Human RNA 5′-kinase (hClp1) can function as a tRNA splicing enzyme in vivo

RNA

Volumn 14, Issue 9, 2008, Pages 1737-1745

  Ramirez, Alejandro ^a   Shuman, Stewart ^a,b   Schwer, Beate ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

mRNA 3 processing; Polynucleotide kinase activity; RNA end healing

Indexed keywords

ADENOSINE TRIPHOSPHATE; NUCLEIC ACID BINDING PROTEIN; POLYNUCLEOTIDE 5' HYDROXYL KINASE; PROTEIN CLP1; RNA LIGASE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVE SITE; GENE DOSAGE; GENE MUTATION; GENE OVEREXPRESSION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA SPLICING; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; BINDING SITES; GENE DOSAGE; GENETIC COMPLEMENTATION TEST; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR PROTEINS; PHOSPHORIC DIESTER HYDROLASES; PHOSPHOTRANSFERASES; POLYNUCLEOTIDE 5'-HYDROXYL-KINASE; POLYNUCLEOTIDE LIGASES; PROTEIN STRUCTURE, TERTIARY; RNA SPLICING; RNA, TRANSFER; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION FACTORS;

ANIMALIA; MAMMALIA; SACCHAROMYCETALES;

EID: 50649088948     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1142908     Document Type: Article

References (44)

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. Amrani, N., Minet, M., Wyers, F., Dufour, M., Aggerbeck, L., and Lacroute, F. 1997. PCF11 encodes a third protein component of yeast cleavage and polyadenylation factor I. Mol. Cell. Biol. 17: 1102-1109.
3. Braun, P.E., Lee, J., and Gravel, M. 2004. 2′,3′-Cyclic nucleotide 3′-phoshodiesterase: Structure, biology and function. Myelin Biol. Disord. 1: 499-521.
4. de Vries, H., Rüegsegger, U., Hübner, 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.
5. 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.
6. 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.
7. Filipowicz, W. and Shatkin, A.J. 1983. Origin of splice junction phosphate in tRNAs processed by HeLa cell extract. Cell 32: 547-557.
8. Filipowicz, W., Konarska, M., Gross, H.J., and Shatkin, A.J. 1983. RNA 39-terminal phosphate cyclase activity and RNA ligation in HeLa cell extract. Nucleic Acids Res. 11: 1405-1418.
9. 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.
10. Greer, C.L., Peebles, C.L., Gegenheimer, P., and Abelson, J. 1983. Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell 32: 537-546.
11. 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.
12. Güldener, U., Heck, S., Fielder, T., Beinhauer, J., and Hegemann, J.H. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24: 2519-2524.
13. Harding, H.P., Lackey, J.G., Hsu, H.C., Zhang, Y., Deng, J., Xu, R.M., Dhama, M.J., and Ron, D. 2008. An intact unfolded protein response in Trpt1 knockout mice reveals phylogenic divergence in pathways for RNA ligation. RNA 14: 225-232.
14. Knapp, G., Ogden, R.C., Peebles, C.L., and Abelson, J. 1979. Splicing of yeast tRNA precursors: Structure of the reaction intermediates. Cell 18: 37-45.
15. Konarska, M., Filipowicz, W., Domdey, H., and Gross, H.J. 1981. Formation of a 29-phosphomonoester, 39,59-phosphodiester linkage by a novel RNA ligase in wheat germ. Nature 293: 112-116.
16. Konarska, M., Filipowicz, W., and Gross, H.J. 1982. RNA ligation via 2′-phosphomonoester, 3′,5′-phosphodiester linkage: Requirement of 2′,3′-cyclic phosphate termini and involvement of a 5′-hydroxyl polynucleotide kinase. Proc. Natl. Acad. Sci. 79: 1474-1478.
17. Lappe-Siefke, C., Goebbels, S., Gravel, M., Nicksch, E., Lee, J., Braun, P.E., Griffiths, I.R., and Nave, K.A. 2003. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33: 366-374.
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. Li, H., Trotta, C.R., and Abelson, J. 1998. Crystal structure and evolution of a transfer RNA splicing enzyme. Science 280: 279-284.
20. Mazumder, R., Iyer, L., Vasudevan, S., and Aravind, L. 2002. Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase family. Nucleic Acids Res. 30: 5229-5243.
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 39-end formation. Proc. Natl. Acad. Sci. 94: 7897-7902.
22. 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.
23. Paushkin, S.V., Patel, M., Furia, B.S., Peltz, S.W., and Trotta, C.R. 2004. Identification of a human endonuclease complex reveals a link between tRNA splicing and pre-mRNA 3′-end formation. Cell 117: 311-321.
24. Peebles, C.L., Gegenheimer, P., and Abelson, J. 1983. Precise excision of intervening sequences from precursor tRNAs by a membrane-associated yeast endonuclease. Cell 32: 525-536.
25. Ron, D. and Walter, P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8: 519-529.
26. 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.
27. Sawaya, R., Schwer, B., and Shuman, S. 2003. Genetic and biochemical analysis of the functional domains of yeast tRNA ligase. J. Biol. Chem. 278: 43298-43398.
28. 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.
29. Schwer, B., Aronova, A., Ramirez, A., Braun, P., and Shuman, S. 2008. Mammalian 2′,3′ cyclic nucleotide phosphodiesterase (CNP) can function as a tRNA splicing enzyme in vivo. RNA 14: 204-210.
30. Shuman, S. and Hurwitz, J. 1979. 5′-Hydroxyl polyribonucleotide kinase from HeLa cell nuclei. Purification and properties. J. Biol. Chem. 254: 10396-10404.
31. Spinelli, S.L., Malik, H.S., Consaul, S.A., and Phizicky, E.M. 1998. A functional homolog of a yeast tRNA splicing enzyme is conserved in higher eukaryotes and in Escherichia coli. Proc. Natl. Acad. Sci. 95: 14136-14141.
32. Trotta, C.R., Miao, F., Arn, E.A., Stevens, S.W., Ho, C.K., Rauhut, R., and Abelson, J.N. 1997. The yeast tRNA splicing endonuclease: A tetrameric enzyme with two active site subunits homologous to the archaeal tRNA endonucleases. Cell 89: 849-858.
33. Trotta, C.R., Paushkin, S.V., Patel, M., Li, H., and Peltz, S.W. 2006. Cleavage of pre-tRNAs by the splicing endonuclease requires a composite active site. Nature 441: 375-377.
34. Wang, L.K. and Shuman, S. 2001. Domain structure and mutational analysis of T4 polynucleotide kinase. J. Biol. Chem. 276: 26868-26874.
35. Wang, L.K. and Shuman, S. 2002. Mutational analysis defines the 5′ kinase and 3′ phosphatase active sites of T4 polynucleotide kinase. Nucleic Acids Res. 30: 1073-1080.
36. Wang, L.K. and Shuman, S. 2005. Structure-function analysis of yeast tRNA ligase. RNA 11: 966-975.
37. 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.
38. 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.
39. 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.
40. Xue, S., Calvin, K., and Li, H. 2006. RNA recognition and cleavage by a splicing endonuclease. Science 312: 906-910.
41. Yoshihisa, T., Yunoki-Esaki, K., Ohshima, C., Tanaka, N., and Endo, T. 2003. Possibility of cytoplasmic pre-tRNA splicing: The yeast tRNA splicing endonuclease mainly localizes on the mitochondria. Mol. Biol. Cell 14: 3266-3279.
42. Yoshihisa, T., Ohshima, C., Yunoki-Esaki, K., and Endo, T. 2007. Cytoplasmic splicing of tRNA in Saccharomyces cerevisiae. Genes Cells 12: 285-297.
43. Zillman, M., Gorovsky, M.A., and Phizicky, E.M. 1991. Conserved mechanism of tRNA splicing in eukaryotes. Mol. Cell. Biol. 11: 5410-5416.
44. 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.