Characterization of a thermostable archaeal polynucleotide kinase homologous to human Clp1

RNA

Volumn 15, Issue 5, 2009, Pages 923-931

  Jain, Ruchi ^a   Shuman, Stewart ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Phosphotransferase; RNA end healing; TRNA splicing

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALANINE; ASPARTIC ACID; CLP1 ENZYME; DNA; ENDOPEPTIDASE CLP; LYSINE; MESSENGER RNA; OLIGONUCLEOTIDE; PHOSPHATE; PHOSPHOTRANSFERASE; POLYNUCLEOTIDE 5' HYDROXYL KINASE; RECOMBINANT PROTEIN; RNA; SODIUM CHLORIDE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; CATALYSIS; ENZYME ACTIVITY; GENE MUTATION; GENETIC CONSERVATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; PYROCOCCUS HORIKOSHII; SEQUENCE HOMOLOGY; THERMOSTABILITY;

AMINO ACID SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PHOSPHOTRANSFERASES; POLYNUCLEOTIDE 5'-HYDROXYL-KINASE; PYROCOCCUS HORIKOSHII; RNA; RNA LIGASE (ATP); TEMPERATURE; TRANSCRIPTION FACTORS;

ARCHAEA; EUKARYOTA; PYROCOCCUS; SACCHAROMYCETALES;

EID: 65249152520     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1492809     Document Type: Article

References (45)

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. Barrangou, R., Fremauzx, C., Deveau, H., Richards, M., Boyaval, P., Moineau, S., Romero, D.A., and Horvath, P. 2007. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315: 1709-1712.
3. Bernstein, N.K., Williams, R.S., Rakovszky, M.L., Cui, D., Green, R., Galicia,S.,Koch,C.A.,Cass,C.E.,Durocher,D., Weinfeld,M., et al. 2005. The molecular architecture of the mammalian DNA repair enzyme, polynucleotide kinase. Mol. Cell 17: 657-670.
4. Blasius, M., Buob, R., Shevlev, I.V., and Hubscher, U. 2007. Enzymes involved in DNA ligation and end healing in the radioresistant bacterium Deinococcus radiodurans. BMC Mol. Biol. 8: 69.
5. Blondal, T., Hjorleifsdottir, S., Aevarsson, A., Fridjonsson, O.H., Skirnisdottir, S., Wheat, J.O., Hermannsdottir, A.G., Hreggvidsson, G.O., Smith,A.V.,and Kristjansson,J.K.2005. Characterization of a 5'-polynucleotide kinase/3'-phosphatase from bacteriophage RM378. J. Biol. Chem. 280: 5188-5194.
6. Brooks, M.A., Meslet-Caliere, L., Graille, M., Kuhn, J., Blondeau, K., Myllykallio, H., and van Tilbeurgh, H. 2008. The structure of an archaeal homodimeric ligase which has RNA circularization activity. Protein Sci. 17: 1336-1345.
7. Brouns, S.J.J., Jore, M.M., Lundgren, M., Westra, E.R., Slijkhui, R.J.H., Snijders, A.P.L., Dickman, M.J., Makarova, K.S., Koonin, E.V., and van der Oost, J. 2008. Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321: 960-964.
8. Chiu, Y. and Rana, T.M. 2002. RNAi in human cells: Basic structural and functional features of small interfering RNA. Mol. Cell 10: 549-561.
9. de Vries, H., Riiegsegger, U., Hubner, W., Friedlein, A., Langen, H., and Keller, W. 2000. Human pre-mRNA cleavage factor IIm contains homologs of yeast proteins and bridges two other cleavage factors. EMBO J. 21: 5895-5904.
10. 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.
11. Englert, M. and Beier, H. 2005. Plant tRNA ligases are multifunctional enzymes that have diverged in sequence and substrate specificity from RNA ligases of other phylogenetic origins. Nucleic Acids Res. 33: 388-399.
12. Filipowicz, W. and Shatkin, A.J. 1983. Origin of splice junction phosphate in tRNAs processed by HeLa cell extract. Cell 32: 547-557.
13. Filipowicz, W., Konarska, M., Gross, H.J., and Shatkin, A.J. 1983. RNA 3'-terminal phosphate cyclase activity and RNA ligation in HeLa cell extract. Nucleic Acids Res. 11: 1405-1418.
14. 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.
15. Gross, S. and Moore, C.L. 2001. Five subunits are required for reconstitution of the cleavage and polyadenylation activities of Saccharomyces cerevisiae cleavage factor I. Proc. Natl. Acad. Sci. 98: 6080-6085.
16. Hale, C., Kleppe, K., Termns, R.M., and Terns, M.P. 2008. Prokaryotic silencing (psi)RNAs in Pyrococcus furiosus. RNA 14: 2572-2579.
17. Ho, C.K. and Shuman, S. 2002. Bacteriophage T4 RNA ligase 2 (gp24.1) exemplifies a family of RNA ligases found in all phylogenetic domains. Proc. Natl. Acad. Sci. 99: 12709-12714.
18. Laski, F.A., Fire, A.Z., RajBhandary, U.L., and Sharp. P.A. 1983. Characterization of tRNA precursor splicing in mammalian extracts. J. Biol. Chem. 258: 11974-11980.
19. Martins, A. and Shuman, S. 2004. Characterization of a baculovirus enzyme with RNA ligase, polynucleotide 5' kinase and polynucle- otide 3' phosphatase activities. J. Biol. Chem. 279: 18220-18231.
20. Martins, A. and Shuman, S. 2005. An end-healing enzyme from Clostridium thermocellum with 5' kinase, 2',3' phosphatase, and adenylyltransferase activities. RNA 11: 1271-1280.
21. Minvielle-Sebastia, L., Preker, P.J., Wiederkehr, T., Strahm, Y., and Keller, W. 1997. The major yeast poly(A)-binding protein is associated with cleavage factor IA and functions in pre-messenger RNA 3'-end formation. Proc. Natl. Acad. Sci. 94: 7897-7902.
22. Mossessova, E. and Lima, C.D. 2000. Ulp1-SUMO crystal structure and genetic analysis reveal conserved interactions and a regulatory element essential for cell growth in yeast. Mol. Cell 5: 865-876.
23. Nandakumar, J., Schwer, B., Schaffrath, R., and Shuman, S. 2008. RNA repair: An antidote to cytotoxic eukaryal RNA damage. Mol. Cell 31: 278-286.
24. Noble, C.G., Beuth, B., and Taylor, I.A. 2007. Structure of a nucleotide-bound Clp1-Pcf11 polyadenylation factor. Nucleic Acids Res. 35: 87-89.
25. Novogrodsky, A. and Hurwitz, J. 1966. The enzymatic phosphoryla- tion of ribonucleic acid and deoxyribonucleic acid: Phosphoryla- tion at 5'-hydroxyl termini. J. Biol. Chem. 241: 2923-2932.
26. Novogrodsky,A.,Tal,M.,Traub,A.,andHurwitz,J.1966.The enzymatic phosphorylation of ribonucleic acid and deoxyribonucleic acid: Further properties of the 5'-hydroxyl polynucleotide kinase. J. Biol. Chem. 241: 2933-2943.
27. Nykänen, A., Haley, B., and Zamore, P.D. 2001. ATP requirements and small interfering RNA structure in the RNA interference pathway. Cell 107: 309-321.
28. Pascal, J.M. 2008. DNA and RNA ligases: Structural variations and shared mechanisms. Curr. Opin. Struct. Biol. 18: 96-105.
29. Ramirez, A., Shuman, S., and Schwer, B. 2008. Human RNA 5'-kinase (hClp1) can function as a tRNA splicing enzyme in vivo. RNA 14: 1737-1745.
30. Richardson, C.C. 1965. Phosphorylation of nucleic acid by an enzyme from T4 bacteriophage-infected Escherichia coli. Proc. Natl. Acad. Sci. 54: 158-165.
31. Salgia, S.R., Singh, S.J., Gurha, P., and Gupta, R. 2003. Two reactions of Haloferax volcanii RNA splicing enzymes: Joining of exons and circularization of introns. RNA 9: 319-330.
32. Schwer, B., Sawaya, R., Ho, C.K., and Shuman, S. 2004. Portability and fidelity of RNA-repair systems. Proc. Natl. Acad. Sci. 101: 2788-2793.
33. Shuman, S. and Hurwitz, J. 1979. 5' Hydroxyl polyribonucleotide kinase from HeLa cell nuclei. J. Biol. Chem. 254: 10396-10404.
34. Starotsina, N.G., Marshburn, S., Johnson, L.S., Eddy, S.R., Terns, R.M., and Terns, M.P. 2004. Circular box C/D RNAs in Pyrococcus furiosus. Proc. Natl. Acad. Sci. 101: 14097-14101.
35. Stevens, A. 2001. 5'-Exoribonuclease 1: Xrn1. Methods Enzymol. 342: 251-259.
36. Torchia, C., Takagi, Y., and Ho, C.K. 2008. Archaeal RNA ligase is a homodimeric protein that catalyzes intramolecular ligation of single-strand RNA and DNA. Nucleic Acids Res. 36: 6218-6227.
37. van de Sande, J.H., Kleppe, K., and Khorana, H.G. 1973. Reversal of bacteriophage T4 induced polynucleotide kinase action. Biochemistry 12: 5050-5055.
38. Wang, L.K. and Shuman, S. 2001. Domain structure and mutational analysis of T4 polynucleotide kinase. J. Biol. Chem. 276: 26868-26874.
39. Wang, L.K. and Shuman, S. 2002. Mutational analysis defines the 5' kinase and 3' phosphatase active sites ofT4 polynucleotide kinase. Nucleic Acids Res. 30: 1073-1080.
40. 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.
41. Wang, L.K., Schwer, B., Englert, M., Beier, H., and Shuman, S. 2006. Structure-function analysis of the kinase-CPD domain of yeast tRNA ligase (Trl1) and requirements for complementation of tRNA splicing by a plant Trl1 homolog. Nucleic Acids Res. 34: 517-527.
42. Weitzer, S. and Martinez, J. 2007. The human RNA kinase hClp1 is active on 3' transfer RNA exons and short interfering RNAs. Nature 447: 2222-2226.
43. Zhu, H., Yin, S., and Shuman, S. 2004. Characterization of poly- nucleotide kinase/phosphatase enzymes from mycobacteriophages Omega and Cjw1 and vibriophage KVP40. J. Biol. Chem. 279: 26358-26369.
44. Zillman, M., Gorovsky, M.A., and Phizicky, E.M. 1991. Conserved mechanism of tRNA splicing in eukaryotes. Mol. Cell. Biol. 11: 5410-5416.
45. Zofallova, L., Guo, Y., and Gupta, R. 2000. Junction phosphate is derived from the precursor in the tRNA spliced by the archaeon Haloferax volcanii cell extract. RNA 6: 1019-1030.