Skip to main content Accessibility help
×
Home

Folding of a universal ribozyme: the ribonuclease P RNA

  • Nathan J. Baird (a1) (a2), Xing-Wang Fang (a3), Narayanan Srividya (a3), Tao Pan (a3) and Tobin R. Sosnick (a2) (a3)...

Abstract

Ribonuclease P is among the first ribozymes discovered, and is the only ubiquitously occurring ribozyme besides the ribosome. The bacterial RNase P RNA is catalytically active without its protein subunit and has been studied for over two decades as a model system for RNA catalysis, structure and folding. This review focuses on the thermodynamic, kinetic and structural frameworks derived from the folding studies of bacterial RNase P RNA.

Copyright

Corresponding author

*Correspondence may be addressed to either T. Sosnick or T. Pan at: 929 E. 57th St., Chicago, IL 60637, USA.
Tel.: (773) 218-5950; Fax: (773) 702-0439; Email: trsosnic@uchicago.edu
Tel.: (773) 702-4179; Fax: (773) 702-0439; Email: taopan@uchicago.edu

References

Hide All
Abkevich, V. I., Gutin, A. M. & Shakhnovich, E. I. (1994). Specific nucleus as the transition state for protein folding: evidence from the lattice model. Biochemistry 33, 1002610036.
Altman, S. & Kirsebom, L. (1999). Ribonuclease P. In The RNA World, Second Edition (eds Gesteland, R. F., Cech, T. R. and Atkins, J. F.), pp. 351380. New York: Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
Baird, N. J., Srividya, N., Krasilnikov, A. S., Mondragon, A., Sosnick, T. R. & Pan, T. (2006). Structural basis for altering the stability of homologous RNAs from a mesophilic and a thermophilic bacterium. RNA 12, 598606.
Baird, N. J., Westhof, E., Qin, H., Pan, T. & Sosnick, T. R. (2005). Structure of a folding intermediate reveals the interplay between core and peripheral elements in RNA folding. Journal of Molecular Biology 352, 712722.
Ban, N., Nissen, P., Hansen, J., Moore, P. B. & Steitz, T. A. (2000). The complete atomic structure of the large ribosomal subunit at 2·4 A resolution. Science 289, 905920.
Bartley, L. E., Zhuang, X., Das, R., Chu, S. & Herschlag, D. (2003). Exploration of the transition state for tertiary structure formation between an RNA helix and a large structured RNA. Journal of Molecular Biology 328, 10111026.
Bassi, G. S., Murchie, A. I., Walter, F., Clegg, R. M. & Lilley, D. M. (1997). Ion-induced folding of the hammerhead ribozyme: a fluorescence resonance energy transfer study. EMBO Journal 16, 74817489.
Bertone, P., Stolc, V., Royce, T. E., Rozowsky, J. S., Urban, A. E., Zhu, X., Rinn, J. L., Tongprasit, W., Samanta, M., Weissman, S. et al. (2004). Global identification of human transcribed sequences with genome tiling arrays. Science 306, 22422246.
Bokinsky, G., Rueda, D., Misra, V. K., Rhodes, M. M., Gordus, A., Babcock, H. P., Walter, N. G. & Zhuang, X. (2003). Single-molecule transition-state analysis of RNA folding. Proceedings of the National Academy of Sciences USA 100, 93029307.
Brown, J. W. (1999). The Ribonuclease P Database. Nucleic Acids Research 27, 314.
Brown, J. W., Haas, E. S. & Pace, N. R. (1993). Characterization of ribonuclease P RNAs from thermophilic bacteria. Nucleic Acids Research 21, 671679.
Cantor, C. & Schimmel, P. (1980). Biophysical Chemistry: Part II. New York: W. H. Freeman and Co.
Cate, J. H., Hanna, R. L. & Doudna, J. A. (1997). A magnesium ion core at the heart of a ribozyme domain. Nature Structural Biology 4, 553558.
Celander, D. W. & Cech, T. R. (1991). Visualizing the higher order folding of a catalytic RNA molecule. Science 251, 401407.
Cheng, J., Kapranov, P., Drenkow, J., Dike, S., Brubaker, S., Patel, S., Long, J., Stern, D., Tammana, H., Helt, G. et al. (2005). Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308, 11491154.
Chin, K., Sharp, K. A., Honig, B. & Pyle, A. M. (1999). Calculating the electrostatic properties of RNA provides new insights into molecular interactions and function. Nature Structural Biology 6, 10551061.
Das, R., Travers, K. J., Bai, Y. & Herschlag, D. (2005). Determining the Mg2+ stoichiometry for folding an RNA metal ion core. Journal of the American Chemical Society 127, 82728273.
Doherty, E. A. & Doudna, J. A. (1997). The P4-P6 domain directs higher order folding of the Tetrahymena ribozyme core. Biochemistry 36, 31593169.
Draper, D. E., Grilley, D. & Soto, A. M. (2005). Ions and RNA folding. Annual Review of Biophysics and Biomolecular Structures 34, 221243.
Ehresmann, C., Baudin, F., Mougel, M., Romby, P., Ebel, J. P. & Ehresmann, B. (1987). Probing the structure of RNAs in solution. Nucleic Acids Research 15, 91099128.
Fang, X., Littrell, K., Yang, X., Henderson, S. J., Siefert, S., Thiyagarajan, P., Pan, T. & Sosnick, T. R. (2000). Mg2+-dependent compaction and folding of yeast tRNA(Phe) and the catalytic domain of the B. subtilis RNase P RNA determined by small-angle X-ray scattering. Biochemistry 39, 1110711113.
Fang, X., Pan, T. & Sosnick, T. R. (1999a). Mg2+-dependent folding of a large ribozyme without kinetic traps. Nature Structural Biology 6, 10911095.
Fang, X., Pan, T. & Sosnick, T. R. (1999b). A thermodynamic framework and cooperativity in the tertiary folding of a Mg2+-dependent ribozyme. Biochemistry 38, 1684016846.
Fang, X. W., Golden, B. L., Littrell, K., Shelton, V., Thiyagarajan, P., Pan, T. & Sosnick, T. R. (2001). The thermodynamic origin of the stability of a thermophilic ribozyme. Proceedings of the National Academy of Sciences USA 98, 43554360.
Fang, X. W., Thiyagarajan, P., Sosnick, T. R. & Pan, T. (2002). The rate-limiting step in the folding of a large ribozyme without kinetic traps. Proceedings of the National Academy of Sciences USA 99, 85188523.
Feng, H., Vu, N. D., Zhou, Z. & Bai, Y. (2004). Structural examination of Phi value analysis in protein folding. Biochemistry 43, 1432514331.
Fenley, M. O., Manning, G. S. & Olson, W. K. (1990). Approach to the limit of counterion condensation. Biopolymers 30, 11911203.
Ferre-D'Amare, A. R., Zhou, K. & Doudna, J. A. (1998). Crystal structure of a hepatitis delta virus ribozyme. Nature 395, 567574.
Fersht, A. R., Matouschek, A. & Serrano, L. (1992). The folding of an enzyme. I. Theory of protein engineering analysis of stability and pathway of protein folding. Journal of Molecular Biology 224, 771782.
Frank, D. N. & Pace, N. R. (1998). Ribonuclease P: unity and diversity in a tRNA processing ribozyme. Annual Review of Biochemistry 67, 153180.
Galtier, N. & Lobry, J. R. (1997). Relationships between genomic G+C content, RNA secondary structures, and optimal growth temperature in prokaryotes. Journal of Molecular Evolution 44, 632636.
Goldenberg, D. P. (1992). Mutational analysis of protein folding and stability. In Protein Folding (ed. Creighton, T. E.), pp. 353403. New York: W. H. Freeman.
Gray, D. M., Hung, S. H. & Johnson, K. H. (1995). Absorption and circular dichroism spectroscopy of nucleic acid duplexes and triplexes. Methods in Enzymology 246, 1934.
Guo, F. & Cech, T. R. (2002). Evolution of Tetrahymena ribozyme mutants with increased structural stability. Nature Structural Biology 9, 855861.
Guo, Z. Y. & Thirumalai, D. (1995). Kinetics of protein-folding: nucleation mechanism, time scales, and pathways. Biopolymers 36, 83102.
Ha, T., Zhuang, X., Kim, H. D., Orr, J. W., Williamson, J. R. & Chu, S. (1999). Ligand-induced conformational changes observed in single RNA molecules. Proceedings of the National Academy of Sciences USA 96, 90779082.
Heilman-Miller, S. L., Thirumalai, D. & Woodson, S. A. (2001). Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations. Journal of Molecular Biology 306, 11571166.
Heilman-Miller, S. L. & Woodson, S. A. (2003). Perturbed folding kinetics of circularly permuted RNAs with altered topology. Journal of Molecular Biology 328, 385394.
Helm, L. & Hertz, H. G. (1981). The hydration of the alkaline earth metal ions Mg2+, Ca2+, Sr2+ and Ba2+, a nuclear magnetic relaxation study involving the quadrupole moment of the ionic nuclei. Zeitschrift für Physikalische Chemie 127, 2344.
Hermann, T. & Westhof, E. (1998). Exploration of metal ion binding sites in RNA folds by Brownian-dynamics simulations. Structure 6, 13031314.
Jovine, L., Djordjevic, S. & Rhodes, D. (2000). The crystal structure of yeast phenylalanine tRNA at 2·0 A resolution: cleavage by Mg2+ in 15-year-old crystals. Journal of Molecular Biology 301, 401414.
Kapranov, P., Cawley, S. E., Drenkow, J., Bekiranov, S., Strausberg, R. L., Fodor, S. P. & Gingeras, T. R. (2002). Large-scale transcriptional activity in chromosomes 21 and 22. Science 296, 916919.
Kazantsev, A. V., Krivenko, A. A., Harrington, D. J., Holbrook, S. R., Adams, P. D. & Pace, N. R. (2005). Crystal structure of a bacterial ribonuclease P RNA. Proceedings of the National Academy of Sciences USA 102, 1339213397.
Kent, O., Chaulk, S. G. & MacMillan, A. M. (2000). Kinetic analysis of the M1 RNA folding pathway. Journal of Molecular Biology 304, 699705.
Kim, H. D., Nienhaus, G. U., Ha, T., Orr, J. W., Williamson, J. R. & Chu, S. (2002). Mg2+-dependent conformational change of RNA studied by fluorescence correlation and FRET on immobilized single molecules. Proceedings of the National Academy of Sciences USA 99, 42844289.
Klein, D. J., Moore, P. B. & Steitz, T. A. (2004). The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA 10, 13661379.
Kowalak, J. A., Dalluge, J. J., McCloskey, J. A. & Stetter, K. O. (1994). The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry 33, 78697876.
Krantz, B. A., Dothager, R. S. & Sosnick, T. R. (2004). Discerning the structure and energy of multiple transition states in protein folding using psi-analysis. Journal of Molecular Biology 337, 463475.
Krantz, B. A., Moran, L. B., Kentsis, A. & Sosnick, T. R. (2000). D/H amide kinetic isotope effects reveal when hydrogen bonds form during protein folding. Nature Structural Biology 7, 6271.
Krantz, B. A. & Sosnick, T. R. (2001). Engineered metal binding sites map the heterogeneous folding landscape of a coiled coil. Nature Structural Biology 8, 10421047.
Krantz, B. A., Srivastava, A. K., Nauli, S., Baker, D., Sauer, R. T. & Sosnick, T. R. (2002). Understanding protein hydrogen bond formation with kinetic H/D amide isotope effects. Nature Structural Biology 9, 458463.
Krasilnikov, A. S., Xiao, Y., Pan, T. & Mondragon, A. (2004). Basis for structural diversity in homologous RNAs. Science 306, 104107.
Krasilnikov, A. S., Yang, X., Pan, T. & Mondragon, A. (2003). Crystal structure of the specificity domain of ribonuclease P. Nature 421, 760764.
Laing, L. G., Gluick, T. C. & Draper, D. E. (1994). Stabilization of RNA structure by Mg ions. Specific and non-specific effects. Journal of Molecular Biology 237, 577587.
Latham, J. A. & Cech, T. R. (1989). Defining the inside and outside of a catalytic RNA molecule. Science 245, 276282.
Liphardt, J., Onoa, B., Smith, S. B., Tinoco, I. J. & Bustamante, C. (2001). Reversible unfolding of single RNA molecules by mechanical force. Science 292, 733737.
Loria, A. & Pan, T. (1996). Domain structure of the ribozyme from eubacterial ribonuclease P. RNA 2, 551563.
Manning, G. S. (1978). Limiting laws and counterion condensation in polyelectrolyte solutions. V. Further development of the chemical model. Biophysical Chemistry 9, 6570.
Massire, C., Jaeger, L. & Westhof, E. (1998). Derivation of the three-dimensional architecture of bacterial ribonuclease P RNAs from comparative sequence analysis. Journal of Molecular Biology 279, 773793.
Matthews, C. R. (1987). Effects of point mutations on the folding of globular proteins. Methods in Enzymology 154, 498511.
Misra, V. K. & Draper, D. E. (2000). Mg2+ binding to tRNA revisited: the nonlinear Poisson-Boltzmann model. Journal of Molecular Biology 299, 813825.
Misra, V. K. & Draper, D. E. (2002). The linkage between magnesium binding and RNA folding. Journal of Molecular Biology 317, 507521.
Misra, V. K., Shiman, R. & Draper, D. E. (2003). A thermodynamic framework for the magnesium-dependent folding of RNA. Biopolymers 69, 118136.
Moore, M. J. & Sharp, P. A. (1992). Site-specific modification of pre-mRNA: the 2′-hydroxyl groups at the splice sites. Science 256, 992997.
Myers, J. K., Pace, C. N. & Scholtz, J. M. (1995). Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Science 4, 21382148.
Pace, C. N. (1986). Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods in Enzymology 131, 266280.
Pan, J., Thirumalai, D. & Woodson, S. A. (1997). Folding of RNA involves parallel pathways. Journal of Molecular Biology 273, 713.
Pan, T. (1995a). Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P. Biochemistry 34, 902909.
Pan, T. (1995b). Novel RNA substrates for the ribozyme from Bacillus subtilis ribonuclease P identified by in vitro selection. Biochemistry 34, 84588464.
Pan, T. (2000). Probing RNA structure and function using circular permutation. Methods in Enzymology 317, 313330.
Pan, T., Artsimovitch, I., Fang, X., Landick, R. & Sosnick, T. R. (1999a). Folding of a large ribozyme during transcription and the effect of the elongation factor NusA. Proceedings of the National Academy of Sciences USA 96, 95459550.
Pan, T., Fang, X. & Sosnick, T. R. (1999b). Pathway modulation, circular permutation and rapid RNA folding under kinetic control. Journal of Molecular Biology 286, 721731.
Pan, T. & Jakacka, M. (1996). Multiple substrate binding sites in the ribozyme from Bacillus subtilis RNase P. EMBO Journal 15, 22492255.
Pan, T. & Sosnick, T. (2006). RNA folding during transcription. Annual Review of Biophysics and Biomolecular Structures 35, 161175.
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 Structural Biology 4, 931938.
Plaxco, K. W., Simons, K. T. & Baker, D. (1998). Contact order, transition state placement and the refolding rates of single domain proteins. Journal of Molecular Biology 277, 985994.
Plaxco, K. W., Simons, K. T., Ruczinski, I. & Baker, D. (2000). Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics. Biochemistry 39, 1117711183.
Puglisi, J. D. & Jr.Tinoco, I. (1989). Absorbance melting curves of RNA. Methods in Enzymology 180, 304325.
Qin, H., Sosnick, T. R. & Pan, T. (2001). Modular construction of a tertiary RNA structure: the specificity domain of the Bacillus subtilis RNase P RNA. Biochemistry 40, 1120211210.
Rupert, P. B. & Ferre-D'Amare, A. R. (2001). Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410, 780786.
Russell, R., Zhuang, X., Babcock, H. P., Millett, I. S., Doniach, S., Chu, S. & Herschlag, D. (2002). Exploring the folding landscape of a structured RNA. Proceedings of the National Academy of Sciences USA 99, 155160.
Jr.SantaLucia, J., Kierzek, R. & Turner, D. H. (1990). Effects of GA mismatches on the structure and thermodynamics of RNA internal loops. Biochemistry 29, 88138819.
Sclavi, B., Woodson, S., Sullivan, M., Chance, M. R. & Brenowitz, M. (1997). Time-resolved synchrotron X-ray ‘footprinting’, a new approach to the study of nucleic acid structure and function: application to protein-DNA interactions and RNA folding. Journal of Molecular Biology 266, 144159.
Seifert, S., Winans, R. E., Tiede, D. M. & Thiyagarajan, P. (2000). Design and performance of a ASAXS instrument at the Advanced Photon Source. Journal of Applied Crystallography 33, 782784.
Shelton, V. M., Sosnick, T. R. & Pan, T. (1999). Applicability of urea in the thermodynamic analysis of secondary and tertiary RNA folding. Biochemistry 38, 1683116839.
Shi, H. & Moore, P. B. (2000). The crystal structure of yeast phenylalanine tRNA at 1·93 A resolution: a classic structure revisited. RNA 6, 10911105.
Silverman, S. K. & Cech, T. R. (2001). An early transition state for folding of the P4-P6 RNA domain. RNA 7, 161166.
Sosnick, T. R., Dothager, R. S. & Krantz, B. A. (2004). Differences in the folding transition state of ubiquitin indicated by phi and psi analyses. Proceedings of the National Academy of Sciences USA 101, 1737717382.
Sosnick, T. R., Fang, X. & Shelton, V. M. (2000). Application of circular dichroism to study RNA folding transitions. Methods in Enzymology 317, 393409.
Sosnick, T. R., Mayne, L. & Englander, S. W. (1996). Molecular collapse: The rate-limiting step in two-state cytochrome c folding. Proteins 24, 413–426.
Sosnick, T. R. & Pan, T. (2003). RNA folding: models and perspectives. Current Opinion in Structural Biology 13, 309316.
Sosnick, T. R. & Pan, T. (2004). Reduced contact order and RNA folding rates. Journal of Molecular Biology 342, 13591365.
Stolc, V., Gauhar, Z., Mason, C., Halasz, G., van Batenburg, M. F., Rifkin, S. A., Hua, S., Herreman, T., Tongprasit, W., Barbano, P. E., et al. (2004). A gene expression map for the euchromatic genome of Drosophila melanogaster. Science 306, 655660.
Svergun, D. I. & Koch, M. H. J. (2003). Small-angle scattering studies of biological macromolecules in solution. Reports on Progress in Physics 66, 17351782.
Swisher, J. F., Su, L. J., Brenowitz, M., Anderson, V. E. & Pyle, A. M. (2002). Productive folding to the native state by a group II intron ribozyme. Journal of Molecular Biology 315, 297310.
Thirumalai, D. & Hyeon, C. (2005). RNA and protein folding: common themes and variations. Biochemistry 44, 49574970.
Torres-Larios, A., Swinger, K. K., Krasilnikov, A. S., Pan, T. & Mondragon, A. (2005). Crystal structure of the RNA component of bacterial ribonuclease P. Nature 437, 584587.
Treiber, D. K., Rook, M. S., Zarrinkar, P. P. & Williamson, J. R. (1998). Kinetic intermediates trapped by native interactions in RNA folding. Science 279, 19431946.
Treiber, D. K. & Williamson, J. R. (2001). Beyond kinetic traps in RNA folding. Current Opinion in Structural Biology 11, 309314.
Turner, D. H. & Sugimoto, N. (1988). RNA structure prediction. Annual Review of Biophysics and Biophysical Chemistry 17, 167192.
Walter, F., Murchie, A. I. H. & Lilley, D. M. J. (1998). Folding of the four-way RNA junction of the hairpin ribozyme. Biochemistry 37, 1762917636.
Wong, T., Sosnick, T. R. & Pan, T. (2005). Mechanistic insights on the folding of a large ribozyme during transcription. Biochemistry 44, 7535–7342.
Woodson, S. A. (2002). Folding mechanisms of group I ribozymes: role of stability and contact order. Biochemical Society Transactions 30, 11661169.
Woodson, S. A. (2005). Metal ions and RNA folding: a highly charged topic with a dynamic future. Current Opinion in Chemical Biology 9, 104109.
Woody, R. W. (1995). Circular dichroism. Methods in Enzymology 246, 3471.
Xie, Z., Srividya, N., Sosnick, T. R., Pan, T. & Scherer, N. F. (2004). Single-molecule studies highlight conformational heterogeneity in the early folding steps of a large ribozyme. Proceedings of the National Academy of Sciences USA 101, 534539.
Zarrinkar, P. P., Wang, J. & Williamson, J. R. (1996). Slow folding kinetics of RNase P RNA. RNA 2, 564573.
Zarrinkar, P. P. & Williamson, J. R. (1996). The kinetic folding pathway of the Tetrahymena ribozyme reveals possible similarities between RNA and protein folding [see comments]. Nature Structural Biology 3, 432438.
Zhuang, X., Bartley, L. E., Babcock, H. P., Russell, R., Ha, T., Herschlag, D. & Chu, S. (2000). A single-molecule study of RNA catalysis and folding. Science 288, 20482051.
Zhuang, X., Kim, H., Pereira, M. J., Babcock, H. P., Walter, N. G. & Chu, S. (2002). Correlating structural dynamics and function in single ribozyme molecules. Science 296, 14731476.

Folding of a universal ribozyme: the ribonuclease P RNA

  • Nathan J. Baird (a1) (a2), Xing-Wang Fang (a3), Narayanan Srividya (a3), Tao Pan (a3) and Tobin R. Sosnick (a2) (a3)...

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed