The Atlantic salmon Z-DNA binding protein kinase phosphorylates translation initiation factor 2 alpha and constitutes a unique orthologue to the mammalian dsRNA-activated protein kinase R

FEBS Journal

Volumn 275, Issue 1, 2008, Pages 184-197

  Bergan, Veronica ^a   Jagus, Rosemary ^b   Lauksund, Silje ^a   Kileng, Øyvind ^a   Robertsen, Børre ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Atlantic salmon; Phosphorylation; Protein kinase; Translation initiation factor 2 alpha; Z DNA binding

Indexed keywords

DNA Z; DOUBLE STRANDED RNA; INITIATION FACTOR 1A; INTERFERON; PROTEIN KINASE;

ARTICLE; ATLANTIC SALMON; ESCHERICHIA COLI; IN VITRO STUDY; KIDNEY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; ORTHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CLONING, MOLECULAR; DNA, COMPLEMENTARY; DNA, Z-FORM; EIF-2 KINASE; EUKARYOTIC INITIATION FACTOR-2; FISH PROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHYLOGENY; SALMO SALAR; SEQUENCE ALIGNMENT; UP-REGULATION;

ESCHERICHIA COLI; MAMMALIA; ONCORHYNCHUS TSHAWYTSCHA; SALMO SALAR; VERTEBRATA;

EID: 37349051331     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2007.06188.x     Document Type: Article

References (64)

1. Wek RC, Jiang HY Anthony TG (2006) Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34, 7 11.
2. Clemens MJ (2005) Translational control in virus-infected cells: models for cellular stress responses. Semin Cell Dev Biol 16, 13 20.
3. Gebauer F Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5, 827 835.
4. Pavitt GD (2005) eIF2B, a mediator of general and gene-specific translational control. Biochem Soc Trans 33, 1487 1492.
5. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C Esteban M (2006) Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol Mol Biol Rev 70, 1032 1060.
6. He B (2006) Viruses, endoplasmic reticulum stress, and interferon responses. Cell Death Differ 13, 393 403.
7. Williams BR (2001) Signal integration via PKR. Sci STKE 2001, RE2.
8. Wang S, Raven JF, Baltzis D, Kazemi S, Brunet DV, Hatzoglou M, Tremblay ML Koromilas AE (2006) The catalytic activity of the eIF2alpha kinase PKR is required to negatively regulate Stat1 and Stat3 via the activation of the tyrosine phosphatase TC-PTP. J Biol Chem 281, 9439 9449.
9. Bonnet MC, Daurat C, Ottone C Meurs EF (2006) The N-terminus of PKR is responsible for the activation of the NF-kappaB signaling pathway by interacting with the IKK complex. Cell Signal 18, 1864 1875.
10. Takizawa T, Tatematsu C Nakanishi Y (2002) Double-stranded RNA-activated protein kinase interacts with apoptosis signal-regulating kinase: 1. Implications for apoptosis signaling pathways. Eur J Biochem 269, 6126 6132.
11. Cuddihy AR, Wong AH, Tam NW, Li S Koromilas AE (1999) The double-stranded RNA activated protein kinase PKR physically associates with the tumor suppressor p53 protein and phosphorylates human p53 on serine 392 in vitro. Oncogene 18, 2690 2702.
12. Dey M, Cao C, Dar AC, Tamura T, Ozato K, Sicheri F Dever TE (2005) Mechanistic link between PKR dimerization, autophosphorylation, and eIF2alpha substrate recognition. Cell 122, 901 913.
13. Lemaire PA, Lary J Cole JL (2005) Mechanism of PKR activation: dimerization and kinase activation in the absence of double-stranded RNA. J Mol Biol 345, 81 90.
14. Fasciano S, Hutchins B, Handy I Patel RC (2005) Identification of the heparin-binding domains of the interferon-induced protein kinase, PKR. FEBS J 272, 1425 1439.
15. Ung TL, Cao C, Lu J, Ozato K Dever TE (2001) Heterologous dimerization domains functionally substitute for the double-stranded RNA binding domains of the kinase PKR. EMBO J 20, 3728 3737.
16. Patel RC Sen GC (1998) PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J 17, 4379 4390.
17. Ito T, Yang M May WS (1999) RAX, a cellular activator for double-stranded RNA-dependent protein kinase during stress signaling. J Biol Chem 274, 15427 15432.
18. Hu CY, Zhang YB, Huang GP, Zhang QY Gui JF (2004) Molecular cloning and characterisation of a fish PKR-like gene from cultured CAB cells induced by UV-inactivated virus. Fish Shellfish Immunol 17, 353 366.
19. Rothenburg S, Deigendesch N, Dittmar K, Koch-Nolte F, Haag F, Lowenhaupt K Rich A (2005) 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 102, 1602 1607.
20. Rich A Zhang S (2003) Timeline: Z-DNA: the long road to biological function. Nat Rev Genet 4, 566 572.
21. Herbert A Rich A (2001) The role of binding domains for dsRNA and Z-DNA in the in vivo editing of minimal substrates by ADAR1. Proc Natl Acad Sci USA 98, 12132 12137.
22. Brown BA II., Lowenhaupt K, Wilbert CM, Hanlon EB Rich A (2000) The zalpha domain of the editing enzyme dsRNA adenosine deaminase binds left-handed Z-RNA as well as Z-DNA. Proc Natl Acad Sci USA 97, 13532 13536.
23. Ha SC, Van Quyen D, Hwang HY, Oh DB, Brown BA II., Lee SM, Park HJ, Ahn JH, Kim KK Kim YG (2006) Biochemical characterization and preliminary X-ray crystallographic study of the domains of human ZBP1 bound to left-handed Z-DNA. Biochim Biophys Acta 1764, 320 323.
24. Schwartz T, Behlke J, Lowenhaupt K, Heinemann U Rich A (2001) Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat Struct Biol 8, 761 765.
25. Takaoka A, Wang Z, Choi MK, Yanai H, Negishi H, Ban T, Lu Y, Miyagishi M, Kodama T, Honda K et al. (2007) DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 448, 501 505.
26. Kim YG, Muralinath M, Brandt T, Pearcy M, Hauns K, Lowenhaupt K, Jacobs BL Rich A (2003) A role for Z-DNA binding in vaccinia virus pathogenesis. Proc Natl Acad Sci USA 100, 6974 6979.
27. Herbert A Rich A (1999) Left-handed Z-DNA: structure and function. Genetica 106, 37 47.
28. Liu LF Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84, 7024 7027.
29. Robertsen B, Bergan V, Rokenes T, Larsen R Albuquerque A (2003) Atlantic salmon interferon genes: cloning, sequence analysis, expression, and biological activity. J Interferon Cytokine Res 23, 601 612.
30. Wergeland HI Jakobsen RA (2001) A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV). Dis Aquat Organ 44, 183 190.
31. Craig AW, Cosentino GP, Donze O Sonenberg N (1996) The kinase insert domain of interferon-induced protein kinase PKR is required for activity but not for interaction with the pseudosubstrate K3L. J Biol Chem 271, 24526 24533.
32. Romano PR, Garcia-Barrio MT, Zhang X, Wang Q, Taylor DR, Zhang F, Herring C, Mathews MB, Qin J Hinnebusch AG (1998) Autophosphorylation in the activation loop is required for full kinase activity in vivo of human and yeast eukaryotic initiation factor 2alpha kinases PKR and GCN2. Mol Cell Biol 18, 2282 2297.
33. Tamura K, Dudley J, Nei M Kumar S (2007) Mega4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596 1599.
34. Eck RV Dayhoff MO (1966) Atlas of Protein Sequence and Structure. National Biomedical Research Foundation, Silver Springs, MD.
35. Saitou N Nei M (1987) The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406 425.
36. Rzhetsky A Nei M (1992) Statistical properties of the ordinary least-squares, generalized least-squares, and minimum-evolution methods of phylogenetic inference. J Mol Evol 35, 367 375.
37. Hovanessian AG (1989) The double stranded RNA-activated protein kinase induced by interferon: dsRNA-PK. J Interferon Res 9, 641 647.
38. Barber GN, Tomita J, Hovanessian AG, Meurs E Katze MG (1991) Functional expression and characterization of the interferon-induced double-stranded RNA activated P68 protein kinase from Escherichia coli. Biochemistry 30, 10356 10361.
39. Jammi NV Beal PA (2001) Phosphorylation of the RNA-dependent protein kinase regulates its RNA-binding activity. Nucleic Acids Res 29, 3020 3029.
40. Taylor DR, Lee SB, Romano PR, Marshak DR, Hinnebusch AG, Esteban M Mathews MB (1996) Autophosphorylation sites participate in the activation of the double-stranded-RNA-activated protein kinase PKR. Mol Cell Biol 16, 6295 6302.
41. Price NT Proud CG (1990) Phosphorylation of protein synthesis initiation factor: 2. Identification of the site in the alpha-subunit phosphorylated in reticulocyte lysates. Biochim Biophys Acta 1054, 83 88.
42. Jagus R Gray MM (1994) Proteins that interact with PKR. Biochimie 76, 779 791.
43. Chong KL, Feng L, Schappert K, Meurs E, Donahue TF, Friesen JD, Hovanessian AG Williams BR (1992) Human p68 kinase exhibits growth suppression in yeast and homology to the translational regulator GCN2. EMBO J 11, 1553 1562.
44. Barber GN, Tomita J, Garfinkel MS, Meurs E, Hovanessian A Katze MG (1992) Detection of protein kinase homologues and viral RNA-binding domains utilizing polyclonal antiserum prepared against a baculovirus-expressed ds RNA-activated 68,000-Da protein kinase. Virology 191, 670 679.
45. Cai R Williams BR (1998) Mutations in the double-stranded RNA-activated protein kinase insert region that uncouple catalysis from eIF2alpha binding. J Biol Chem 273, 11274 11280.
46. Zhang F, Romano PR, Nagamura-Inoue T, Tian B, Dever TE, Mathews MB, Ozato K Hinnebusch AG (2001) Binding of double-stranded RNA to protein kinase PKR is required for dimerization and promotes critical autophosphorylation events in the activation loop. J Biol Chem 276, 24946 24958.
47. Deigendesch N, Koch-Nolte F Rothenburg S (2006) ZBP1 subcellular localization and association with stress granules is controlled by its Z-DNA binding domains. Nucleic Acids Res 34, 5007 5020.
48. Kedersha NL, Gupta M, Li W, Miller I Anderson P (1999) RNA-binding proteins TIA-1 and TIAR link the phosphorylation of eIF-2 alpha to the assembly of mammalian stress granules. J Cell Biol 147, 1431 1442.
49. Anderson P Kedersha N (2002) Visibly stressed: the role of eIF2, TIA-1, and stress granules in protein translation. Cell Stress Chaperones 7, 213 221.
50. Anderson P Kedersha N (2006) RNA granules. J Cell Biol 172, 803 808.
51. Mazroui R, Sukarieh R, Bordeleau ME, Kaufman RJ, Northcote P, Tanaka J, Gallouzi I Pelletier J (2006) Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2alpha phosphorylation. Mol Biol Cell 17, 4212 4219.
52. Gracey AY, Fraser EJ, Li W, Fang Y, Taylor RR, Rogers J, Brass A Cossins AR (2004) Coping with cold: an integrative, multitissue analysis of the transcriptome of a poikilothermic vertebrate. Proc Natl Acad Sci USA 101, 16970 16975.
53. Thomis DC Samuel CE (1992) 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 89, 10837 10841.
54. Dever TE, Chen JJ, Barber GN, Cigan AM, Feng L, Donahue TF, London IM, Katze MG Hinnebusch AG (1993) Mammalian eukaryotic initiation factor 2 alpha kinases functionally substitute for GCN2 protein kinase in the GCN4 translational control mechanism of yeast. Proc Natl Acad Sci USA 90, 4616 4620.
55. Gessner RV, Quigley GJ, Wang AH, van der Marel GA, van Boom JH Rich A (1985) Structural basis for stabilization of Z-DNA by cobalt hexaammine and magnesium cations. Biochemistry 24, 237 240.
56. Bauer C Wang AH (1997) Bridged cobalt amine complexes induce DNA conformational changes effectively. J Inorg Biochem 68, 129 135.
57. Lamark T, Perander M, Outzen H, Kristiansen K, Overvatn A, Michaelsen E, Bjorkoy G Johansen T (2003) Interaction codes within the family of mammalian Phox and Bem1p domain-containing proteins. J Biol Chem 278, 34568 34581.
58. Kimball SR, Antonetti DA, Brawley RM Jefferson LS (1991) Mechanism of inhibition of peptide chain initiation by amino acid deprivation in perfused rat liver. Regulation involving inhibition of eukaryotic initiation factor 2 alpha phosphatase activity. J Biol Chem 266, 1969 1976.
59. Kimball SR, Horetsky RL, Jagus R Jefferson LS (1998) Expression and purification of the alpha-subunit of eukaryotic initiation factor eIF2: use as a kinase substrate. Protein Expr Purif 12, 415 419.
60. Carroll K, Elroy-Stein O, Moss B Jagus R (1993) Recombinant vaccinia virus K3L gene product prevents activation of double-stranded RNA-dependent, initiation factor 2 alpha-specific protein kinase. J Biol Chem 268, 12837 12842.
61. Kim YG, Lowenhaupt K, Oh DB, Kim KK Rich A (2004) 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 101, 1514 1518.
62. Hanks SK Hunter T (1995) Protein kinases: 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9, 576 596.
63. Felsenstein J (1985) Confidence limits on phylogenetics: an approach using the bootstrap. Evolution 96, 783 791.
64. Nei M Kumar S (2000) Molecular Evolution and Pholygenetics. Oxford University Press, New York, NY.