RNA-dependent protein kinase PKR and the Z-DNA binding orthologue PKZ differ in their capacity to mediate initiation factor eIF2α-dependent inhibition of protein synthesis and virus-induced stress granule formation

Virology

Volumn 443, Issue 1, 2013, Pages 48-58

  Taghavi, Nora ^a   Samuel, Charles E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Double stranded RNA; Innate immunity; PKR; PKZ; Protein kinase; Stress granule

Indexed keywords

ARGININE; DNA Z; GLUTAMIC ACID; INITIATION FACTOR 2ALPHA; LYSINE; MUTANT PROTEIN; PROTEIN KINASE; PROTEIN KINASE R; PROTEIN KINASE Z; RNA DEPENDENT PROTEIN KINASE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CATALYSIS; CELL GRANULE; CELL STRESS; CONTROLLED STUDY; ENZYME DEFICIENCY; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; VIRUS CELL INTERACTION;

ANIMALS; CYTOPLASMIC GRANULES; DNA-ACTIVATED PROTEIN KINASE; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMANS; MEASLES VIRUS; PROTEIN BIOSYNTHESIS; VIRUS REPLICATION; ZEBRAFISH;

MAMMALIA;

EID: 84879780909     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.04.020     Document Type: Article

References (67)

1. Ablasser A., Bauernfeind F., Hartmann G., Latz E., Fitzgerald K.A., Hornung V. RIG-I-dependent sensing of poly(dA:dT) through the induction of an RNA polymerase III-transcribed RNA intermediate. Nat. Immunol. 2009, 10:1065-1072.
2. Anderson P., Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 2008, 33:141-150.
3. Balvay L., Soto Rifo R., Ricci E.P., Decimo D., Ohlmann T. Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta 2009, 1789:542-557.
4. Barber G.N. The dsRNA-dependent protein kinase, PKR and cell death. Cell Death Differ. 2005, 12:563-570.
5. Barber G.N., Wambach M., Wong M.L., Dever T.E., Hinnebusch A.G., Katze M.G. Translational regulation by the interferon-induced double-stranded-RNA-activated 68-kDa protein kinase. Proc. Natl. Acad. Sci. USA 1993, 90:4621-4625.
6. Bushell M., Sarnow P. Hijacking the translation apparatus by RNA viruses. J. Cell Biol. 2002, 158:395-399.
7. Chiu Y.H., Macmillan J.B., Chen Z.J. RNA polymerase III detects cytosolic DNA and induces type I interferons through the RIG-I pathway. Cell 2009, 138:576-591.
8. Courtney S.C., Scherbik S.V., Stockman B.M., Brinton M.A. West nile virus infections suppress early viral RNA synthesis and avoid inducing the cell stress granule response. J. Virol. 2012, 86:3647-3657.
9. Dar A.C., Dever T.E., Sicheri F. Higher-order substrate recognition of eIF2α by the RNA-dependent protein kinase PKR. Cell 2005, 122:887-900.
10. Deniz N., Lenarcic E.M., Landry D.M., Thompson S.R. Translation initiation factors are not required for Dicistroviridae IRES function in vivo. RNA 2009, 15:932-946.
11. Devaux P., von Messling V., Songsungthong W., Springfeld C., Cattaneo R. Tyrosine 110 in the measles virus phosphoprotein is required to block STAT1 phosphorylation. Virology 2007, 360:72-83.
12. Fierro-Monti I., Mathews M.B. Proteins binding to duplexed RNA: one motif, multiple functions. Trends Biochem. Sci. 2000, 25:241-246.
13. Garaigorta U., Chisari F.V. Hepatitis C virus blocks interferon effector function by inducing protein kinase R phosphorylation. Cell Host Microbe 2009, 6:513-522.
14. Garaigorta U., Heim M.H., Boyd B., Wieland S., Chisari F.V. Hepatitis C virus (HCV) induces formation of stress granules whose proteins regulate HCV RNA replication and virus assembly and egress. J. Virol. 2012, 86:11043-11056.
15. Garcia M.A., Gil J., Ventoso I., Guerra S., Domingo E., Rivas C., Esteban M. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 2006, 70:1032-1060.
16. Garrey J.L., Lee Y.Y., Au H.H., Bushell M., Jan E. Host and viral translational mechanisms during cricket paralysis virus infection. J. Virol. 2010, 84:1124-1138.
17. He Y., Tan S.L., Tareen S.U., Vijaysri S., Langland J.O., Jacobs B.L., Katze M.G. Regulation of mRNA translation and cellular signaling by hepatitis C virus nonstructural protein NS5A. J. Virol. 2001, 75:5090-5098.
18. Herbert A., Alfken J., Kim Y.G., Mian I.S., Nishikura K., Rich A. A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase. Proc. Natl. Acad. Sci. USA 1997, 94:8421-8426.
19. Herbert A., Schade M., Lowenhaupt K., Alfken J., Schwartz T., Shlyakhtenko L.S., Lyubchenko Y.L., Rich A. The Zalpha domain from human ADAR1 binds to the Z-DNA conformer of many different sequences. Nucleic Acids Res. 1998, 26:3486-3493.
20. Hu C.Y., Zhang Y.B., Huang G.P., Zhang Q.Y., Gui J.F. Molecular cloning and characterisation of a fish PKR-like gene from cultured CAB cells induced by UV-inactivated virus. Fish Shellfish Immunol. 2004, 17:353-366.
21. Jan E., Sarnow P. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol. 2002, 324:889-902.
22. Katze M.G., Wambach M., Wong M.L., Garfinkel M., Meurs E., Chong K., Williams B.R., Hovanessian A.G., Barber G.N. Functional expression and RNA binding analysis of the interferon-induced, double-stranded RNA-activated, 68,000-Mr protein kinase in a cell-free system. Mol. Cell Biol. 1991, 11:5497-5505.
23. Kaufman R.J., Davies M.V., Pathak V.K., Hershey J.W. The phosphorylation state of eucaryotic initiation factor 2 alters translational efficiency of specific mRNAs. Mol. Cell Biol. 1989, 9:946-958.
24. Kieft J.S. Viral IRES RNA structures and ribosome interactions. Trends Biochem. Sci. 2008, 33:274-283.
25. Kim Y.G., Lowenhaupt K., Oh D.B., Kim K.K., Rich A. Evidence that vaccinia virulence factor E3L binds to Z-DNA in vivo: Implications for development of a therapy for poxvirus infection. Proc. Natl. Acad. Sci. USA 2004, 101:1514-1518.
26. Kim Y.G., Muralinath M., Brandt T., Pearcy M., Hauns K., Lowenhaupt K., Jacobs B.L., Rich A. A role for Z-DNA binding in vaccinia virus pathogenesis. Proc. Natl. Acad. Sci. USA 2003, 100:6974-6979.
27. Komar A.A., Hatzoglou M. Internal ribosome entry sites in cellular mRNAs: mystery of their existence. J. Biol. Chem. 2005, 280:23425-23428.
28. Kramer G. Two phosphorylation sites on eIF-2α. FEBS Lett. 1990, 267:181-182.
29. Lindquist M.E., Mainou B.A., Dermody T.S., Crowe J.E. Activation of protein kinase R is required for induction of stress granules by respiratory syncytial virus but dispensable for viral replication. Virology 2011, 413:103-110.
30. Ling J., Morley S.J., Traugh J.A. Inhibition of cap-dependent translation via phosphorylation of eIF4G by protein kinase Pak2. Embo J. 2005, 24:4094-4105.
31. Liu T.K., Zhang Y.B., Liu Y., Sun F., Gui J.F. Cooperative roles of fish protein kinase containing Z-DNA binding domains and double-stranded RNA-dependent protein kinase in interferon-mediated antiviral response. J. Virol 2011, 85:12769-12780.
32. Lushnikov A.Y., Brown B.A., Oussatcheva E.A., Potaman V.N., Sinden R.R., Lyubchenko Y.L. Interaction of the Zalpha domain of human ADAR1 with a negatively supercoiled plasmid visualized by atomic force microscopy. Nucleic Acids Res. 2004, 32:4704-4712.
33. McAllister C.S., Taghavi N., Samuel C.E. Protein kinase PKR amplification of interferon beta induction occurs through initiation factor eIF-2alpha-mediated translational control. J. Biol. Chem 2012, 287:36384-36392.
34. McAllister C.S., Toth A.M., Zhang P., Devaux P., Cattaneo R., Samuel C.E. Mechanisms of protein kinase PKR-mediated amplification of beta interferon induction by C protein-deficient measles virus. J. Virol. 2010, 84:380-386.
35. McCormack S.J., Ortega L.G., Doohan J.P., Samuel C.E. Mechanism of interferon action motif I of the interferon-induced, RNA-dependent protein kinase (PKR) is sufficient to mediate RNA-binding activity. Virology 1994, 198:92-99.
36. McCormack S.J., Thomis D.C., Samuel C.E. Mechanism of interferon action: identification of a RNA binding domain within the N-terminal region of the human RNA-dependent P1/eIF-2 alpha protein kinase. Virology 1992, 188:47-56.
37. McKenna S.A., Lindhout D.A., Kim I., Liu C.W., Gelev V.M., Wagner G., Puglisi J.D. Molecular framework for the activation of RNA-dependent protein kinase. J. Biol. Chem. 2007, 282:11474-11486.
38. Nallagatla S.R., Toroney R., Bevilacqua P.C. Regulation of innate immunity through RNA structure and the protein kinase PKR. Curr. Opin. Struct. Biol. 2011, 21:119-127.
39. Okonski K.M., Samuel C.E. Stress granule formation induced by measles virus is protein kinase PKR dependent and impaired by RNA adenosine deaminase ADAR1. J. Virol. 2013, 87:756-766.
40. Patterson J.B., Thomis D.C., Hans S.L., Samuel C.E. Mechanism of interferon action: double-stranded RNA-specific adenosine deaminase from human cells is inducible by alpha and gamma interferons. Virology 1995, 210:508-511.
41. Pestova T.V., Hellen C.U. Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev. 2003, 17:181-186.
42. Pfaller C.K., Li Z., George C.X., Samuel C.E. Protein kinase PKR and RNA adenosine deaminase ADAR1: new roles for old players as modulators of the interferon response. Curr. Opin. Immunol. 2011, 23:573-582.
43. Pindel A., Sadler A. The role of protein kinase R in the interferon response. J. Interferon Cytokine Res. 2011, 31:59-70.
44. Rothenburg S., Deigendesch N., Dey M., Dever T.E., Tazi L. Double-stranded RNA-activated protein kinase PKR of fishes and amphibians: varying the number of double-stranded RNA binding domains and lineage-specific duplications. BMC Biol. 2008, 6:12.
45. Rothenburg S., Deigendesch N., Dittmar K., Koch-Nolte F., Haag F., Lowenhaupt K., Rich A. A PKR-like eukaryotic initiation factor 2alpha kinase from zebrafish contains Z-DNA binding domains instead of dsRNA binding domains. Proc. Natl. Acad. Sci. USA 2005, 102:1602-1607.
46. Ruggieri A., Dazert E., Metz P., Hofmann S., Bergeest J.P., Mazur J., Bankhead P., Hiet M.S., Kallis S., Alvisi G., Samuel C.E., Lohmann V., Kaderali L., Rohr K., Frese M., Stoecklin G., Bartenschlager R. Dynamic oscillation of translation and stress granule formation mark the cellular response to virus infection. Cell Host Microbe 2012, 12:71-85.
47. Samuel C.E. Mechanism of interferon action. Kinetics of interferon action in mouse L929 cells: phosphorylation of protein synthesis initiation factor elF-2 and ribosome-associated protein P1. Virology 1979, 93:281-285.
48. Samuel C.E. The eIF-2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 1993, 268:7603-7606.
49. Samuel C.E. Antiviral actions of interferons. Clin. Microbiol. Rev. 2001, 14:778-809.
50. Schwartz T., Behlke J., Lowenhaupt K., Heinemann U., Rich A. Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat. Struct. Biol. 2001, 8:761-765.
51. Shi J., Hershey J.W., Nelson M.A. Phosphorylation of the eukaryotic initiation factor 3f by cyclin-dependent kinase 11 during apoptosis. FEBS Lett. 2009, 583:971-977.
52. Smith J.A., Schmechel S.C., Raghavan A., Abelson M., Reilly C., Katze M.G., Kaufman R.J., Bohjanen P.R., Schiff L.A. Reovirus induces and benefits from an integrated cellular stress response. J. Virol. 2006, 80:2019-2033.
53. Sudhakar A., Krishnamoorthy T., Jain A., Chatterjee U., Hasnain S.E., Kaufman R.J., Ramaiah K.V. Serine 48 in initiation factor 2 alpha (eIF2 alpha) is required for high-affinity interaction between eIF2 alpha(P) and eIF2B. Biochemistry 1999, 38:15398-15405.
54. Taghavi N., Samuel C.E. Protein kinase PKR catalytic activity is required for the PKR-dependent activation of mitogen-activated protein kinases and amplification of interferon beta induction following virus infection. Virology 2012, 427:208-216.
55. Takaoka A., Wang Z., Choi M.K., Yanai H., Negishi H., Ban T., Lu Y., Miyagishi M., Kodama T., Honda K., Ohba Y., Taniguchi T. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007, 448:501-505.
56. Thomis D.C., Samuel C.E. Mechanism of interferon action: autoregulation of RNA-dependent P1/eIF-2 alpha protein kinase (PKR) expression in transfected mammalian cells. Proc. Natl. Acad. Sci. USA 1992, 89:10837-10841.
57. Thomis D.C., Samuel C.E. Mechanism of interferon action: evidence for intermolecular autophosphorylation and autoactivation of the interferon-induced, RNA-dependent protein kinase PKR. J. Virol. 1993, 67:7695-7700.
58. Toth A.M., Devaux P., Cattaneo R., Samuel C.E. Protein kinase PKR mediates the apoptosis induction and growth restriction phenotypes of C protein-deficient measles virus. J. Virol. 2009, 83:961-968.
59. Toth A.M., Zhang P., Das S., George C.X., Samuel C.E. Interferon action and the double-stranded RNA-dependent enzymes ADAR1 adenosine deaminase and PKR protein kinase. Prog. Nucleic Acid Res. Mol. Biol. 2006, 81:369-434.
60. Tourriere H., Chebli K., Zekri L., Courselaud B., Blanchard J.M., Bertrand E., Tazi J. The RasGAP-associated endoribonuclease G3BP assembles stress granules. J. Cell Biol. 2003, 160:823-831.
61. Wang Y., Samuel C.E. Adenosine deaminase ADAR1 increases gene expression at the translational level by decreasing protein kinase PKR-dependent eIF-2alpha phosphorylation. J. Mol. Biol. 2009, 393:777-787.
62. Wek R.C., Jiang H.Y., Anthony T.G. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 2006, 34:7-11.
63. White J.P., Lloyd R.E. Regulation of stress granules in virus systems. Trends Microbiol. 2012, 20:175-183.
64. Williams, B.R., 2001. Signal integration via PKR. Sci STKE, 2001, re2.
65. Xu Z., Williams B.R. The B56alpha regulatory subunit of protein phosphatase 2A is a target for regulation by double-stranded RNA-dependent protein kinase PKR. Mol. Cell. Biol. 2000, 20:5285-5299.
66. Zhang P., Langland J.O., Jacobs B.L., Samuel C.E. Protein kinase PKR-dependent activation of mitogen-activated protein kinases occurs through mitochondrial adapter IPS-1 and is antagonized by vaccinia virus E3L. J. Virol. 2009, 83:5718-5725.
67. Zhang P., Samuel C.E. Protein kinase PKR plays a stimulus- and virus-dependent role in apoptotic death and virus multiplication in human cells. J. Virol. 2007, 81:8192-8200.