Baculovirus protein PK2 subverts eIF2α kinase function by mimicry of its kinase domain C-lobe

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 32, 2015, Pages E4364-E4373

  Li, John J ^a,b   Cao, Chune ^c   Fixsen, Sarah M ^d   Young, Janet M ^e   Ono, Chikako ^f,h   Bando, Hisanori ^f   Elde, Nels C ^d   Katsuma, Susumu ^g   Dever, Thomas E ^c   Sicheri, Frank ^a,b   Shokat, Kevan M ⁱ  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^e Fred Hutchinson Cancer Research Center   (United States)

^f HOKKAIDO UNIVERSITY   (Japan)

^g UNIVERSITY OF TOKYO   (Japan)

^h OSAKA UNIVERSITY   (Japan)

ⁱ UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

EIF2 kinase inhibition; HRI; Lobe swap; PKR; Viral mimicry

Indexed keywords

PROTEIN KINASE R; PROTEIN PK2; UNCLASSIFIED DRUG; VIRUS PROTEIN; BACULOVIRUS PK2; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME PHOSPHORYLATION; HORIZONTAL GENE TRANSFER; MOLECULAR MIMICRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; VIRUS GENOME; ANIMAL; BACULOVIRIDAE; BOMBYX; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; VIROLOGY;

EUKARYOTA; HEXAPODA;

ANIMALS; BACULOVIRIDAE; BOMBYX; CELL LINE; DNA MUTATIONAL ANALYSIS; EIF-2 KINASE; MODELS, MOLECULAR; MOLECULAR MIMICRY; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS;

EID: 84938930755     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1505481112     Document Type: Article

References (35)

1. Dever TE, Dar AC, Sicheri D (2009) The eIF2a Kinases. Translational Control in Biology and Medicine (Cold Spring Harbor Lab Press, Cold Spring Harbor,NY), pp 319-344.
2. Pavitt GD, Ron D (2012) New insights into translational regulation in the endoplasmic reticulum unfolded protein response. Cold Spring Harb Perspect Biol 4(6).
3. Kozak CA, Villar CJ, Voytek P (1989) Genetic aspects of oncogenesis by murine leukemia viruses in wild mice. Crit Rev Oncog 1(2): 127-144.
4. Dever TE (2002) Gene-specific regulation by general translation factors. Cell 108(4): 545-556.
5. 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(14): 3728-3737.
6. Dar AC, Sicheri F (2002) X-ray crystal structure and functional analysis of vaccinia virus K3L reveals molecular determinants for PKR subversion and substrate recognition. Mol Cell 10(2): 295-305.
7. Dey M, et al. (2005) Mechanistic link between PKR dimerization, autophosphorylation, and eIF2alpha substrate recognition. Cell 122(6): 901-913.
8. Taylor SS, Haste NM, Ghosh G (2005) PKR and eIF2alpha: Integration of kinase dimerization, activation, and substrate docking. Cell 122(6): 823-825.
9. García MA, Meurs EF, Esteban M (2007) The dsRNA protein kinase PKR: Virus and cell control. Biochimie 89(6-7): 799-811.
10. Kawagishi-Kobayashi M, Silverman JB, Ung TL, Dever TE (1997) Regulation of the protein kinase PKR by the vaccinia virus pseudosubstrate inhibitor K3L is dependent on residues conserved between the K3L protein and the PKR substrate eIF2alpha. Mol Cell Biol 17(7): 4146-4158.
11. Kawagishi-Kobayashi M, Cao C, Lu J, Ozato K, Dever TE (2000) Pseudosubstrate inhibition of protein kinase PKR by swine pox virus C8L gene product. Virology 276(2): 424-434.
12. Seo EJ, et al. (2008) Protein kinase PKR mutants resistant to the poxvirus pseudosubstrate K3L protein. Proc Natl Acad Sci USA 105(44): 16894-16899.
13. Chang HW, Jacobs BL (1993) Identification of a conserved motif that is necessary for binding of the vaccinia virus E3L gene products to double-stranded RNA. Virology 194(2): 537-547.
14. Ho CK, Shuman S (1996) Mutational analysis of the vaccinia virus E3 protein defines amino acid residues involved in E3 binding to double-stranded RNA. J Virol 70(4): 2611-2614.
15. Romano PR, et al. (1998) Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: Role of complex formation and the E3 N-terminal domain. Mol Cell Biol 18(12): 7304-7316.
16. Clarke PA, Mathews MB (1995) Interactions between the double-stranded RNA binding motif and RNA: Definition of the binding site for the interferon-induced protein kinase DAI (PKR) on adenovirus VA RNA. RNA 1(1): 7-20.
17. Wahid AM, Coventry VK, Conn GL (2008) Systematic deletion of the adenovirusassociated RNAI terminal stem reveals a surprisingly active RNA inhibitor of doublestranded RNA-activated protein kinase. J Biol Chem 283(25): 17485-17493.
18. Dzananovic E, et al. (2014) Solution conformation of adenovirus virus associated RNAI and its interaction with PKR. J Struct Biol 185(1): 48-57.
19. Li Y, Miller LK (1995) Expression and functional analysis of a baculovirus gene encoding a truncated protein kinase homolog. Virology 206(1): 314-323.
20. Dever TE, et al. (1998) Disruption of cellular translational control by a viral truncated eukaryotic translation initiation factor 2alpha kinase homolog. Proc Natl Acad Sci USA 95(8): 4164-4169.
21. Dar AC, Dever TE, Sicheri F (2005) Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell 122(6): 887-900.
22. Elde NC, Child SJ, Geballe AP, Malik HS (2009) Protein kinase R reveals an evolutionary model for defeating viral mimicry. Nature 457(7228): 485-489.
23. Elde NC, Malik HS (2009) The evolutionary conundrum of pathogen mimicry. Nat Rev Microbiol 7(11): 787-797.
24. Rothenburg S, Seo EJ, Gibbs JS, Dever TE, Dittmar K (2009) Rapid evolution of protein kinase PKR alters sensitivity to viral inhibitors. Nat Struct Mol Biol 16(1): 63-70.
25. Dauber B, Wolff T (2009) Activation of the Antiviral Kinase PKR and Viral Countermeasures. Viruses 1(3): 523-544.
26. Chen JJ (2007) Regulation of protein synthesis by the heme-regulated eIF2alpha kinase: Relevance to anemias. Blood 109(7): 2693-2699.
27. Igarashi J, et al. (2008) Elucidation of the heme binding site of heme-regulated eukaryotic initiation factor 2alpha kinase and the role of the regulatory motif in heme sensing by spectroscopic and catalytic studies of mutant proteins. J Biol Chem 283(27): 18782-18791.
28. Zeth K, et al. (2011) Molecular basis of actin nucleation factor cooperativity: Crystal structure of the Spir-1 kinase non-catalytic C-lobe domain (KIND)-formin-2 formin SPIR interaction motif (FSI) complex. J Biol Chem 286(35): 30732-30739.
29. Vizcarra CLKB, et al. (2011) Structure and function of the interacting domains of Spire and Fmn-family formins. Proc Natl Acad Sci USA 108(29): 11884-11889.
30. Aarti I, Rajesh K, Ramaiah KV (2010) Phosphorylation of eIF2 alpha in Sf9 cells: A stress, survival and suicidal signal. Apoptosis 15(6): 679-692.
31. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75(4): 805-816.
32. Reid GA, Schatz G (1982) Import of proteins into mitochondria. Yeast cells grown in the presence of carbonyl cyanidem-chlorophenylhydrazone accumulate massive amounts of some mitochondrial precursor polypeptides. J Biol Chem 257(21): 13056-13061.
33. Katsuma S, et al. (2012) The baculovirus uses a captured host phosphatase to induce enhanced locomotory activity in host caterpillars. PLoS Pathog 8(4): E1002644.
34. Ono C, et al. (2012) Phenotypic grouping of 141 BmNPVs lacking viral gene sequences. Virus Res 165(2): 197-206.
35. Katsuma S, et al. (2012) Baculovirus-encoded protein BV/ODV-E26 determines tissue tropism and virulence in lepidopteran insects. J Virol 86(5): 2545-2555.