Robust expression of vault RNAs induced by influenza A virus plays a critical role in suppression of PKR-mediated innate immunity

Nucleic Acids Research

Volumn 43, Issue 21, 2015, Pages 10321-10337

  Li, Fang ^a   Chen, Yuhai ^a   Zhang, Zhaoyuan ^a,b   Ouyang, Jing ^a   Wang, Yi ^a   Yan, Ruoxiang ^c   Huang, Shile ^d   Gao, George Fu ^a   Guo, Guijie ^a   Chen, Ji Long ^a,c  

^a INSTITUTE OF MICROBIOLOGY   (China)

^b ANHUI UNIVERSITY   (China)

^c FUJIAN AGRICULTURE AND FORESTRY UNIVERSITY   (China)

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

Author keywords

[No Author keywords available]

Indexed keywords

NONSTRUCTURAL PROTEIN 1; PROTEIN KINASE R; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VAULT RNA; INS1 PROTEIN, INFLUENZA VIRUS; INTERFERON; VIRAL PROTEIN;

A549 CELL LINE; ACUTE LUNG INJURY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RESPONSE; DNA MICROARRAY; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA A; INFLUENZA A VIRUS; INNATE IMMUNITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE; UPREGULATION; VIRUS REPLICATION; ANIMAL; C57BL MOUSE; CELL LINE; DISEASE RESISTANCE; GENETICS; IMMUNOLOGY; METABOLISM; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY;

ANIMALS; CELL LINE; DISEASE RESISTANCE; EIF-2 KINASE; FEMALE; HUMANS; IMMUNITY, INNATE; INFLUENZA A VIRUS; INTERFERONS; MICE; MICE, INBRED C57BL; ORTHOMYXOVIRIDAE INFECTIONS; RNA, UNTRANSLATED; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84983426932     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1078     Document Type: Article

References (68)

1. Meurs, E., Chong, K., Galabru, J., Thomas, N.S., Kerr, I.M., Williams, B.R. and Hovanessian, A.G. (1990) Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell, 62, 379-390.
2. de Haro, C., Mendez, R. and Santoyo, J. (1996) The eIF-2alpha kinases and the control of protein synthesis. FASEB J., 10, 1378-1387.
3. Kumar, A., Haque, J., Lacoste, J., Hiscott, J. and Williams, B.R. (1994) Double-stranded RNA-dependent protein kinase activates transcription factor NF-kappa B by phosphorylating I kappa B. Proc. Natl. Acad. Sci. U.S.A., 91, 6288-6292.
4. Sudha, G., Yamunadevi, S., Tyagi, N., Das, S. and Srinivasan, N. (2012) Structural and molecular basis of interaction of HCV non-structural protein 5A with human casein kinase 1alpha and PKR. BMC Struct. Biol., 12, 28.
5. Sharma, S., tenOever, B.R., Grandvaux, N., Zhou, G.P., Lin, R. and Hiscott, J. (2003) Triggering the interferon antiviral response through an IKK-related pathway. Science, 300, 1148-1151.
6. Schneider, W.M., Chevillotte, M.D. and Rice, C.M. (2014) Interferon-stimulated genes: a complex web of host defenses. Annu. Rev. Immunol., 32, 513-545.
7. Katze, M.G., He, Y. and Gale, M. Jr (2002) Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol., 2, 675-687.
8. Langland, J.O., Cameron, J.M., Heck, M.C., Jancovich, J.K. and Jacobs, B.L. (2006) Inhibition of PKR by RNA and DNA viruses. Virus Res., 119, 100-110.
9. Katze, M.G., Tomita, J., Black, T., Krug, R.M., Safer, B. and Hovanessian, A. (1988) Influenza virus regulates protein synthesis during infection by repressing autophosphorylation and activity of the cellular 68, 000-Mr protein kinase. J. Virol., 62, 3710-3717.
10. Lu, Y., Wambach, M., Katze, M.G. and Krug, R.M. (1995) Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology, 214, 222-228.
11. Lee, T.G., Tang, N., Thompson, S., Miller, J. and Katze, M.G. (1994) The 58, 000-dalton cellular inhibitor of the interferon-induced double-stranded RNA-activated protein kinase (PKR) is a member of the tetratricopeptide repeat family of proteins. Mol. Cell .Biol., 14, 2331-2342.
12. Tan, S.L. and Katze, M.G. (1998) Biochemical and genetic evidence for complex formation between the influenza A virus NS1 protein and the interferon-induced PKR protein kinase. J. Interf. Cytok. Res., 18, 757-766.
13. Melville, M.W., Tan, S.L., Wambach, M., Song, J., Morimoto, R.I. and Katze, M.G. (1999) The cellular inhibitor of the PKR protein kinase, P58(IPK), is an influenza virus-activated co-chaperone that modulates heat shock protein 70 activity. J. Biol. Chem., 274, 3797-3803.
14. Tan, S.L., Gale, M.J. Jr and Katze, M.G. (1998) Double-stranded RNA-independent dimerization of interferon-induced protein kinase PKR and inhibition of dimerization by the cellular P58IPK inhibitor. Mol. Cell. Biol., 18, 2431-2443.
15. Bergmann, M., Garcia-Sastre, A., Carnero, E., Pehamberger, H., Wolff, K., Palese, P. and Muster, T. (2000) Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J. Virol., 74, 6203-6206.
16. Chien, C.Y., Xu, Y.J., Xiao, R., Aramini, J.M., Sahasrabudhe, P.V., Krug, R.M. and Montelione, G.T. (2004) Biophysical characterization of the complex between double-stranded RNA and the N-terminal domain of the NS1 protein from influenza A virus: Evidence for a novel RNA-binding mode. Biochemistry, 43, 1950-1962.
17. Min, J.Y. and Krug, R.M. (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.
18. Falcon, A.M., Fortes, P., Marion, R.M., Beloso, A. and Ortin, J. (1999) Interaction of influenza virus NS1 protein and the human homologue of Staufen in vivo and in vitro. Nucleic Acids Res., 27, 2241-2247.
19. Khaperskyy, D.A., Hatchette, T.F. and McCormick, C. (2012) Influenza A virus inhibits cytoplasmic stress granule formation. FASEB J., 26, 1629-1639.
20. Gottwein, E. and Cullen, B.R. (2008) Viral and cellular microRNAs as determinants of viral pathogenesis and immunity. Cell Host Microbe, 3, 375-387.
21. Zhang, Q., Chen, C.Y., Yedavalli, V.S. and Jeang, K.T. (2013) NEAT1 long noncoding RNA and paraspeckle bodies modulate HIV-1 posttranscriptional expression. Mbio, 4, e00596-e00512.
22. Imamura, K., Imamachi, N., Akizuki, G., Kumakura, M., Kawaguchi, A., Nagata, K., Kato, A., Kawaguchi, Y., Sato, H., Yoneda, M. et al. (2014) Long noncoding RNA NEAT1-dependent SFPQ relocation from promoter region to paraspeckle mediates IL8 expression upon immune stimuli. Mol. Cell., 53, 393-406.
23. Winterling, C., Koch, M., Koeppel, M., Garcia-Alcalde, F., Karlas, A. and Meyer, T.F. (2014) Evidence for a crucial role of a host non-coding RNA in influenza A virus replication. RNA Biol., 11, 66-75.
24. Ouyang, J., Zhu, X., Chen, Y., Wei, H., Chen, Q., Chi, X., Qi, B., Zhang, L., Zhao, Y., Gao, G.F. et al. (2014) NRAV, a long noncoding RNA, modulates antiviral responses through suppression of interferon-stimulated gene transcription. Cell Host Microbe, 16, 616-626.
25. Kambara, H., Niazi, F., Kostadinova, L., Moonka, D.K., Siegel, C.T., Post, A.B., Carnero, E., Barriocanal, M., Fortes, P., Anthony, D.D. et al. (2014) Negative regulation of the interferon response by an interferon-induced long non-coding RNA. Nucleic Acids Res., 42, 10668-10680.
26. Yoshikawa, T., Takata, A., Otsuka, M., Kishikawa, T., Kojima, K., Yoshida, H. and Koike, K. (2012) Silencing of microRNA-122 enhances interferon-alpha signaling in the liver through regulating SOCS3 promoter methylation. Sci. Rep., 2, 637.
27. Hou, J., Wang, P., Lin, L., Liu, X., Ma, F., An, H., Wang, Z. and Cao, X. (2009) MicroRNA-146a feedback inhibits RIG-I-dependent Type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol., 183, 2150-2158.
28. Wang, P., Hou, J., Lin, L., Wang, C., Liu, X., Li, D., Ma, F., Wang, Z. and Cao, X. (2010) Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J .Immunol., 185, 6226-6233.
29. Kedersha, N.L. and Rome, L.H. (1986) Isolation and characterization of a novel ribonucleoprotein particle: large structures contain a single species of small RNA. J. Cell .Biol., 103, 699-709.
30. Kedersha, N.L., Heuser, J.E., Chugani, D.C. and Rome, L.H. (1991) Vaults. III. Vault ribonucleoprotein particles open into flower-like structures with octagonal symmetry. J. Cell .Biol., 112, 225-235.
31. Kickhoefer, V.A., Rajavel, K.S., Scheffer, G.L., Dalton, W.S., Scheper, R.J. and Rome, L.H. (1998) Vaults are up-regulated in multidrug-resistant cancer cell lines. J. Biol. Chem., 273, 8971-8974.
32. Nandy, C., Mrazek, J., Stoiber, H., Grasser, F.A., Huttenhofer, A. and Polacek, N. (2009) Epstein-barr virus-induced expression of a novel human vault RNA. J. Mol. Biol., 388, 776-784.
33. Kong, L.B., Siva, A.C., Kickhoefer, V.A., Rome, L.H. and Stewart, P.L. (2000) RNA location and modeling of a WD40 repeat domain within the vault. RNA, 6, 890-900.
34. Persson, H., Kvist, A., Vallon-Christersson, J., Medstrand, P., Borg, A. and Rovira, C. (2009) The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat. Cell. Biol., 11, 1268-1271.
35. Mrazek, J., Kreutmayer, S.B., Grasser, F.A., Polacek, N. and Huttenhofer, A. (2007) Subtractive hybridization identifies novel differentially expressed ncRNA species in EBV-infected human B cells. Nucleic Acids Res., 35, e73.
36. Lee, K., Kunkeaw, N., Jeon, S.H., Lee, I., Johnson, B.H., Kang, G.Y., Bang, J.Y., Park, H.S., Leelayuwat, C. and Lee, Y.S. (2011) Precursor miR-886, a novel noncoding RNA repressed in cancer, associates with PKR and modulates its activity. RNA, 17, 1076-1089.
37. Kunkeaw, N., Jeon, S.H., Lee, K., Johnson, B.H., Tanasanvimon, S., Javle, M., Pairojkul, C., Chamgramol, Y., Wongfieng, W., Gong, B. et al. (2013) Cell death/proliferation roles for nc886, a non-coding RNA, in the protein kinase R pathway in cholangiocarcinoma. Oncogene, 32, 3722-3731.
38. Lee, H.S., Lee, K., Jang, H.J., Lee, G.K., Park, J.L., Kim, S.Y., Kim, S.B., Johnson, B.H., Zo, J.I., Lee, J.S. et al. (2014) Epigenetic silencing of the non-coding RNA nc886 provokes oncogenes during human esophageal tumorigenesis. Oncotarget, 5, 3472-3481.
39. Lee, K.S., Park, J.L., Lee, K., Richardson, L.E., Johnson, B.H., Lee, H.S., Lee, J.S., Kim, S.B., Kwon, O.H., Song, K.S. et al. (2014) nc886, a non-coding RNA of anti-proliferative role, is suppressed by CpG DNA methylation in human gastric cancer. Oncotarget, 5, 3944-3955.
40. Wang, S., Li, H., Chen, Y., Wei, H., Gao, G.F., Liu, H., Huang, S. and 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.
41. Wei, H., Wang, S., Chen, Q., Chen, Y., Chi, X., Zhang, L., Huang, S., Gao, G.F. and 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.
42. Wang, S., Chi, X., Wei, H., Chen, Y., Chen, Z., Huang, S. and Chen, J.L. (2014) Influenza A virus-induced degradation of eukaryotic translation initiation factor 4B contributes to viral replication by suppressing IFITM3 protein expression. J. Virol., 88, 8375-8385.
43. Ideue, T., Hino, K., Kitao, S., Yokoi, T. and Hirose, T. (2009) Efficient oligonucleotide-mediated degradation of nuclear noncoding RNAs in mammalian cultured cells. RNA, 15, 1578-1587.
44. Guo, G., Qiu, X., Wang, S., Chen, Y., Rothman, P.B., Wang, Z., Chen, Y., Wang, G. and Chen, J.L. (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.
45. Lerner, R.A. and Hodge, L.D. (1969) Nonpermissive infections of mammalian cells: synthesis of inluenza virus genome in HeLa cells. Proc. Natl. Acad. Sci. U.S.A., 64, 544-551.
46. Duan, W., Chan, J.H., McKay, K., Crosby, J.R., Choo, H.H., Leung, B.P., Karras, J.G. and Wong, W.S. (2005) Inhaled p38alpha mitogen-activated protein kinase antisense oligonucleotide attenuates asthma in mice. Am. J. Respir. Crit. Care. Med., 171, 571-578.
47. Tanaka, M. and Nyce, J.W. (2001) Respirable antisense oligonucleotides: a new drug class for respiratory disease. Respir. Res., 2, 5-9.
48. Iwasaki, A. and Pillai, P.S. (2014) Innate immunity to influenza virus infection. Nat. Rev. Immunol., 14, 315-328.
49. Jeon, S.H., Lee, K., Lee, K.S., Kunkeaw, N., Johnson, B.H., Holthauzen, L.M., Gong, B., Leelayuwat, C. and Lee, Y.S. (2012) Characterization of the direct physical interaction of nc886, a cellular non-coding RNA, and PKR. FEBS. Lett., 586, 3477-3484.
50. Konig, R., Stertz, S., Zhou, Y., Inoue, A., Hoffmann, H.H., Bhattacharyya, S., Alamares, J.G., Tscherne, D.M., Ortigoza, M.B., Liang, Y. et al. (2010) Human host factors required for influenza virus replication. Nature, 463, 813-817.
51. Karlas, A., Machuy, N., Shin, Y., Pleissner, K.P., Artarini, A., Heuer, D., Becker, D., Khalil, H., Ogilvie, L.A., Hess, S. et al. (2010) Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature, 463, 818-822.
52. Sessions, O.M., Barrows, N.J., Souza-Neto, J.A., Robinson, T.J., Hershey, C.L., Rodgers, M.A., Ramirez, J.L., Dimopoulos, G., Yang, P.L., Pearson, J.L. et al. (2009) Discovery of insect and human dengue virus host factors. Nature, 458, 1047-1050.
53. Gack, M.U., Albrecht, R.A., Urano, T., Inn, K.S., Huang, I.C., Carnero, E., Farzan, M., Inoue, S., Jung, J.U. and Garcia-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.
54. Varga, Z.T., Grant, A., Manicassamy, B. and 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.
55. Bushell, M. and Sarnow, P. (2002) Hijacking the translation apparatus by RNA viruses. J. Cell Biol., 158, 395-399.
56. Garcia-Sastre, A. and Biron, C.A. (2006) Type 1 interferons and the virus-host relationship: a lesson in detente. Science, 312, 879-882.
57. Garcia, M.A., Meurs, E.F. and Esteban, M. (2007) The dsRNA protein kinase PKR: virus and cell control. Biochimie, 89, 799-811.
58. Peters, G.A., Hartmann, R., Qin, J. and Sen, G.C. (2001) Modular structure of PACT: distinct domains for binding and activating PKR. Mol. Cell. Biol., 21, 1908-1920.
59. Williams, B.R.G. (1999) PKR; a sentinel kinase for cellular stress. Oncogene, 18, 6112-6120.
60. Goodman, A.G., Fornek, J.L., Medigeshi, G.R., Perrone, L.A., Peng, X., Dyer, M.D., Proll, S.C., Knoblaugh, S.E., Carter, V.S., Korth, M.J. et al. (2009) P58(IPK): a novel 'CIHD' member of the host innate defense response against pathogenic virus infection. Plos Pathog., 5, e1000438.
61. Clerzius, G., Gelinas, J.F. and Gatignol, A. (2011) Multiple levels of PKR inhibition during HIV-1 replication. Rev.Med. Virol., 21, 42-53.
62. Gale, M. Jr, Blakely, C.M., Kwieciszewski, B., Tan, S.L., Dossett, M., Tang, N.M., Korth, M.J., Polyak, S.J., Gretch, D.R. and Katze, M.G. (1998) Control of PKR protein kinase by hepatitis C virus nonstructural 5A protein: molecular mechanisms of kinase regulation. Mol. Cell. Biol., 18, 5208-5218.
63. Hale, B.G., Randall, R.E., Ortin, J. and Jackson, D. (2008) The multifunctional NS1 protein of influenza A viruses. J. Gen. Virol., 89, 2359-2376.
64. Rajsbaum, R., Albrecht, R.A., Wang, M.K., Maharaj, N.P., Versteeg, G.A., Nistal-Villan, E., Garcia-Sastre, A. and Gack, M.U. (2012) Species-specific inhibition of RIG-I ubiquitination and IFN induction by the influenza A virus NS1 protein. PLoS Pathog., 8, e1003059.
65. Zheng, D.L., Zhang, L., Cheng, N., Xu, X., Deng, Q., Teng, X.M., Wang, K.S., Zhang, X., Huang, J. and Han, Z.G. (2009) Epigenetic modification induced by hepatitis B virus X protein via interaction with de novo DNA methyltransferase DNMT3A. J. Hepatol., 50, 377-387.
66. Li, W., Sun, W., Liu, L., Yang, F., Li, Y.K., Chen, Y.N., Fang, J.L., Zhang, W.J., Wu, J.G. and Zhu, Y. (2010) IL-32: A Host Proinflammatory Factor against Influenza Viral Replication Is Upregulated by Aberrant Epigenetic Modifications during Influenza A Virus Infection. J. Immunol., 185, 5056-5065.
67. Tang, B.K., Zhao, R.H., Sun, Y., Zhu, Y., Zhong, J.A., Zhao, G.P. and Zhu, N.S. (2011) Interleukin-6 expression was regulated by epigenetic mechanisms in response to influenza virus infection or dsRNA treatment. Mol. Immunol., 48, 1001-1008.
68. Amort, M., Nachbauer, B., Tuzlak, S., Kieser, A., Schepers, A., Villunger, A. and Polacek, N. (2015) Expression of the vault RNA protects cells from undergoing apoptosis. Nat. Commun., 6, 7030.