Fluorescence-activated cell sorting-based analysis reveals an asymmetric induction of interferon-stimulated genes in response to seasonal influenza A virus

Journal of Virology

Volumn 89, Issue 14, 2015, Pages 6982-6993

  von Recum Knepper, Jessica ^a,b   Sadewasser, Anne ^a   Weinheimer, Viola K ^a,c   Wolff, Thorsten ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

^b BURNHAM INSTITUTE   (United States)

^c FEDERAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON; NONSTRUCTURAL PROTEIN 1; STAT PROTEIN; VIRUS ANTIGEN; CPSF30 PROTEIN, HUMAN; INS1 PROTEIN, INFLUENZA VIRUS; MUTANT PROTEIN; VIRUS PROTEIN;

ANTIGEN EXPRESSION; ARTICLE; BINDING SITE; CELL CULTURE; CELL POPULATION; CHINA; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE MUTATION; GENE PRODUCT; GENETIC POLYMORPHISM; HOST CELL; HUMAN; HUMAN CELL; IFIT1 GENE; IMMUNE RESPONSE; INFLUENZA VIRUS A; INFLUENZA VIRUS A H7N9; INTERFERON STIMULATED GENE; ISG15 GENE; MXA GENE; NONHUMAN; PARACRINE SIGNALING; PHENOTYPE; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN BINDING; QUANTITATIVE ANALYSIS; VIRUS REPLICATION; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; INFLUENZA A VIRUS; METABOLISM; PROCEDURES; SINGLE CELL ANALYSIS;

AVES; INFLUENZA A VIRUS;

CHINA; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLUENZA A VIRUS; INTERFERONS; MUTANT PROTEINS; SINGLE-CELL ANALYSIS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84931088379     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00857-15     Document Type: Article

References (62)

1. Shaw ML, Palese P. 2013. Orthomyxoviridae. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed (electronic). Lippincott Williams & Wilkins, Philadelphia, PA.
2. Wright PF, Neumann G, Kawaoka Y. 2013. Orthomyxoviruses. In Knipe DM, Howley PM, Cohen JI, Griffin DE, Lamb RA, Martin MA, Racaniello VR, Roizman B (ed), Fields virology, 6th ed (electronic). Lippincott Williams & Wilkins, Philadelphia, PA.
3. Reperant LA, Kuiken T, Osterhaus AD. 2012. Adaptive pathways of zoonotic influenza viruses: from exposure to establishment in humans. Vaccine 30:4419-4434. http://dx.doi.org/10.1016/j.vaccine.2012.04.049.
4. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89:1-47. http://dx.doi.org/10.1099/vir.0.83391-0.
5. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reise Sousa C, Matsuura Y, Fujita T, Akira S. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101-105. http://dx.doi.org/10.1038/nature04734.
6. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, Weber F, Reise Sousa C. 2006. RIG-I-mediated antiviral responses to singlestranded RNA bearing 5'-phosphates. Science 314:997-1001. http://dx.doi.org/10.1126/science.1132998.
7. Ivashkiv LB, Donlin LT. 2014. Regulation of type I interferon responses. Nat Rev Immunol 14:36-49. http://dx.doi.org/10.1038/nri3581.
8. Platanias LC. 2005. Mechanisms of type-I-and type-II-interferonmediated signalling. Nat Rev Immunol 5:375-386. http://dx.doi.org/10.1038/nri1604.
9. Der SD, Zhou A, Williams BR, Silverman RH. 1998. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc Natl Acad Sci USA 95:15623-15628. http://dx.doi.org/10.1073/pnas.95.26.15623.
10. 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 472:481-485. http://dx.doi.org/10.1038/nature09907.
11. Grandvaux N, Servant MJ, ten Oever B, Sen GC, Balachandran S, Barber GN, Lin R, Hiscott J. 2002. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J Virol 76:5532-5539. http://dx.doi.org/10.1128/JVI.76.11.5532-5539.2002.
12. Durbin RK, Kotenko SV, Durbin JE. 2013. Interferon induction and function at the mucosal surface. Immunol Rev 255:25-39. http://dx.doi.org/10.1111/imr.12101.
13. Sadler AJ, Williams BR. 2008. Interferon-inducible antiviral effectors. Nat Rev Immunol 8:559-568. http://dx.doi.org/10.1038/nri2314.
14. Schoggins JW, Rice CM. 2011. Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1:519-525. http://dx.doi.org/10.1016/j.coviro.2011.10.008.
15. Horisberger MA, Staeheli P, Haller O. 1983. Interferon induces a unique protein in mouse cells bearing a gene for resistance to influenza virus. Proc Natl Acad Sci USA 80:1910-1914. http://dx.doi.org/10.1073/pnas.80.7.1910.
16. Pichlmair A, Lassnig C, Eberle CA, Gorna MW, Baumann CL, Burkard TR, Burckstummer T, Stefanovic A, Krieger S, Bennett KL, Rulicke T, Weber F, Colinge J, Muller M, Superti-Furga G. 2011. IFIT1 is an antiviral protein that recognizes 5'-triphosphate RNA. Nat Immunol 12: 624-630. http://dx.doi.org/10.1038/ni.2048.
17. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, Osiak A, Levine B, Schmidt RE, Garcia-Sastre A, Leib DA, Pekosz A, Knobeloch KP, Horak I, Virgin HW, IV. 2007. IFNstimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc Natl Acad Sci USA 104:1371-1376. http://dx.doi.org/10.1073/pnas.0607038104.
18. Hsiang TY, Zhao C, Krug RM. 2009. Interferon-induced ISG15 conjugation inhibits influenzaAvirus gene expression and replication in human cells. J Virol 83:5971-5977. http://dx.doi.org/10.1128/JVI.01667-08.
19. Versteeg GA, Garcia-Sastre A. 2010. Viral tricks to grid-lock the type I interferon system. Curr Opin Microbiol 13:508-516. http://dx.doi.org/10.1016/j.mib.2010.05.009.
20. Krug RM, Garcia-Sastre A. 2013. The NS1 protein: a master regulator of host and viral functions, p 114-132. In Webster RG, Monto AS, Braciale TJ, Lamb RA (ed), Textbook of influenza, 2nd ed. John Wiley & Sons, Ltd, Oxford, United Kingdom.
21. Wolff T, Ludwig S. 2009. Influenza viruses control the vertebrate type I interferon system: factors, mechanisms, and consequences. J Interferon Cytokine Res 29:549-557. http://dx.doi.org/10.1089/jir.2009.0066.
22. Ehrhardt C, Wolff T, Pleschka S, Planz O, Beermann W, Bode JG, Schmolke M, Ludwig S. 2007. Influenza A virus NS1 protein activates the PI3K/Akt pathway to mediate antiapoptotic signaling responses. J Virol 81:3058-3067. http://dx.doi.org/10.1128/JVI.02082-06.
23. Hale BG, Randall RE, Ortin J, Jackson D. 2008. The multifunctional NS1 protein of influenza A viruses. J Gen Virol 89:2359-2376. http://dx.doi.org/10.1099/vir.0.2008/004606-0.
24. Opitz B, Rejaibi A, Dauber B, Eckhard J, Vinzing M, Schmeck B, Hippenstiel S, Suttorp N, Wolff T. 2007. IFNbeta induction by influenza A virus is mediated by RIG-I which is regulated by the viral NS1 protein. Cell Microbiol 9:930-938. http://dx.doi.org/10.1111/j.1462-5822.2006.00841.x.
25. Wolff T, O'Neill RE, Palese P. 1996. Interaction cloning of NS1-I, a human protein that binds to the nonstructural NS1 proteins of influenzaA and B viruses. J Virol 70:5363-5372.
26. Wolff T, O'Neill RE, Palese P. 1998. NS1-binding protein (NS1-BP): a novel human protein that interacts with the influenza A virus nonstructural NS1 protein is relocalized in the nuclei of infected cells. J Virol 72: 7170-7180.
27. Kochs G, Garcia-Sastre A, Martinez-Sobrido L. 2007. Multiple antiinterferon actions of the influenza A virus NS1 protein. J Virol 81:7011-7021. http://dx.doi.org/10.1128/JVI.02581-06.
28. Varga ZT, Grant A, Manicassamy B, Palese P. 2012. Influenza virus protein PB1-F2 inhibits the induction of type I interferon by binding to MAVS and decreasing mitochondrial membrane potential. J Virol 86: 8359-8366. http://dx.doi.org/10.1128/JVI.01122-12.
29. Zhao Z, Yi C, Zhao L, Wang S, Zhou L, Hu Y, Zou W, Chen H, Jin M. 2014. PB2-588I enhances 2009 H1N1 pandemic influenza virus virulence by increasing viral replication and exacerbating PB2 inhibition of beta interferon expression. J Virol 88:2260-2267. http://dx.doi.org/10.1128/JVI.03024-13.
30. Hayman A, Comely S, Lackenby A, Hartgroves LC, Goodbourn S, McCauley JW, Barclay WS. 2007. NS1 proteins of avian influenza A viruses can act as antagonists of the human alpha/beta interferon response. J Virol 81:2318-2327. http://dx.doi.org/10.1128/JVI.01856-06.
31. Noah DL, Twu KY, Krug RM. 2003. 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 307:386-395. http://dx.doi.org/10.1016/S0042-6822(02)00127-7.
32. Chen S, Short JA, Young DF, Killip MJ, Schneider M, Goodbourn S, Randall RE. 2010. Heterocellular induction of interferon by negativesense RNA viruses. Virology 407:247-255. http://dx.doi.org/10.1016/j.virol.2010.08.008.
33. Snijder B, Pelkmans L. 2011. Origins of regulated cell-to-cell variability. Nat Rev Mol Cell Biol 12:119-125. http://dx.doi.org/10.1038/nrm3044.
34. Hu J, Nudelman G, Shimoni Y, Kumar M, Ding Y, Lopez C, Hayot F, Wetmur JG, Sealfon SC. 2011. Role of cell-to-cell variability in activating a positive feedback antiviral response in human dendritic cells. PLoS One 6:e16614. http://dx.doi.org/10.1371/journal.pone.0016614.
35. Hwang SY, Hur KY, Kim JR, Cho KH, Kim SH, Yoo JY. 2013. Biphasic RLR-IFN-beta response controls the balance between antiviral immunity and cell damage. J Immunol 190:1192-1200. http://dx.doi.org/10.4049/jimmunol.1202326.
36. Zhao M, Zhang J, Phatnani H, Scheu S, Maniatis T. 2012. Stochastic expression of the interferon-beta gene. PLoS Biol 10:e1001249. http://dx.doi.org/10.1371/journal.pbio.1001249.
37. Rand U, Rinas M, Schwerk J, Nohren G, Linnes M, Kroger A, Flossdorf M, Kaly-Kullai K, Hauser H, Hofer T, Koster M. 2012. Multi-layered stochasticity and paracrine signal propagation shape the type-I interferon response. Mol Syst Biol 8:584. http://dx.doi.org/10.1038/msb.2012.17.
38. Das K, Ma LC, Xiao R, Radvansky B, Aramini J, Zhao L, Marklund J, Kuo RL, Twu KY, Arnold E, Krug RM, Montelione GT. 2008. Structural basis for suppression of a host antiviral response by influenza A virus. Proc Natl Acad Sci USA 105:13093-13098. http://dx.doi.org/10.1073/pnas.0805213105.
39. Krug RM, Yuan W, Noah DL, Latham AG. 2003. Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309:181-189. http://dx.doi.org/10.1016/S0042-6822(03)00119-3.
40. Matthaei M, Budt M, Wolff T. 2013. Highly pathogenic H5N1 influenza A virus strains provoke heterogeneous IFN-alpha/beta responses that distinctively affect viral propagation in human cells. PLoS One 8:e56659. http://dx.doi.org/10.1371/journal.pone.0056659.
41. Steidle S, Martinez-Sobrido L, Mordstein M, Lienenklaus S, Garcia-Sastre A, Staheli P, Kochs G. 2010. Glycine 184 in nonstructural protein NS1 determines the virulence of influenza A virus strain PR8 without affecting the host interferon response. J Virol 84:12761-12770. http://dx.doi.org/10.1128/JVI.00701-10.
42. Twu KY, Noah DL, Rao P, Kuo RL, Krug RM. 2006. The CPSF30 binding site on the NS1A protein of influenza A virus is a potential antiviral target. J Virol 80:3957-3965. http://dx.doi.org/10.1128/JVI.80.8.3957-3965.2006.
43. Park MS, Garcia-Sastre A, Cros JF, Basler CF, Palese P. 2003. Newcastle disease virus V protein is a determinant of host range restriction. J Virol 77:9522-9532. http://dx.doi.org/10.1128/JVI.77.17.9522-9532.2003.
44. Knepper J, Schierhorn KL, Becher A, Budt M, Tonnies M, Bauer TT, Schneider P, Neudecker J, Ruckert JC, Gruber AD, Suttorp N, Schweiger B, Hippenstiel S, Hocke AC, Wolff T. 2013. The novel human influenza A(H7N9) virus is naturally adapted to efficient growth in human lung tissue. mBio 4:e00601-13. http://dx.doi.org/10.1128/mBio.00601-13.
45. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, Bier K, Robb N, Vreede F, Barclay W, Fodor E, Reise Sousa C. 2010. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 140: 397-408. http://dx.doi.org/10.1016/j.cell.2010.01.020.
46. Sevilla-Reyes EE, Chavaro-Perez DA, Piten-Isidro E, Gutierrez-Gonzalez LH, Santos-Mendoza T. 2013. Protein clustering and RNA phylogenetic reconstruction of the influenza A virus NS1 protein allow an update in classification and identification of motif conservation. PLoS One 8:e63098. http://dx.doi.org/10.1371/journal.pone.0063098.
47. Ping J, Keleta L, Forbes NE, Dankar S, Stecho W, Tyler S, Zhou Y, Babiuk L, Weingartl H, Halpin RA, Boyne A, Bera J, Hostetler J, Fedorova NB, Proudfoot K, Katzel DA, Stockwell TB, Ghedin E, Spiro DJ, Brown EG. 2011. Genomic and protein structural maps of adaptive evolution of human influenza A virus to increased virulence in the mouse. PLoS One 6:e21740. http://dx.doi.org/10.1371/journal.pone.0021740.
48. Twu KY, Kuo RL, Marklund J, Krug RM. 2007. The H5N1 influenza virus NS genes selected after 1998 enhance virus replication in mammalian cells. J Virol 81:8112-8121. http://dx.doi.org/10.1128/JVI.00006-07.
49. Dankar SK, Miranda E, Forbes NE, Pelchat M, Tavassoli A, Selman M, Ping J, Jia J, Brown EG. 2013. Influenza A/Hong Kong/156/1997(H5N1) virus NS1 gene mutations F103L and M106I both increase IFN antagonism, virulence and cytoplasmic localization but differ in binding to RIG-I and CPSF30. Virol J 10:243. http://dx.doi.org/10.1186/1743-422X-10-243.
50. Diaz MO, Ziemin S, Le Beau MM, Pitha P, Smith SD, Chilcote RR, Rowley JD. 1988. Homozygous deletion of the alpha-and beta 1-interferon genes in human leukemia and derived cell lines. Proc Natl Acad Sci USA 85:5259-5263. http://dx.doi.org/10.1073/pnas.85.14.5259.
51. Garcia-Sastre A. 2011. Induction and evasion of type I interferon responses by influenza viruses. Virus Res 162:12-18. http://dx.doi.org/10.1016/j.virusres.2011.10.017.
52. Kochs G, Koerner I, Thiel L, Kothlow S, Kaspers B, Ruggli N, Summerfield A, Pavlovic J, Stech J, Staeheli P. 2007. Properties of H7N7 influenza A virus strain SC35M lacking interferon antagonist NS1 in mice and chickens. J Gen Virol 88:1403-1409. http://dx.doi.org/10.1099/vir.0.82764-0.
53. Khaperskyy DA, Emara MM, Johnston BP, Anderson P, Hatchette TF, McCormick C. 2014. Influenza A virus host shutoff disables antiviral stress-induced translation arrest. PLoS Pathog 10:e1004217. http://dx.doi.org/10.1371/journal.ppat.1004217.
54. Kainov DE, Muller KH, Theisen LL, Anastasina M, Kaloinen M, Muller CP. 2011. Differential effects of NS1 proteins of human pandemic H1N1/2009, avian highly pathogenic H5N1, and low pathogenic H5N2 influenza A viruses on cellular pre-mRNA polyadenylation and mRNA translation. J Biol Chem 286:7239-7247. http://dx.doi.org/10.1074/jbc.M110.203489.
55. Nacken W, Anhlan D, Hrincius ER, Mostafa A, Wolff T, Sadewasser A, Pleschka S, Ehrhardt C, Ludwig S. 2014. Activation of c-Jun N-terminal kinase upon influenza A virus (IAV) infection is independent of pathogen-related receptors but dependent on amino acid sequence variations of IAV NS1. J Virol 88:8843-8852. http://dx.doi.org/10.1128/JVI.00424-14.
56. WHO. 23 February 2015, posting date. Human infections with avian influenza A(H7N9) virus. WHO, Geneva, Switzerland. http://www.who.int/influenza/human_animal_interface/influenza_h7n9/RiskAssessment_H7N9_23Feb20115.pdf?ua=1.
57. Ayllon J, Domingues P, Rajsbaum R, Miorin L, Schmolke M, Hale BG, Garcia-Sastre A. 2014. A single amino acid substitution in the novel H7N9 influenza A virus NS1 protein increases CPSF30 binding and virulence. J Virol 88:12146-12151. http://dx.doi.org/10.1128/JVI.01567-14.
58. Hale BG, Steel J, Medina RA, Manicassamy B, Ye J, Hickman D, Hai R, Schmolke M, Lowen AC, Perez DR, Garcia-Sastre A. 2010. Inefficient control of host gene expression by the 2009 pandemic H1N1 influenza A virus NS1 protein. J Virol 84:6909-6922. http://dx.doi.org/10.1128/JVI.00081-10.
59. Hogner K, Wolff T, Pleschka S, Plog S, Gruber AD, Kalinke U, Walmrath HD, Bodner J, Gattenlohner S, Lewe-Schlosser P, Matrosovich M, Seeger W, Lohmeyer J, Herold S. 2013. Macrophage-expressed IFN-beta contributes to apoptotic alveolar epithelial cell injury in severe influenza virus pneumonia. PLoS Pathog 9:e1003188. http://dx.doi.org/10.1371/journal.ppat.1003188.
60. Pothlichet J, Meunier I, Davis BK, Ting JP, Skamene E, von Messling V, Vidal SM. 2013. Type I IFN triggers RIG-I/TLR3/NLRP3-dependent inflammasome activation in influenza A virus infected cells. PLoS Pathog 9:e1003256. http://dx.doi.org/10.1371/journal.ppat.1003256.
61. Perez-Cidoncha M, Killip MJ, Asensio VJ, Fernandez Y, Bengoechea JA, Randall RE, Ortin J. 2014. Generation of replication-proficient influenza virus NS1 point mutants with interferon-hyperinducer phenotype. PLoS One 9:e98668. http://dx.doi.org/10.1371/journal.pone.0098668.
62. Fribourg M, Hartmann B, Schmolke M, Marjanovic N, Albrecht RA, Garcia-Sastre A, Sealfon SC, Jayaprakash C, Hayot F. 2014. Model of influenza A virus infection: dynamics of viral antagonism and innate immune response. J Theor Biol 351:47-57. http://dx.doi.org/10.1016/j.jtbi.2014.02.029.