Single-cell studies of IFN-β promoter activation by wild-type and NS1-defective influenza a viruses

Journal of General Virology

Volumn 98, Issue 3, 2017, Pages 357-363

  Killip, M J ^a,b   Jackson, D ^a   Perez Cidoncha M ^a   Fodor, E ^b   Randall, R E ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

IFN; Influenza virus; Innate immune response; Interferon; Interferon antagonist; NS1

Indexed keywords

BETA INTERFERON; DOUBLE STRANDED RNA; INTERFERON; INTERFERON REGULATORY FACTOR 3; MESSENGER RNA; MESSENGER RNA PRECURSOR; MYXOVIRUS RESISTANCE PROTEIN A; NONSTRUCTURAL PROTEIN 1; VIRUS ANTIGEN; GREEN FLUORESCENT PROTEIN; INS1 PROTEIN, INFLUENZA VIRUS; MX1 PROTEIN, HUMAN; MYXOVIRUS RESISTANCE PROTEIN; VIRAL PROTEIN;

A-549 CELL LINE; ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLUENZA A; INFLUENZA A VIRUS (H1N1); INTERFERON INDUCTION; LUNG EPITHELIUM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RNA-BINDING DOMAIN; SATELLITE VIRUS; SINGLE CELL ANALYSIS; VIRUS PARTICLE; VIRUS REPLICATION; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; INFLUENZA; INFLUENZA A VIRUS; METABOLISM; PHYSIOLOGY; TRANSCRIPTION INITIATION; VIROLOGY; VIRUS ENTRY;

GREEN FLUORESCENT PROTEINS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; INTERFERON-BETA; MYXOVIRUS RESISTANCE PROTEINS; PROMOTER REGIONS, GENETIC; SINGLE-CELL ANALYSIS; TRANSCRIPTIONAL ACTIVATION; VIRAL NONSTRUCTURAL PROTEINS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 85016959780     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000687     Document Type: Article

References (48)

1. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008;89:1-47.
2. Baum A, Sachidanandam R, García-Sastre A. Preference of RIG-I for short viral RNA molecules in infected cells revealed by nextgeneration sequencing. Proc Natl Acad Sci USA 2010;107:16303-16308.
3. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010;140:397-408.
4. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006;441:101-105.
5. Killip MJ, Smith M, Jackson D, Randall RE. Activation of the interferon induction cascade by influenza a viruses requires viral RNA synthesis and nuclear export. J Virol 2014;88:3942-3952.
6. Weber M, Sediri H, Felgenhauer U, Binzen I, Bänfer S et al. Influenza virus adaptation PB2-627K modulates nucleocapsid inhibition by the pathogen sensor RIG-I. Cell Host Microbe 2015;17: 309-319.
7. Benitez AA, Panis M, Xue J, Varble A, Shim JV et al. In vivo RNAi screening identifies MDA5 as a significant contributor to the cellular defense against influenza A virus. Cell Rep 2015;11:1714-1726.
8. Dudek SE, Wixler L, Nordhoff C, Nordmann A, Anhlan D et al. The influenza virus PB1-F2 protein has interferon antagonistic activity. Biol Chem 2011;392:1135-1144.
9. Varga ZT, Ramos I, Hai R, Schmolke M, García-Sastre A et al. The influenza virus protein PB1-F2 inhibits the induction of type I interferon at the level of the MAVS adaptor protein. PLoS Pathog 2011;7:e1002067.
10. Graef KM, Vreede FT, Lau YF, McCall AW, Carr SM et al. The PB2 subunit of the influenza virus RNA polymerase affects virulence by interacting with the mitochondrial antiviral signaling protein and inhibiting expression of beta interferon. J Virol 2010;84:8433-8445.
11. Iwai A, Shiozaki T, Kawai T, Akira S, Kawaoka Y et al. Influenza A virus polymerase inhibits type I interferon induction by binding to interferon beta promoter stimulator 1. J Biol Chem 2010;285: 32064-32074.
12. García-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE et al. Influenza A virus lacking the NS1 gene replicates in interferondeficient systems. Virology 1998;252:324-330.
13. Egorov A, Brandt S, Sereinig S, Romanova J, Ferko B et al. Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J Virol 1998;72:6437-6441.
14. Kochs G, Koerner I, Thiel L, Kothlow S, Kaspers B et al. Properties of H7N7 influenza A virus strain SC35M lacking interferon antagonist NS1 in mice and chickens. J Gen Virol 2007;88:1403-1409.
15. Qian XY, Chien CY, Lu Y, Montelione GT, Krug RM. An amino-terminal polypeptide fragment of the influenza virus NS1 protein possesses specific RNA-binding activity and largely helical backbone structure. RNA 1995;1:948-956.
16. Newby CM, Sabin L, Pekosz A. The RNA binding domain of influenza A virus NS1 protein affects secretion of tumor necrosis factor alpha, interleukin-6, and interferon in primary murine tracheal epithelial cells. J Virol 2007;81:9469-9480.
17. Donelan NR, Basler CF, García-Sastre A. A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J Virol 2003;77:13257-13266.
18. Steidle S, Martínez-Sobrido L, Mordstein M, Lienenklaus S, García-Sastre A et al. Glycine 184 in nonstructural protein NS1 determines the virulence of influenza A virus strain PR8 without affecting the host interferon response. J Virol 2010;84:12761-12770.
19. Gack MU, Albrecht RA, Urano T, Inn KS, Huang IC et al. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 2009;5: 439-449.
20. Guo Z, Chen LM, Zeng H, Gomez JA, Plowden J et al. NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I. Am J Respir Cell Mol Biol 2007; 36:263-269.
21. Mibayashi M, Martínez-Sobrido L, Loo YM, C_ardenas WB, Gale M Jr et al. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 2007;81:514-524.
22. Opitz B, Rejaibi A, Dauber B, Eckhard J, Vinzing M et al. IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell Microbiol 2007;9:930-938.
23. Twu KY, Noah DL, Rao P, Kuo RL, Krug RM. The CPSF30 binding site on the NS1A protein of influenza A virus is a potential antiviral target. J Virol 2006;80:3957-3965.
24. Noah DL, Twu KY, Krug RM. Cellular antiviral responses against influenza A virus are countered at the posttranscriptional level by the viral NS1A protein via its binding to a cellular protein required for the 3′ end processing of cellular pre-mRNAS. Virology 2003; 307:386-395.
25. das K, Ma LC, Xiao R, Radvansky B, Aramini J et al. Structural basis for suppression of a host antiviral response by influenza A virus. Proc Natl Acad Sci USA 2008;105:13093-13098.
26. Hayman A, Comely S, Lackenby A, Murphy S, McCauley J et al. Variation in the ability of human influenza A viruses to induce and inhibit the IFN-beta pathway. Virology 2006;347:52-64.
27. Kuo RL, Zhao C, Malur M, Krug RM. Influenza A virus strains that circulate in humans differ in the ability of their NS1 proteins to block the activation of IRF3 and interferon-b transcription. Virology 2010;408:146-158.
28. Chen S, Short JA, Young DF, Killip MJ, Schneider M et al. Heterocellular induction of interferon by negative-sense RNA viruses. Virology 2010;407:247-255.
29. Killip MJ, Fodor E, Randall RE. Influenza virus activation of the interferon system. Virus Res 2015;209:11-22.
30. Killip MJ, Young DF, Ross CS, Chen S, Goodbourn S et al. Failure to activate the IFN-β promoter by a paramyxovirus lacking an interferon antagonist. Virology 2011;415:39-46.
31. Killip MJ, Young DF, Gatherer D, Ross CS, Short JA et al. Deep sequencing analysis of defective genomes of parainfluenza virus 5 and their role in interferon induction. J Virol 2013;87:4798-4807.
32. Killip MJ, Young DF, Precious BL, Goodbourn S, Randall RE. Activation of the beta interferon promoter by paramyxoviruses in the absence of virus protein synthesis. J Gen Virol 2012;93:299-307.
33. Kochs G, García-Sastre A, Martínez-Sobrido L. Multiple anti-interferon actions of the influenza A virus NS1 protein. J Virol 2007;81: 7011-7021.
34. Kuo RL, Krug RM. Influenza A virus polymerase is an integral component of the CPSF30-NS1A protein complex in infected cells. J Virol 2009;83:1611-1616.
35. Steidle S, Martínez-Sobrido L, Mordstein M, Lienenklaus S, García-Sastre A et al. Glycine 184 in nonstructural protein NS1 determines the virulence of influenza A virus strain PR8 without affecting the host interferon response. J virol 2010;84:12761-12770.
36. Wang W, Riedel K, Lynch P, Chien CY, Montelione GT et al. RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. RNA 1999;5:195-205.
37. Min JY, Krug RM. The primary function of RNA binding by the influenza A virus NS1 protein in infected cells: inhibiting the 2’-5’ oligo (A) synthetase/RNase L pathway. Proc Natl Acad Sci USA 2006;103:7100-7105.
38. Jackson D, Killip MJ, Galloway CS, Russell RJ, Randall RE. Loss of function of the influenza A virus NS1 protein promotes apoptosis but this is not due to a failure to activate phosphatidylinositol 3-kinase (PI3K). Virology 2010;396:94-105.
39. Strähle L, Marq JB, Brini A, Hausmann S, Kolakofsky D et al. Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J Virol 2007;81:12227-12237.
40. Kallfass C, Lienenklaus S, Weiss S, Staeheli P. Visualizing the beta interferon response in mice during infection with influenza A viruses expressing or lacking nonstructural protein 1. J Virol 2013;87:6925-6930.
41. von Recum-Knepper J, Sadewasser A, Weinheimer VK, Wolff T. Fluorescence-activated cell sorting-based analysis reveals an asymmetric induction of interferon-stimulated genes in response to seasonal influenza A virus. J Virol 2015;89:6982-6993.
42. Weber M, Gawanbacht A, Habjan M, Rang A, Borner C et al. Incoming RNA virus nucleocapsids containing a 5-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe 2013;13:336-346.
43. Frensing T, Pflugmacher A, Bachmann M, Peschel B, Reichl U. Impact of defective interfering particles on virus replication and antiviral host response in cell culture-based influenza vaccine production. Appl Microbiol Biotechnol 2014;98 8999-9008.
44. Ngunjiri JM, Buchek GM, Mohni KN, Sekellick MJ, Marcus PI. Influenza virus subpopulations: exchange of lethal H5N1 virus NS for H1N1 virus NS triggers de novo generation of defective-interfering particles and enhances interferon-inducing particle efficiency. J Interferon Cytokine Res 2013;33:99-107.
45. Scott PD, Meng B, Marriott AC, Easton AJ, Dimmock NJ. Defective interfering influenza A virus protects in vivo against disease caused by a heterologous influenza B virus. J Gen Virol 2011;92: 2122-2132.
46. Scott PD, Meng B, Marriott AC, Easton AJ, Dimmock NJ. Defective interfering virus protects elderly mice from influenza. Virol J 2011;8:212.
47. Pérez-Cidoncha M, Killip MJ, Oliveros JC, Asensio VJ, Fernández Y et al. An unbiased genetic screen reveals the polygenic nature of the influenza virus anti-interferon response. J Virol 2014;88: 4632-4646.
48. Tapia K, Kim WK, Sun Y, Mercado-López X, Dunay E et al. Defective viral genomes arising in vivo provide critical danger signals for the triggering of lung antiviral immunity. PLoS Pathog 2013;9: e1003703.