Influenza A virus-induced degradation of eukaryotic translation initiation factor 4B contributes to viral replication by suppressing IFITM3 protein expression

Journal of Virology

Volumn 88, Issue 15, 2014, Pages 8375-8385

  Wang, Song ^a   Chi, Xiaojuan ^b   Wei, Haitao ^a   Chen, Yuhai ^a   Chen, Zhilong ^b   Huang, Shile ^c   Chen, Ji Long ^a,b  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

^c LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4B; INTERFERON; INTERFERON INDUCED TRANSMEMBRANE PROTEIN 3; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EPITHELIUM CELL; IMMUNE RESPONSE; INFLUENZA VIRUS A; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RNA DEGRADATION; SURVIVAL TIME; TRANSLATION INITIATION; UPREGULATION; VIRUS IMMUNITY; VIRUS REPLICATION; VIRUS TITRATION; WEIGHT REDUCTION;

ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EPITHELIAL CELLS; EUKARYOTIC INITIATION FACTORS; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE EVASION; INFLUENZA A VIRUS; LUNG; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; ORTHOMYXOVIRIDAE INFECTIONS; PROTEIN BIOSYNTHESIS; PROTEOLYSIS; RNA-BINDING PROTEINS; SPLEEN; SURVIVAL ANALYSIS; THYMUS GLAND; VIRUS REPLICATION;

EID: 84903888416     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00126-14     Document Type: Article

References (56)

1. Lam TT, Wang J, Shen Y, Zhou B, Duan L, Cheung CL, Ma C, Lycett SJ, Leung CY, Chen X, Li L, Hong W, Chai Y, Zhou L, Liang H, Ou Z, Liu Y, Farooqui A, Kelvin DJ, Poon LL, Smith DK, Pybus OG, Leung GM, Shu Y, Webster RG, Webby RJ, Peiris JS, Rambaut A, Zhu H, Guan Y. 2013. The genesis and source of the H7N9 influenza viruses causing human infections in China. Nature 502:241-244. http://dx.doi.org/10.1038/nature12515.
2. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86. http://dx.doi.org/10.1111/j.1600-065X.2008.00737.x.
3. Takaoka A, Yanai H. 2006. Interferon signalling network in innate defence. Cell. Microbiol. 8:907-922. http://dx.doi.org/10.1111/j.1462-5822.2006.00716.x.
4. Mordstein M, Neugebauer E, Ditt V, Jessen B, Rieger T, Falcone V, Sorgeloos F, Ehl S, Mayer D, Kochs G, Schwemmle M, Gunther S, Drosten C, Michiels T, Staeheli P. 2010. Lambda interferon renders epithelial cells of the respiratory and gastrointestinal tracts resistant to viral infections. J. Virol. 84:5670-5677. http://dx.doi.org/10.1128/JVI.00272-10.
5. Wei H, Wang S, Chen Q, Chen Y, Chi X, Zhang L, Huang S, Gao GF, Chen J-L. 2014. Suppression of interferon lambda signaling by SOCS-1 results in their excessive production during influenza virus Infection. PLoS Pathog. 10:e1003845. http://dx.doi.org/10.1371/journal.ppat.1003845.
6. D'Cunha J, Knight E, Haas AL, Truitt RL, Borden EC. 1996. Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc. Natl. Acad. Sci. U.S.A. 93:211-215. http://dx.doi.org/10.1073/pnas.93.1.211.
7. Holzinger D, Jorns C, Stertz S, Boisson-Dupuis S, Thimme R, Weidmann M, Casanova J-L, Haller O, Kochs G. 2007. Induction of MxA gene expression by influenza A virus requires type I or type III intereIF4B feron signaling. J. Virol. 81:7776-7785. http://dx.doi.org/10.1128/JVI.00546-06.
8. Rebouillat D, Hovanessian AG. 1999. The human 2', 5'-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. J. Interferon Cytokine Res. 19:295-308. http://dx.doi.org/10.1089/107999099313992.
9. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, Ryan BJ, Weyer JL, van der Weyden L, Fikrig E, Adams DJ, Xavier RJ, Farzan M, Elledge SJ. 2009. The IFITM proteins mediate cellular resistance to influenzaAH1N1 virus, West Nile virus, and dengue virus. Cell 139:1243-1254. http://dx.doi.org/10.1016/j.cell.2009.12.017.
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. Pauli E-K, Schmolke M, Wolff T, Viemann D, Roth J, Bode JG, Ludwig S. 2008. Influenza A virus inhibits type I IFN signaling via NF-κB dependent induction of SOCS-3 expression. PLoS Pathog. 4:e1000196. http://dx.doi.org/10.1371/journal.ppat.1000196.
12. Walsh D, Mohr I. 2011. Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol. 9:860-875. http://dx.doi.org/10.1038/nrmicro2655.
13. Mohr I, Sonenberg N. 2012. Host translation at the nexus of infection and immunity. Cell Host Microbe 12:470-483. http://dx.doi.org/10.1016/j.chom.2012.09.006.
14. Walsh D, Mathews MB, Mohr I. 2013. Tinkering with translation: protein synthesis in virus-infected cells. Cold Spring Harb. Perspect. Biol. 5:a012351. http://dx.doi.org/10.1101/cshperspect.a012351.
15. García-Sastre A, Biron CA. 2006. Type 1 interferons and the virus-host relationship: a lesson in detente. Science 312:879-882. http://dx.doi.org/10.1126/science.1125676.
16. Gainey MD, Dillon PJ, Clark KM, Manuse MJ, Parks GD. 2008. Paramyxovirus-induced shutoff of host and viral protein synthesis: role of the P and V proteins in limiting PKR activation. J. Virol. 82:828-839. http://dx.doi.org/10.1128/JVI.02023-07.
17. Williams B. 1999. PKR; a sentinel kinase for cellular stress. Oncogene 18:6112-6120. http://dx.doi.org/10.1038/sj.onc.1203127.
18. Katze MG, He Y, Gale M. 2002. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2:675-687. http://dx.doi.org/10.1038/nri888.
19. Walsh D, Arias C, Perez C, Halladin D, Escandon M, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Mohr I. 2008. Eukaryotic translation initiation factor 4F architectural alterations accompany translation initiation factor redistribution in poxvirus-infected cells. Mol. Cell. Biol. 28: 2648-2658. http://dx.doi.org/10.1128/MCB.01631-07.
20. Walsh D, Perez C, Notary J, Mohr I. 2005. Regulation of the translation initiation factor eIF4F by multiple mechanisms in human cytomegalovirus-infected cells. J. Virol. 79:8057-8064. http://dx.doi.org/10.1128/JVI.79.13.8057-8064.2005.
21. Herdy B, Jaramillo M, Svitkin YV, Rosenfeld AB, Kobayashi M, Walsh D, Alain T, Sean P, Robichaud N, Topisirovic I, Furic L, Dowling RJ, Sylvestre A, Rong L, Colina R, Costa-Mattioli M, Fritz JH, Olivier M, Brown E, Mohr I, Sonenberg N. 2012. Translational control of the activation of transcription factor NF-kappaB and production of type I interferon by phosphorylation of the translation factor eIF4E. Nat. Immunol. 13:543-550. http://dx.doi.org/10.1038/ni.2291.
22. Aragón T, de la Luna S, Novoa I, Carrasco L, Ortín J, Nieto A. 2000. Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol. Cell. Biol. 20: 6259-6268. http://dx.doi.org/10.1128/MCB.20.17.6259-6268.2000.
23. Yángüez E, Castello A, Welnowska E, Carrasco L, Goodfellow I, Nieto A. 2011. Functional impairment of eIF4A and eIF4G factors correlates with inhibition of influenza virus mRNA translation. Virology 413:93-102. http://dx.doi.org/10.1016/j.virol.2011.02.012.
24. Yang J, Wang J, Chen K, Guo G, Xi R, Rothman PB, Whitten D, Zhang L, Huang S, Chen J-L. 2013. eIF4B phosphorylation by Pim kinases plays a critical role in cellular transformation by Abl oncogenes. Cancer Res. 73:4898-4908. http://dx.doi.org/10.1158/0008-5472.CAN-12-4277.
25. Rogers GW, Richter NJ, Merrick WC. 1999. Biochemical and kinetic characterization of the RNAhelicase activity of eukaryotic initiation factor 4A. J. Biol. Chem. 274:12236-12244. http://dx.doi.org/10.1074/jbc.274.18.12236.
26. Ochs K, Saleh L, Bassili G, Sonntag VH, Zeller A, Niepmann M. 2002. Interaction of translation initiation factor eIF4B with the poliovirus internal ribosome entry site. J. Virol. 76:2113-2122. http://dx.doi.org/10.1128/jvi.76.5.2113-2122.2002.
27. Kuang E, Fu B, Liang Q, Myoung J, Zhu F. 2011. Phosphorylation of eukaryotic translation initiation factor 4B (EIF4B) by open reading frame 45/p90 ribosomal S6 kinase (ORF45/RSK) signaling axis facilitates protein translation during Kaposi sarcoma-associated herpesvirus (KSHV) lytic replication. J. Biol. Chem. 286:41171-41182. http://dx.doi.org/10.1074/jbc.M111.280982.
28. Kroczynska B, Kaur S, Katsoulidis E, Majchrzak-Kita B, Sassano A, Kozma SC, Fish EN, Platanias LC. 2009. Interferon-dependent engagement of eukaryotic initiation factor 4B via S6 kinase (S6K)-and ribosomal protein S6K-mediated signals. Mol. Cell. Biol. 29:2865-2875. http://dx.doi.org/10.1128/MCB.01537-08.
29. Hsiang T-Y, 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.
30. Zhao C, Hsiang T-Y, Kuo R-L, Krug RM. 2010. ISG15 conjugation system targets the viral NS1 protein in influenza A virus-infected cells. Proc. Natl. Acad. Sci. U.S.A. 107:2253-2258. http://dx.doi.org/10.1073/pnas.0909144107.
31. Lenschow DJ, Lai C, Frias-Staheli N, Giannakopoulos NV, Lutz A, Wolff T, Osiak A, Levine B, Schmidt RE, García-Sastre A. 2007. IFNstimulated gene 15 functions as a critical antiviral molecule against influenza, herpes, and Sindbis viruses. Proc. Natl. Acad. Sci. U.S.A. 104:1371-1376. http://dx.doi.org/10.1073/pnas.0607038104.
32. Wang S, Li H, Chen Y, Wei H, Gao GF, Liu H, Huang S, Chen J-L. 2012. Transport of influenza virus neuraminidase (NA) to host cell surface is regulated by ARHGAP21 and Cdc42 proteins. J. Biol. Chem. 287:9804-9816. http://dx.doi.org/10.1074/jbc.M111.312959.
33. Guo G, Qiu X, Wang S, Chen Y, Rothman P, Wang Z, Wang G, Chen J. 2010. Oncogenic E17K mutation in the pleckstrin homology domain of AKT1 promotes v-Abl-mediated pre-B-cell transformation and survival of Pim-deficient cells. Oncogene 29:3845-3853. http://dx.doi.org/10.1038/onc.2010.149.
34. Feeley EM, Sims JS, John SP, Chin CR, Pertel T, Chen L-M, Gaiha GD, Ryan BJ, Donis RO, Elledge SJ. 2011. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog. 7:e1002337. http://dx.doi.org/10.1371/journal.ppat.1002337.
35. Desai SD, Wood LM, Tsai Y-C, Hsieh T-S, Marks JR, Scott GL, Giovanella BC, Liu LF. 2008. ISG15 as a novel tumor biomarker for drug sensitivity. Mol. Cancer Ther. 7:1430-1439. http://dx.doi.org/10.1158/1535-7163.MCT-07-2345.
36. Fan K, Jia Y, Wang S, Li H, Wu D, Wang G, Chen J-L. 2012. Role of Itk signalling in the interaction between influenza A virus and T-cells. J. Gen. Virol. 93:987-997. http://dx.doi.org/10.1099/vir.0.041228-0.
37. Lyles DS. 2000. Cytopathogenesis and inhibition of host gene expression by RNA viruses. Microbiol. Mol. Biol. Rev. 64:709-724. http://dx.doi.org/10.1128/MMBR.64.4.709-724.2000.
38. Adams J. 2004. The proteasome: a suitable antineoplastic target. Nat. Rev. Cancer 4:349-360. http://dx.doi.org/10.1038/nrc1361.
39. Alfonso R, Rodriguez A, Rodriguez P, Lutz T, Nieto A. 2013. CHD6, a cellular repressor of influenza virus replication, is degraded in human alveolar epithelial cells and mice lungs during infection. J. Virol. 87:4534-4544. http://dx.doi.org/10.1128/JVI.00554-12.
40. Haye K, Burmakina S, Moran T, García-Sastre A, Fernandez-Sesma A. 2009. The NS1 protein of a human influenza virus inhibits type I interferon production and the induction of antiviral responses in primary human dendritic and respiratory epithelial cells. J. Virol. 83:6849-6862. http://dx.doi.org/10.1128/JVI.02323-08.
41. Gack MU, Albrecht RA, Urano T, Inn K-S, Huang I, 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.
42. Rajsbaum R, Albrecht RA, Wang MK, Maharaj NP, Versteeg GA, Nistal-Villán E, García-Sastre A, Gack MU. 2012. Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog. 8:e1003059. http://dx.doi.org/10.1371/journal.ppat.1003059.
43. 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.
44. Schoggins JW, Macduff DA, Imanaka N, Gainey MD, Shrestha B, Eitson JL, Mar KB, Richardson RB, Ratushny AV, Litvak V, Dabelic R, Manicassamy B, Aitchison JD, Aderem A, Elliott RM, Garcia-Sastre A, Racaniello V, Snijder EJ, Yokoyama WM, Diamond MS, Virgin HW, Rice CM. 2014. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505:691-695. http://dx.doi.org/10.1038/nature12862.
45. Raught B, Peiretti F, Gingras A-C, Livingstone M, Shahbazian D, Mayeur GL, Polakiewicz RD, Sonenberg N, Hershey JW. 2004. Phosphorylation of eucaryotic translation initiation factor 4B Ser422 is modulated by S6 kinases. EMBO J. 23:1761-1769. http://dx.doi.org/10.1038/sj.emboj.7600193.
46. Shahbazian D, Parsyan A, Petroulakis E, Topisirovic I, Martineau Y, Gibbs BF, Svitkin Y, Sonenberg N. 2010. Control of cell survival and proliferation by mammalian eukaryotic initiation factor 4B. Mol. Cell. Biol. 30:1478-1485. http://dx.doi.org/10.1128/MCB.01218-09.
47. Darnell JE, Jr, Kerr IM, Stark GR. 1994. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264:1415-1420. http://dx.doi.org/10.1126/science.8197455.
48. Weidner JM, Jiang D, Pan X-B, Chang J, Block TM, Guo J-T. 2010. Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J. Virol. 84: 12646-12657. http://dx.doi.org/10.1128/JVI.01328-10.
49. Lu J, Pan Q, Rong L, Liu S-L, Liang C. 2011. The IFITM proteins inhibit HIV-1 infection. J. Virol. 85:2126-2137. http://dx.doi.org/10.1128/JVI.01531-10.
50. Jiang D, Weidner JM, Qing M, Pan XB, Guo H, Xu C, Zhang X, Birk A, Chang J, Shi PY, Block TM, Guo JT. 2010. Identification of five interferon-induced cellular proteins that inhibit West Nile virus and dengue virus infections. J. Virol. 84:8332-8341. http://dx.doi.org/10.1128/JVI.02199-09.
51. Huang IC, Bailey CC, Weyer JL, Radoshitzky SR, Becker MM, Chiang JJ, Brass AL, Ahmed AA, Chi X, Dong L, Longobardi LE, Boltz D, Kuhn JH, Elledge SJ, Bavari S, Denison MR, Choe H, Farzan M. 2011. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 7:e1001258. http://dx.doi.org/10.1371/journal.ppat.1001258.
52. Everitt AR, Clare S, Pertel T, John SP, Wash RS, Smith SE, Chin CR, Feeley EM, Sims JS, Adams DJ, Wise HM, Kane L, Goulding D, Digard P, Anttila V, Baillie JK, Walsh TS, Hume DA, Palotie A, Xue Y, Colonna V, Tyler-Smith C, Dunning J, Gordon SB, Smyth RL, Openshaw PJ, Dougan G, Brass AL, Kellam P. 2012. IFITM3 restricts the morbidity and mortality associated with influenza. Nature 484:519-523. http://dx.doi.org/10.1038/nature10921.
53. Wakim LM, Gupta N, Mintern JD, Villadangos JA. 2013. Enhanced survival of lung tissue-resident memory CD8+ T cells during infection with influenza virus due to selective expression of IFITM3. Nat. Immunol. 14:238-245. http://dx.doi.org/10.1038/ni.2525.
54. Li K, Markosyan RM, Zheng Y-M, Golfetto O, Bungart B, Li M, Ding S, He Y, Liang C, Lee JC, Gratton E, Cohen FS, Liu S-L. 2013. IFITM proteins restrict viral membrane hemifusion. PLoS Pathog. 9:e1003124. http://dx.doi.org/10.1371/journal.ppat.1003124.
55. Amini-Bavil-Olyaee S, Choi YJ, Lee JH, Shi M, Huang I, Farzan M, Jung JU. 2013. The antiviral effector IFITM3 disrupts intracellular cholesterol homeostasis to block viral entry. Cell Host Microbe 13:452-464. http://dx.doi.org/10.1016/j.chom.2013.03.006.
56. Desai TM, Marin M, Chin CR, Savidis G, Brass AL, Melikyan GB. 2014. IFITM3 restricts influenza A virus entry by blocking the formation of fusion pores following virus-endosome hemifusion. PLoS Pathog. 10: e1004048. http://dx.doi.org/10.1371/journal.ppat.1004048.