAS: unifying concepts in sensing and responding to cytosolic nucleic acids. Nat. Rev. Immunol. 14 (2014), 521–528.
80. Huang, Y., Li, M.H., Hou, M., Xie, Y., Peginterferon alfa-2a for the treatment of chronic hepatitis C in the era of direct-acting antivirals. HBPD INT 16 (2017), 470–479.
81. Hwang, M., Bergmann, C.C., Alpha/Beta Interferon (IFN-α/β) signaling in astrocytes mediates protection against viral encephalomyelitis and regulates IFN-γ-dependent responses. J. Virol., 92, 2018 e01901-17.
82. Hyde, J.L., Gardner, C.L., Kimura, T., White, J.P., Liu, G., Trobaugh, D.W., Huang, C., Tonelli, M., Paessler, S., Takeda, K., et al. A viral RNA structural element alters host recognition of nonself RNA. Science 343 (2014), 783–787.
83. Ingle, H., Peterson, S.T., Baldridge, M.T., Distinct effects of type I and III interferons on enteric viruses. Viruses, 10, 2018, E46.
84. Isaacs, A., Lindenmann, J., Virus interference. I. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 147 (1957), 258–267.
85. Isaacs, A., Lindenmann, J., Valentine, R.C., Virus interference. II. Some properties of interferon. Proc. R. Soc. Lond. B Biol. Sci. 147 (1957), 268–273.
86. Jacobs, L., O'Malley, J., Freeman, A., Ekes, R., Intrathecal interferon reduces exacerbations of multiple sclerosis. Science 214 (1981), 1026–1028.
87. Jagger, B.W., Miner, J.J., Cao, B., Arora, N., Smith, A.M., Kovacs, A., Mysorekar, I.U., Coyne, C.B., Diamond, M.S., Gestational stage and IFN-λ signaling regulate ZIKV infection in utero. Cell Host Microbe 22 (2017), 366–376.e3.
88. Jakimovski, D., Kolb, C., Ramanathan, M., Zivadinov, R., Weinstock-Guttman, B., Interferon β for multiple sclerosis. Cold Spring Harb. Perspect. Med., 8, 2018, a032003.
89. Janssen, H.L., van Zonneveld, M., Senturk, H., Zeuzem, S., Akarca, U.S., Cakaloglu, Y., Simon, C., So, T.M., Gerken, G., de Man, R.A., et al. HBV 99-01 Study Group, Rotterdam Foundation for Liver Research. Pegylated interferon alfa-2b alone or in combination with lamivudine for HBeAg-positive chronic hepatitis B: a randomised trial. Lancet 365 (2005), 123–129.
90. Jewell, N.A., Cline, T., Mertz, S.E., Smirnov, S.V., Flaño, 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. 84 (2010), 11515–11522.
91. Jilg, N., Lin, W., Hong, J., Schaefer, E.A., Wolski, D., Meixong, J., Goto, K., Brisac, C., Chusri, P., Fusco, D.N., et al. Kinetic differences in the induction of interferon stimulated genes by interferon-α and interleukin 28B are altered by infection with hepatitis C virus. Hepatology 59 (2014), 1250–1261.
92. Johansson, C., Wetzel, J.D., He, J., Mikacenic, C., Dermody, T.S., Kelsall, B.L., Type I interferons produced by hematopoietic cells protect mice against lethal infection by mammalian reovirus. J. Exp. Med. 204 (2007), 1349–1358.
93. Jordan, W.J., Eskdale, J., Srinivas, S., Pekarek, V., Kelner, D., Rodia, M., Gallagher, G., Human interferon lambda-1 (IFN-lambda1/IL-29) modulates the Th1/Th2 response. Genes Immun. 8 (2007), 254–261.
94. Kagan, J.C., Su, T., Horng, T., Chow, A., Akira, S., Medzhitov, R., TRAM couples endocytosis of Toll-like receptor 4 to the induction of interferon-beta. Nat. Immunol. 9 (2008), 361–368.
95. Kappos, L., Wiendl, H., Selmaj, K., Arnold, D.L., Havrdova, E., Boyko, A., Kaufman, M., Rose, J., Greenberg, S., Sweetser, M., et al. Daclizumab HYP versus Interferon Beta-1a in Relapsing Multiple Sclerosis. N. Engl. J. Med. 373 (2015), 1418–1428.
96. Kernbauer, E., Ding, Y., Cadwell, K., An enteric virus can replace the beneficial function of commensal bacteria. Nature 516 (2014), 94–98.
97. Key, F.M., Peter, B., Dennis, M.Y., Huerta-Sánchez, E., Tang, W., Prokunina-Olsson, L., Nielsen, R., Andrés, A.M., Selection on a variant associated with improved viral clearance drives local, adaptive pseudogenization of interferon lambda 4 (IFNL4). PLoS Genet., 10, 2014, e1004681.
98. Khan, U.T., Tanasescu, R., Constantinescu, C.S., PEGylated IFNβ-1a in the treatment of multiple sclerosis. Expert Opin. Biol. Ther. 15 (2015), 1077–1084.
99. Kirkwood, J.M., Strawderman, M.H., Ernstoff, M.S., Smith, T.J., Borden, E.C., Blum, R.H., Interferon alfa-2b adjuvant therapy of high-risk resected cutaneous melanoma: the Eastern Cooperative Oncology Group Trial EST 1684. J. Clin. Oncol. 14 (1996), 7–17.
100. Kirkwood, J.M., Ibrahim, J.G., Sosman, J.A., Sondak, V.K., Agarwala, S.S., Ernstoff, M.S., Rao, U., High-dose interferon alfa-2b significantly prolongs relapse-free and overall survival compared with the GM2-KLH/QS-21 vaccine in patients with resected stage IIB-III melanoma: results of intergroup trial E1694/S9512/C509801. J. Clin. Oncol. 19 (2001), 2370–2380.
101. Klein, R.S., Hunter, C.A., Protective and pathological immunity during central nervous system infections. Immunity 46 (2017), 891–909.
102. Klinkhammer, J., Schnepf, D., Ye, L., Schwaderlapp, M., Gad, H.H., Hartmann, R., Garcin, D., Mahlakõiv, T., Staeheli, P., IFN-λ prevents influenza virus spread from the upper airways to the lungs and limits virus transmission. eLife, 7, 2018, e33354.
103. Kohli, A., Zhang, X., Yang, J., Russell, R.S., Donnelly, R.P., Sheikh, F., Sherman, A., Young, H., Imamichi, T., Lempicki, R.A., et al. Distinct and overlapping genomic profiles and antiviral effects of Interferon-λ and -α on HCV-infected and noninfected hepatoma cells. J. Viral Hepat. 19 (2012), 843–853.
104. Koltsida, O., Hausding, M., Stavropoulos, A., Koch, S., Tzelepis, G., Ubel, C., Kotenko, S.V., Sideras, P., Lehr, H.A., Tepe, M., et al. IL-28A (IFN-λ2) modulates lung DC function to promote Th1 immune skewing and suppress allergic airway disease. EMBO Mol. Med. 3 (2011), 348–361.
105. Kotenko, S.V., Durbin, J.E., Contribution of type III interferons to antiviral immunity: location, location, location. J. Biol. Chem. 292 (2017), 7295–7303.
106. Kotenko, S.V., Gallagher, G., Baurin, V.V., Lewis-Antes, A., Shen, M., Shah, N.K., Langer, J.A., Sheikh, F., Dickensheets, H., Donnelly, R.P., IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4 (2003), 69–77.
107. Krause, C.D., Pestka, S., Cut, copy, move, delete: The study of human interferon genes reveal multiple mechanisms underlying their evolution in amniotes. Cytokine 76 (2015), 480–495.
108. Kumar, A., Hou, S., Airo, A.M., Limonta, D., Mancinelli, V., Branton, W., Power, C., Hobman, T.C., Zika virus inhibits type-I interferon production and downstream signaling. EMBO Rep. 17 (2016), 1766–1775.
109. LaFleur, D.W., Nardelli, B., Tsareva, T., Mather, D., Feng, P., Semenuk, M., Taylor, K., Buergin, M., Chinchilla, D., Roshke, V., et al. Interferon-kappa, a novel type I interferon expressed in human keratinocytes. J. Biol. Chem. 276 (2001), 39765–39771.
110. Lasfar, A., Lewis-Antes, A., Smirnov, S.V., Anantha, S., Abushahba, W., Tian, B., Reuhl, K., Dickensheets, H., Sheikh, F., Donnelly, R.P., et al. Characterization of the mouse IFN-lambda ligand-receptor system: IFN-lambdas exhibit antitumor activity against B16 melanoma. Cancer Res. 66 (2006), 4468–4477.
111. Lasfar, A., Gogas, H., Zloza, A., Kaufman, H.L., Kirkwood, J.M., IFN-λ cancer immunotherapy: new kid on the block. Immunotherapy 8 (2016), 877–888.
112. Lau, G.K., Piratvisuth, T., Luo, K.X., Marcellin, P., Thongsawat, S., Cooksley, G., Gane, E., Fried, M.W., Chow, W.C., Paik, S.W., et al., Peginterferon Alfa-2a HBeAg-Positive Chronic Hepatitis B Study Group. Peginterferon Alfa-2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N. Engl. J. Med. 352 (2005), 2682–2695.
113. Lazear, H.M., Lancaster, A., Wilkins, C., Suthar, M.S., Huang, A., Vick, S.C., Clepper, L., Thackray, L., Brassil, M.M., Virgin, H.W., et al. IRF-3, IRF-5, and IRF-7 coordinately regulate the type I IFN response in myeloid dendritic cells downstream of MAVS signaling. PLoS Pathog., 9, 2013, e1003118.
114. Lazear, H.M., Daniels, B.P., Pinto, A.K., Huang, A.C., Vick, S.C., Doyle, S.E., Gale, M. Jr., Klein, R.S., Diamond, M.S., Interferon-λ restricts West Nile virus neuroinvasion by tightening the blood-brain barrier. Sci. Transl. Med., 7, 2015, 284ra59.
115. Lazear, H.M., Nice, T.J., Diamond, M.S., Interferon-λ: immune functions at barrier surfaces and beyond. Immunity 43 (2015), 15–28.
116. Lazear, H.M., Govero, J., Smith, A.M., Platt, D.J., Fernandez, E., Miner, J.J., Diamond, M.S., A mouse model of Zika virus pathogenesis. Cell Host Microbe 19 (2016), 720–730.
117. Le Bon, A., Schiavoni, G., D'Agostino, G., Gresser, I., Belardelli, F., Tough, D.F., Type i interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 14 (2001), 461–470.
118. + T cells stimulated by virus-induced type I interferon. Nat. Immunol. 4 (2003), 1009–1015.
119. Le Bon, A., Thompson, C., Kamphuis, E., Durand, V., Rossmann, C., Kalinke, U., Tough, D.F., Cutting edge: enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J. Immunol. 176 (2006), 2074–2078.
120. Lee, S.J., Kim, W.J., Moon, S.K., Role of the p38 MAPK signaling pathway in mediating interleukin-28A-induced migration of UMUC-3 cells. Int. J. Mol. Med. 30 (2012), 945–952.
121. LeMessurier, K.S., Häcker, H., Chi, L., Tuomanen, E., Redecke, V., Type I interferon protects against pneumococcal invasive disease by inhibiting bacterial transmigration across the lung. PLoS Pathog., 9, 2013, e1003727.
122. Li, W., Lewis-Antes, A., Huang, J., Balan, M., Kotenko, S.V., Regulation of apoptosis by type III interferons. Cell Prolif. 41 (2008), 960–979.
123. Lin, Q., Dong, C., Cooper, M.D., Impairment of T and B cell development by treatment with a type I interferon. J. Exp. Med. 187 (1998), 79–87.
124. Lin, J.D., Feng, N., Sen, A., Balan, M., Tseng, H.C., McElrath, C., Smirnov, S.V., Peng, J., Yasukawa, L.L., Durbin, R.K., et al. Distinct roles of type I and type III interferons in intestinal immunity to homologous and heterologous rotavirus infections. PLoS Pathog., 12, 2016, e1005600.
125. Litinskiy, M.B., Nardelli, B., Hilbert, D.M., He, B., Schaffer, A., Casali, P., Cerutti, A., DCs induce CD40-independent immunoglobulin class switching through BLyS and APRIL. Nat. Immunol. 3 (2002), 822–829.
126. Mahlakõiv, T., Hernandez, P., Gronke, K., Diefenbach, A., Staeheli, P., Leukocyte-derived IFN-α/β and epithelial IFN-λ constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLoS Pathog., 11, 2015, e1004782.
127. Mahony, R., Gargan, S., Roberts, K.L., Bourke, N., Keating, S.E., Bowie, A.G., O'Farrelly, C., Stevenson, N.J., A novel anti-viral role for STAT3 in IFN-α signalling responses. Cell. Mol. Life Sci. 74 (2017), 1755–1764.
128. Manns, M.P., McHutchison, J.G., Gordon, S.C., Rustgi, V.K., Shiffman, M., Reindollar, R., Goodman, Z.D., Koury, K., Ling, M., Albrecht, J.K., Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet 358 (2001), 958–965.
129. Marcello, T., Grakoui, A., Barba-Spaeth, G., Machlin, E.S., Kotenko, S.V., MacDonald, M.R., Rice, C.M., Interferons alpha and lambda inhibit hepatitis C virus replication with distinct signal transduction and gene regulation kinetics. Gastroenterology 131 (2006), 1887–1898.
130. Martin, P.K., Marchiando, A., Xu, R., Rudensky, E., Yeung, F., Schuster, S.L., Kernbauer, E., Cadwell, K., Autophagy proteins suppress protective type I interferon signalling in response to the murine gut microbiota. Nat. Microbiol. 3 (2018), 1131–1141.
131. Martinelli, S., Urosevic, M., Daryadel, A., Oberholzer, P.A., Baumann, C., Fey, M.F., Dummer, R., Simon, H.U., Yousefi, S., Induction of genes mediating interferon-dependent extracellular trap formation during neutrophil differentiation. J. Biol. Chem. 279 (2004), 44123–44132.
132. McHutchison, J.G., Lawitz, E.J., Shiffman, M.L., Muir, A.J., Galler, G.W., McCone, J., Nyberg, L.M., Lee, W.M., Ghalib, R.H., Schiff, E.R., et al., IDEAL Study Team. Peginterferon alfa-2b or alfa-2a with ribavirin for treatment of hepatitis C infection. N. Engl. J. Med. 361 (2009), 580–593.
133. Mendoza, J.L., Schneider, W.M., Hoffmann, H.H., Vercauteren, K., Jude, K.M., Xiong, A., Moraga, I., Horton, T.M., Glenn, J.S., de Jong, Y.P., et al. The IFN-λ-IFN-λR1-IL-10Rβ complex reveals structural features underlying type III IFN functional plasticity. Immunity 46 (2017), 379–392.
134. Meuwissen, M.E., Schot, R., Buta, S., Oudesluijs, G., Tinschert, S., Speer, S.D., Li, Z., van Unen, L., Heijsman, D., Goldmann, T., et al. Human USP18 deficiency underlies type 1 interferonopathy leading to severe pseudo-TORCH syndrome. J. Exp. Med. 213 (2016), 1163–1174.
135. Miner, J.J., Cao, B., Govero, J., Smith, A.M., Fernandez, E., Cabrera, O.H., Garber, C., Noll, M., Klein, R.S., Noguchi, K.K., et al. Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165 (2016), 1081–1091.
136. Misumi, I., Whitmire, J.K., IFN-λ exerts opposing effects on T cell responses depending on the chronicity of the virus infection. J. Immunol. 192 (2014), 3596–3606.
137. Mocellin, S., Pasquali, S., Rossi, C.R., Nitti, D., Interferon alpha adjuvant therapy in patients with high-risk melanoma: a systematic review and meta-analysis. J. Natl. Cancer Inst. 102 (2010), 493–501.
138. Morrow, M.P., Pankhong, P., Laddy, D.J., Schoenly, K.A., Yan, J., Cisper, N., Weiner, D.B., Comparative ability of IL-12 and IL-28B to regulate Treg populations and enhance adaptive cellular immunity. Blood 113 (2009), 5868–5877.
139. + T cell differentiation. Sci. Immunol., 1, 2016, eaah3565.
140. Muir, A.J., Shiffman, M.L., Zaman, A., Yoffe, B., de la Torre, A., Flamm, S., Gordon, S.C., Marotta, P., Vierling, J.M., Lopez-Talavera, J.C., et al. Phase 1b study of pegylated interferon lambda 1 with or without ribavirin in patients with chronic genotype 1 hepatitis C virus infection. Hepatology 52 (2010), 822–832.
141. Muir, A.J., Arora, S., Everson, G., Flisiak, R., George, J., Ghalib, R., Gordon, S.C., Gray, T., Greenbloom, S., Hassanein, T., et al., EMERGE study group. A randomized phase 2b study of peginterferon lambda-1a for the treatment of chronic HCV infection. J. Hepatol. 61 (2014), 1238–1246.
142. Müller, U., Steinhoff, U., Reis, L.F., Hemmi, S., Pavlovic, J., Zinkernagel, R.M., Aguet, M., Functional role of type I and type II interferons in antiviral defense. Science 264 (1994), 1918–1921.
143. Nagarajan, U.M., Prantner, D., Sikes, J.D., Andrews, C.W. Jr., Goodwin, A.M., Nagarajan, S., Darville, T., Type I interferon signaling exacerbates Chlamydia muridarum genital infection in a murine model. Infect. Immun. 76 (2008), 4642–4648.
144. Nakamura, S., Davis, K.M., Weiser, J.N., Synergistic stimulation of type I interferons during influenza virus coinfection promotes Streptococcus pneumoniae colonization in mice. J. Clin. Invest. 121 (2011), 3657–3665.
145. Newsome, S.D., Kieseier, B.C., Arnold, D.L., Shang, S., Liu, S., Hung, S., Sabatella, G., Subgroup and sensitivity analyses of annualized relapse rate over 2 years in the ADVANCE trial of peginterferon beta-1a in patients with relapsing-remitting multiple sclerosis. J. Neurol. 263 (2016), 1778–1787.
146. Ng, C.T., Sullivan, B.M., Teijaro, J.R., Lee, A.M., Welch, M., Rice, S., Sheehan, K.C., Schreiber, R.D., Oldstone, M.B., Blockade of interferon Beta, but not interferon alpha, signaling controls persistent viral infection. Cell Host Microbe 17 (2015), 653–661.
147. Nice, T.J., Baldridge, M.T., McCune, B.T., Norman, J.M., Lazear, H.M., Artyomov, M., Diamond, M.S., Virgin, H.W., Interferon-λ cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347 (2015), 269–273.
148. Numasaki, M., Tagawa, M., Iwata, F., Suzuki, T., Nakamura, A., Okada, M., Iwakura, Y., Aiba, S., Yamaya, M., IL-28 elicits antitumor responses against murine fibrosarcoma. J. Immunol. 178 (2007), 5086–5098.
149. Odendall, C., Dixit, E., Stavru, F., Bierne, H., Franz, K.M., Durbin, A.F., Boulant, S., Gehrke, L., Cossart, P., Kagan, J.C., Diverse intracellular pathogens activate type III interferon expression from peroxisomes. Nat. Immunol. 15 (2014), 717–726.
150. Odendall, C., Voak, A.A., Kagan, J.C., Type III IFNs are commonly induced by bacteria-sensing TLRs and reinforce epithelial barriers during infection. J. Immunol. 199 (2017), 3270–3279.
151. Okabayashi, T., Kojima, T., Masaki, T., Yokota, S., Imaizumi, T., Tsutsumi, H., Himi, T., Fujii, N., Sawada, N., Type-III interferon, not type-I, is the predominant interferon induced by respiratory viruses in nasal epithelial cells. Virus Res. 160 (2011), 360–366.
152. Okanoue, T., Sakamoto, S., Itoh, Y., Minami, M., Yasui, K., Sakamoto, M., Nishioji, K., Katagishi, T., Nakagawa, Y., Tada, H., et al. Side effects of high-dose interferon therapy for chronic hepatitis C. J. Hepatol. 25 (1996), 283–291.
153. Oke, V., Brauner, S., Larsson, A., Gustafsson, J., Zickert, A., Gunnarsson, I., Svenungsson, E., IFN-λ1 with Th17 axis cytokines and IFN-α define different subsets in systemic lupus erythematosus (SLE). Arthritis Res. Ther., 19, 2017, 139.
154. Osterlund, P.I., Pietilä, 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. 179 (2007), 3434–3442.
155. Paun, A., Pitha, P.M., The IRF family, revisited. Biochimie 89 (2007), 744–753.
156. Pervolaraki, K., Stanifer, M.L., Münchau, S., Renn, L.A., Albrecht, D., Kurzhals, S., Senís, E., Grimm, D., Schröder-Braunstein, J., Rabin, R.L., Boulant, S., Type I and type III interferons display different dependency on mitogen-activated protein kinases to mount an antiviral state in the human gut. Front. Immunol., 8, 2017, 459.
157. Pervolaraki, K., Rastgou Talemi, S., Albrecht, D., Bormann, F., Bamford, C., Mendoza, J.L., Garcia, K.C., McLauchlan, J., Höfer, T., Stanifer, M.L., Boulant, S., Differential induction of interferon stimulated genes between type I and type III interferons is independent of interferon receptor abundance. PLoS Pathog., 14, 2018, e1007420.
158. Pfaller, C.K., Li, Z., George, C.X., Samuel, C.E., Protein kinase PKR and RNA adenosine deaminase ADAR1: new roles for old players as modulators of the interferon response. Curr. Opin. Immunol. 23 (2011), 573–582.
159. Phillips, S., Mistry, S., Riva, A., Cooksley, H., Hadzhiolova-Lebeau, T., Plavova, S., Katzarov, K., Simonova, M., Zeuzem, S., Woffendin, C., et al. Peg-interferon lambda treatment induces robust innate and adaptive immunity in chronic hepatitis B patients. Front. Immunol., 8, 2017, 621.
160. Pichlmair, A., Lassnig, C., Eberle, C.A., Górna, M.W., Baumann, C.L., Burkard, T.R., Bürckstümmer, T., Stefanovic, A., Krieger, S., Bennett, K.L., et al. IFIT1 is an antiviral protein that recognizes 5′-triphosphate RNA. Nat. Immunol. 12 (2011), 624–630.
161. Platanias, L.C., Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 5 (2005), 375–386.
162. Pott, J., Mahlakõiv, 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. USA 108 (2011), 7944–7949.
163. Prokunina-Olsson, L., Muchmore, B., Tang, W., Pfeiffer, R.M., Park, H., Dickensheets, H., Hergott, D., Porter-Gill, P., Mumy, A., Kohaar, I., et al. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat. Genet. 45 (2013), 164–171.
164. Pulverer, J.E., Rand, U., Lienenklaus, S., Kugel, D., Zietara, N., Kochs, G., Naumann, R., Weiss, S., Staeheli, P., Hauser, H., Köster, M., Temporal and spatial resolution of type I and III interferon responses in vivo. J. Virol. 84 (2010), 8626–8638.
165. Quicke, K.M., Bowen, J.R., Johnson, E.L., McDonald, C.E., Ma, H., O'Neal, J.T., Rajakumar, A., Wrammert, J., Rimawi, B.H., Pulendran, B., et al. Zika virus infects human placental macrophages. Cell Host Microbe 20 (2016), 83–90.
166. Reichard, O., Norkrans, G., Frydén, A., Braconier, J.H., Sönnerborg, A., Weiland, O., The Swedish Study Group. Randomised, double-blind, placebo-controlled trial of interferon alpha-2b with and without ribavirin for chronic hepatitis C. Lancet 351 (1998), 83–87.
167. Reis, L.F., Ruffner, H., Stark, G., Aguet, M., Weissmann, C., Mice devoid of interferon regulatory factor 1 (IRF-1) show normal expression of type I interferon genes. EMBO J. 13 (1994), 4798–4806.
168. Reiser, J., Hurst, J., Voges, M., Krauss, P., Münch, P., Iftner, T., Stubenrauch, F., High-risk human papillomaviruses repress constitutive kappa interferon transcription via E6 to prevent pathogen recognition receptor and antiviral-gene expression. J. Virol. 85 (2011), 11372–11380.
169. Renauld, J.C., Class II cytokine receptors and their ligands: key antiviral and inflammatory modulators. Nat. Rev. Immunol. 3 (2003), 667–676.
170. Richardson, R.B., Ohlson, M.B., Eitson, J.L., Kumar, A., McDougal, M.B., Boys, I.N., Mar, K.B., De La Cruz-Rivera, P.C., Douglas, C., Konopka, G., et al. A CRISPR screen identifies IFI6 as an ER-resident interferon effector that blocks flavivirus replication. Nat. Microbiol. 3 (2018), 1214–1223.
171. Rincon-Orozco, B., Halec, G., Rosenberger, S., Muschik, D., Nindl, I., Bachmann, A., Ritter, T.M., Dondog, B., Ly, R., Bosch, F.X., et al. Epigenetic silencing of interferon-kappa in human papillomavirus type 16-positive cells. Cancer Res. 69 (2009), 8718–8725.
172. Rodero, M.P., Crow, Y.J., Type I interferon-mediated monogenic autoinflammation: The type I interferonopathies, a conceptual overview. J. Exp. Med. 213 (2016), 2527–2538.
173. Rothlin, C.V., Ghosh, S., Zuniga, E.I., Oldstone, M.B., Lemke, G., TAM receptors are pleiotropic inhibitors of the innate immune response. Cell 131 (2007), 1124–1136.
174. Sabat, R., IL-10 family of cytokines. Cytokine Growth Factor Rev. 21 (2010), 315–324.
175. Sammicheli, S., Kuka, M., Di Lucia, P., de Oya, N.J., De Giovanni, M., Fioravanti, J., Cristofani, C., Maganuco, C.G., Fallet, B., Ganzer, L., et al. Inflammatory monocytes hinder antiviral B cell responses. Sci. Immunol., 1, 2016, eaah6789.
176. Sanchis, A., Cerveró, L., Bataller, A., Tortajada, J.L., Huguet, J., Crow, Y.J., Ali, M., Higuet, L.J., Martínez-Frías, M.L., Genetic syndromes mimic congenital infections. J. Pediatr. 146 (2005), 701–705.
177. Sancho-Shimizu, V., Perez de Diego, R., Jouanguy, E., Zhang, S.Y., Casanova, J.L., Inborn errors of anti-viral interferon immunity in humans. Curr. Opin. Virol. 1 (2011), 487–496.
178. Sarasin-Filipowicz, M., Oakeley, E.J., Duong, F.H., Christen, V., Terracciano, L., Filipowicz, W., Heim, M.H., Interferon signaling and treatment outcome in chronic hepatitis C. Proc. Natl. Acad. Sci. USA 105 (2008), 7034–7039.
179. Sato, A., Ohtsuki, M., Hata, M., Kobayashi, E., Murakami, T., Antitumor activity of IFN-lambda in murine tumor models. J. Immunol. 176 (2006), 7686–7694.
180. Schneider, W.M., Chevillotte, M.D., Rice, C.M., Interferon-stimulated genes: a complex web of host defenses. Annu. Rev. Immunol. 32 (2014), 513–545.
181. Schoggins, J.W., Interferon-stimulated genes: roles in viral pathogenesis. Curr. Opin. Virol. 6 (2014), 40–46.
182. Schoggins, J.W., Recent advances in antiviral interferon-stimulated gene biology. F1000Res., 7, 2018, 309.
183. Schreiber, G., The molecular basis for differential type I interferon signaling. J. Biol. Chem. 292 (2017), 7285–7294.
184. Shaw, A.E., Hughes, J., Gu, Q., Behdenna, A., Singer, J.B., Dennis, T., Orton, R.J., Varela, M., Gifford, R.J., Wilson, S.J., Palmarini, M., Fundamental properties of the mammalian innate immune system revealed by multispecies comparison of type I interferon responses. PLoS Biol., 15, 2017, e2004086.
185. Sheppard, P., Kindsvogel, W., Xu, W., Henderson, K., Schlutsmeyer, S., Whitmore, T.E., Kuestner, R., Garrigues, U., Birks, C., Roraback, J., et al. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4 (2003), 63–68.
186. Snell, L.M., McGaha, T.L., Brooks, D.G., Type I Interferon in Chronic Virus Infection and Cancer. Trends Immunol. 38 (2017), 542–557.
187. Sommereyns, C., Paul, S., Staeheli, P., Michiels, T., IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog., 4, 2008, e1000017.
188. Sorgeloos, F., Kreit, M., Hermant, P., Lardinois, C., Michiels, T., Antiviral type I and type III interferon responses in the central nervous system. Viruses 5 (2013), 834–857.
189. Souza-Fonseca-Guimaraes, F., Young, A., Mittal, D., Martinet, L., Bruedigam, C., Takeda, K., Andoniou, C.E., Degli-Esposti, M.A., Hill, G.R., Smyth, M.J., NK cells require IL-28R for optimal in vivo activity. Proc. Natl. Acad. Sci. USA 112 (2015), E2376–E2384.
190. Srinivas, S., Dai, J., Eskdale, J., Gallagher, G.E., Megjugorac, N.J., Gallagher, G., Interferon-lambda1 (interleukin-29) preferentially down-regulates interleukin-13 over other T helper type 2 cytokine responses in vitro. Immunology 125 (2008), 492–502.
191. Steed, A.L., Christophi, G.P., Kaiko, G.E., Sun, L., Goodwin, V.M., Jain, U., Esaulova, E., Artyomov, M.N., Morales, D.J., Holtzman, M.J., et al. The microbial metabolite desaminotyrosine protects from influenza through type I interferon. Science 357 (2017), 498–502.
192. Stifter, S.A., Matthews, A.Y., Mangan, N.E., Fung, K.Y., Drew, A., Tate, M.D., Soares da Costa, T.P., Hampsey, D., Mayall, J., Hansbro, P.M., et al. Defining the distinct, intrinsic properties of the novel type I interferon, IFNε. J. Biol. Chem. 293 (2018), 3168–3179.
193. Suspène, R., Guétard, D., Henry, M., Sommer, P., Wain-Hobson, S., Vartanian, J.P., Extensive editing of both hepatitis B virus DNA strands by APOBEC3 cytidine deaminases in vitro and in vivo. Proc. Natl. Acad. Sci. USA 102 (2005), 8321–8326.
194. Svensson, A., Bellner, L., Magnusson, M., Eriksson, K., Role of IFN-alpha/beta signaling in the prevention of genital herpes virus type 2 infection. J. Reprod. Immunol. 74 (2007), 114–123.
195. Tasker, C., Subbian, S., Gao, P., Couret, J., Levine, C., Ghanny, S., Soteropoulos, P., Zhao, X., Landau, N., Lu, W., Chang, T.L., IFN-ε protects primary macrophages against HIV infection. JCI Insight, 1, 2016, e88255.
196. Teijaro, J.R., Ng, C., Lee, A.M., Sullivan, B.M., Sheehan, K.C., Welch, M., Schreiber, R.D., de la Torre, J.C., Oldstone, M.B., Persistent LCMV infection is controlled by blockade of type I interferon signaling. Science 340 (2013), 207–211.
197. Terrault, N.A., Bzowej, N.H., Chang, K.M., Hwang, J.P., Jonas, M.M., Murad, M.H., American Association for the Study of Liver Diseases. AASLD guidelines for treatment of chronic hepatitis B. Hepatology 63 (2016), 261–283.
198. Tezuka, Y., Endo, S., Matsui, A., Sato, A., Saito, K., Semba, K., Takahashi, M., Murakami, T., Potential anti-tumor effect of IFN-λ2 (IL-28A) against human lung cancer cells. Lung Cancer 78 (2012), 185–192.
199. The IFNB Multiple Sclerosis Study Group. Interferon beta-1b is effective in relapsing-remitting multiple sclerosis. I. Clinical results of a multicenter, randomized, double-blind, placebo-controlled trial. Neurology 43 (1993), 655–661.
200. 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. Structural linkage between ligand discrimination and receptor activation by type I interferons. Cell 146 (2011), 621–632.
201. Thorlacius, G.E., Wahren-Herlenius, M., Rönnblom, L., An update on the role of type I interferons in systemic lupus erythematosus and Sjögren's syndrome. Curr. Opin. Rheumatol. 30 (2018), 471–481.
202. van Boxel-Dezaire, A.H., Rani, M.R., Stark, G.R., Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25 (2006), 361–372.
203. Vilcek, J., Fifty years of interferon research: aiming at a moving target. Immunity 25 (2006), 343–348.
204. Voigt, E.A., Yin, J., Kinetic differences and synergistic antiviral effects between type I and type III interferon signaling indicate pathway independence. J. Interferon Cytokine Res. 35 (2015), 734–747.
205. Wack, A., Terczyńska-Dyla, E., Hartmann, R., Guarding the frontiers: the biology of type III interferons. Nat. Immunol. 16 (2015), 802–809.
206. Wang, W.B., Levy, D.E., Lee, C.K., STAT3 negatively regulates type I IFN-mediated antiviral response. J. Immunol. 187 (2011), 2578–2585.
207. Wells, A.I., Coyne, C.B., Type III Interferons in Antiviral Defenses at Barrier Surfaces. Trends Immunol. 39 (2018), 848–858.
208. Wilcox, D.R., Folmsbee, S.S., Muller, W.J., Longnecker, R., The type I interferon response determines differences in choroid plexus susceptibility between newborns and adults in herpes simplex virus encephalitis. MBio, 7, 2016 e00437–e16.
209. Wilson, E.B., Yamada, D.H., Elsaesser, H., Herskovitz, J., Deng, J., Cheng, G., Aronow, B.J., Karp, C.L., Brooks, D.G., Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science 340 (2013), 202–207.
210. Witte, E., Kokolakis, G., Witte, K., Warszawska, K., Friedrich, M., Christou, D., Kirsch, S., Sterry, W., Volk, H.D., Sabat, R., Wolk, K., Interleukin-29 induces epithelial production of CXCR3A ligands and T-cell infiltration. J. Mol. Med. (Berl.) 94 (2016), 391–400.
211. Wolk, K., Witte, K., Witte, E., Raftery, M., Kokolakis, G., Philipp, S., Schönrich, G., Warszawska, K., Kirsch, S., Prösch, S., et al. IL-29 is produced by T(H)17 cells and mediates the cutaneous antiviral competence in psoriasis. Sci. Transl. Med., 5, 2013, 204ra129.
212. Wongthida, P., Diaz, R.M., Galivo, F., Kottke, T., Thompson, J., Pulido, J., Pavelko, K., Pease, L., Melcher, A., Vile, R., Type III IFN interleukin-28 mediates the antitumor efficacy of oncolytic virus VSV in immune-competent mouse models of cancer. Cancer Res. 70 (2010), 4539–4549.
213. Wu, Q., Yang, Q., Lourenco, E., Sun, H., Zhang, Y., Interferon-lambda1 induces peripheral blood mononuclear cell-derived chemokines secretion in patients with systemic lupus erythematosus: its correlation with disease activity. Arthritis Res. Ther., 13, 2011, R88.
214. Wu, Q., Yang, Q., Sun, H., Li, M., Zhang, Y., La Cava, A., Serum IFN-λ1 is abnormally elevated in rheumatoid arthritis patients. Autoimmunity 46 (2013), 40–43.
215. Yan, N., Immune diseases associated with TREX1 and STING dysfunction. J. Interferon Cytokine Res. 37 (2017), 198–206.
216. Yao, J.C., Guthrie, K.A., Moran, C., Strosberg, J.R., Kulke, M.H., Chan, J.A., LoConte, N., McWilliams, R.R., Wolin, E.M., Mattar, B., et al. Phase III prospective randomized comparison trial of depot octreotide plus interferon alfa-2b versus depot octreotide plus bevacizumab in patients with advanced carcinoid tumors: SWOG S0518. J. Clin. Oncol. 35 (2017), 1695–1703.
217. Yockey, L.J., Iwasaki, A., Interferons and proinflammatory cytokines in pregnancy and fetal development. Immunity 49 (2018), 397–412.
218. Yockey, L.J., Varela, L., Rakib, T., Khoury-Hanold, W., Fink, S.L., Stutz, B., Szigeti-Buck, K., Van den Pol, A., Lindenbach, B.D., Horvath, T.L., Iwasaki, A., Vaginal exposure to Zika virus during pregnancy leads to fetal brain infection. Cell 166 (2016), 1247–1256.e4.
219. Yockey, L.J., Jurado, K.A., Arora, N., Millet, A., Rakib, T., Milano, K.M., Hastings, A.K., Fikrig, E., Kong, Y., Horvath, T.L., et al. Type I interferons instigate fetal demise after Zika virus infection. Sci. Immunol., 3, 2018, eaao1680.
220. Zanoni, I., Granucci, F., Broggi, A., Interferon (IFN)-λ takes the helm: immunomodulatory roles of type III IFNs. Front. Immunol., 8, 2017, 1661.
221. Zhang, X., Brann, T.W., Zhou, M., Yang, J., Oguariri, R.M., Lidie, K.B., Imamichi, H., Huang, D.W., Lempicki, R.A., Baseler, M.W., et al. Cutting edge: Ku70 is a novel cytosolic DNA sensor that induces type III rather than type I IFN. J. Immunol. 186 (2011), 4541–4545.
222. Zhang, X., Bogunovic, D., Payelle-Brogard, B., Francois-Newton, V., Speer, S.D., Yuan, C., Volpi, S., Li, Z., Sanal, O., Mansouri, D., et al. Human intracellular ISG15 prevents interferon-α/β over-amplification and auto-inflammation. Nature 517 (2015), 89–93.
223. Zhou, Z., Hamming, O.J., Ank, N., Paludan, S.R., Nielsen, A.L., Hartmann, R., 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 (2007), 7749–7758.