Recent insights into the structure and function of the ribonucleoprotein enzyme ribonuclease P

Current Opinion in Structural Biology

Volumn 13, Issue 3, 2003, Pages 325-333

  Harris, Michael E ^a   Christian, Eric L ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RIBONUCLEASE P; RNA;

BACTERIUM; CATALYSIS; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SUBSTRATE COMPLEX; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; PRIORITY JOURNAL; REVIEW; RNA PROCESSING;

BACTERIA (MICROORGANISMS);

EID: 0038170017     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(03)00069-1     Document Type: Review

References (67)

1. Kurz J.C., Fierke C.A. Ribonuclease P: a ribonucleoprotein enzyme. Curr. Opin. Chem. Biol. 4:2000;553-558 A concise and articulate review of the basic issues that are important for understanding substrate binding and catalysis by bacterial RNase P, focusing on literature up to 2000. This review is of particular interest as it underscores the importance of understanding the properties of RNase P within the broad context of biological catalysis.
2. Christian E.L., Zahler N.H., Kaye N.M., Harris M.E. Analysis of substrate recognition by the ribonucleoprotein endonuclease RNase P. Methods. 28:2002;307-322.
3. Hall T.A., Brown J.W. The ribonuclease P family. Methods Enzymol. 341:2001;56-77.
4. Gopalan V., Vioque A., Altman S. RNase P: variations and uses. J. Biol. Chem. 277:2002;6759-6762.
5. Xiao S., Scott F., Fierke C.A., Engelke D.R. Eukaryotic ribonuclease P: a plurality of ribonucleoprotein enzymes. Annu. Rev. Biochem. 71:2002;165-189.
6. Jarrous N. Human ribonuclease P: subunits, function, and intranuclear localization. RNA. 8:2002;1-7.
7. Guerrier-Takada C., Gardiner K., Marsh T., Pace N., Altman S. The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell. 35:1983;849-857.
8. Pannucci J.A., Haas E.S., Hall T.A., Harris J.K., Brown J.W. RNase P RNAs from some Archaea are catalytically active. Proc. Natl. Acad. Sci. USA. 96:1999;7803-7808.
9. Hall T.A., Brown J.W. Archaeal RNase P has multiple protein subunits homologous to eukaryotic nuclear RNase P proteins. RNA. 8:2002;296-306.
10. Crary S.M., Niranjanakumari S., Fierke C.A. The protein component of Bacillus subtilis ribonuclease P increases catalytic efficiency by enhancing interactions with the 5′ leader sequence of pre-tRNAAsp. Biochemistry. 37:1998;9409-9416.
11. Kurz J.C., Niranjanakumari S., Fierke C.A. Protein component of Bacillus subtilis RNase P specifically enhances the affinity for precursor-tRNAAsp. Biochemistry. 37:1998;2393-2400.
12. Niranjanakumari S., Stams T., Crary S.M., Christianson D.W., Fierke C.A. Protein component of the ribozyme ribonuclease P alters substrate recognition by directly contacting precursor tRNA. Proc. Natl. Acad. Sci. USA. 95:1998;15212-15217.
13. Brown J.W. The Ribonuclease P Database. Nucleic Acids Res. 27:1999;314.
14. Frank D.N., Adamidi C., Ehringer M.A., Pitulle C., Pace N.R. Phylogenetic-comparative analysis of the eukaryal ribonuclease P RNA. RNA. 6:2000;1895-1904.
15. Harris J.K., Haas E.S., Williams D., Frank D.N., Brown J.W. New insight into RNase P RNA structure from comparative analysis of the archaeal RNA. RNA. 7:2001;220-232.
16. Pan T. Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry. 34:1995;902-909.
17. Loria A., Pan T. Domain structure of the ribozyme from eubacterial ribonuclease P. RNA. 2:1996;551-563.
18. Mobley E.M., Pan T. Design and isolation of ribozyme-substrate pairs using RNase P-based ribozymes containing altered substrate binding sites. Nucleic Acids Res. 27:1999;4298-4304.
19. Pan T., Jakacka M. Multiple substrate binding sites in the ribozyme from Bacillus subtilis RNase P. EMBO J. 15:1996;2249-2255.
20. Nolan J.M., Burke D.H., Pace N.R. Circularly permuted tRNAs as specific photoaffinity probes of ribonuclease P RNA structure. Science. 261:1993;762-765.
21. LaGrandeur T.E., Huttenhofer A., Noller H.F., Pace N.R. Phylogenetic comparative chemical footprint analysis of the interaction between ribonuclease P RNA and tRNA. EMBO J. 13:1994;3945-3952.
22. Knap A.K., Wesolowski D., Altman S. Protection from chemical modification of nucleotides in complexes of M1 RNA, the catalytic subunit of RNase P from E. coli, and tRNA precursors. Biochimie. 72:1990;779-790.
23. Pan T., Loria A., Zhong K. Probing of tertiary interactions in RNA: 2′-hydroxyl-base contacts between the RNase P RNA and pre-tRNA. Proc. Natl. Acad. Sci. USA. 92:1995;12510-12514.
24. Loria A., Pan T. Recognition of the T stem-loop of a pre-tRNA substrate by the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry. 36:1997;6317-6325.
25. Kirsebom L.A., Svard S.G. Base pairing between Escherichia coli RNase P RNA and its substrate. EMBO J. 13:1994;4870-4876.
26. 2+ ions by ribonuclease P. Biochemistry. 37:1998;7277-7283.
27. Burgin A.B., Pace N.R. Mapping the active site of ribonuclease P RNA using a substrate containing a photoaffinity agent. EMBO J. 9:1990;4111-4118.
28. Christian E.L., McPheeters D.S., 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.
29. Christian E.L., Harris M.E. The track of the pre-tRNA 5′ leader in the ribonuclease P ribozyme-substrate complex. Biochemistry. 38:1999;12629-12638.
30. Kufel J., 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.
31. Loria A., Pan T. 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. 29:2001;1892-1897.
32. Vioque A., Arnez J., Altman S. Protein-RNA interactions in the RNase P holoenzyme from Escherichia coli. J. Mol. Biol. 202:1988;835-848.
33. Talbot S.J., Altman S. Gel retardation analysis of the interaction between C5 protein and M1 RNA in the formation of the ribonuclease P holoenzyme from Escherichia coli. Biochemistry. 33:1994;1399-1405.
34. Loria A., Niranjanakumari S., Fierke C.A., Pan T. Recognition of a pre-tRNA substrate by the Bacillus subtilis RNase P holoenzyme. Biochemistry. 37:1998;15466-15473.
35. Biswas R., Ledman D.W., Fox R.O., Altman S., Gopalan V. Mapping RNA-protein interactions in ribonuclease P from Escherichia coli using disulfide-linked EDTA-Fe. J. Mol. Biol. 296:2000;19-31.
36. Tsai H.Y., Masquida B., Biswas R., Westhof E., Gopalan V. Molecular modeling of the three-dimensional structure of the bacterial RNase P holoenzyme. J. Mol. Biol. 325:2003;661-675.
37. Rox C., Feltens R., Pfeiffer T., Hartmann R.K. Potential contact sites between the protein and RNA subunit in the Bacillus subtilis RNase P holoenzyme. J. Mol. Biol. 315:2002;551-560.
38. Sharkady S.M., Nolan J.M. Bacterial ribonuclease P holoenzyme crosslinking analysis reveals protein interaction sites on the RNA subunit. Nucleic Acids Res. 29:2001;3848-3856.
39. Jovanovic M., Sanchez R., Altman S., Gopalan V. Elucidation of structure-function relationships in the protein subunit of bacterial RNase P using a genetic complementation approach. Nucleic Acids Res. 30:2002;5065-5073.
40. Henkels C.H., Kurz J.C., Fierke C.A., Oas T.G. Linked folding and anion binding of the Bacillus subtilis ribonuclease P protein. Biochemistry. 40:2001;2777-2789 Initial biophysical analysis of RNase P protein structure and folding by CD and NMR reveals a structure that is intrinsically unfolded, requiring binding of anions to form the native structure. This new information impacts studies of ribonucleoprotein assembly and raises the issue of how conformational flexibility might influence function.
41. ••].
42. •], describes the unexpected formation of functional dimers of the B. subtilis holoenzyme. The authors characterize the sensitivity of dimer formation to substrate binding and provide support for the hypothesis that dimer formation contributes to the ability of the RNA subunit to undergo autolytic processing.
43. Loria A., Pan T. The 3′ substrate determinants for the catalytic efficiency of the Bacillus subtilis RNase P holoenzyme suggest autolytic processing of the RNase P RNA in vivo. RNA. 6:2000;1413-1422.
44. Hardt W.D., Warnecke J.M., Hartmann R.K. Recent approaches to probe functional groups in ribonuclease P RNA by modification interference. Mol. Biol. Rep. 22:1995;161-169.
45. Hardt W.D., Erdmann V.A., Hartmann R.K. Rp-deoxy-phosphorothioate modification interference experiments identify 2′-OH groups in RNase P RNA that are crucial to tRNA binding. RNA. 2:1996;1189-1198.
46. Heide C., Pfeiffer T., Nolan J.M., Hartmann R.K. Guanosine 2-NH2 groups of Escherichia coli RNase P RNA involved in intramolecular tertiary contacts and direct interactions with tRNA. RNA. 5:1999;102-116.
47. Siew D., Zahler N.H., Cassano A.G., Strobel S.A., Harris M.E. Identification of adenosine functional groups involved in substrate binding by the ribonuclease P ribozyme. Biochemistry. 38:1999;1873-1883.
48. Easterwood T.R., Harvey S.C. Ribonuclease P RNA: models of the 15/16 bulge from Escherichia coli and the P15 stem loop of Bacillus subtilis. RNA. 3:1997;577-585.
49. Heide C., Feltens R., Hartmann R.K. Purine N7 groups that are crucial to the interaction of Escherichia coli RNAse P RNA with tRNA. RNA. 7:2001;958-968.
50. Busch S., Kirsebom L.A., Notbohm H., Hartmann R.K. Differential role of the intermolecular base-pairs G292-C(75) and G293-C(74) in the reaction catalyzed by Escherichia coli RNase P RNA. J. Mol. Biol. 299:2000;941-951.
51. Brannvall M., Fredrik Pettersson B.M., Kirsebom L.A. The residue immediately upstream of the RNase P cleavage site is a positive determinant. Biochimie. 84:2002;693-703.
52. Zahler NH, Christian EL, Harris ME: Recognition of the pre-tRNA 5′ leader sequence by the active site of the RNase P ribozyme. RNA 2003, in press.
53. Zuleeg T., Hansen A., Pfeiffer T., Schubel H., Kreutzer R., Hartmann R.K., Limmer S. Correlation between processing efficiency for ribonuclease P minimal substrates and conformation of the nucleotide -1 at the cleavage position. Biochemistry. 40:2001;3363-3369.
54. Krasilnikov A.S., Yang X., Pan T., Mondragon A. Crystal structure of the specificity domain of ribonuclease P. Nature. 421:2003;760-764 The first description of the three-dimensional structure of a large portion of the B. subtilis RNase P RNA. In addition to the wealth of new information on RNA structure, we can now marvel at the remarkable structure formed by J11/12-J12/11, the clustering of functional groups involved in substrate binding and how phylogenetically variable elements are accommodated by the core domain structure.
55. Brannvall M., Kirsebom L.A. Metal ion cooperativity in ribozyme cleavage of RNA. Proc. Natl. Acad. Sci. USA. 98:2001;12943-12947.
56. Brannvall M., Mikkelsen N.E., Kirsebom L.A. Monitoring the structure of Escherichia coli RNase P RNA in the presence of various divalent metal ions. Nucleic Acids Res. 29:2001;1426-1432.
57. Brannvall M., Pettersson B.M., 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.
58. Harris M.E., Pace N.R. Identification of phosphates involved in catalysis by the ribozyme RNase P RNA. RNA. 1:1995;210-218.
59. Christian E.L., Kaye N.M., Harris M.E. Helix P4 is a divalent metal ion binding site in the conserved core of the ribonuclease P ribozyme. RNA. 6:2000;511-519.
60. Kaye N.M., Christian E.L., Harris M.E. NAIM and site-specific functional group modification analysis of RNase P RNA: magnesium dependent structure within the conserved P1-P4 multi-helix junction contributes to catalysis. Biochemistry. 41:2002;4533-4545.
61. Christian E.L., Kaye N.M., Harris M.E. Evidence for a polynuclear metal ion binding site in the catalytic core of the ribonuclease P ribozyme. EMBO J. 21:2002;2253-2262 Analysis of the effects of site-specific functional group modification provides evidence of a cluster of metal ion interactions in the universally conserved core of RNase P RNA.
62. Kaye N.M., Zahler N.H., Christian E.L., Harris M.E. Conservation of helical structure contributes to functional metal ion interactions in the catalytic domain of ribonuclease pRNA. J. Mol. Biol. 324:2002;429-442.
63. Schmitz M., Tinoco I. Jr. Solution structure and metal-ion binding of the P4 element from bacterial RNase P RNA. RNA. 6:2000;1212-1225.
64. Crary S.M., Kurz J.C., Fierke C.A. Specific phosphorothioate substitutions probe the active site of Bacillus subtilis ribonuclease P. RNA. 8:2002;933-947.
65. Kurz J.C., Fierke C.A. The affinity of magnesium binding sites in the Bacillus subtilis RNase P x pre-tRNA complex is enhanced by the protein subunit. Biochemistry. 41:2002;9545-9558 In an extension of the work described in [64], this paper systematically evaluates the effect of the protein subunit on the binding of different classes of metal ions important for RNase P RNA folding, substrate binding and catalysis. Evidence that the protein enhances the affinity of metal ions involved in catalysis is provided, underscoring the intimate relationship between the protein subunit and the active site of the catalytic RNA subunit.
66. Massire C., Jaeger L., Westhof E. Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. J. Mol. Biol. 279:1998;773-793.
67. Chen J.L., Nolan J.M., Harris M.E., Pace N.R. Comparative photocross-linking analysis of the tertiary structures of Escherichia coli and Bacillus subtilis RNase P RNAs. EMBO J. 17:1998;1515-1525.