Conservation of helical structure contributes to functional metal ion interactions in the catalytic domain of ribonuclease P RNA

Journal of Molecular Biology

Volumn 324, Issue 3, 2002, Pages 429-442

  Kaye, Nicholas M ^a   Zahler, Nathan H ^a   Christian, Eric L ^a   Harris, Michael E ^a  

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

Author keywords

Metal ion; Ribonuclease P; Ribozyme; RNA structure; Terbium

Indexed keywords

MAGNESIUM ION; METAL ION; RIBONUCLEASE P; RIBOZYME; RNA; TERBIUM;

ARTICLE; BINDING SITE; CATALYSIS; CHEMICAL INTERACTION; CRYSTAL STRUCTURE; DISSOCIATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; MUTATION; PRIORITY JOURNAL; TITRIMETRY;

EID: 0036445585     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01094-X     Document Type: Article

References (80)

1. Kurz, J. C. & Fierke, C. A. (2000). Ribonuclease P: A ribonucleoprotein enzyme. Curr. Opin. Chem. Biol. 4, 553-558.
2. Frank, D. N. & Pace, N. R. (1998). Ribonuclease P: Unity and diversity in a tRNA processing ribozyme. Annu. Rev. Biochem. 67, 153-180.
3. Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N. & Altman, S. (1983). The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell, 35, 849-857.
4. Pannucci, J. A., Haas, E. S., Hall, T. A., Harris, J. K. & Brown, J. W. (1999). RNase P RNAs from some Archaea are catalytically active. Proc. Natl. Acad. Sci. USA, 96, 7803-7808.
5. Darr, S. C., Pace, B. & Pace, N. R. (1990). Characterization of ribonuclease P from the archaebacterium Sulfolobus solfataricus. J. Biol. Chem. 265, 12927-12932.
6. Brown, J. W. & Haas, E. S. (1995). Ribonuclease P structure and function in Archaea. Mol. Biol. Rep. 22, 131-134.
7. Xiao, S., Houser-Scott, F. & Engelke, D. R. (2001). Eukaryotic ribonuclease P: Increased complexity to cope with the nuclear pre-tRNA pathway. J. Cell. Physiol. 187, 11-20.
8. Haas, E. S., Armbruster, D. W., Vucson, B. M., Daniels, C. J. & Brown, J. W. (1996). Comparative analysis of ribonuclease P RNA structure in Archaea. Nucl. Acids Res. 24, 1252-1259.
9. Frank, D. N., Adamidi, C., Ehringer, M. A., Pitulle, C. & Pace, N. R. (2000). Phylogenetic-comparative analysis of the eukaryal ribonuclease P RNA. RNA, 6, 1895-1904.
10. Harris, J. K., Haas, E. S., Williams, D., Frank, D. N. & Brown, J. W. (2001). New insight into RNase P RNA structure from comparative analysis of the archaeal RNA. RNA, 7, 220-232.
11. Chen, J. L. & Pace, N. R. (1997). Identification of the universally conserved core of ribonuclease P RNA. RNA, 3, 557-560.
12. Brown, J. W. (1999). The ribonuclease P database. Nucl. Acids Res. 27, 314.
13. Schmitt, M. E., Bennett, J. L., Dairaghi, D. J. & Clayton, D. A. (1993). Secondary structure of RNase MRP RNA as predicted by phylogenetic comparison. FASEB J. 7, 208-213.
14. Reilly, T. H. & Schmitt, M. E. (1995). The yeast Saccharomyces cerevisiae, RNase P/MRP ribonucleo-protein endoribonuclease family. Mol. Biol. Rep. 22, 87-93.
15. Reddy, R. & Shimba, S. (1995). Structural and functional similarities between MRP and RNase P. Mol. Biol. Rep. 22, 81-85.
16. Collins, L. J., Moulton, V. & Penny, D. (2000). Use of RNA secondary structure for studying the evolution of RNase P and RNase MRP. J. Mol. Evol. 51, 194-204.
17. Hardt, W. D., Warnecke, J. M., Erdmann, V. A. & Hartmann, R. K. (1995). Rp-phosphorothioate modifications in RNase P RNA that interfere with tRNA binding. EMBO J. 14, 2935-2944.
18. Frank, D. N., Ellington, A. E. & Pace, N. R. (1996). In vitro selection of RNase P RNA reveals optimized catalytic activity in a highly conserved structural domain. RNA, 2, 1179-1188.
19. Siew, D., Zahler, N. H., Cassano, A. G., Strobel, S. A. & Harris, M. E. (1999). Identification of adenosine functional groups involved in substrate binding by the ribonuclease P ribozyme. Biochemistry, 38, 1873-1883.
20. Christian, E. L., Kaye, N. M. & Harris, M. E. (2000). Helix P4 is a divalent metal ion binding site in the conserved core of the ribonuclease P ribozyme. RNA, 6, 511-519.
21. Kaye, N. M., Christian, E. I. & Harris, M. E. (2002). 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. In press.
22. Christian, E. L., McPheeters, D. S. & Harris, M. E. (1998). 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, 17618-17628.
23. Christian, E. L. & Harris, M. E. (1999). The track of the pre-tRNA 5′ leader in the ribonuclease P ribozyme-substrate complex. Biochemistry, 38, 12629-12638.
24. Kufel, J. & 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.
25. Harris, M. E. & Pace, N. R. (1995). Identification of phosphates involved in catalysis by the ribozyme RNase P RNA. RNA, 1, 210-218.
26. Kazantsev, A. V. & Pace, N. R. (1998). Identification by modification-interference of purine N-7 and ribose 2′-OH groups critical for catalysis by bacterial ribonuclease P. RNA, 4, 937-947.
27. Frank, D. N. & Pace, N. R. (1997). In vitro selection for altered divalent metal specificity in the RNase P RNA. Proc. Natl. Acad. Sci. USA, 94, 14355-14360.
28. Schmitz, M. & Tinoco, I., Jr (2000). Solution structure and metal-ion binding of the P4 element from bacterial RNase P RNA. RNA, 6, 1212-1225.
29. Christian, E. L., Kaye, N. M. & Harris, M. E. (2002). Evidence for a polynuclear metal ion binding site in the catalytic domain of ribonuclease P RNA. EMBO J. 21, 2253-2262.
30. Hargittai, M. R. & Musier-Forsyth, K. (2000). Use of terbium as a probe of tRNA tertiary structure and folding. RNA, 6, 1672-1680.
31. Sigel, R. K., Vaidya, A. & Pyle, A. M. (2000). Metal ion binding sites in a group II intron core. Nature Struct. Biol. 7, 1111-1116.
32. Vaidya, A. & Suga, H. (2001). Diverse roles of metal ions in acyl-transferase ribozymes. Biochemistry, 40, 7200-7210.
33. Walter, N. G., Yang, N. & Burke, J. M. (2000). Probing non-selective cation binding in the hairpin ribozyme with Tb(III). J. Mol. Biol. 298, 539-555.
34. Misra, V. K. & Draper, D. E. (1998). On the role of magnesium ions in RNA stability. Biopolymers, 48, 113-135.
35. Bukhman, Y. V. & Draper, D. E. (1997). Affinities and selectivities of divalent cation binding sites within an RNA tertiary structure. J. Mol. Biol. 273, 1020-1031.
36. Zarrinkar, P. P., Wang, J. & Williamson, J. R. (1996). Slow folding kinetics of RNase P RNA. RNA, 2, 564-573.
37. Loria, A. & Pan, T. (1996). Domain structure of the ribozyme from eubacterial ribonuclease P. RNA, 2, 551-563.
38. Pan, T. & Sosnick, T. R. (1997). Intermediates and kinetic traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nature Struct. Biol. 4, 931-938.
39. Kent, O., Chaulk, S. G. & MacMillan, A. M. (2000). Kinetic analysis of the M1 RNA folding pathway. J. Mol. Biol. 304, 699-705.
40. Guerrier-Takada, C., Haydock, K., Allen, L. & Altman, S. (1986). Metal ion requirements and other aspects of the reaction catalyzed by M1 RNA, the RNA subunit of ribonuclease P from Escherichia coli. Biochemistry, 25, 1509-1515.
41. Smith, D., Burgin, A. B., Haas, E. S. & Pace, N. R. (1992). Influence of metal ions on the ribonuclease P reaction. Distinguishing substrate binding from catalysis. J. Biol. Chem. 267, 2429-2436.
42. Pan, T. (1995). Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry, 34, 902-909.
43. Beebe, J. A., Kurz, J. C. & Fierke, C. A. (1996). Magnesium ions are required by Bacillus subtilis ribonuclease P RNA for both binding and cleaving precursor tRNAAsp. Biochemistry, 35, 10493-10505.
44. Brannvall, M. & Kirsebom, L. A. (2001). Metal ion cooperativity in ribozyme cleavage of RNA. Proc. Natl. Acad. Sci. USA, 98, 12943-12947.
45. Brannvall, M., Mikkelsen, N. E. & Kirsebom, L. A. (2001). Monitoring the structure of Escherichia coli RNase P RNA in the presence of various divalent metal ions. Nucl. Acids Res. 29, 1426-1432.
46. Perreault, J. P. & Altman, S. (1993). Pathway of activation by magnesium ions of substrates for the catalytic subunit of RNase P from Escherichia coli. J. Mol. Biol. 230, 750-756.
47. Smith, D. & Pace, N. R. (1993). Multiple magnesium ions in the ribonuclease P reaction mechanism. Biochemistry, 32, 5273-5281.
48. Warnecke, J. M., Held, R., Busch, S. & Hartmann, R. K. (1999). Role of metal ions in the hydrolysis reaction catalyzed by RNase P RNA from Bacillus subtilis. J. Mol. Biol. 290, 433-445.
49. James, B. D., Olsen, G. J., Liu, J. S. & Pace, N. R. (1988). The secondary structure of ribonuclease P RNA, the catalytic element of a ribonucleoprotein enzyme. Cell, 52, 19-26.
50. Brown, J. W. et al. (1996). Comparative analysis of ribonuclease P RNA using gene sequences from natural microbial populations reveals tertiary structural elements. Proc. Natl. Acad. Sci. USA, 93, 3001-3006.
51. Pace, N. R. & Waugh, D. S. (1991). Design of simplified ribonuclease P RNA by phylogenetic comparison. Methods Enzymol. 203, 500-510.
52. Siegel, R. W., Banta, A. B., Haas, E. S., Brown, J. W. & Pace, N. R. (1996). Mycoplasma fermentans simplifies our view of the catalytic core of ribonuclease P RNA. RNA, 2, 452-462.
53. Cate, J. H. et al. (1996). Crystal structure of a group I ribozyme domain: Principles of RNA packing. Science, 273, 1678-1685.
54. Golden, B. L., Gooding, A. R., Podell, E. R. & Cech, T. R. (1998). A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science, 282, 259-264.
55. Ortoleva-Donnelly, L., Szewczak, A. A., Gutell, R. R. & Strobel, S. A. (1998). The chemical basis of adenosine conservation throughout the Tetrahymena ribozyme. RNA, 4, 498-519.
56. Strobel, S. A., Ortoleva-Donnelly, L., Ryder, S. P., Cate, J. H. & Moncoeur, E. (1998). Complementary sets of noncanonical base pairs mediate RNA helix packing in the group I intron active site. Nature Struct. Biol. 5, 60-66.
57. Szewczak, A. A., Ortoleva-Donnelly, L., Ryder, S. P., Moncoeur, E. & Strobel, S. A. (1998). A minor groove RNA triple helix within the catalytic core of a group I intron. Nature Struct. Biol. 5, 1037-1042.
58. Cate, J. H. & Doudna, J. A. (1996). Metal-binding sites in the major groove of a large ribozyme domain. Structure, 4, 1221-1229.
59. Zito, K., Huttenhofer, A. & Pace, N. R. (1993). Lead-catalyzed cleavage of ribonuclease P RNA as a probe for integrity of tertiary structure. Nucl. Acids Res. 21, 5916-5920.
60. Ciesiolka, J., Hardt, W. D., Schlegl, J., Erdmann, V. A. & Hartmann, R. K. (1994). Lead-ion-induced cleavage of RNase P RNA. Eur. J. Biochem. 219, 49-56.
61. Hardt, W. D. & Hartmann, R. K. (1996). Mutational analysis of the joining regions flanking helix P18 in E. coli RNase P RNA. J. Mol. Biol. 259, 422-433.
62. Heide, C., Pfeiffer, T., Nolan, J. M. & Hartmann, R. K. (1999). Guanosine 2-NH2 groups of Escherichia coli RNase P RNA involved in intramolecular tertiary contacts and direct interactions with tRNA. RNA, 5, 102-116.
63. Celander, D. W. & Cech, T. R. (1991). Visualizing the higher order folding of a catalytic RNA molecule. Science, 251, 401-407.
64. Heuer, T. S., Chandry, P. S., Belfort, M., Celander, D. W. & Cech, T. R. (1991). Folding of group I introns from bacteriophage T4 involves internalization of the catalytic core. Proc. Natl. Acad. Sci. USA, 88, 11105-11109.
65. Swisher, J., Duarte, C. M., Su, L. J. & Pyle, A. M. (2001). Visualizing the solvent-inaccessible core of a group II intron ribozyme. EMBO J. 20, 2051-2061.
66. Wedekind, J. E. & McKay, D. B. (1999). Crystal structure of a lead-dependent ribozyme revealing metal binding sites relevant to catalysis. Nature Struct. Biol. 6, 261-268.
67. Ippolito, J. A. & Steitz, T. A. (1998). A 1.3 Å resolution crystal structure of the HIV-1 trans-activation response region RNA stem reveals a metal ion-dependent bulge conformation. Proc. Natl. Acad. Sci. USA, 95, 9819-9824.
68. Xiong, Y. & Sundaralingam, M. (2000). Two crystal forms of helix II of Xenopus laevis 5 S rRNA with a cytosine bulge. RNA, 6, 1316-1324.
69. Konforti, B. B. et al. (1998). Ribozyme catalysis from the major groove of group II intron domain 5. Mol. Cell, 1, 433-441.
70. Gordon, P. M. & Piccirilli, J. A. (2001). Metal ion coordination by the AGC triad in domain 5 contributes to group II intron catalysis. Nature Struct. Biol. 8, 893-898.
71. Christian, E. L. & Yarus, M. (1993). Metal coordination sites that contribute to structure and catalysis in the group I intron from Tetrahymena. Biochemistry, 32, 4475-4480.
72. Szewczak, A. A., Kosek, A. B., Piccirilli, J. A. & Strobel, S. A. (2002). Identification of an active site ligand for a group I ribozyme catalytic metal ion. Biochemistry, 41, 2516-2525.
73. Madhani, H. D. & Guthrie, C. (1992). A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell, 71, 803-817.
74. Costa, M., Christian, E. L. & Michel, F. (1998). Differential chemical probing of a group II self-splicing intron identifies bases involved in tertiary interactions and supports an alternative secondary structure model of domain V. RNA, 4, 1055-1068.
75. Yean, S. L., Wuenschell, G., Termini, J. & Lin, R. J. (2000). Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature, 408, 881-884.
76. Dulau, L., Cheyrou, A., Dubourdieu, D. & Aigle, M. (1989). Directed mutagenesis using PCR. Nucl. Acids Res. 17, 2873.
77. Beebe, J. A. & Fierke, C. A. (1994). A kinetic mechanism for cleavage of precursor tRNA(Asp) catalyzed by the RNA component of Bacillus subtilis ribonuclease P. Biochemistry, 33, 10294-10304.
78. Hardt, W. D., Schlegl, J., Erdmann, V. A. & Hartmann, R. K. (1993). Gel retardation analysis of E. coli M1 RNA-tRNA complexes. Nucl. Acids Res. 21, 3521-3527.
79. Massire, C., Jaeger, L. & Westhof, E. (1998). Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. J. Mol. Biol. 279, 773-793.
80. Chen, J. L., Nolan, J. M., Harris, M. E. & Pace, N. R. (1998). Comparative photocross-linking analysis of the tertiary structures of Escherichia coli and Bacillus subtilis RNase P RNAs. EMBO J. 17, 1515-1525.