The Exocyclic Amine at the RNase P Cleavage Site Contributes to Substrate Binding and Catalysis

Journal of Molecular Biology

Volumn 359, Issue 3, 2006, Pages 572-584

  Kikovska, Ema ^a   Brännvall, Mathias ^a   Kirsebom, Leif A ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

divalent metal ions; ribozyme; RNA processing; RNase P; tRNA precursors

Indexed keywords

AMINE; MAGNESIUM; RIBONUCLEASE P;

ARTICLE; BASE PAIRING; CATALYSIS; PRIORITY JOURNAL; PROTEIN BINDING; RNA CLEAVAGE;

EID: 33646775015     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.03.040     Document Type: Article

References (60)

1. Altman S., and Kirsebom L.A. Ribonuclease P. In: Gesteland R.F., Cech T., and Atkins J.F. (Eds). The RNA World. 2nd edit. (1999), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY 351-380
2. Kikovska E., Brännvall M., Kufel J., and Kirsebom L.A. Substrate discrimination in RNase P RNA-mediated cleavage: importance of the structural environment of the RNase P cleavage site. Nucl. Acids Res. 33 (2005) 2012-2021
3. Smith J.D. Transcription and processing of transfer RNA precursors. Prog. Nucl. Acid Res. Mol. Biol. 16 (1976) 25-73
4. Burkard U., Willis I., and Söll D. Processing of histidine transfer RNA precursors. Abnormal cleavage site for RNase P. J. Biol. Chem. 263 (1988) 2447-2451
5. His precursors by the catalytic RNA component of RNase P. J. Biol. Chem. 263 (1988) 652-657
6. Ser. J. Mol. Biol. 203 (1988) 549-553
7. Kirsebom L.A., and Svärd S.G. The kinetics and specificity of cleavage by RNase P is mainly dependent on the structure of the amino acid acceptor stem. Nucl. Acids Res. 20 (1992) 425-432
8. Svärd S.G., and Kirsebom L.A. Several regions of a tRNA precursor determine the Escherichia coli RNase P cleavage site. J. Mol. Biol. 227 (1992) 1019-1031
9. Kufel J., and Kirsebom L.A. Different cleavage sites are aligned differently in the active site of M1 RNA, the catalytic subunit of Escherichia coli RNase P. Proc. Natl Acad. Sci. USA 93 (1996) 6085-6090
10. Loria A., and Pan T. Recognition of the 5′ leader and the acceptor stem of a pre-tRNA substrate by the ribozyme from Bacillus subtilis RNase P. Biochemistry 37 (1998) 10126-10133
11. Kirsebom L.A., Svärd S.G., and RNase P. RNase P processing of tRNA precursors. In: Krupp G., and Gaur R.K. (Eds). Ribozyme Biochemistry and Biotechnology (2000), Eaton Publishing, Natick, MA 111-131
12. Perreault J.P., and Altman S. Important 2′-hydroxyl groups in model substrates for M1 RNA, the catalytic RNA subunit of RNase P from Escherichia coli. J. Mol. Biol. 226 (1992) 399-409
13. Tallsjö A., Kufel J., and Kirsebom L.A. Interaction between Escherichia coli RNase P RNA and the discriminator base results in slow product release. RNA 2 (1996) 299-307
14. Doudna J.A., and Cech T.R. The chemical repertoire of natural ribozymes. Nature 418 (2002) 222-228
15. Sprinzl M., Horn C., Brown M., Ioudovitch A., and Steinberg S. Compilation of tRNA sequences and sequences of tRNA genes. Nucl. Acids Res. 26 (1998) 148-153
16. Brännvall M., and Kirsebom L.A. Manganese ions induce miscleavage in the Escherichia coli RNase P RNA-catalyzed reaction. J. Mol. Biol. 292 (1999) 53-63
17. Brännvall M., and Kirsebom L.A. Metal ion cooperativity in ribozyme cleavage of RNA. Proc. Natl Acad. Sci. USA 98 (2001) 12943-12947
18. Brännvall M., Fredrik Pettersson B.M., and Kirsebom L.A. The residue immediately upstream of the RNase P cleavage site is a positive determinant. Biochimie 84 (2002) 693-703
19. Brännvall M., Pettersson B.M., and Kirsebom L.A. Importance of the +73/294 interaction in Escherichia coli RNase P RNA substrate complexes for cleavage and metal ion coordination. J. Mol. Biol. 325 (2003) 697-709
20. Brännvall M., Kikovska E., and Kirsebom L.A. Cross talk between the +73/294 interaction and the cleavage site in RNase P RNA mediated cleavage. Nucl. Acids Res. 32 (2004) 5418-5429
21. Kikovska E., Mikkelsen N.-E., and Kirsebom L.A. The naturally trans acting ribozyme RNase P RNA has leadzyme properties. Nucl. Acids Res. 33 (2005) 6920-6930
22. Zahler N.H., Christian E.L., and Harris M.E. Recognition of the 5′ leader of pre-tRNA substrates by the active site of ribonuclease P. RNA 9 (2003) 734-745
23. Tsai H.Y., Masquida B., Biswas R., Westhof E., and Gopalan V. Molecular modeling of the three-dimensional structure of the bacterial RNase P holoenzyme. J. Mol. Biol. 325 (2003) 661-675
24. Miller P.S., Bhan P., and Kan L.-S. Synthesis and interactions of oligodeoxyribonucleotides containing 2′-amino-2′-deoxyuridine. Nucleosides Nucleotides 12 (1993) 785-792
25. Aurup H., Tuschl T., Benseler F., Ludwig J., and Eckstein F. Oligonucleotide duplexes containing 2′-amino-2′-deoxycytidines: thermal stability and chemical reactivity. Nucl. Acids Res. 22 (1994) 20-24
26. Burkard U., and Söll D. The unusually long amino acid acceptor stem of Escherichia coli selenocysteine tRNA results from abnormal cleavage by RNase P. Nucl. Acids Res. 16 (1988) 11617-11624
27. Mans R.M., Guerrier-Takada C., Altman S., and Pleij C.W. Interaction of RNase P from Escherichia coli with pseudoknotted structures in viral RNAs. Nucl. Acids Res. 18 (1990) 3479-3487
28. Svärd S.G., and Kirsebom L.A. Determinants of Escherichia coli RNase P cleavage site selection: a detailed in vitro and in vivo analysis. Nucl. Acids Res. 21 (1993) 427-434
29. Burgin A.B., and Pace N.R. Mapping the active site of ribonuclease P RNA using a substrate containing a photoaffinity agent. EMBO J. 9 (1990) 4111-4118
30. Harris M.E., Kazantsev A.V., Chen J.L., and Pace N.R. Analysis of the tertiary structure of the ribonuclease P ribozyme-substrate complex by site-specific photoaffinity crosslinking. RNA 3 (1997) 561-576
31. Christian E.L., McPheeters D.S., and Harris M.E. Identification of individual nucleotides in the bacterial ribonuclease P ribozyme adjacent to the pre-tRNA cleavage site by short-range photo-cross-linking. Biochemistry 37 (1998) 17618-17628
32. LaGrandeur T.E., Huttenhofer A., Noller H.F., and Pace N.R. Phylogenetic comparative chemical footprint analysis of the interaction between ribonuclease P RNA and tRNA. EMBO J. 13 (1994) 3945-3952
33. Kazantsev A.V., and Pace N.R. Identification by modification-interference of purine N-7 and ribose 2′-OH groups critical for catalysis by bacterial ribonuclease P. RNA 4 (1998) 937-947
34. Heide C., Busch S., Feltens R., and Hartmann R.K. Distinct modes of mature and precursor tRNA binding to Escherichia coli RNase P RNA revealed by NAIM analyses. RNA 7 (2001) 553-564
35. Kaye N.M., Christian E.L., and Harris M.E. NAIM and site-specific functional group modification analysis of RNase P RNA: magnesium dependent structure within the conserved P1-P4 multihelix junction contributes to catalysis. Biochemistry 41 (2002) 4533-4545
36. Torres-Larios A., Swinger K.K., Krasilnikov A.S., Pan T., and Mondragon A. Crystal structure of the RNA component of bacterial ribonuclease P. Nature 437 (2005) 584-587
37. Kazantsev A.V., Krivenko A.A., Harrington D.J., Holbrook S.R., Adams P.D., and Pace N.R. Crystal structure of a bacterial ribonuclease P RNA. Proc. Natl Acad. Sci. USA 102 (2005) 13392-13397
38. Brännvall M., and Kirsebom L.A. Complexity in orchestration of chemical groups near different cleavage sites in RNase P RNA-mediated cleavage. J. Mol. Biol. 351 (2005) 251-257
39. Lumelsky N., and Altman S. Selection and characterization of randomly produced mutants in the gene coding for M1 RNA. J. Mol. Biol. 202 (1988) 443-454
40. Hardt W.D., and Hartmann R.K. Mutational analysis of the joining regions flanking helix P18 in E. coli RNase P RNA. J. Mol. Biol. 259 (1996) 422-433
41. Pomeranz Krummel D.A., Kent O., MacMillan A.M., and Altman S. Evidence for helical unwinding of an RNA substrate by the RNA enzyme RNase P: use of an interstrand disulfide crosslink in substrate. J. Mol. Biol. 295 (2000) 1113-1118
42. Kufel J., and Kirsebom L.A. Residues in Escherichia coli RNase P RNA important for cleavage site selection and divalent metal ion binding. J. Mol. Biol. 263 (1996) 685-698
43. Saenger W. Principles of Nucleic Acid Structure (1984), Springer, New York
44. Klein D.J., Moore P.B., and Steitz T.A. The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA 10 (2004) 1366-1379
45. Haas E.S., and Brown J.W. Evolutionary variation in bacterial RNase P RNAs. Nucl. Acids Res. 26 (1998) 4093-4099
46. Brännvall M., Mattsson J.G., Svärd S.G., and Kirsebom L.A. RNase P RNA structure and cleavage reflect the primary structure of tRNA genes. J. Mol. Biol. 283 (1998) 771-783
47. Loria A., Niranjanakumari S., Fierke C.A., and Pan T. Recognition of a pre-tRNA substrate by the Bacillus subtilis RNase P holoenzyme. Biochemistry 37 (1998) 15466-15473
48. Kleineidam R.G., Pitulle C., Sproat B., and Krupp G. Efficient cleavage of pre-tRNAs by E. coli RNAse P RNA requires the 2′-hydroxyl of the ribose at the cleavage site. Nucl. Acids Res. 21 (1993) 1097-1101
49. Kahle D., Wehmeyer U., Char S., and Krupp G. The methylation of one specific guanosine in a pre-tRNA prevents cleavage by RNase P and by the catalytic M1 RNA. Nucl. Acids Res. 18 (1990) 837-844
50. Persson T., Cuzic S., and Hartmann R.K. Catalysis by RNase P RNA: unique features and unprecedented active site plasticity. J. Biol. Chem. 278 (2003) 43394-43401
51. Konforti B.B., Abramovitz D.L., Duarte C.M., Karpeisky A., Beigelman L., and Pyle A.M. Ribozyme catalysis from the major groove of group II intron domain 5. Mol. Cell 1 (1998) 433-441
52. Rupert P.B., and Ferre-D'Amare A.R. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410 (2001) 780-786
53. Rupert P.B., Massey A.P., Sigurdsson S.T., and Ferre-D'Amare A.R. Transition state stabilization by a catalytic RNA. Science 298 (2002) 1421-1424
54. Fedor M.J. The role of metal ions in RNA catalysis. Curr. Opin. Struct. Biol. 12 (2002) 289-295
55. Milligan J.F., Groebe D.R., Whiterell G.W., and Uhlenbeck O.C. Oligoribonucleotide synthesis using T7 RNA polymerase and DNA templates. Nucl. Acids Res. 15 (1987) 8783-8798
56. Brännvall M., Mattsson J.G., Svärd S.G., and Kirsebom L.A. RNase P RNA structure and cleavage reflect the primary structure of tRNA genes. J. Mol. Biol. 283 (1998) 771-783
57. Kufel J., and Kirsebom L.A. The P15-loop of Escherichia coli RNase P RNA is an autonomous divalent metal ion binding domain. RNA 4 (1998) 777-788
58. Beebe J.A., and Fierke C.A. A kinetic mechanism for cleavage of precursor tRNA(Asp) catalyzed by the RNA component of Bacillus subtilis ribonuclease P. Biochemistry 33 (1994) 10294-10304
59. Warnecke J.M., Held R., Busch S., and Hartmann R.K. Role of metal ions in the hydrolysis reaction catalyzed by RNase P RNA from Bacillus subtilis. J. Mol. Biol. 290 (1999) 433-445
60. Kirsebom L.A., and Svärd S.G. Base-pairing between Escherichia coli RNase P RNA and its substrate. EMBO J. 13 (1994) 4870-4876