High-throughput identification of loss-of-function mutations for anti-interferon activity in the influenza a virus ns segment

Journal of Virology

Volumn 88, Issue 17, 2014, Pages 10157-10164

  Wu, Nicholas C ^a,b   Young, Arthur P ^a   Al Mawsawi, Laith Q ^a   Anders Olson, C ^a   Feng, Jun ^a   Qi, Hangfei ^a   Luan, Harding H ^a   Li, Xinmin ^a   Wu, Ting Ting ^a   Sun, Ren ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; NS PROTEIN, INFLUENZA VIRUS; VIRUS PROTEIN; VIRUS RNA;

ANTAGONISTS AND INHIBITORS; DEFICIENCY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HIGH THROUGHPUT SEQUENCING; IMMUNOLOGY; INFLUENZA VIRUS A; METABOLISM; MOLECULAR BIOLOGY; MUTATION; PHYSIOLOGY; PROCEDURES; VIROLOGY;

HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INFLUENZA A VIRUS; INTERFERON TYPE I; MOLECULAR BIOLOGY; MUTATION; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS; VIROLOGY;

EID: 84910670272     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01494-14     Document Type: Article

References (50)

1. 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.
2. Rehwinkel J, Tan CP, Goubau D, Schulz O, Pichlmair A, Bier K, Robb N, Vreede F, Barclay W, Fodor E, Reis e 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.
3. Gack MU, Shin YC, Joo C-H, Urano T, Liang C, Sun L, Takeuchi O, Akira S, Chen Z, Inoue S, Jung JU. 2007. Trim25 ring-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 446:916-920. http://dx.doi.org/10.1038/nature05732.
4. Yoneyama M, Fujita T. 2009. RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 227:54-65. http://dx.doi.org/10.1111/j.1600-065X.2008.00727.x.
5. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao S-M, Maniatis T. 2003. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491-496. http://dx.doi.org/10.1038/ni921.
6. Yoneyama M, Suhara W, Fujita T. 2002. Control of IRF-3 activation by phosphorylation. J. Interferon Cytokine Res. 22:73-76. http://dx.doi.org/10.1089/107999002753452674.
7. Hou F, Sun L, Zheng H, Skaug B, Jiang Q-X, Chen ZJ. 2011. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell 146:448-461. http://dx.doi.org/10.1016/j.cell.2011.06.041.
8. Hiscott J, Pitha P, Genin P, Nguyen H, Heylbroeck C, Mamane Y, Algarte M, Lin R. 1999. Triggering the interferon response: the role of IRF-3 transcription factor. J. Interferon Cytokine Res. 19:1-13. http://dx.doi.org/10.1089/107999099314360.
9. 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.
10. Taniguchi T, Takaoka A. 2001. A weak signal for strong responses: interferon-alpha/beta revisited. Nat. Rev. Mol. Cell Biol. 2:378-386. http://dx.doi.org/10.1038/35073080.
11. Hale BG, Randall RE, Ortn 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.
12. Talon J, Horvath CM, Polley R, Basler CF, Muster T, Palese P, García-Sastre A. 2000. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:7989-7996. http://dx.doi.org/10.1128/JVI.74.17.7989-7996.2000.
13. Ludwig S, Wang X, Ehrhardt C, Zheng H, Donelan N, Planz O, Pleschka S, García-Sastre A, Heins G, Wolff T. 2002. The influenza A virus NS1 protein inhibits activation of Jun N-terminal kinase and AP-1 transcription factors. J. Virol. 76:11166-11171. http://dx.doi.org/10.1128/JVI.76.21.11166-11171.2002.
14. Wang X, Li M, Zheng H, Muster T, Palese P, Beg AA, García-Sastre A. 2000. InfluenzaAvirus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J. Virol. 74:11566-11573. http://dx.doi.org/10.1128/JVI.74.24.11566-11573.2000.
15. Bergmann M, Garcia-Sastre A, Carnero E, Pehamberger H, Wolff K, Palese P, Muster T. 2000. Influenza virus NS1 protein counteracts PKRmediated inhibition of replication. J. Virol. 74:6203-6206. http://dx.doi.org/10.1128/JVI.74.13.6203-6206.2000.
16. Min J-Y, Krug RM. 2006. 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. U. S. A. 103:7100-7105. http://dx.doi.org/10.1073/pnas.0602184103.
17. Panda D, Das A, Dinh PX, Subramaniam S, Nayak D, Barrows NJ, Pearson JL, Thompson J, Kelly DL, Ladunga I, Pattnaik AK. 2011. RNAi screening reveals requirement for host cell secretory pathway in infection by diverse families of negative-strand RNA viruses. Proc. Natl. Acad. Sci. U. S. A. 108:19036-19041. http://dx.doi.org/10.1073/pnas.1113643108.
18. König R, Stertz S, Zhou Y, Inoue A, Hoffmann H-H, Bhattacharyya S, Alamares JG, Tscherne DM, Ortigoza MB, Liang Y, Gao Q, Andrews SE, Bandyopadhyay S, Jesus PD, Tu BP, Pache L, Shih C, Orth A, Bonamy G, Miraglia L, Ideker T, García-Sastre A, Young JAT, Palese P, Shaw ML, Chanda SK. 2010. Human host factors required for influenza virus replication. Nature 463:813-817. http://dx.doi.org/10.1038/nature08699.
19. Karlas A, Machuy N, Shin Y, Pleissner K-P, Artarini A, Heuer D, Becker D, Khalil H, Ogilvie LA, Hess S, Murer AP, Mller E, Wolff T, Rudel T, Meyer TF. 2010. Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 463:818-822. http://dx.doi.org/10.1038/nature08760.
20. Shapira SD, Gat-Viks I, Shum BOV, Dricot A, de Grace MM, Wu L, Gupta PB, Hao T, Silver SJ, Root DE, Hill DE, Regev A, Hacohen N. 2009. A physical and regulatory map of host-influenza interactions reveals pathways in H1N1 infection. Cell 139:1255-1267. http://dx.doi.org/10.1016/j.cell.2009.12.018.
21. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P. 2008. Cellular proteins in influenza virus particles. PLoS Pathog. 4:e1000085. http://dx.doi.org/10.1371/journal.ppat.1000085.
22. Arumugaswami V, Remenyi R, Kanagavel V, Sue EY, Ho TN, Liu C, Fontanes V, Dasgupta A, Sun R. 2008. High-resolution functional profiling of hepatitis C virus genome. PLoS Pathog. 4:e1000182. http://dx.doi.org/10.1371/journal.ppat.1000182.
23. Heaton NS, Sachs D, Chen C-J, Hai R, Palese P. 2013. Genome-wide mutagenesis of influenza virus reveals unique plasticity of the hemagglutinin and NS1 proteins. Proc. Natl. Acad. Sci. U. S. A. 110:20248-20253. http://dx.doi.org/10.1073/pnas.1320524110.
24. Beitzel BF, Bakken RR, Smith JM, Schmaljohn CS. 2010. High-resolution functional mapping of the Venezuelan equine encephalitis virus genome by insertional mutagenesis and massively parallel sequencing. PLoS Pathog. 6:e1001146. http://dx.doi.org/10.1371/journal.ppat.1001146.
25. Wu NC, Young AP, Dandekar S, Wijersuriya H, Al-Mawsawi LQ, Wu T-T, Sun R. 2013. Systematic identification of h274y compensatory mutations in influenza A virus neuraminidase by high-throughput screening. J. Virol. 87:1193-1199. http://dx.doi.org/10.1128/JVI.01658-12.
26. Neumann G, Watanabe T, Ito H, Watanabe S, Goto H, Gao P, Hughes M, Perez DR, Donis R, Hoffmann E, Hobom G, Kawaoka Y. 1999. Generation of influenza A viruses entirely from cloned cDNAs. Proc. Natl. Acad. Sci. U. S. A. 96:9345-9350. http://dx.doi.org/10.1073/pnas.96.16.9345.
27. Hwang S, Kim KS, Flano E, Wu T-T, Tong LM, Park AN, Song MJ, Sanchez DJ, O'Connell RM, Cheng G, Sun R. 2009. Conserved herpesviral kinase promotes viral persistence by inhibiting the IRF-3-mediated type I interferon response. Cell Host Microbe 5:166-178. http://dx.doi.org/10.1016/j.chom.2008.12.013.
28. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754-1760. http://dx.doi.org/10.1093/bioinformatics/btp324.
29. Kinde I, Wu J, Papadopoulos N, Kinzler KW, Vogelstein B. 2011. Detection and quantification of rare mutations with massively parallel sequencing. Proc. Natl. Acad. Sci. U. S. A. 108:9530-9535. http://dx.doi.org/10.1073/pnas.1105422108.
30. Nobusawa E, Sato K. 2006. Comparison of the mutation rates of human influenza A and B viruses. J. Virol. 80:3675-3678. http://dx.doi.org/10.1128/JVI.80.7.3675-3678.2006.
31. García-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324-330. http://dx.doi.org/10.1006/viro.1998.9508.
32. Wang W, Riedel K, Lynch P, Chien CY, Montelione GT, Krug RM. 1999. 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 5:195-205. http://dx.doi.org/10.1017/S1355838299981621.
33. Donelan NR, Basler CF, García-Sastre A. 2003. 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. 77:13257-13266. http://dx.doi.org/10.1128/JVI.77.24.13257-13266.2003.
34. Seo SH, Hoffmann E, Webster RG. 2002. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat. Med. 8:950-954. http://dx.doi.org/10.1038/nm757.
35. Hayman A, Comely S, Lackenby A, Hartgroves LCS, 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.
36. Kellogg EH, Leaver-Fay A, Baker D. 2011. Role of conformational sampling in computing mutation-induced changes in protein structure and stability. Proteins 79:830-838. http://dx.doi.org/10.1002/prot.22921.
37. Gack MU, Albrecht RA, Urano T, Inn K-S, Huang I-C, Carnero E, Farzan M, Inoue S, Jung JU, García-Sastre A. 2009. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host Microbe 5:439-449. http://dx.doi.org/10.1016/j.chom.2009.04.006.
38. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737. http://dx.doi.org/10.1038/ni1087.
39. Richt JA, García-Sastre A. 2009. Attenuated influenza virus vaccines with modified NS1 proteins. Curr. Top. Microbiol. Immunol. 333:177-195. http://dx.doi.org/10.1007/978-3-540-92165-3_9.
40. Zhou B, Li Y, Speer SD, Subba A, Lin X, Wentworth DE. 2012. Engineering temperature sensitive live attenuated influenza vaccines from emerging viruses. Vaccine 30:3691-3702. http://dx.doi.org/10.1016/j.vaccine.2012.03.025.
41. Whittle JRR, Zhang R, Khurana S, King LR, Manischewitz J, Golding H, Dormitzer PR, Haynes BF, Walter EB, Moody MA, Kepler TB, Liao H-X, Harrison SC. 2011. Broadly neutralizing human antibody that recognizes the receptor-binding pocket of influenza virus hemagglutinin. Proc. Natl. Acad. Sci. U. S. A. 108:14216-14221. http://dx.doi.org/10.1073/pnas.1111497108.
42. Ekiert DC, Wilson IA. 2012. Broadly neutralizing antibodies against influenza virus and prospects for universal therapies. Curr. Opin. Virol. 2:134-141. http://dx.doi.org/10.1016/j.coviro.2012.02.005.
43. Edinger TO, Pohl MO, Stertz S. 2014. Entry of influenza A virus: host factors and antiviral targets. J. Gen. Virol. 95:263-277. http://dx.doi.org/10.1099/vir.0.059477-0.
44. Blight KJ, McKeating JA, Rice CM. 2002. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 76: 13001-13014. http://dx.doi.org/10.1128/JVI.76.24.13001-13014.2002.
45. Lohmann V, Körner F, Koch J, Herian U, Theilmann L, Bartenschlager R. 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285:110-113. http://dx.doi.org/10.1126/science.285.5424.110.
46. Lindenbach BD, Evans MJ, Syder AJ, Wölk B, Tellinghuisen TL, Liu CC, Maruyama T, Hynes RO, Burton DR, McKeating JA, Rice CM. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623-626. http://dx.doi.org/10.1126/science.1114016.
47. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, Rabson A, Martin MA. 1986. Production of acquired immunodeficiency syndromeassociated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol. 59:284-291.
48. Pleschka S, Jaskunas R, Engelhardt OG, Zrcher T, Palese P, García-Sastre A. 1996. A plasmid-based reverse genetics system for influenza A virus. J. Virol. 70:4188-4192.
49. Pérez-Cidoncha M, Killip MJ, Oliveros JC, Asensio VJ, Fernández Y, Bengoechea JA, Randall RE, Ortín J. 2014. An unbiased genetic screen reveals the polygenic nature of the influenza virus anti-interferon response. J. Virol. 88:4632-4646. http://dx.doi.org/10.1128/JVI.00014-14.
50. Bornholdt ZA, Prasad BV. 2006. X-ray structure of influenza virus NS1 effector domain. Nat. Struct. Mol. Biol. 13:559-560. http://dx.doi.org/10.1038/nsmb1099.