Structures of bacterial polynucleotide kinase in a Michaelis complex with GTPMg2+ and 5′-OH oligonucleotide and a product complex with GDPMg2+ and 5′-PO4 oligonucleotide reveal a mechanism of general acid-base catalysis and the determinants of phosphoacceptor recognition

Nucleic Acids Research

Volumn 42, Issue 2, 2014, Pages 1152-1161

  Das, Ushati ^a   Wang, Li Kai ^a   Smith, Paul ^a   Jacewicz, Agata ^a   Shuman, Stewart ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIAL ENZYME; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANOSINE DIPHOSPHATE; OLIGONUCLEOTIDE; POLYNUCLEOTIDE 5' HYDROXYL KINASE;

ARTICLE; BACTERIOPHAGE T4; BINDING SITE; CATALYSIS; CATALYST; CHEMICAL REACTION; CLOSTRIDIUM THERMOCELLUM; CRYSTAL STRUCTURE; CRYSTALLIZATION; DIFFRACTION; ENZYME STRUCTURE; MICHAELIS CONSTANT; MUTATIONAL ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; STEREOCHEMISTRY;

BACTERIAL PROTEINS; BACTERIOPHAGE T4; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; CLOSTRIDIUM THERMOCELLUM; CRYSTALLOGRAPHY; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; MODELS, MOLECULAR; MUTATION; OLIGONUCLEOTIDES; PHOSPHATES; POLYNUCLEOTIDE 5'-HYDROXYL-KINASE;

EID: 84893294280     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt936     Document Type: Article

References (26)

1. Amitsur, M., Levitz, R. and Kaufman, G. (1987) Bacteriophage T4 anticodon nuclease, polynucleotide kinase, and RNA ligase reprocess the host lysine tRNA. EMBO J., 6, 2499-2503.
2. Martins, A. and Shuman, S. (2005) An end-healing enzyme from Clostridium thermocellum with 50 kinase, 20, 30 phosphatase, and adenylyltransferase activities. RNA, 11, 1271-1280.
3. Chan, C.M., Zhou, C. and Huang, R.H. (2009) Reconstituting bacterial RNA repair and modification in vitro. Science, 326, 247.
4. Jain, R. and Shuman, S. (2010) Bacterial Hen1 is a 30 terminal RNA ribose 20O-methyltransferase component of a bacterial RNA repair cassette. RNA, 16, 316-323.
5. Zhang, C., Chan, C.M., Wang, P. and Huang, R.H. (2012) Probing the substrate specificity of the bacterial Pnkp/Hen1 RNA repair system using synthetic RNAs. RNA, 18, 335-344.
6. Wang, L.K., Das, U., Smith, P. and Shuman, S. (2012) Structure and mechanism of the polynucleotide kinase component of the bacterial Pnkp-Hen1 RNA repair system. RNA, 18, 2277-2286.
7. Wang, L.K., Smith, P. and Shuman, S. (2013) Structure and mechanism of the 20, 30 phosphatase component of the bacterial Pnkp-Hen1 RNA repair system. Nucleic Acids Res, 41, 5864-5873.
8. Smith, P., Wang, L.K., Nair, P.A. and Shuman, S. (2012) The adenylyltransferase domain of bacterial Pnkp defines a unique RNA ligase family. Proc. Natl Acad. Sci. USA, 109, 2296-2301.
9. Keppetipola, N. and Shuman, S. (2006) Mechanism of the phosphatase component of Clostridium thermocellum polynucleotide kinase-phosphatase. RNA, 12, 73-82.
10. Keppetipola, N. and Shuman, S. (2006) Distinct enzymic functional groups are required for the phosphomonoesterase and phosphodiesterase activities of Clostridium thermocellum polynucleotide kinase/phosphatase. J. Biol. Chem., 281, 19251-19259.
11. Keppetipola, N. and Shuman, S. (2007) Characterization of the 20, 30 cyclic phosphodiesterase activities of Clostridium thermocellum polynucleotide kinase-phosphatase and bacteriophage-phosphatase. Nucleic Acids Res., 35, 7721-7732.
12. Keppetipola, N., Nandakumar, J. and Shuman, S. (2007) Reprogramming the tRNA splicing activity of a bacterial RNA repair enzyme. Nucleic Acids Res., 35, 3624-3630.
13. Wang, P., Chan, C.M., Christensen, D., Zhang, C., Selvadurai, K. and Huang, R.H. (2012) Molecular basis of bacterial protein Hen1 activating the ligase activity of bacterial protein Pnkp for RNA repair. Proc Natl Acad. Sci. USA, 109, 13248-13253.
14. Chan, C.M., Zhou, C., Brunzelle, J.S. and Huang, R.H. (2009) Structural and biochemical insights into 20-O-methylation at the 30-terminal nucleotide of RNA by Hen1. Proc. Natl Acad. Sci. USA, 106, 17699-17704.
15. Jain, R. and Shuman, S. (2011) Active site mapping and substrate specificity of bacterial Hen1, a manganese-dependent 30 terminal RNA ribose 20O-methyltransferase. RNA, 17, 429-438.
16. Das, U., Wang, L.K., Smith, P. and Shuman, S. (2013) Structural and biochemical analysis of the phosphate donor specificity of the polynucleotide kinase component of the bacterial Pnkp-Hen1 RNA repair system. Biochemistry, 52, 4734-4743.
17. Wang, L.K., Lima, C.D. and Shuman, S. (2002) Structure and mechanism of T4 polynucleotide kinase-an RNA repair enzyme. EMBO J., 21, 3873-3880.
18. Galburt, E.A., Pelletier, J., Wilson, G. and Stoddard, B.L. (2002) Structure of a tRNA repair enzyme and molecular biology workhorse: T4 polynucleotide kinase. Structure, 10, 1249-1260.
19. Zhu, H., Yin, S. and Shuman, S. (2004) Characterization of polynucleotide kinase/phosphatase enzymes from mycobacteriophages Omega and Cjw1 and vibriophage KVP40. J. Biol. Chem., 279, 26358-26369.
20. Martins, A. and Shuman, S. (2004) Characterization of a baculovirus enzyme with RNA ligase, polynucleotide 50 kinase and polynucleotide 30 phosphatase activities. J. Biol. Chem., 279, 18220-18231.
21. Wang, L.K. and Shuman, S. (2001) Domain structure and mutational analysis of T4 polynucleotide kinase. J. Biol. Chem., 276, 26868-26874.
22. Wang, L.K. and Shuman, S. (2002) Mutational analysis defines the 50 kinase and 30 phosphatase active sites of T4 polynucleotide kinase. Nucleic Acids Res., 30, 1073-1080.
23. Eastberg, J.H., Pelletier, J. and Stoddard, B.L. (2004) Recognition of DNA substrates by bacteriophage T4 polynucleotide kinase. Nucleic Acids Res., 32, 653-660.
24. Jarvest, R.L. and Lowe, G. (1981) The stereochemical course of the phosphoryl transfer reaction catalyzed by polynucleotide kinase (bacteriophage-T4-infected Escherichia coli B). Biochem. J., 199, 273-276.
25. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr., D60, 2126-2132.
26. Adams, P.D., Grosse-Kunstleve, R.W., Hung, L.W., Ioerger, T.R., McCoy, A.J., Moriarty, N.W., Read, R.J., Sacchettini, J.C., Sauter, N.K. and Terwilliger, T.C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr., D58, 1948-1954.