Interferon-λ Mediates Non-redundant Front-Line Antiviral Protection against Influenza Virus Infection without Compromising Host Fitness

Immunity

Volumn 46, Issue 5, 2017, Pages 875-890.e6

  Galani, Ioanna E ^a   Triantafyllia, Vasiliki ^a   Eleminiadou, Evridiki Evangelia ^a   Koltsida, Ourania ^a   Stavropoulos, Athanasios ^a   Manioudaki, Maria ^a   Thanos, Dimitris ^a   Doyle, Sean E ^b   Kotenko, Sergei V ^c   Thanopoulou, Kalliopi ^a   Andreakos, Evangelos ^a  

^a BIOMEDICAL RESEARCH FOUNDATION   (Greece)

^b BRISTOL MYERS SQUIBB   (United States)

^c The State University of New Jersey   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; AUTACOID; CYTOKINE;

ANTIVIRAL ACTIVITY; ARTICLE; CYTOKINE PRODUCTION; EPITHELIUM CELL; FITNESS; HOST; HOST RESISTANCE; IMMUNOPATHOLOGY; INFLUENZA; LETHALITY; LEUKOCYTE; LUNG INJURY; MOUSE; NEUTROPHIL; NEUTROPHILIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL; UPREGULATION; VIRUS REPLICATION; VIRUS RESISTANCE; WEIGHT REDUCTION; ANIMAL; BIOSYNTHESIS; CLUSTER ANALYSIS; DISEASE MODEL; DISEASE RESISTANCE; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; INFLUENZA A VIRUS; INFLUENZA, HUMAN; KNOCKOUT MOUSE; LUNG; MALE; METABOLISM; MORTALITY; ORTHOMYXOVIRUS INFECTION; PATHOLOGY; REPORTER GENE; REPRODUCTIVE FITNESS; RESPIRATORY MUCOSA; VIROLOGY; VIRUS LOAD;

ANIMALS; CLUSTER ANALYSIS; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE RESISTANCE; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENES, REPORTER; GENETIC FITNESS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION MEDIATORS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; INTERFERON-GAMMA; LUNG; MALE; MICE; MICE, KNOCKOUT; NEUTROPHILS; ORTHOMYXOVIRIDAE INFECTIONS; RESPIRATORY MUCOSA; VIRAL LOAD; VIRUS REPLICATION;

EID: 85019434694     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2017.04.025     Document Type: Article

References (37)

1. Abram, C.L., Roberge, G.L., Hu, Y., Lowell, C.A., Comparative analysis of the efficiency and specificity of myeloid-Cre deleting strains using ROSA-EYFP reporter mice. J. Immunol. Methods 408 (2014), 89–100.
2. 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.
3. 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.
4. 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.
5. Brandes, M., Klauschen, F., Kuchen, S., Germain, R.N., A systems analysis identifies a feedforward inflammatory circuit leading to lethal influenza infection. Cell 154 (2013), 197–212.
6. Contoli, M., Message, S.D., Laza-Stanca, V., Edwards, M.R., Wark, P.A., Bartlett, N.W., Kebadze, T., Mallia, P., Stanciu, L.A., Parker, H.L., et al. Role of deficient type III interferon-lambda production in asthma exacerbations. Nat. Med. 12 (2006), 1023–1026.
7. 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.
8. 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.
9. Davidson, S., Crotta, S., McCabe, T.M., Wack, A., Pathogenic potential of interferon αβ in acute influenza infection. Nat. Commun., 5, 2014, 3864.
10. Davidson, S., McCabe, T.M., Crotta, S., Gad, H.H., Hessel, E.M., Beinke, S., Hartmann, R., Wack, A., IFNλ is a potent anti-influenza therapeutic without the inflammatory side effects of IFNα treatment. EMBO Mol. Med. 8 (2016), 1099–1112.
11. Durbin, R.K., Kotenko, S.V., Durbin, J.E., Interferon induction and function at the mucosal surface. Immunol. Rev. 255 (2013), 25–39.
12. Galani, I.E., Andreakos, E., Neutrophils in viral infections: Current concepts and caveats. J. Leukoc. Biol. 98 (2015), 557–564.
13. Galani, I.E., Koltsida, O., Andreakos, E., Type III interferons (IFNs): emerging master regulators of immunity. Adv. Exp. Med. Biol. 850 (2015), 1–15.
14. Hernández, P.P., Mahlakõiv, T., Yang, I., Schwierzeck, V., Nguyen, N., Guendel, F., Gronke, K., Ryffel, B., Hölscher, C., Dumoutier, L., et al. Interferon-λ and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nat. Immunol. 16 (2015), 698–707.
15. Iwasaki, A., Pillai, P.S., Innate immunity to influenza virus infection. Nat. Rev. Immunol. 14 (2014), 315–328.
16. 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.
17. 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.
18. 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.
19. 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.
20. Lazear, H.M., Nice, T.J., Diamond, M.S., Interferon-λ: Immune Functions at Barrier Surfaces and Beyond. Immunity 43 (2015), 15–28.
21. 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.
22. 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.
23. McNab, F., Mayer-Barber, K., Sher, A., Wack, A., O'Garra, A., Type I interferons in infectious disease. Nat. Rev. Immunol. 15 (2015), 87–103.
24. Medina, R.A., García-Sastre, A., Influenza A viruses: new research developments. Nat. Rev. Microbiol. 9 (2011), 590–603.
25. 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.
26. Mennechet, F.J., Uzé, G., Interferon-lambda-treated dendritic cells specifically induce proliferation of FOXP3-expressing suppressor T cells. Blood 107 (2006), 4417–4423.
27. Mordstein, M., Kochs, G., Dumoutier, L., Renauld, J.C., Paludan, S.R., Klucher, K., Staeheli, P., Interferon-lambda contributes to innate immunity of mice against influenza A virus but not against hepatotropic viruses. PLoS Pathog., 4, 2008, e1000151.
28. Mordstein, M., Neugebauer, E., Ditt, V., Jessen, B., Rieger, T., Falcone, V., Sorgeloos, F., Ehl, S., Mayer, D., Kochs, G., et al. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J. Virol. 84 (2010), 5670–5677.
29. 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.
30. 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.
31. Okubo, T., Hogan, B.L., Hyperactive Wnt signaling changes the developmental potential of embryonic lung endoderm. J. Biol., 3, 2004, 11.
32. Passegué, E., Wagner, E.F., Weissman, I.L., JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells. Cell 119 (2004), 431–443.
33. 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.
34. 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.
35. 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.
36. Smee, D.F., von Itzstein, M., Bhatt, B., Tarbet, E.B., Exacerbation of influenza virus infections in mice by intranasal treatments and implications for evaluation of antiviral drugs. Antimicrob. Agents Chemother. 56 (2012), 6328–6333.
37. Wack, A., Terczyńska-Dyla, E., Hartmann, R., Guarding the frontiers: the biology of type III interferons. Nat. Immunol. 16 (2015), 802–809.