Evidence that binding of C5 protein to P RNA enhances ribozyme catalysis by influencing active site metal ion affinity

RNA

Volumn 13, Issue 9, 2007, Pages 1505-1515

  Sun, Lei ^a   Harris, Michael E ^a  

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

Author keywords

Active site; Catalysis; Ribonucleoprotein; Ribozyme; RNase P

Indexed keywords

CADMIUM; COGNATE PROTEIN; GLYCINE DEHYDROGENASE (DECARBOXYLATING); MAGNESIUM ION; METAL ION; PROTEIN SUBUNIT; RIBONUCLEASE P; RIBONUCLEOPROTEIN; RIBOZYME; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONTROLLED STUDY; ESCHERICHIA COLI; HYDROLYSIS KINETICS; IONIC STRENGTH; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MODIFICATION; PROTEIN SECONDARY STRUCTURE; QUANTITATIVE ANALYSIS; THERMODYNAMICS;

BINDING SITES; CADMIUM; CATALYSIS; CATIONS, DIVALENT; ESCHERICHIA COLI PROTEINS; MAGNESIUM; METALS; PROTEIN BINDING; PROTEIN SUBUNITS; RIBONUCLEASE P; RNA, CATALYTIC;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 34548371821     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.571007     Document Type: Article

References (62)

1. Asp catalyzed by the RNA component of Bacillus subtilis ribonuclease P. Biochemistry 33: 10294-10304.
2. Asp. Biochemistry 35: 10493-10505.
3. Buck, A.H., Dalby, A.B., Poole, A.W., Kazantsev, A.V., and Pace, N.R. 2005a. Protein activation of a ribozyme: The role of bacterial RNase P protein. EMBO J. 24: 3360-3368.
4. Buck, A.H., Kazantsev, A.V., Dalby, A.B., and Pace, N.R. 2005b. Structural perspective on the activation of RNAse P RNA by protein. Nat. Struct. Mol. Biol. 12: 958-964.
5. Caprara, M.G., Chatterjee, P., Solem, A., Brady-Passerini, K.L., and Kaspar, B.J. 2007. An allosteric-feedback mechanism for protein-assisted group I intron splicing. RNA 13: 211-222.
6. Cassano, A.G., Anderson, V.E., and Harris, M.E. 2002. Evidence for direct attack by hydroxide in phosphodiester hydrolysis. J. Am. Chem. Soc. 124: 10964-10965.
7. Cassano, A.G., Anderson, V.E., and Harris, M.E. 2004. Analysis of solvent nucleophile isotope effects: Evidence for concerted mechanisms and nucleophilic activation by metal coordination in nonenzymatic and ribozyme-catalyzed phosphodiester hydrolysis. Biochemistry 43: 10547-10559.
8. 2+ coordinated to the pro-RP oxygen of the scissile bond. Biochemistry 36: 2425-2438.
9. Christian, E.L. 2002. Identification and characterization of metal ion binding by thiophilic metal ion rescue. In Handbook of RNA biochemistry (eds. R.K. Hartmann et al.), pp. 319-341. Wiley-VCH, Berlin.
10. Christian, E.L., Smith, K.M., Perera, N., and Harris, M.E. 2006. The P4 metal binding site in RNase P RNA affects active site metal affinity through substrate positioning. RNA 12: 1463-1467.
11. Cowan, J.A. 1998. Metal activation of enzymes in nucleic acid biochemistry. Chem. Rev. 98: 1067-1088.
12. Day-Storms, J.J., Niranjanakumari, S., and Fierke, C.A. 2004. Ionic interactions between PRNA and P protein in Bacillus subtilis RNase P characterized using a magnetocapture-based assay. RNA 10: 1595-1608.
13. DeRose, V.J. 2003. Metal ion binding to catalytic RNA molecules. Curr. Opin. Struct. Biol. 13: 317-324.
14. Draper, D.E., Grilley, D., and Soto, A.M. 2005. Ions and RNA folding. Annu. Rev. Biophys. Biomol. Struct. 34: 221-243.
15. Egea, P.F., Stroud, R.M., and Walter, P. 2005. Targeting proteins to membranes: Structure of the signal recognition particle. Curr. Opin. Struct. Biol. 15: 213-220.
16. Evans, D., Marquez, S.M., and Pace, N.R. 2006. RNase P: Interface of the RNA and protein worlds. Trends Biochem. Sci. 31: 333-341.
17. Phe and the catalytic domain of the B. subtilis RNase P RNA determined by small-angle X-ray scattering. Biochemistry 39: 11107-11113.
18. Farruggia, G., Iotti, S., Prodi, L., Montalti, M., Zaccheroni, N., Savage, P.B., Trapani, V., Sale, P., and Wolf, F.I. 2005. 8-Hydroxyquinoline derivatives as fluorescent sensors for magnesium in living cells. J. Am. Chem. Soc. 128: 344-350.
19. Frank, D.N. and Pace, N.R. 1997. In vitro selection for altered divalent metal specificity in the RNase P RNA. Proc. Natl. Acad. Sci. 94: 14355-14360.
20. Froschauer, E.M., Kolisek, M., Dieterich, F., Schweigel, M., and Schweyen, J.J. 2004. Fluorescence measurements of free (Mg) by use of mag-fura 2 in Salmonella enterica. FEMS Microbiol. Lett. 237: 49-55.
21. Gordon, P.M. and Piccirilli, J.A. 2001. Metal ion coordination by the AGC triad in domain 5 contributes to group II intron catalysis. Nat. Struct. Biol. 8: 893-898.
22. Guo, X., Campbell, F.E., Sun, L., Christian, E.L., Anderson, V.E., and Harris, M.E. 2006. RNA-dependent folding and stabilization of C5 protein during assembly of the E. coli RNase P holoenzyme. J. Mol. Biol. 360: 190-203.
23. Haas, E.S. and Brown, J.W. 1998. Evolutionary variation in bacterial RNase P RNAs. Nucleic Acids Res. 26: 4093-4099.
24. Haas, E.S., Brown, J.W., Pitulle, C., and Pace, N.R. 1994. Further perspective on the catalytic core and secondary structure of ribonuclease P RNA. Proc. Natl. Acad. Sci. 91: 2527-2531.
25. Ho, Y. and Waring, R.B. 1999. The maturase encoded by a group I intron from Aspergillus nidulans stabilizes RNA tertiary structure and promotes rapid splicing. J. Mol. Biol. 292: 987-1001.
26. Hopper, A.K. 2006. Cellular dynamics of small RNAs. Crit. Rev. Biochem. Mol. Biol. 41: 3-19.
27. Hougland, J.L., Kravchuk, A.V., Herschlag, D., and Piccirilli, J.A. 2005. Functional identification of catalytic metal ion binding sites within RNA. PLoS Biol. 3: e277.
28. Hsieh, J., Andrews, A.J., and Fierke, C.A. 2004. Roles of protein subunits in RNA-protein complexes: Lessons from ribonuclease P. Biopolymers 73: 79-89.
29. Jankowsky, E. and Bowers, H. 2006. Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res. 34: 4181-4188.
30. Jovanovic, M., Sanchez, R., Altman, S., and Gopalan, V. 2002. Elucidation of structure-function relationships in the protein subunit of bacterial RNase P using a genetic complementation approach. Nucleic Acids Res. 30: 5065-5073.
31. Kazantsev, A.V. and Pace, N.R. 2006. Bacterial RNase P: A new view of an ancient enzyme. Nat. Rev. Microbiol. 4: 729-740.
32. Kent, O., Chaulk, S.G., and MacMillan, A.M. 2000. Kinetic analysis of the M1 RNA folding pathway. J. Mol. Biol. 304: 699-705.
33. Kurz, J.C. and Fierke, C.A. 2000. Ribonuclease P: A ribonucleoprotein enzyme. Curr. Opin. Chem. Biol. 4: 553-558.
34. Kurz, J.C. and Fierke, C.A. 2002. The affinity of magnesium binding sites in the Bacillus subtilis RNase P x pre-tRNA complex is enhanced by the protein subunit. Biochemistry 41: 9545-9558.
35. Lambowitz, A.M. and Zimmerly, S. 2004. Mobile group II introns. Annu. Rev. Genet. 38: 1-35.
36. Lehman, N. and Joyce, G.F. 1993. Evolution in vitro of an RNA enzyme with altered metal dependence. Nature 361: 182-185.
37. Loria, A. and Pan, T. 1999. The cleavage step of ribonuclease P catalysis is determined by ribozyme-substrate interactions both distal and proximal to the cleavage site. Biochemistry 38: 8612-8620.
38. Loria, A., Niranjanakumari, S., Fierke, C.A., and Pan, T. 1998. Recognition of a pre-tRNA substrate by the Bacillus subtilis RNase P holoenzyme. Biochemistry 37: 15466-15473.
39. Nelson, J.A., Shepotinovskaya, I., and Uhlenbeck, O.C. 2005. Hammerheads derived from sTRSV show enhanced cleavage and ligation rate constants. Biochemistry 44: 14577-14585.
40. 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. 95: 15212-15217.
41. Pan, T. and 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. Nat. Struct. Biol. 4: 931-938.
42. 2+ complexes of adenine nucleotides and thionucleotides and rate constants for formation and dissociation of MgATP and MgADP. Biochemistry 23: 5262-5271.
43. Peracchi, A., Beigelman, L., Scott, E.C., Uhlenbeck, O.C., and Herschlag, D. 1997. Involvement of a specific metal ion in the transition of the hammerhead ribozyme to its catalytic conformation. J. Biol. Chem. 272: 26822-26826.
44. Persson, T., Cuzic, S., and Hartmann, R.K. 2003. Catalysis by RNase P RNA: Unique features and unprecedented active site plasticity. J. Biol. Chem. 278: 43394-43401.
45. Piccirilli, J.A., Vyle, J.S., Caruthers, M.H., and Cech, T.R. 1993. Metal ion catalysis in the Tetrahymena ribozyme reaction. Nature 361: 85-88.
46. Roychowdhury-Saha, M. and Burke, D.H. 2006. Extraordinary rates of transition metal ion-mediated ribozyme catalysis. RNA 12: 1846-1852.
47. Shan, S.O. and Herschlag, D. 2002. Dissection of a metal-ionmediated conformational change in Tetrahymena ribozyme catalysis. RNA 8: 861-872.
48. Shan, S., Yoshida, A., Sun, S., Piccirilli, J.A., and Herschlag, D. 1999. Three metal ions at the active site of the Tetrahymena group I ribozyme. Proc. Natl. Acad. Sci. 96: 12299-12304.
49. Shan, S., Kravchuk, A.V., Piccirilli, J.A., and Herschlag, D. 2001. Defining the catalytic metal ion interactions in the Tetrahymena ribozyme reaction. Biochemistry 40: 5161-5171.
50. Smith, D. and Pace, N.R. 1993. Multiple magnesium ions in the ribonuclease P reaction mechanism. Biochemistry 32: 5273-5281.
51. Smith, D., Burgin, A.B., Haas, E.S., and Pace, N.R. 1992. Influence of metal ions on the ribonuclease P reaction. Distinguishing substrate binding from catalysis. J. Biol. Chem. 267: 2429-2436.
52. Stahley, M.R. and Strobel, S.A. 2005. Structural evidence for a two-metal-ion mechanism of group I intron splicing. Science 309: 1587-1590.
53. Stahley, M.R. and Strobel, S.A. 2006. RNA splicing: Group I intron crystal structures reveal the basis of splice site selection and metal ion catalysis. Curr. Opin. Struct. Biol. 16: 319-326.
54. Steitz, T.A. and Steitz, J.A. 1993. A general two-metal-ion mechanism for catalytic RNA. Proc. Natl. Acad. Sci. 90: 6498-6502.
55. Stoddard, B.L. 2006. Homing endonuclease structure and function. Q. Rev. Biophys. 38: 49-95.
56. Sun, L., Campbell, 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.
57. Tinsley, R.A., Harris, D.A., and Walter, N.G. 2004. Magnesium dependence of the amplified conformational switch in the trans-acting hepatitis delta virus ribozyme. Biochemistry 43: 8935-8945.
58. Torres-Larios, A., Swinger, K.K., Krasilnikov, A.S., Pan, T., and Mondragon, A. 2005. Crystal structure of the RNA component of bacterial ribonuclease P. Nature 437: 584-587.
59. 2+ ribozyme by a single Rp-phosphorothioate modification in the precursor tRNA at the RNase P cleavage site. Proc. Natl. Acad. Sci. 93: 8924-8928.
60. Weeks, K.M. and Cech, T.R. 1995. Protein facilitation of group I intron splicing by assembly of the catalytic core and the 5′-splicesite domain. Cell 82: 221-230.
61. Zahler, N.H., Sun, L., Christian, E.L., and Harris, M.E. 2005. The pre-tRNA nucleotide base and 2′-hydroxyl at N(-1) contribute to fidelity in tRNA processing by RNase P. J. Mol. Biol. 345: 969-985.
62. Zarrinkar, P.P., Wang, J., and Williamson, J.R. 1996. Slow folding kinetics of RNase P RNA. RNA 2: 564-573.