Distinct Z-DNA binding mode of a PKR-like protein kinase containing a Z-DNA binding domain (PKZ)

Nucleic Acids Research

Volumn 42, Issue 9, 2014, Pages 5937-5948

  Kim, Doyoun ^a   Hur, Jeonghwan ^a   Park, Kwangsoo ^a   Bae, Sangsu ^b   Shin, Donghyuk ^c   Ha, Sung Chul ^d   Hwang, Hye Yeon ^a   Hohng, Sungchul ^b   Lee, Joon Hwa ^e   Lee, Sangho ^c   Kim, Yang Gyun ^c   Kim, Kyeong Kyu ^a  

^a Sungkyunkwan University School of Medicine   (South Korea)

^b Seoul National University   (South Korea)

^c Sungkyunkwan University   (South Korea)

^d Pohang University of Science and Technology (POSTECH)   (South Korea)

^e Gyeongsang National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RIBONUCLEIC ACID ACTIVATED PROTEIN KINASE LIKE PROTEIN KINASE; PHOSPHATE; PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; CIRCULAR DICHROISM; CRYSTAL STRUCTURE; DNA BINDING; GOLDFISH; INNATE IMMUNITY; MUTAGENESIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; Z DNA BINDING DOMAIN;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA, Z-FORM; EIF-2 KINASE; FISH PROTEINS; GOLDFISH; HYDROGEN BONDING; KINETICS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; SODIUM CHLORIDE;

EID: 84901356184     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku189     Document Type: Article

References (51)

1. Holcik, M. and Sonenberg, N. (2005) Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol., 6, 318-327
2. Samuel, C.E. (1993) The eIF-2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem., 268, 7603-7606
3. Wek, R.C., Jiang, H.Y. and Anthony, T.G. (2006) Coping with stress: EIF2 kinases and translational control. Biochem. Soc. Trans., 34, 7-11
4. Williams, B.R. (1999) PKR: A sentinel kinase for cellular stress. Oncogene, 18, 6112-6120
5. Wu, S. and Kaufman, R.J. (1997) A model for the double-stranded RNA (dsRNA)-dependent dimerization and activation of the dsRNA-Activated protein kinase PKR. J. Biol. Chem., 272, 1291-1296
6. Tan, S.L., Gale, M.J. Jr and Katze, M.G. (1998) Double-stranded RNA-independent dimerization of interferon-induced protein kinase PKR and inhibition of dimerization by the cellular P58IPK inhibitor. Mol. Cell. Biol., 18, 2431-2443
7. Su, J., Zhu, Z. andWang, Y. (2008) Molecular cloning, characterization and expression analysis of the PKZ gene in rare minnow Gobiocypris rarus. Fish Shellfish Immunol., 25, 106-113
8. Bergan, V., Jagus, R., Lauksund, S., Kileng, O. and Robertsen, B. (2008) 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 J., 275, 184-197. (Pubitemid 350294074
9. Rothenburg, S., Deigendesch, N., Dittmar, K., Koch-Nolte, F., Haag, F., Lowenhaupt, K. and 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. U.S.A., 102, 1602-1607
10. Hu, C.Y., Zhang, Y.B., Huang, G.P., Zhang, Q.Y. and Gui, J.F. (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
11. Rich, A. (1993) DNA comes in many forms. Gene, 135, 99-109
12. Johnston, B.H. (1992) Generation and detection of Z-DNA. Methods Enzymol., 211, 127-158
13. Rich, A. and Zhang, S. (2003) Timeline: Z-DNA: The long road to biological function. Nat. Rev. Genet., 4, 566-572
14. Behe, M. and Felsenfeld, G. (1981) Effects of methylation on a synthetic polynucleotide: The B-Z transition in poly(dG-m5dC).poly(dG-m5dC). Proc. Natl. Acad. Sci. U.S.A., 78, 1619-1623
15. Mamajanov, I., Engelhart, A.E., Bean, H.D. and Hud, N.V. (2010) DNA and RNA in anhydrous media: Duplex, triplex, and G-quadruplex secondary structures in a deep eutectic solvent. Angew. Chem. Int. Ed. Engl., 49, 6310-6314
16. Rahmouni, A.R. and Wells, R.D. (1989) Stabilization of Z DNA in vivo by localized supercoiling. Science, 246, 358-363
17. Kim, D., Lee, Y.H., Hwang, H.Y., Kim, K.K. and Park, H.J. (2010) Z-DNA binding proteins as targets for structure-based virtual screening. Curr. Drug Targets, 11, 335-344
18. Herbert, A., Lowenhaupt, K., Spitzner, J. and Rich, A. (1995) Chicken double-stranded RNA adenosine deaminase has apparent specificity for Z-DNA. Proc. Natl. Acad. Sci. U.S.A., 92, 7550-7554
19. Schwartz, T., Behlke, J., Lowenhaupt, K., Heinemann, U. and 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
20. Kim, Y.G., Muralinath, M., Brandt, T., Pearcy, M., Hauns, K., Lowenhaupt, K., Jacobs, B.L. and Rich, A. (2003) A role for Z-DNA binding in vaccinia virus pathogenesis. Proc. Natl. Acad. Sci. U.S.A., 100, 6974-6979
21. Liu, T.K., Zhang, Y.B., Liu, Y., Sun, F. and Gui, J.F. (2011) 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., 85, 12769-12780
22. Takaoka, A., Wang, Z., Choi, M.K., 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. (Pubitemid 47123520
23. Takaoka, A. and Taniguchi, T. (2008) Cytosolic DNA recognition for triggering innate immune responses. Adv. Drug Deliv. Rev., 60, 847-857
24. Wang, Z., Choi, M.K., Ban, T., Yanai, H., Negishi, H., Lu, Y., Tamura, T., Takaoka, A., Nishikura, K. and Taniguchi, T. (2008) Regulation of innate immune responses by DAI (DLM-1/ZBP1) and other DNA-sensing molecules. Proc. Natl. Acad. Sci. U.S.A., 105, 5477-5482
25. Schwartz, T., Rould, M.A., Lowenhaupt, K., Herbert, A. and Rich, A. (1999) Crystal structure of the Zalpha domain of the human editing enzyme ADAR1 bound to left-handed Z-DNA. Science, 284, 1841-1845
26. Ha, S.C., Lokanath, N.K., Van Quyen, D., Wu, C.A., Lowenhaupt, K., Rich, A., Kim, Y.G. and Kim, K.K. (2004) A poxvirus protein forms a complex with left-handed Z-DNA: Crystal structure of a Yatapoxvirus Zalpha bound to DNA. Proc. Natl. Acad. Sci. U.S.A., 101, 14367-14372
27. Ha, S.C., Kim, D., Hwang, H.Y., Rich, A., Kim, Y.G. and Kim, K.K. (2008) The crystal structure of the second Z-DNA binding domain of human DAI (ZBP1) in complex with Z-DNA reveals an unusual binding mode to Z-DNA. Proc. Natl. Acad. Sci. U.S.A., 105, 20671-20676
28. Quyen, D.V., Ha, S.C., Lowenhaupt, K., Rich, A., Kim, K.K. and Kim, Y.G. (2007) Characterization of DNA-binding activity of Z alpha domains from poxviruses and the importance of the beta-wing regions in converting B-DNA to Z-DNA. Nucleic Acids Res., 35, 7714-7720
29. Wu, C.X., Wang, S.J., Lin, G. and Hu, C.Y. (2010) The Zalpha domain of PKZ from Carassius auratus can bind to d(GC)(n) in negative supercoils. Fish Shellfish Immunol., 28, 783-788
30. Kim, D., Hwang, H.Y., Kim, Y.G. and Kim, K.K. (2009) Crystallization and preliminary X-ray crystallographic studies of the Z-DNA-binding domain of a PKR-like kinase (PKZ) in complex with Z-DNA. Acta Crystallogr. F Struct. Biol. Cryst. Commun., 65, 267-270
31. Ha, S.C., Lowenhaupt, K., Rich, A., Kim, Y.G. and Kim, K.K. (2005) Crystal structure of a junction between B-DNA and Z-DNA reveals two extruded bases. Nature, 437, 1183-1186. (Pubitemid 41509358
32. Vagin, A. and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr., 66, 22-25
33. Murshudov, G.N., Vagin, A.A. and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr., 53, 240-255
34. Cowtan, K. (1994) dm: An automated procedure for phase improvement by density modification. Joint CCP4 ESF-EACBM Newsl. Protein Crystallogr., 31, 34-38
35. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tool for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132
36. Chen, V.B., Arendall, W.B. III, Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S. and Richardson, D.C. (2010) MolProbity: All-Atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr., 66, 12-21
37. DeLano, W.L. (2002) The PyMOL Molecular Graphics System. . DeLano Scientific, Palo Alto, CA
38. Kim, K., Khayrutdinov, B.I., Lee, C.K., Cheong, H.K., Kang, S.W., Park, H., Lee, S., Kim, Y.G., Jee, J., Rich, A. et al. (2011) Solution structure of the Zbeta domain of human DNA-dependent activator of IFN-regulatory factors and its binding modes to B-And Z-DNAs. Proc. Natl. Acad. Sci. U.S.A., 108, 6921-6926
39. Ha, S.C., Choi, J., Hwang, H.Y., Rich, A., Kim, Y.G. and Kim, K.K. (2009) The structures of non-CG-repeat Z-DNAs co-crystallized with the Z-DNA-binding domain, hZ alpha(ADAR1). Nucleic Acids Res., 37, 629-637
40. Lee, Y.M., Kim, H.E., Lee, E.H., Seo, Y.J., Lee, A.R. and Lee, J.H. (2012) NMR investigation on the DNA binding and B-Z transition pathway of the Zalpha domain of human ADAR1. Biophys. Chem., 172C, 18-25
41. Bae, S., Kim, D., Kim, K.K., Kim, Y.G. and Hohng, S. (2011) Intrinsic Z-DNA is stabilized by the conformational selection mechanism of Z-DNA-binding proteins. J. Am. Chem. Soc., 133, 668-671
42. von Hippel, P.H. and Berg, O.G. (1989) Facilitated target location in biological systems. J. Biol. Chem., 264, 675-678
43. Abrescia, N.A., Huynh-Dinh, T. and Subirana, J.A. (2002) Nickel-guanine interactions in DNA: Crystal structure of nickel-d[CGTGTACACG]2. J. Biol. Inorg. Chem., 7, 195-199
44. Gao, Y.G., Sriram, M. and Wang, A.H. (1993) Crystallographic studies of metal ion-DNA interactions: Different binding modes of cobalt(II), copper(II) and barium(II) to N7 of guanines in Z-DNA and a drug-DNA complex. Nucleic Acids Res., 21, 4093-4101. (Pubitemid 23258727
45. Mandal, P.K., Venkadesh, S. and Gautham, N. (2012) Interactions of Mn(2+) with a non-self-complementary Z-Type DNA duplex. Acta Crystallogr. F Struct. Biol. Cryst. Commun., 68, 1420-1426
46. Rothenburg, S., Deigendesch, N., Dey, M., Dever, T.E. and Tazi, L. (2008) 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., 6, 12
47. Tome, A.R., Kus, K., Correia, S., Paulo, L.M., Zacarias, S., de Rosa, M., Figueiredo, D., Parkhouse, R.M. and Athanasiadis, A. (2013) Crystal structure of a poxvirus-like zalpha domain from cyprinid herpesvirus 3. J. Virol., 87, 3998-4004
48. Liu, R., Liu, H., Chen, X., Kirby, M., Brown, P.O. and Zhao, K. (2001) Regulation of CSF1 promoter by the SWI/SNF-like BAF complex. Cell, 106, 309-318. (Pubitemid 32772615
49. Xu, Y.Z., Thuraisingam, T., Marino, R. and Radzioch, D. (2011) Recruitment of SWI/SNF complex is required for transcriptional activation of the SLC11A1 gene during macrophage differentiation of HL-60 cells. J. Biol. Chem., 286, 12839-12849
50. Zhao, J., Bacolla, A., Wang, G. and Vasquez, K.M. (2010) Non-B DNA structure-induced genetic instability and evolution. Cell. Mol. Life Sci., 67, 43-62
51. Ray, B.K., Dhar, S., Shakya, A. and Ray, A. (2011) Z-DNA-forming silencer in the first exon regulates human ADAM-12 gene expression. Proc. Natl. Acad. Sci. U.S.A., 108, 103-108