Specific inhibition of the PKR-mediated antiviral response by the murine cytomegalovirus proteins m142 and m143

Journal of Virology

Volumn 83, Issue 3, 2009, Pages 1260-1270

  Budt, Matthias ^a   Niederstadt, Lars ^a   Valchanova, Ralitsa S ^a,c   Jonjić, Stipan ^b   Brune, Wolfram ^a  

^a ROBERT KOCH INSTITUTE   (Germany)

^b UNIVERSITY OF RIJEKA   (Croatia)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOMEGALOVIRUS ANTIGEN M142; CYTOMEGALOVIRUS ANTIGEN M143; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOMEGALOVIRUS; IMMUNOPRECIPITATION; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; VACCINIA VIRUS; VIRUS INHIBITION; VIRUS REPLICATION; VIRUS STRAIN; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DNA, VIRAL; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; MICE; MOLECULAR SEQUENCE DATA; NIH 3T3 CELLS; PHOSPHORYLATION; RNA, DOUBLE-STRANDED; VIRAL PROTEINS;

MAIZE CHLOROTIC MOTTLE VIRUS; MURID HERPESVIRUS 1; SIMPLEXVIRUS; VACCINIA VIRUS;

EID: 59749084920     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01558-08     Document Type: Article

References (67)

1. Adamo, J. E., J. Schroer, and T. Shenk. 2004. Human cytomegalovirus TRS1 protein is required for efficient assembly of DNA-containing capsids. J. Virol. 78:10221-10229.
2. Balachandran, S., E. Thomas, and G. N. Barber. 2004. A FADD-dependent innate immune mechanism in mammalian cells. Nature 432:401-405.
3. Berlanga, J. J., I. Ventoso, H. P. Harding, J. Deng, D. Ron, N. Sonenberg, L. Carrasco, and C. de Haro. 2006. Antiviral effect of the mammalian translation initiation factor 2α kinase GCN2 against RNA viruses. EMBO J. 25: 1730-1740.
4. Brune, W., M. Nevels, and T. Shenk. 2003. Murine cytomegalovirus m41 open reading frame encodes a Golgi-localized antiapoptotic protein. J. Virol. 77:11633-11643.
5. Brune, W., M. Wagner, and M. Messerle. 2006. Manipulating cytomegalovirus genomes by BAC mutagenesis: strategies and applications, p. 61-89. In M. J. Reddehase (ed.), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Wymondham, United Kingdom.
6. Cassady, K. A., and M. Gross. 2002. The herpes simplex virus type 1 U(S)11 protein interacts with protein kinase R in infected cells and requires a 30-amino-acid sequence adjacent to a kinase substrate domain. J. Virol. 76:2029-2035.
7. Chang, H. W., J. C. Watson, and B. L. Jacobs. 1992. The E3L gene of vaccinia virus encodes an inhibitor of the interferon-induced, double-stranded RNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 89:4825-4829.
8. Child, S. J., M. Hakki, K. L. De Niro, and A. P. Geballe. 2004. Evasion of cellular antiviral responses by human cytomegalovirus TRS1 and IRS1. J. Virol. 78:197-205.
9. Child, S. J., L. K. Hanson, C. E. Brown, D. M. Janzen, and A. P. Geballe. 2006. Double-stranded RNA binding by a heterodimeric complex of murine cytomegalovirus m142 and m143 proteins. J. Virol. 80:10173-10180.
10. Clemens, M. J., and A. Elia. 1997. The double-stranded RNA-dependent protein kinase PKR: structure and function. J. Interferon Cytokine Res. 17:503-524.
11. Davies, M. V., H. W. Chang, B. L. Jacobs, and R. J. Kaufman. 1993. The E3L and K3L vaccinia virus gene products stimulate translation through inhibition of the double-stranded RNA-dependent protein kinase by different mechanisms. J. Virol. 67:1688-1692.
12. Deng, J., H. P. Harding, B. Raught, A. C. Gingras, J. J. Berlanga, D. Scheuner, R. J. Kaufman, D. Ron, and N. Sonenberg. 2002. Activation of GCN2 in UV-irradiated cells inhibits translation. Curr. Biol. 12:1279-1286.
13. Desloges, N., M. Rahaus, and M. H. Wolff. 2005. Varicella-zoster virus does not significantly induce cell defence mechanism mediated by the 2-5A/ RNase L pathway during its replication cycle. Med. Microbiol. Immunol. 194:25-31.
14. Floyd-Smith, G., E. Slattery, and P. Lengyel. 1981. Interferon action: RNA cleavage pattern of a (2′-5′)oligoadenylate-dependent endonuclease. Science 212:1030-1032.
15. Garcia, M. A., E. F. Meurs, and M. Esteban. 2007. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89:799-811.
16. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R. A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103:8459-8464.
17. Hakki, M., E. E. Marshall, K. L. De Niro, and A. P. Geballe. 2006. Binding and nuclear relocalization of protein kinase R by human cytomegalovirus TRS1. J. Virol. 80:11817-11826.
18. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271-274.
19. Harvey, D. M., and A. J. Levine. 1991. p53 alteration is a common event in the spontaneous immortalization of primary BALB/c murine embryo fibroblasts. Genes Dev. 5:2375-2385.
20. 134. 5 protein of herpes simplex virus 1 complexes with protein phosphatase 1α to dephosphorylate the α subunit of the eukaryotic translation initiation factor 2 and preclude the shutoff of protein synthesis by double-stranded RNA-activated protein kinase. Proc. Natl. Acad. Sci. USA 94:843-848.
21. Hersh, C. L., R. E. Brown, W. K. Roberts, E. A. Swyryd, I. M. Kerr, and G. R. Stark. 1984. Simian virus 40-infected, interferon-treated cells contain 2′,5′-oligoadenylates which do not activate cleavage of RNA. J. Biol. Chem. 259:1731-1737.
22. Hornung, V., J. Ellegast, S. Kim, K. Brzozka, A. Jung, H. Kato, H. Poeck, S. Akira, K. K. Conzelmann, M. Schlee, S. Endres, and G. Hartmann. 2006. 5′-Triphosphate RNA is the ligand for RIG-I. Science 314:994-997.
23. Hovanessian, A. G., and J. Justesen. 2007. The human 2′-5′oligoadenylate synthetase family: unique interferon-inducible enzymes catalyzing 2′-5′ instead of 3′-5′ phosphodiester bond formation. Biochimie 89:779-788.
24. Jiang, H.-Y., S. A. Wek, B. C. McGrath, D. Lu, T. Hai, H. P. Harding, X. Wang, D. Ron, D. R. Cavener, and R. C. Wek. 2004. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24:1365-1377.
25. Jiang, Z., M. Zamanian-Daryoush, H. Nie, A. M. Silva, B. R. Williams, and X. Li. 2003. Poly(I-C)-induced Toll-like receptor 3 (TLR3)-mediated activation of NFκB and MAP kinase is through an interleukin-1 receptor-associated kinase (IRAK)-independent pathway employing the signaling components TLR3-TRAF6-TAK1-TAB2-PKR. J. Biol. Chem. 278:16713-16719.
26. Jordan, R., L. Wang, T. M. Graczyk, T. M. Block, and P. R. Romano. 2002. Replication of a cytopathic strain of bovine viral diarrhea virus activates PERK and induces endoplasmic reticulum stress-mediated apoptosis of MDBK cells. J. Virol. 76:9588-9599.
27. Jurak, I., and W. Brune. 2006. Induction of apoptosis limits cytomegalovirus cross-species infection. EMBO J. 25:2634-2642.
28. Kato, H., O. Takeuchi, E. Mikamo-Satoh, R. Hirai, T. Kawai, K. Matsushita, A. Hiiragi, T. S. Dermody, T. Fujita, and S. Akira. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205: 1601-1610.
29. Kim, Y. G., M. Muralinath, T. Brandt, M. Pearcy, K. Hauns, K. Lowenhaupt, B. L. Jacobs, and A. Rich. 2003. A role for Z-DNA binding in vaccinia virus pathogenesis. Proc. Natl. Acad. Sci. USA 100:6974-6979.
30. Kostura, M., and M. B. Mathews. 1989. Purification and activation of the double-stranded RNA-dependent eIF-2 kinase DAI. Mol. Cell. Biol. 9:1576-1586.
31. Kuhen, K. L., X. Shen, E. R. Carlisle, A. L. Richardson, H. U. Weier, H. Tanaka, and C. E. Samuel. 1996. Structural organization of the human gene (PKR) encoding an interferon-inducible RNA-dependent protein kinase (PKR) and differences from its mouse homolog. Genomics 36:197-201.
32. Lee, M. S., and Y. J. Kim. 2007. Pattern-recognition receptor signaling initiated from extracellular, membrane, and cytoplasmic space. Mol. Cells 23:1-10.
33. Li, S., J. Y. Min, R. M. Krug, and G. C. Sen. 2006. Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349:13-21.
34. Lu, L., A. P. Han, and J. J. Chen. 2001. Translation initiation control by heme-regulated eukaryotic initiation factor 2α kinase in erythroid cells under cytoplasmic stresses. Mol. Cell. Biol. 21:7971-7980.
35. Lu, Y., M. Wambach, M. G. Katze, and R. M. Krug. 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.
36. Mack, C., A. Sickmann, D. Lembo, and W. Brune. 2008. Inhibition of proinflammatory and innate immune signaling pathways by a cytomegalovirus RIP1-interacting protein. Proc. Natl. Acad. Sci. USA 105:3094-3099.
37. Mahy, B. W. J., and H. O. Kangro. 1996. Virology methods manual. Academic Press, San Diego, CA.
38. Menard, C., M. Wagner, Z. Ruzsics, K. Holak, W. Brune, A. E. Campbell, and U. H. Koszinowski. 2003. Role of murine cytomegalovirus US22 gene family members in replication in macrophages. J. Virol. 77:5557-5570.
39. Meurs, E. F., Y. Watanabe, S. Kadereit, G. N. Barber, M. G. Katze, K. Chong, B. R. Williams, and A. G. Hovanessian. 1992. Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus growth. J. Virol. 66:5805-5814.
40. Meylan, E., K. Burns, K. Hofmann, V. Blancheteau, F. Martinon, M. Kelliher, and J. Tschopp. 2004. RIP1 is an essential mediator of Toll-like receptor 3-induced NF-κB activation. Nat. Immunol. 5:503-507.
41. Michallet, M. C., E. Meylan, M. A. Ermolaeva, J. Vazquez, M. Rebsamen, J. Curran, H. Poeck, M. Bscheider, G. Hartmann, M. Konig, U. Kalinke, M. Pasparakis, and J. Tschopp. 2008. TRADD protein is an essential component of the RIG-like helicase antiviral pathway. Immunity 28:651-661.
42. Mohr, I., and Y. Gluzman. 1996. A herpesvirus genetic element which affects translation in the absence of the viral GADD34 function. EMBO J. 15:4759-4766.
43. Mohr, I. J., T. Pe'ery, and M. B. Mathews. 2007. Protein synthesis and translational control during viral infection, p. 545-599. In M. B. Mathews, N. Sonenberg, and J. W. B. Hershey (ed.), Translational control in biology and medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
44. Mulvey, M., J. Poppers, D. Sternberg, and I. Mohr. 2003. Regulation of eIF2α phosphorylation by different functions that act during discrete phases in the herpes simplex virus type 1 life cycle. J. Virol. 77:10917-10928.
45. Pari, G. S., and D. G. Anders. 1993. Eleven loci encoding trans-acting factors are required for transient complementation of human cytomegalovirus ori-Lyt-dependent DNA replication. J. Virol. 67:6979-6988.
46. Patel, R. C., P. Stanton, N. M. McMillan, B. R. Williams, and G. C. Sen. 1995. The interferon-inducible double-stranded RNA-activated protein kinase self-associates in vitro and in vivo. Proc. Natl. Acad. Sci. USA 92:8283-8287.
47. Pichlmair, A., O. Schulz, C. P. Tan, T. I. Naslund, P. Liljestrom, F. Weber, and C. Reis e Sousa. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314:997-1001.
48. Redwood, A. J., M. Messerle, N. L. Harvey, C. M. Hardy, U. H. Koszinowski, M. A. Lawson, and G. R. Shellam. 2005. Use of a murine cytomegalovirus K181-derived bacterial artificial chromosome as a vaccine vector for immunocontraception. J. Virol. 79:2998-3008.
49. Roberts, W. K., A. Hovanessian, R. E. Brown, M. J. Clemens, and I. M. Kerr. 1976. Interferon-mediated protein kinase and low-molecular-weight inhibitor of protein synthesis. Nature 264:477-480.
50. Sadler, A. J., and B. R. Williams. 2008. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 8:559-568.
51. Saito, T., and M. Gale, Jr. 2007. Principles of intracellular viral recognition. Curr. Opin. Immunol. 19:17-23.
52. Sanchez, R., and I. Mohr. 2007. Inhibition of cellular 2′-5′ oligoadenylate synthetase by the herpes simplex virus type 1 Us11 protein. J. Virol. 81:3455-3464.
53. Schlee, M., W. Barchet, V. Hornung, and G. Hartmann. 2007. Beyond double-stranded RNA-type I IFN induction by 3pRNA and other viral nucleic acids. Curr. Top. Microbiol. Immunol. 316:207-230.
54. Sen, G. C., and S. N. Sarkar. 2007. The interferon-stimulated genes: targets of direct signaling by interferons, double-stranded RNA, and viruses. Curr. Top. Microbiol. Immunol. 316:233-250.
55. Silverman, R. H. 2007. Viral encounters with 2′,5′- oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81:12720-12729.
56. Simon, C. O., C. K. Seckert, N. K. A. Grizmek, and M. J. Reddehase. 2006. Murine model of cytomegalovirus latency and reactivation: the silencing/desilencing and immune sensing hypothesis, p. 483-500. In M. J. Reddehase (ed.), Cytomegaloviruses: molecular biology and immunology. Caister Academic Press, Wymondham, United Kingdom.
57. Sudhakar, A., A. Ramachandran, S. Ghosh, S. E. Hasnain, R. J. Kaufman, and K. V. Ramaiah. 2000. Phosphorylation of serine 51 in initiation factor 2′ (eIF2′) promotes complex formation between eIF2 alpha(P) and eIF2B and causes inhibition in the guanine nucleotide exchange activity of eIF2B. Biochemistry 39:12929-12938.
58. Takeuchi, O., and S. Akira. 2007. Recognition of viruses by innate immunity. Immunol. Rev. 220:214-224.
59. Thomis, D. C., and C. E. Samuel. 1995. Mechanism of interferon action: characterization of the intermolecular autophosphorylation of PKR, the interferon-inducible, RNA-dependent protein kinase. J. Virol. 69:5195-5198.
60. Upton, J. W., W. J. Kaiser, and E. S. Mocarski. 2008. Cytomegalovirus M45 cell death suppression requires receptor-interacting protein (RIP) homotypic interaction motif (RHIM)-dependent interaction with RIP1. J. Biol. Chem. 283:16966-16970.
61. Urano, F., X. Wang, A. Bertolotti, Y. Zhang, P. Chung, H. P. Harding, and D. Ron. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287:664-666.
62. Valchanova, R. S., M. Picard-Maureau, M. Budt, and W. Brune. 2006. Murine cytomegalovirus m142 and m143 are both required to block protein kinase R-mediated shutdown of protein synthesis. J. Virol. 80:10181-10190.
63. Weber, F., V. Wagner, S. B. Rasmussen, R. Hartmann, and S. R. Paludan. 2006. Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J. Virol. 80:5059-5064.
64. Wek, S. A., S. Zhu, and R. C. Wek. 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2α protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15:4497-4506.
65. Wreschner, D. H., J. W. McCauley, J. J. Skehel, and I. M. Kerr. 1981. Interferon action - sequence specificity of the ppp(A2′p)nA- dependent ribonuclease. Nature 289:414-417.
66. Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14: 6095-6106.
67. Zhou, A., J. Paranjape, T. L. Brown, H. Nie, S. Naik, B. Dong, A. Chang, B. Trapp, R. Fairchild, C. Colmenares, and R. H. Silverman. 1997. Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J. 16:6355-6363.