Intracellular warfare between human influenza viruses and human cells: The roles of the viral NS1 protein

Virology

Volumn 309, Issue 2, 2003, Pages 181-189

  Krug, Robert M ^a   Yuan, Weiming ^a   Noah, Diana L ^a   Latham, Anita Ghate ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; DOUBLE STRANDED RNA; GENOMIC RNA; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; MESSENGER RNA; MYXOVIRUS RESISTANCE PROTEIN; PROTEIN; PROTEIN KINASE; PROTEIN KINASE R; PROTEIN NS1; PROTEIN NS1A; PROTEIN NS1B; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

AMINO ACID SEQUENCE; ANTIVIRAL ACTIVITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CHICKEN; COMPLEX FORMATION; CYTOKINE PRODUCTION; DATA BASE; DNA RESPONSIVE ELEMENT; EPIDEMIC; GENETIC TRANSCRIPTION; HONG KONG; HUMAN; INFLUENZA VIRUS; INFLUENZA VIRUS A; INFLUENZA VIRUS B; LUNG ALVEOLUS CELL; LUNG ALVEOLUS EPITHELIUM; MICROBIOLOGICAL EXAMINATION; MOLECULAR WEIGHT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; RNA PROCESSING; RNA SYNTHESIS; RNA TRANSCRIPTION; SHORT SURVEY; VIRUS CELL INTERACTION; VIRUS EXAMINATION; VIRUS INFECTION; VIRUS ISOLATION; VIRUS MUTANT; VIRUS RECOMBINANT; VIRUS REPLICATION; VIRUS TRANSMISSION;

GALLUS GALLUS; INFLUENZA VIRUS; INFLUENZAVIRUS A; INFLUENZAVIRUS B; RNA VIRUSES;

EID: 0037565268     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0042-6822(03)00119-3     Document Type: Short Survey

References (86)

1. Bandyopadhyay S.K., Leonard G.T. Jr., Bandyopadhyay T., Stark G.R., Sen G.C. Transcriptional induction by double-stranded RNA is mediated by interferon- stimulated response elements without activation of interferon-stimulated gene factor 3. J. Biol. Chem. 270:1995;19624-19629.
2. Bergmann M., Garcia-Sastre A., Carnero E., Pehamberger H., Wolff K., Palese P., Muster T. Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J. Virol. 74:2000;6203-6206.
3. Biron C.A., Sen G.C. Interferons and other cytokines. Knipe D.M., Howley P.M. Fields Virology, fourth ed. 2001;321-351 Lippincott Williams & Wilkins, Philadelphia.
4. Boyle K.A., Pietropaolo R.L., Compton T. Engagement of the cellular receptor for glycoprotein B of human cytomegalovirus activates the interferon-responsive pathway. Mol. Cell. Biol. 19:1999;3607-3613.
5. Carritt B., Kok K., van den Berg A., Osinga J., Pilz A., Hofstra R.M., Davis M.B., van der Veen A.Y., Rabbitts P.H., Gulati K. A gene from human chromosome region 3p21 with reduced expression in small cell lung cancer. Cancer Res. 52:1992;1536-1541.
6. Chen C., Krug R.M. Selective nuclear export of viral mRNAs in influenza-virus- infected cells. Trends Microbiol. 8:2000;376-383.
7. Chen Z., Li Y., Krug R.M. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′ end processing machinery. EMBO J. 18:1999;2273-2283.
8. Chien C., Tejero R., Huang Y., Zimmerman D.E., Rios C.B., Krug R.M., Montelione G.T. A novel RNA-binding motif in influenza A virus non-structural protein 1. Nat. Struct. Biol. 4:1997;891-895.
9. Chin K.C., Cresswell P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc. Natl. Acad. Sci. USA. 98:2001;15125-15130.
10. D'Acquisto, F., Ghosh, S. (2001). PACT and PKR: turning on NF-kappaB in the absence of virus. Sci STKE 2001, RE1.
11. Daly C., Reich N.C. Double-stranded RNA activates novel factors that bind to the interferon- stimulated response element. Mol. Cell. Biol. 13:1993;3756-3764.
12. Daly C., Reich N.C. Characterization of specific DNA-binding factors activated by double-stranded RNA as positive regulators of interferon alpha/beta-stimulated genes. J. Biol. Chem. 270:1995;23739-23746.
13. Darnell J.E. Jr., Kerr I.M., Stark G.R. Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science. 264:1994;1415-1421.
14. Der S.D., Zhou A., Williams B.R., Silverman R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. USA. 95:1998;15623-15628.
15. Egorov A., Brandt S., Sereinig S., Romanova J., Ferko B., Katinger D., Grassauer A., Alexandrova G., Katinger H., Muster T. Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J. Virol. 72:1998;6437-6441.
16. Flory E., Kunz M., Scheller C., Jassoy C., Stauber R., Rapp U.R., Ludwig S. Influenza virus-induced NF-kappaB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IkappaB kinase. J. Biol. Chem. 275:2000;8307-8314.
17. Garcia-Sastre A. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology. 279:2001;375-384.
18. Garcia-Sastre A., Egorov A., Matassov D., Brandt S., Levy D.E., Durbin J.E., Palese P., Muster T. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology. 252:1998;324-330.
19. Geiss G.K., An M.C., Bumgarner R.E., Hammersmark E., Cunningham D., Katze M.G. Global impact of influenza virus on cellular pathways is mediated by both replication-dependent and -independent events. J. Virol. 75:2001;4321-4331.
20. Geiss G.K., Salvatore M., Tumpey T.M., Carter V.S., Wang X., Basler C.F., Taubenberger J.K., Bumgarner R.E., Palese P., Katze M.G., Garcia-Sastre A. Cellular transcriptional profiling in influenza A virus-infected lung epithelial cells the role of the nonstructural NS1 protein in the evasion of the host innate defense and its potential contribution to pandemic influenza . Proc. Natl. Acad. Sci. USA. 99:2002;10736-10741.
21. Guo J., Peters K.L., Sen G.C. Induction of the human protein P56 by interferon, double-stranded RNA, or virus infection. Virology. 267:2000;209-219.
22. Hatada E., Saito S., Fukuda R. Mutant influenza viruses with a defective NS1 protein cannot block the activation of PKR in infected cells. J. Virol. 73:1999;2425-2433.
23. Hatada E.R., Fukuda R. Binding of influenza A virus NS1 protein to dsRNA in vitro. J. Gen. Virol. 73:1992;3325-3329.
24. Hiscott J., Kwon H., Genin P. Hostile takeovers viral appropriation of the NF-kappaB pathway . J. Clin. Invest. 107:2001;143-151.
25. Huang Q., Liu do N., Majewski P., Schultele A.C., Korn J.M., Young R.A., Lander E.S., Hacohen N. The plasticity of dendritic cell responses to pathogens and their components. Science. 294:2001;870-875.
26. Issacs A., Lindemann J. Virus interference. 1. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 147:1957;258-267.
27. Ito T., Yang M., May W.S. RAX, a cellular activator for double-stranded RNA-dependent protein kinase during stress signaling. J. Biol. Chem. 274:1999;15427-15432.
28. Iwamura T., Yoneyama M., Yamaguchi K., Suhara W., Mori W., Shiota K., Okabe Y., Namiki H., Fujita T. Induction of IRF-3/-7 kinase and NF-kappaB in response to double-stranded RNA and virus infection common and unique pathways . Genes Cells. 6:2001;375-388.
29. Julkunen I., Sareneva T., Pirhonen J., Ronni T., Melen K., Matikainen S. Molecular pathogenesis of influenza A virus infection and virus-induced regulation of cytokine gene expression. Cytokine Growth Factor Rev. 12:2001;171-180.
30. Katze M.G., Krug R.M. Metabolism and expression of RNA polymerase II transcripts in influenza virus-infected cells. Mol. Cell. Biol. 4:1984;2198-2206.
31. Kim M.-J., Latham A.G., Krug R.M. Human influenza viruses activate an interferon-independent transcription of cellular antiviral genes the outcome with influenza A virus is unique . Proc. Natl. Acad. Sci. USA. 99:2002;10096-10101.
32. Kok K., Hofstra R., Pilz A., van den Berg A., Terpstra P., Buys C.H., Carritt B. A gene in the chromosomal region 3p21 with greatly reduced expression in lung cancer is similar to the gene for ubiquitin-activating enzyme. Proc. Natl. Acad. Sci. USA. 90:1993;6071-6075.
33. Kok K., Van den Berg A., Veldhuis P.M., Franke M., Terpstra P., Buys C.H. The genomic structure of the human UBE1L gene. Gene Expr. 4:1995;163-175.
34. Lamb R.A., Krug R.M. Orthomyxoviridae the viruses and their replication . Knipe D.M., Howley P.M. Fields Virology, fourth ed. 2001;1487-1532 Lippincott Williams & Wilkins, Philadelphia.
35. Li Y., Chen Z.Y., Wang W., Baker C.C., Krug R.M. The 3′-end-processing factor CPSF is required for the splicing of single-intron pre-mRNAs in vivo. RNA. 7:2001;920-931.
36. Li Y., Yamakita Y., Krug R.M. Regulation of a nuclear export signal by an adjacent inhibitory sequence the effector domain of the influenza virus NS1 protein . Proc. Natl. Acad. Sci. USA. 95:1998;4864-4869.
37. Liu J., Lynch P.A., Chien C., Montelione G.T., Krug R.M., Berman H.M. Crystal structure of the unique multifunctional RNA-binding domain of the influenza virus NS1 protein. Nat. Struct. Biol. 4:1997;896-899.
38. Liu L.Q., Ilaria R. Jr., Kingsley P.D., Iwama A., van Etten R.A., Palis J., Zhang D.E. A novel ubiquitin-specific protease, UBP43, cloned from leukemia fusion protein AML1-ETO-expressing mice, functions in hematopoietic cell differentiation. Mol. Cell Biol. 19:1999;3029-3038.
39. Loeb K.R., Haas A.L. The interferon-inducible 15-kDa ubiquitin homolog conjugates to intracellular proteins. J. Biol. Chem. 267:1992;7806-7813.
40. Loeb K.R., Haas A.L. Conjugates of ubiquitin cross-reactive protein distribute in a cytoskeletal pattern. Mol. Cell. Biol. 14:1994;8408-8419.
41. Lu Y., Wambach M., Katze M., Krug R.M. Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase (PKR) that phosphorylates the eIF-2 translation initiation factor. Virology. 214:1995;222-228.
42. Malakhov M.P., Malakhov O.A., Kim K.I., Ritchie K.J., Zhang D.-E. UBP43 (USP18) specifically removes ISG15 from conjugated proteins. J. Biol. Chem. 277:2002;9976-9981.
43. Maniatis T., Falvo J.V., Kim T.H., Kim T.K., Lin C.H., Parekh B.S., Wathelet M.G. Structure and function of the interferon-beta enhanceosome. Cold Spring Harb. Symp. Quant. Biol. 63:1998;609-620.
44. Matikainen S., Pirhonen J., Miettinen M., Lehtonen A., Govenius-Vintola C., Sareneva T., Julkunen I. Influenza A and Sendai viruses induce differential chemokine gene expression and transcription factor activation in human macrophages. Virology. 276:2000;138-147.
45. McCormack S.J., Samuel C.E. Mechanism of interferon action RNA-binding activity of full-length and R-domain forms of the RNA-dependent protein kinase PKR - determination of KD values for VAI and TAR RNAs . Virology. 206:1995;511-519.
46. Navarro L., Mowen K., Rodems S., Weaver B., Reich N., Spector D., David M. Cytomegalovirus activates interferon immediate-early response gene expression and an interferon regulatory factor 3-containing interferon-stimulated response element-binding complex. Mol. Cell. Biol. 18:1998;3796-3802.
47. Nemeroff M., Barabino S.M.L., Keller W., Krug R.M. Influenza virus NS1 protein interacts with the 30kD subunit of cleavage and specificity factor and inhibits 3′ end formation of cellular pre-mRNAs. Mol. Cell. 1:1998;991-1000.
48. Noah D.L., Twu K.Y., Krug R.M. Cellular antiviral responses against influenza A virus are countered at the post-transcriptional level by the viral NS1A protein via its binding to a cellular protein required for the 3′ end processing of cellular pre-mRNAs. Virology. 307:2003;386-395.
49. Ohman M., Kallman A.M., Bass B.L. In vitro analysis of the binding of ADAR2 to the pre-mRNA encoding the GluR-B R/G site. RNA. 6:2000;687-697.
50. Osterhaus A.D., Rimmelzwaan G.F., Martina B.E., Bestebroer T.M., Fouchier R.A. Influenza B virus in seals. Science. 288:2000;1051-1053.
51. Pahl H.L., Baeuerle P.A. Expression of influenza virus hemagglutinin activates transcription factor NF-kappa B. J. Virol. 69:1995;1480-1484.
52. Patel C.V., Handy I., Goldsmith T., Patel R.C. PACT, a stress-modulated cellular activator of interferon-induced double-stranded RNA-activated protein kinase, PKR. J. Biol. Chem. 275:2000;37993-37998.
53. Patel R.C., Sen G.C. PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J. 17:1998;4379-4390.
54. Pavlovic J., Haller O., Staeheli P. Human and mouse Mx proteins inhibit different steps of the influenza virus multiplication cycle. J. Virol. 66:1992;2564-2569.
55. Pavlovic J., Zurcher T., Haller O., Staeheli P. Resistance to influenza virus and vesicular stomatitis virus conferred by expression of human MxA protein. J. Virol. 64:1990;3370-3375.
56. Peters G.A., Hartmann R., Qin J., Sen G.C. Modular structure of PACT distinct domains for binding and activating PKR . Mol. Cell. Biol. 21:2001;1908-1920.
57. Poon L.L., Pritlove D.C., Fodor E., Brownlee G.G. Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. J. Virol. 73:1999;3473-3476.
58. Preston C.M., Harman A.N., Nicholl M.J. Activation of interferon response factor-3 in human cells infected with herpes simplex virus type 1 or human cytomegalovirus. J. Virol. 75:2001;8909-8916.
59. Ramos A., Grunert S., Adams J., Micklem D.R., Proctor M.R., Freund S., Bycroft M., St Johnston D., Varani G. RNA recognition by a Staufen double-stranded RNA- binding domain. EMBO J. 19:2000;997-1009.
60. Robertson J.S., Schubert M., Lazzarini R.A. Polyadenylation sites for influenza virus mRNA. J. Virol. 38:1981;157-163.
61. Ronni T., Matikainen S., Sareneva T., Melen K., Pirhonen J., Keskinen P., Julkunen I. Regulation of IFN-α/β, MxA, 2′-5′-oligoadenylate synthetase, and HLA gene expression in influenza A-infected human lung epithelial cells. J. Immunol. 158:1997;2363-2374.
62. Ryter J.M., Schultz S.C. Molecular basis of double-stranded RNA-protein interactions structure of a dsRNA-binding domain complexed with dsRNA . EMBO J. 17:1998;7505-7513.
63. Safer B. 2B or not 2B regulation of the catalytic utilization of eIF-2 . Cell. 33:1983;7-8.
64. Schmedt C., Green S.R., Manche L., Taylor D.R., Ma Y., Mathews M.B. Functional characterization of the RNA-binding domain and motif of the double-stranded RNA-dependent protein kinase DAI (PKR). J. Mol. Biol. 249:1995;29-44.
65. Seo S.H., Hoffmann E., Webster R.G. Lethal H5N1 influenza viruses escape host anti-viral cytokine responses. Nat. Med. 8:2002;950-954.
66. Shimuzu K., Iguchi A., Gomyou R., Ono Y. Influenza virus inhibits cleavage of the HSP70 pre-mRNAs at the polyadenylation site. Virology. 254:1999;213-219.
67. Simmen K.A., Singh J., Luukkonen B.G., Lopper M., Bittner A., Miller N.E., Jackson M.R., Compton T., Fruh K. Global modulation of cellular transcription by human cytomegalovirus is initiated by viral glycoprotein B. Proc. Natl. Acad. Sci. USA. 98:2001;7140-7145.
68. Stark G.R., Kerr I.M., Williams B.R., Silverman R.H., Schreiber R.D. How cells respond to interferons. Annu. Rev. Biochem. 67:1998;227-264.
69. Staehli P., Haller O. Interferon-induced Mx protein a mediator of cellular resistance to influenza virus . Interferon. 8:1987;1-23.
70. Staehli P., Horisberger M.A., Haller O. Mx-dependent resistance to influenza virus is induced by mouse interferons α and β but not γ Virology. 132:1984;456-461.
71. Talon J., Horvath C.M., Polley R., Basler C.F., Muster T., Palese P., Garcia-Sastre A. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:2000;7989-7996.
72. Tan S.L., Katze M.G. Biochemical and genetic evidence for complex formation between the influenza A virus NS1 protein and the interferon-induced PKR protein kinase. J. Interferon Cytokine Res. 18:1998;757-766.
73. Tian B., Mathews M.B. Functional characterization of and cooperation between the double-stranded RNA-binding motifs of the protein kinase PKR. J. Biol. Chem. 276:2001;9936-9944.
74. Wang W., Krug R.M. The RNA-binding and effector domains are conserved to different extents among influenza A and B viruses. Virology. 223:1996;41-50.
75. Wang W., Riedel K., Lynch K., Chien C., Montelione G.T., Krug R.M. 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. 5:1999;195-205.
76. Wang X., Basler C.F., Williams B.R.G., Silverman R.H., Palese P., Garcia-Sastre A. Functional replacement of the carboxy-terminal two-thirds of the influenza A virus NS1 protein with short heterologous dimerization domains. J. Virol. 76:2002;12951-12962.
77. Wang X., Li M., Zheng H., Muster T., Palese P., Beg A.A., Garcia-Sastre A. Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon. J. Virol. 74:2000;11566-11573.
78. Wathelet M.G., Berr P.M., Huez G.A. Regulation of gene expression by cytokines and virus in human cells lacking the type-I interferon locus. Eur. J. Biochem. 206:1992;901-910.
79. Wathelet M.G., Lin C.H., Parekh B.S., Ronco L.V., Howley P.M., Maniatis T. Virus infection induces the assembly of coordinately activated transcription factors on the IFN-beta enhancer in vivo. Mol. Cell. 1:1998;507-518.
80. Weaver B.K., Kumar K.P., Reich N.C. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell. Biol. 18:1998;1359-13568.
81. Williams, B.R. (2001). Signal integration via PKR. Sci STKE 2001, RE2.
82. Wright P.F., Webster R.G. Orthomyxoviruses. Knipe D.M., Howley P.M. Fields Virology, fourth ed. 2001;1533-1579 Lippincott Williams & Wilkins, Philadelphia.
83. Yoneyama M., Suhara W., Fukuhara Y., Fukuda M., Nishida E., Fujita T. Direct triggering of the type I interferon system by virus infection activation of a transcription factor complex containing IRF-3 and CBP/p300 . EMBO J. 17:1998;1087-1095.
84. Yuan W., Aramini J.M., Montelione G.T., Krug R.M. Structural basis for ubiquitin-like ISG15 protein binding to the NS1 protein of influenza B virus a protein- protein interaction function that is not shared by the corresponding N-terminal domain of the NS1 protein of influenza A virus . Virology. 304:2002;291-301.
85. Yuan W., Krug R.M. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20:2001;362-371.
86. Zhu H., Cong J.P., Shenk T. Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs induction of interferon-responsive RNAs . Proc. Natl. Acad. Sci. USA. 94:1997;13985-13990.