Home LiteratureArticle Details
PMID: 20713064 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Magnesium-dependent interaction of PKR with adenovirus VAI.

Journal of molecular biology ·Vol. 402 ·No. 4 ·2010-10-01 ·Pages 638-44

Launer-Felty K, Wong CJ, Wahid AM, Conn GL, Cole JL

Abstract

Protein kinase R (PKR) is an interferon-induced kinase that plays a pivotal role in the innate immunity pathway for defense against viral infection. PKR is activated to undergo autophosphorylation upon binding to RNAs that contain duplex regions. Activated PKR phosphorylates the α-subunit of eukaryotic initiation factor 2, thereby inhibiting protein synthesis in virus-infected cells. Viruses have evolved diverse PKR-inhibitory strategies to evade the antiviral response. Adenovirus encodes virus-associated RNA I (VAI), a highly structured RNA inhibitor that binds PKR but fails to activate. We have characterized the stoichiometry and affinity of PKR binding to define the mechanism of PKR inhibition by VAI. Sedimentation velocity and isothermal titration calorimetry measurements indicate that PKR interactions with VAI are modulated by Mg(2+). Two PKR monomers bind in the absence of Mg(2+), but a single monomer binds in the presence of divalent ion. Known RNA activators of PKR are capable of binding multiple PKR monomers to allow the kinase domains to come into close proximity and thus enhance dimerization. We propose that VAI acts as an inhibitor of PKR because it binds and sequesters a single PKR in the presence of divalent cation.

MeSH Terms
Adenoviridae/immunology,pathogenicity Animals Host-Pathogen Interactions/immunology Humans Immunity, Innate Magnesium Protein Binding Protein Multimerization RNA, Viral/chemistry,metabolism,pharmacology eIF-2 Kinase/antagonists & inhibitors,chemistry,metabolism
Chemicals
RNA, Viral adenovirus associated RNA eIF-2 Kinase Magnesium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Launer-Felty Katherine
Department of Molecular and Cell Biology, University of Connecticut, Storrs, CT 06269, USA.
Wong C Jason
Wahid Ahmed M
Conn Graeme L
Cole James L
References (35)
35 references, click to expand
  1. Viral dsRNA inhibitors prevent self-association and autophosphorylation of PKR.
    J Mol Biol. 2007 Sep 7;372(1):103-13 PMID: 17619024
  2. Functional dissection of adenovirus VAI RNA.
    J Virol. 1989 Aug;63(8):3423-34 PMID: 2746735
  3. Interactions between double-stranded RNA regulators and the protein kinase DAI.
    Mol Cell Biol. 1992 Nov;12(11):5238-48 PMID: 1357546
  4. RNA dimerization promotes PKR dimerization and activation.
    J Mol Biol. 2009 Jul 10;390(2):319-38 PMID: 19445956
  5. Mutational analysis of the central domain of adenovirus virus-associated RNA mandates a revision of the proposed secondary structure.
    J Virol. 1993 Jun;67(6):3534-43 PMID: 8098780
  6. Concentration, compartmentation and metabolic function of intracellular free Mg2+.
    Magnes Res. 2006 Dec;19(4):225-36 PMID: 17402290
  7. Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR.
    Cell. 2005 Sep 23;122(6):887-900 PMID: 16179258
  8. The characteristics of inhibition of protein synthesis by double-stranded ribonucleic acid in reticulocyte lysates.
    J Biol Chem. 1975 Jan 25;250(2):409-17 PMID: 803491
  9. Activation of PKR: an open and shut case?
    Trends Biochem Sci. 2007 Feb;32(2):57-62 PMID: 17196820
  10. Structure of the double-stranded RNA-binding domain of the protein kinase PKR reveals the molecular basis of its dsRNA-mediated activation.
    EMBO J. 1998 Sep 15;17(18):5458-65 PMID: 9736623
  11. In vitro analysis of virus-associated RNA I (VAI RNA): inhibition of the double-stranded RNA-activated protein kinase PKR by VAI RNA mutants correlates with the in vivo phenotype and the structural integrity of the central domain.
    J Virol. 1994 Jul;68(7):4137-51 PMID: 7911532
  12. 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. 2006 May;80(10):5059-64 PMID: 16641297
  13. Viral evasion and subversion of pattern-recognition receptor signalling.
    Nat Rev Immunol. 2008 Dec;8(12):911-22 PMID: 18989317
  14. The double-stranded-RNA-binding motif: interference and much more.
    Nat Rev Mol Cell Biol. 2004 Dec;5(12):1013-23 PMID: 15573138
  15. Structural features of adenovirus 2 virus-associated RNA required for binding to the protein kinase DAI.
    Nucleic Acids Res. 1994 Oct 25;22(21):4364-74 PMID: 7971266
  16. Effect of single-base substitutions in the central domain of virus-associated RNA I on its function.
    J Virol. 1995 Jul;69(7):4299-307 PMID: 7769691
  17. Mechanism of PKR activation: dimerization and kinase activation in the absence of double-stranded RNA.
    J Mol Biol. 2005 Jan 7;345(1):81-90 PMID: 15567412
  18. 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. 1995 Mar;1(1):7-20 PMID: 7489491
  19. Secondary and tertiary structure in the central domain of adenovirus type 2 VA RNA I.
    RNA. 1996 Sep;2(9):937-51 PMID: 8809020
  20. Purification and activation of the double-stranded RNA-dependent eIF-2 kinase DAI.
    Mol Cell Biol. 1989 Apr;9(4):1576-86 PMID: 2725516
  21. 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 PMID: 16891177
  22. Uncoupling of RNA binding and PKR kinase activation by viral inhibitor RNAs.
    J Mol Biol. 2006 May 19;358(5):1270-85 PMID: 16580685
  23. Effects of mutations in stem and loop regions on the structure and function of adenovirus VA RNAI.
    EMBO J. 1988 Sep;7(9):2849-59 PMID: 3181142
  24. Analysis of adenovirus VA RNAI structure and stability using compensatory base pair modifications.
    Nucleic Acids Res. 2008 Mar;36(5):1645-53 PMID: 18250084
  25. Selective binding by the RNA binding domain of PKR revealed by affinity cleavage.
    Biochemistry. 2001 Apr 10;40(14):4272-80 PMID: 11284683
  26. Inhibition of PKR by RNA and DNA viruses.
    Virus Res. 2006 Jul;119(1):100-10 PMID: 16704884
  27. Analysis of PKR structure by small-angle scattering.
    J Mol Biol. 2009 Apr 10;387(4):910-20 PMID: 19232355
  28. The regulation of the protein kinase PKR by RNA.
    Biochimie. 1996;78(11-12):909-14 PMID: 9150867
  29. Analysis of heterologous interacting systems by sedimentation velocity: curve fitting algorithms for estimation of sedimentation coefficients, equilibrium and kinetic constants.
    Biophys Chem. 2004 Mar 1;108(1-3):231-43 PMID: 15043932
  30. Role of the apical stem in maintaining the structure and function of adenovirus virus-associated RNA.
    J Virol. 1992 Apr;66(4):2369-77 PMID: 1548768
  31. Systematic deletion of the adenovirus-associated RNAI terminal stem reveals a surprisingly active RNA inhibitor of double-stranded RNA-activated protein kinase.
    J Biol Chem. 2008 Jun 20;283(25):17485-93 PMID: 18430723
  32. Improved methods for fitting sedimentation coefficient distributions derived by time-derivative techniques.
    Anal Biochem. 2006 Jul 15;354(2):238-46 PMID: 16730633
  33. Interaction of adenovirus VA RNAl with the protein kinase DAI: nonequivalence of binding and function.
    Cell. 1990 Jun 1;61(5):843-52 PMID: 2188737
  34. Mechanism of PKR Activation by dsRNA.
    J Mol Biol. 2008 Aug 29;381(2):351-60 PMID: 18599071
  35. Minor-groove recognition of double-stranded RNA by the double-stranded RNA-binding domain from the RNA-activated protein kinase PKR.
    Biochemistry. 1996 Aug 6;35(31):9983-94 PMID: 8756460
Article Info
Journal
Journal of molecular biology
Abbr.
J Mol Biol
ISSN
1089-8638
Published
2010-10-01
Epub
2010-00-14
Pages
638-44
Language
English
Region
England
NLM ID
2985088R
PMCID
PMC2980848
Subset
IM
Grants
NIAID NIH HHS · R01 AI053615 · United States
NIAID NIH HHS · R01 AI053615-07 · United States
NIAID NIH HHS · AI-53615 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com