Cleavage of model substrates by archaeal RNase P: Role of protein cofactors in cleavage-site selection

Nucleic Acids Research

Volumn 39, Issue 3, 2011, Pages 1105-1116

  Sinapah, Sylvie ^a   Wu, Shiying ^a   Chen, Yu ^a   Pettersson, B M Fredrik ^a   Gopalan, Venkat ^b   Kirsebom, Leif A ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL PROTEIN; COFACTOR PROTEIN; PROTEIN POP5; PROTEIN RPP21; PROTEIN RPP29; PROTEIN RPP30; RIBONUCLEASE P; RNA; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PYROCOCCUS FURIOSUS; RNA SYNTHESIS;

ARCHAEAL PROTEINS; BASE SEQUENCE; ESCHERICHIA COLI PROTEINS; KINETICS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PYROCOCCUS FURIOSUS; RIBONUCLEASE P; RNA, ARCHAEAL; SUBSTRATE SPECIFICITY;

ARCHAEA; BACTERIA (MICROORGANISMS); EUKARYOTA; PYROCOCCUS FURIOSUS;

EID: 79951570571     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq732     Document Type: Article

References (54)

1. Gopalan, V. and Altman, S. (2006) In Gesteland, R.F., Cech, T.R. and Atkins, J.F. (eds), The RNA World, 3rd edn. Cold Spring Harbor Press, Cold Spring Harbor, NY, (http://rna.cshl.edu).
2. Kirsebom, L.A. (2007) RNase P RNA mediated cleavage: Substrate recognition and catalysis. Biochimie, 89, 1183-1194. (Pubitemid 47498685)
3. Kirsebom, L.A. and Trobro, S. (2009) RNase P RNA-mediated cleavage. IUBMB Life, 61, 189-200.
4. Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. and Altman, S. (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell, 35, 849-857. (Pubitemid 14168384)
5. Pannucci, J.A., Haas, E.S., Hall, T.A. and Brown, J.W. (1999) RNase P RNAs from some archaea are catalytically active. Proc. Natl Acad. Sci. USA, 96, 7803-7808. (Pubitemid 29328362)
6. Tsai, H.Y., Pulukkunat, D.K., Woznick, W.K. and Gopalan, V. (2006) Functional reconstitution and characterization of Pyrococcus furiosus RNase P. Proc. Natl Acad. Sci. USA, 103, 16147-16152. (Pubitemid 44715166)
7. Kikovska, E., Svard, S.G. and Kirsebom, L.A. (2007) Eukaryotic RNase P RNA mediates cleavage in the absence of protein. Proc. Natl Acad. Sci. USA, 104, 2062-2067. (Pubitemid 46391352)
8. Li, D., Willkomm, D.K. and Hartmann, R.K. (2008) Minor changes largely restore catalytic activity or archaeal RNase P RNA from Methanothermobacter thermoautotrophicus. Nucleic Acids Res., 37, 231-242.
9. Pulukkunat, D.K. and Gopalan, V. (2008) Studies on Methanocaldococcus jannaschii RNase P reveal insights into the roles of RNA and protein cofactors in RNase P catalysis. Nucleic Acids Res., 36, 4172-4180. (Pubitemid 351984832)
10. Holzmann, J., Frank, P., Loffler, E., Bennett, K.L., Gerner, C. and Rossmanith, W. (2008) RNase P without RNA: identification and functional reconstitution of the human mitochondrial tRNA processing enzyme. Cell, 135, 462-474.
11. Tallsjo, A. and Kirsebom, L.A. (1993) Product release is a rate-limiting step during cleavage by the catalytic RNA subunit of Escherichia coli RNase P. Nucleic Acids Res., 21, 51-57. (Pubitemid 23146292)
12. Peck-Miller, K. and Altman, S. (1991) Kinetics of the processing of the precursor to 4.5 S RNA, a naturally occurring substrate for RNase P from Escherichia coli. J. Mol. Biol., 221, 1-5. (Pubitemid 121003548)
13. Liu, F. and Altman, S. (1994) Differential evolution of substrates for an RNA enzyme in the presence and absence of its protein cofactor. Cell, 77, 1093-1100. (Pubitemid 24208868)
14. Park, B.H., Lee, J.H., Kim, M. and Lee, Y. (2000) Effects of C5 protein on Escherichia coli RNase P catalysis with a precursor tRNAPhe bearing a single mismatch in the acceptor stem. Biochem. Biophys. Res. Commun., 268, 136-140. (Pubitemid 30116624)
15. Loria, A. and Pan, T. (2001) Modular construction for function of a ribonucleoprotein enzyme: the catalytic domain of Bacillus subtilis RNase P complexed with B. subtilis RNase P protein. Nucleic Acids Res., 29, 1892-1897. (Pubitemid 32433273)
16. Buck, A.H., Dalby, A.B., Poole, A.W., Kazantsev, A.V. and Pace, N.R. (2005) Protein activation of a ribozyme: the role of bacterial RNase P protein. EMBO J., 24, 3360-3368. (Pubitemid 41486774)
17. Buck, A.H., Kazantsev, A.V., Dalby, A.B. and Pace, N.R. (2005) Structural perspective on the activation of RNase P RNA by protein. Nat. Struc. Mol. Biol., 12, 958-964.
18. 0 leader sequence of pre-tRNAAsp. Biochemistry, 37, 9409-9416. (Pubitemid 28307696)
19. Sun, L., Campell, F.E., Zahler, N.H. and Harris, M.E. (2006) Evidence that substrate-specific effects of C5 protein lead to uniformity in binding and catalysis by RNase P. EMBO J., 25, 3998-4007. (Pubitemid 44338742)
20. Kurz, J.C. and Fierke, C.A. (2002) The affinity of magnesium binding sites in the Bacillus subtilis RNase P-pre-tRNA complex is enhanced by the protein subunit. Biochemistry, 41, 9545-9548.
21. Sun, L. and Harris, M.E. (2007) Evidence that binding of C5 protein to P RNA enhances ribozyme catalysis by influencing active site metal ion affinity. RNA, 13, 1505-1515. (Pubitemid 47347421)
22. Niranjanakumari, S., Stams, T., Crary, S.M., Christianson, D.W. and Fierke, C.A. (1998) Protein component of the ribozyme ribonuclease P alters substrate recognition by directly contacting precursor tRNA. Proc. Natl Acad. Sci. USA, 95, 15212-15217. (Pubitemid 29018678)
23. Yuan, Y. and Altman, S. (1995) Substrate recognition by human RNase P: identification of small, model substrates for the enzyme. EMBO J., 14, 159-168.
24. 0 terminus of histidine tRNA. Proc. Natl Acad. Sci. USA, 79, 6475-6479. (Pubitemid 13207517)
25. Orellana, O., Cooley, L. and Soll, D. (1986) The additional guanylate at the 5' terminus of Escherichia coli tRNAHis is the result of unusual processing by RNase P. Mol. Cell Biol., 6, 525-529. (Pubitemid 16158127)
26. Carrara, G., Calandra, P., Fruscoloni, P., Doria, M. and Tocchini-Valentini, G.P. (1989) Site selection by Xenopus laevis RNaes P. Cell, 58, 37-45. (Pubitemid 19180077)
27. McClain, W.H., Guerrier-Takada, C. and Altman, S. (1987) Model substrates for an RNA enzyme. Science, 238, 527-530.
28. Brannvall, M., Kikovska, E., Wu, S. and Kirsebom, L.A. (2007) Evidence for induced fit in bacterial RNase P RNA-mediated cleavage. J. Mol. Biol., 372, 1149-1164. (Pubitemid 47374716)
29. Gopalan, V. (2007) Uniformity amid diversity in RNase P. Proc. Natl Acad. Sci. USA, 104, 2031-2302.
30. Milligan, J.F., Groebe, D.R., Withrell, GW. and Uhlenbeck, O.C. (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res., 15, 8783-8798.
31. Brannvall, M., Kikovska, E. and Kirsebom, LA. (2004) Cross talk in RNase P RNA mediated cleavage. Nucleic Acids Res., 32, 5418-5429.
32. Stage-Zimmermann, T. and Uhlenbeck, O.C. (1998) Hammerhead ribozyme kinetics. RNA, 4, 875-889. (Pubitemid 28359759)
33. Kurz, J. and Fierke, CA. (2002) The affinity of magnesium binding sites in the Bacillus subtilis RNase PPre-tRNA complex is enhanced by the protein subunit. Biochemistry, 41, 9545-9558. (Pubitemid 34810030)
34. Brannvall, M. and Kirsebom, LA. (1999) Manganese ions induce miscleavage in the Escherichia coli RNase P RNA-catalyzed reaction. J. Mol. Biol., 292, 53-63. (Pubitemid 29425652)
35. Brannvall, M. and Kirsebom, LA. (2001) Metal ion cooperativity in ribozyme cleavage of RNA. Proc. Natl Acad. Sci. USA, 98, 12943-12947. (Pubitemid 33051299)
36. Brannvall, M. and Kirsebom, LA. (2005) Complexity in orchestration of chemical groups near different cleavage sites in RNase P RNA mediated cleavage. J. Mol. Biol., 351, 251-257. (Pubitemid 41007744)
37. Brannvall, M., Pettersson, B.M.F. and Kirsebom, LA. (2002) The residue immediately upstream of the RNase P cleavage site is a positive determinant. Biochimie, 84, 693-703. (Pubitemid 35363454)
38. Brannvall, M., Petersson, B.M.F. and Kirsebom, LA. (2003) Importance of the +73/294 interaction in Escherichia coli RNase P RNA substrate complexes for cleavage and metal ion coordination. J. Mol. Biol., 325, 697-709. (Pubitemid 36268692)
39. Kikovska, E., Brannvall, M., Kufel, J. and Kirsebom, LA. (2005) Substrate discrimination in RNase P RNA-mediated cleavage: importance of the structural environment of the RNase P cleavage site. Nucleic Acids Res., 33, 2012-2021. (Pubitemid 41748344)
40. Kikovska, E., Mikkelsen, N.-E. and Kirsebom, LA. (2005) The naturally trans-acting ribozyme RNase P RNA has leadzyme properties. Nucleic Acids Res., 33, 6920-6930. (Pubitemid 41830495)
41. Hartmann, R.K. and Erdmann, VA. (1991) Analysis of the gene encoding the RNA subunit of ribonuclease P from T. thermophilus HB8. Nucl. Acids Res., 19, 5957-5964. (Pubitemid 21913010)
42. Xu, Y., Amero, C.D., Pulukkunat, D.K., Gopalan, V. and Foster, M.P. (2009) Solution structure of an archaeal RNase P binary protein complex: Formation of the 30-kDa complex between Pyrococcus furiosus RPP21 and RPP29 is accompanied by coupled protein folding and highlights critical features for protein-protein and protein-RNA interactions. J. Mol. Biol., 393, 1043-1055.
43. Pettersson, B.M.F. and Kirsebom, LA. (2008) The presence of a C-1/G+73 pair in a tRNA precursor influences processing and expression in vivo. J. Mol. Biol., 381, 1089-1097.
44. Terada, A., Yoshida, T. and Kimura, M. (2007) Identification of nucleotide residues essential for RNase P activity from the hyperthermophilic archaeon Pyrococcus horikoshii OT3. Biosci. Biotechnol. Biochem., 71, 1940-1945. (Pubitemid 350113135)
45. Lai, L.B., Vioque, A., Kirsebom, LA. and Gopalan, V. (2010) Unexpected diversity of RNase P, an ancient tRNA processing enzyme: challenges and prospects. FEBS Lett., 584, 287-296.
46. McClain, W.H., Lai, L.B. and Gopalan, V. (2010) Trials, travails and triumphs: an account of RNA catalysis in RNase P. J. Mol. Biol., 397, 627-646.
47. Pan, T. (1995) Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry, 34, 902-909.
48. Green, C.J., Rivera-Leon, R. and Vold, B.S. (1996) The catalytic core of RNase P. Nucleic Acids Res., 24, 1497-1503. (Pubitemid 26118983)
49. Harris, J.K., Haas, E.S., Williams, D., Frank, D.N. and Brown, J.W. (2001) New insight into RNase P RNA structure from comparative analysis of the archaeal RNA. RNA, 7, 220-232. (Pubitemid 33590505)
50. Brown, J. (1999) The ribonuclease P database. Nucleic Acids Res., 27, 314. (Pubitemid 29209471)
51. Kirsebom, L.A. and Svard, S.G. (1994) Base pairing between Escherichia coli RNase P RNA and its substrate. EMBO J., 13, 4870-4876. (Pubitemid 24319370)
52. Svard, S.G., Kagardt, U. and Kirsebom, L.A. (1996) Phylogenetic comparative mutational analysis of the base-pairing between RNase P RNA and its substrate. RNA, 2, 463-472. (Pubitemid 26374240)
53. Kufel, J. and Kirsebom, L.A. (1996) 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, 6085-6090. (Pubitemid 26190807)
54. Massire, C., Jaeger, L. and Westhof, E. (1998) Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. J. Mol. Biol., 279, 773-793. (Pubitemid 28284694)