Kinetic Differences and Synergistic Antiviral Effects Between Type I and Type III Interferon Signaling Indicate Pathway Independence

Journal of Interferon and Cytokine Research

Volumn 35, Issue 9, 2015, Pages 734-747

  Voigt, Emily A ^a,b   Yin, John ^a,b  

^a Wisconsin Electric Machines and Power Electronics Consortium   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

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

ANTIVIRAL ACTIVITY; ARTICLE; DRUG HALF LIFE; DRUG POTENTIATION; DRUG STABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; LUNG ALVEOLUS EPITHELIUM; PRIORITY JOURNAL; RNA VIRUS; UPREGULATION; DRUG EFFECTS; EPITHELIUM CELL; GENETIC TRANSCRIPTION; KINETICS; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VIRUS DISEASES;

ANTIVIRAL AGENTS; CELL LINE, TUMOR; EPITHELIAL CELLS; HUMANS; INTERFERON TYPE I; KINETICS; RNA VIRUSES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; UP-REGULATION; VIRUS DISEASES;

EID: 84941054085     PISSN: 10799907     EISSN: 15577465     Source Type: Journal    
DOI: 10.1089/jir.2015.0008     Document Type: Article

References (54)

1. Ank N, West H, Bartholdy C, Eriksson K, Thomsen AR, Paludan SR. 2006. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J Virol 80(9):4501-4509.
2. Bartee E, McFadden G. 2013. Cytokine synergy: an under appreciated contributor to innate anti-viral immunity. Cytokine 63:237-240.
3. Bliss CI. 1939. The toxicity of poisons applied jointly. Ann Appl Biol 26(3):585-615.
4. Calven J, Yudina Y, Uller L. 2013. Rhinovirus and dsRNA induce RIG-I-like receptors and expression of interferon beta and lambda(1) in human bronchial smooth muscle cells. PLoS One 8(4):11.
5. Curtsinger JM, Mescher MF. 2010. Inflammatory cytokines as a third signal for T cell activation. Curr Opin Immunol 22(3):333-340.
6. Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF. 2005. Cutting edge: type IIFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol 174(8):4465-4469.
7. Dong BH, Xu LL, Zhou AM, Hassel BA, Lee X, Torrence PF, Silverman RH. 1994. Intrinsic molecular activities of the interferon-induced 2-5A-dependent RNase. J Biol Chem 269(19):14153-14158.
8. Doyle SE, Schreckhise H, Khuu-Duong K, Henderson K, Rosler R, Storey H, Yao L, Liu H, Barahmand-pour F, Sivakumar P, et al. 2006. Interleukin-29 uses a type 1 interferon-like program to promote antiviral responses in human hepatocytes. Hepatology 44(4):896-906.
9. Dumoutier L, Tounsi A, Michiels T, Sommereyns C, Kotenko SV, Renauld JC. 2004. 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 279(31):32269-32274.
10. Greco WR, Bravo G, Parsons JC. 1995. The search for synergy - a critical-review from a response-perspective. Pharmacol Rev 47(2):331-385.
11. Haller O, Kochs G. 2002. Interferon-induced mx proteins: dynamin-like GTPases with antiviral activity. Traffic 3(10):710-717.
12. Haller O, Staeheli P, Kochs G. 2007. Interferon-induced Mx proteins in antiviral host defense. Biochimie 89(6-7):812-818.
13. Hervas-Stubbs S, Riezu-Boj JI, Gonzalez I, Mancheno U, Dubrot J, Azpilicueta A, Gabari I, Palazon A, Aranguren A, Ruiz J, et al. 2010. Effects of IFN-alpha as a signal-3 cytokine on human naive and antigen-experienced CD8(+) T cells. Eur J Immunol 40(12):3389-3402.
14. Hewlett PS. 1969. Measurement of potencies of drug mixtures. Biometrics 25(3):477-487.
15. Jewell NA, Cline T, Mertz SE, Smirnov SV, Flano 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. J Virol 84(21):11515-11522.
16. Jilek BL, Zarr M, Sampah ME, Rabi SA, Bullen CK, Lai J, Shen L, Siliciano RF. 2012. A quantitative basis for antiretroviral therapy for HIV-1 infection. Nat Med 18(3):446-451.
17. Khaitov MR, Laza-Stanca V, Edwards MR, Walton RP, Rohde G, Contoli M, Papi A, Stanciu LA, Kotenko SV, Johnston SL. 2009. Respiratory virus induction of alpha-, beta- and lambda-interferons in bronchial epithelial cells and peripheral blood mononuclear cells. Allergy 64(3):375-386.
18. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. 2005. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med 202(5):637-650.
19. Krause CD, Pestka S. 2005. Evolution of the Class 2 cytokines and receptors, and discovery of new friends and relatives. Pharmacol Ther 106(3):299-346.
20. Larkin J, Jin L, Farmen M, Venable D, Huang Y, Tan SL, Glass JI. 2003. Synergistic antiviral activity of human interferon combinations in the hepatitis C virus replicon system. J Interferon Cytokine Res 23(5):247-257.
21. Laskey SB, Siliciano RF. 2014. A mechanistic theory to explain the efficacy of antiretroviral therapy. Nat Rev Microbiol 12(11):772-780.
22. Lehar J, Zimmermann GR, Krueger AS, Molnar RA, Ledell JT, Heilbut AM, Short GF, Giusti LC, Nolan GP, Magid OA, et al. 2007. Chemical combination effects predict connectivity in biological systems. Mol Syst Biol 3:14.
23. Li W, Lewis-Antes A, Huang J, Balan M, Kotenko SV. 2008. Regulation of apoptosis by type III interferons. Cell Prolif 41(6):960-979.
24. Liu SY, Sanchez DJ, Aliyari R, Lu S, Cheng GH. 2012. Systematic identification of type I and type II interferon-induced antiviral factors. Proc Natl Acad Sci U S A 109(11):4239-4244.
25. 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.
26. Megjugorac NJ, Gallagher GE, Gallagher G. 2009. Modulation of human plasmacytoid DC function by IFN-lambda 1 (IL-29). J Leukoc Biol 86(6):1359-1363.
27. Mordstein M, Kochs G, Dumoutier L, Renauld JC, Paludan SR, Klucher K, Staeheli P. 2008. Interferon-lambda contributes to innate immunity of mice against influenza a virus but not against hepatotropic viruses. PLoS Pathog 4(9):e1000151.
28. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Falcone V, Sorgeloos F, Ehl S, Mayer D, Kochs G, et al. 2010. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J Virol 84(11):5670-5677.
29. Munir M, Berg M. 2013. The multiple faces of proteinkinase R in antiviral defense. Virulence 4(1):85-89.
30. Owens CM, Mawhinney C, Grenier JM, Altmeyer R, Lee MS, Borisy AA, Lehar J, Johansen LM. 2010. Chemical combinations elucidate pathway interactions and regulation relevant to hepatitis C replication. Mol Syst Biol 6:13.
31. Pagliaccetti NE, Eduardo R, Kleinstein SH, Mu XJ, Bandi P, Robek MD. 2008. Interleukin-29 functions cooperatively with interferon to induce antiviral gene expression and inhibit hepatitis C virus replication. J Biol Chem 283(44):30079-30089.
32. Peng T, Zhu J, Hwangbo Y, Corey L, Bumgarner RE. 2008. Independent and cooperative antiviral actions of beta interferon and gamma interferon against herpes simplex virus replication in primary human fibroblasts. J Virol 82(4):1934-1945.
33. Pott J, Mahlakoiv T, Mordstein M, Duerr CU, Michiels T, Stockinger S, Staeheli P, Hornef MW. 2011. IFN-lambda determines the intestinal epithelial antiviral host defense. Proc Natl Acad Sci U S A 108(19):7944-7949.
34. Pulverer JE, Rand U, Lienenklaus S, Kugel D, Zietara N, Kochs G, Naumann R, Weiss S, Staeheli P, Hauser H, et al. 2010. Temporal and spatial resolution of type I and III interferon responses in vivo. J Virol 84(17):8626-8638.
35. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47.
36. Rouabhia M, Ross G, Page N, Chakir J. 2002. Interleukin-18 and gamma interferon production by oral epithelial cells in response to exposure to Candida albicans or lipopolysaccharide stimulation. Infect Immun 70(12):7073-7080.
37. Sadler AJ, Williams BRG. 2008. Interferon-inducible antiviral effectors. Nat Rev Immunol 8(7):559-568.
38. Sainz B, LaMarca HL, Garry RF, Morris CA. 2005. Synergistic inhibition of human cytomegalovirus replication by interferon-alpha/beta and interferon-gamma. Virol J 2:13.
39. Sanda C, Weitzel P, Tsukahara T, Schaley J, Edenberg HJ, Stephens MA, McClintick JN, Blatt LM, Li L, Brodsky L, et al. 2006. Differential gene induction by type I and type II interferons and their combination. J Interferon Cytokine Res 26(7):462-472.
40. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472(7344):481-485.
41. Schroth MK, Grimm E, Frindt P, Galagan DM, Konno S, Love R, Gern JE. 1999. Rhinovirus replication causes RANTES production in primary bronchial epithelial cells. Am J Respir Cell Mol Biol 20(6):1220-1228.
42. Sharma M, Sharma S, Roy S, Varma S, Bose M. 2007. Pulmonary epithelial cells are a source of interferon-gamma in response to Mycobacterium tuberculosis infection. Immunol Cell Biol 85(3):229-237.
43. Sheppard P, Kindsvogel W, Xu WF, Henderson K, Schlutsmeyer S, Whitmore TE, Kuestner R, Garrigues U, Birks C, Roraback J, et al. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat Immunol 4(1):63-68.
44. Sorensen H, Cedergreen N, Skovgaard IM, Streibig JC. 2007. An isobole-based statistical model and test for synergism/antagonism in binary mixture toxicity experiments. Environ Ecol Stat 14(4):383-397.
45. Stager S, Kaye PM. 2004. CD8(+) T-cell priming regulated by cytokines of the innate immune system. Trends Mol Med 10(8):366-371.
46. Stawowczyk M, Van Scoy S, Kumar KP, Reich NC. 2011. The interferon stimulated gene 54 promotes apoptosis. J Biol Chem 286(9):7257-7266.
47. Stordeur P, Poulin LF, Craciun L, Zhou L, Schandene L, de Lavareille A, Goriely S, Goldman M. 2002. Cytokine mRNA quantification by real-time PCR. J Immunol Methods 259(1-2):55-64.
48. Tan H, Derrick J, Hong J, Sanda C, Grosse WM, Edenberg HJ, Taylor M, Seiwert S, Blatt LM. 2005. Global transcriptional profiling combination of type I and type II demonstrates the interferon enhances antiviral and immune responses at clinically relevant doses. J Interferon Cytokine Res 25(10):632-649.
49. Voigt E, Inankur B, Baltes A, Yin J. 2013. A quantitative infection assay for human type I, II, and III interferon antiviral activities. Virol J 10:10.
50. Whitaker-Dowling PA, Wilcox DK, Widnell CC, Youngner JS. 1983. Interferon-mediated inhibition of virus penetration. Proc Natl Acad Sci U S A 80(4):1083-1086.
51. Witte K, Witte E, Sabat R, Wolk K. 2010. IL-28A, IL-28B, and IL-29: promising cytokines with type I interferon-like properties. Cytokine Growth Factor Rev 21(4):237-251.
52. Xiao H, Killip MJ, Staeheli P, Randall RE, Jackson D. 2013. The human interferon-induced MxA protein inhibits early stages of influenza A virus infection by retaining the incoming viral genome in the cytoplasm. J Virol 87(23):13053-13058.
53. Zhou AM, Paranjape JM, Der SD, Williams BRG, Silverman RH. 1999. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 258(2):435-440.
54. Zhou ZL, 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.