Compaction of a Bacterial Group I Ribozyme Coincides with the Assembly of Core Helices

Biochemistry

Volumn 43, Issue 6, 2004, Pages 1746-1753

  Perez Salas, Ursula A ^a   Rangan, Prashanth ^b   Krueger, Susan ^a   Briber, R M ^c   Thirumalai, D ^d   Woodson, Sarah A ^b  

^a NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

^d UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CORRELATION METHODS; ELECTROSTATICS; NEUTRON SCATTERING; PHASE TRANSITIONS; RNA; SELF ASSEMBLY;

SELF SPLICING; TERTIARY STRUCTURE;

BIOCHEMISTRY;

MAGNESIUM ION; RIBONUCLEASE; RIBOZYME; RNA; SODIUM ION;

ARTICLE; AZOARCUS; CONCENTRATION (PARAMETERS); ELECTRICITY; NEUTRON SCATTERING; NONHUMAN; PHASE TRANSITION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FOLDING; PROTEIN STRUCTURE; STRUCTURE ANALYSIS;

AZOARCUS; INTRONS; MAGNESIUM CHLORIDE; NEUTRONS; NUCLEIC ACID CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RIBONUCLEASE T1; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA SPLICING; RNA, BACTERIAL; RNA, CATALYTIC; SCATTERING, RADIATION;

AZOARCUS; BACTERIA (MICROORGANISMS); NEGIBACTERIA;

EID: 1042265194     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi035642o     Document Type: Article

References (43)

1. Brion, P., and Westhof, E. (1997) Hierarchy and dynamics of RNA folding, Annu. Rev. Biophys. Biomol. Struct. 26, 113-137.
2. Thirumalai, D., Lee, N., Woodson, S. A., and Klimov, D. (2001) Early events in RNA folding, Annu. Rev. Phys. Chem. 52, 751-762.
3. Sosnick, T. R., and Pan, T. (2003) RNA folding: models and perspectives, Curr. Opin. Struct. Biol. 13, 309-316.
4. Misra, V. K., and Draper, D. E. (1998) On the role of magnesium ions in RNA stability, Biopolymers 48, 113-135.
5. Buchmueller, K. L., Webb, A. E., Richardson, D. A., and Weeks, K. M. (2000) A collapsed, non-native RNA folding state, Nat. Struct. Biol. 7, 362-366.
6. Heilman-Miller, S. L., Thirumalai, D., and Woodson, S. A. (2001) Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations, J. Mol. Biol. 306, 1157-1166.
7. Russell, R., Millett, I. S., Doniach, S., and Herschlag, D. (2000) Small angle X-ray scattering reveals a compact intermediate in RNA folding, Nat. Struct. Biol. 7, 367-370.
8. Fang, X., Littrell, K., Yang, X., Henderson, S. J., Siefert, S., Thiyagarajan, P., Pan, T., and Sosnick, T. R. (2000) Mg(2+)-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, 11107-11113.
9. 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.
10. Russell, R., Millett, I. S., Tate, M. W., Kwok, L. W., Nakatani, B., Gruner, S. M., Mochrie, S. G., Pande, V., Doniach, S., Herschlag, D., and Pollack, L. (2002) Rapid compaction during RNA folding, Proc. Natl. Acad. Sci. U.S.A. 99, 4266-4271.
11. Reinhold-Hurek, B., and Shub, D. A. (1992) Self-splicing introns in tRNA genes of widely divergent bacteria, Nature 357, 173-176.
12. Feigin, L. A., and Svergun, D. I. (1987) Structure Analysis by Small Angle X-ray and Neutron Scattering, Plenum Press, New York.
13. Glatter, O., and Kratky, O. (1982) Small Angle X-ray Scattering, Academic Press, San Diego, CA.
14. Rangan, P., Masquida, B., Westhof, E., and Woodson, S. A. (2003) Assembly of core helices and rapid tertiary folding of a small bacterial group I ribozyme, Proc. Natl. Acad. Sci. U.S.A. 100, 1574-1579.
15. Davanloo, P., Rosenberg, A. H., Dunn, J. J., and Studier, F. W. (1984) Cloning and expression of the gene for bacteriophage T7 RNA polymerase, Proc. Natl. Acad. Sci. U.S.A. 81, 2035-2039.
16. Tanner, M., and Cech, T. (1996) Activity and thermostability of the small self-splicing group I intron in the pre-tRNA(Ile) of the purple bacterium Azoarcus, RNA 2, 74-83.
17. Glinka, C. J., Barker, J. G., Hammouda, B., Krueger, S., Moyer, J. J., and Orts, W. J. (1998) The 30 m small-angle neutron scattering instruments at the National Institute of Standards and Technology, J. Appl. Crystallogr. 31, 430-445.
18. Semenyuk, A. V., and Svergun, D. I. (1991) GNOM - a Program Package for Small-Angle Scattering Data- Processing, J. Appl. Crystallogr. 24, 537-540.
19. Svergun, D. I., Richard, S., Koch, M. H., Sayers, Z., Kuprin, S., and Zaccai, G. (1998) Protein hydration in solution: experimental observation by X-ray and neutron scattering, Proc. Natl. Acad. Sci. U.S.A. 95, 2267-2272.
20. 2+ binding in the group I intron core, J. Mol. Biol. 329, 229-238.
21. Uchida, T., Takamoto, K., He, Q., Chance, M. R., and Brenowitz, M. (2003) Multiple monovalent ion-dependent pathways for the folding of the L-21 Tetrahymena thermophila ribozyme, J. Mol. Biol. 328, 463-478.
22. Michel, F., and Westhof, E. (1990) Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis, J. Mol. Biol. 216, 585-610.
23. Chamberlin, S. I., and Weeks, K. M. (2003) Differential helix stabilities and sites pre-organized for tertiary interactions revealed by monitoring local nucleotide flexibility in the bI5 group I intron RNA, Biochemistry 42, 901-909; Buchmueller, K. L., and Weeks, K. M. (2003) Near native structure in an RNA collapsed state, Biochemistry 42, 13869-13878.
24. Chamberlin, S. I., and Weeks, K. M. (2003) Differential helix stabilities and sites pre-organized for tertiary interactions revealed by monitoring local nucleotide flexibility in the bI5 group I intron RNA, Biochemistry 42, 901-909; Buchmueller, K. L., and Weeks, K. M. (2003) Near native structure in an RNA collapsed state, Biochemistry 42, 13869-13878.
25. Xiao, M., Leibowitz, M. J., and Zhang, Y. (2003) Concerted folding of a Candida ribozyme into the catalytically active structure posterior to a rapid RNA compaction, Nucleic Acids Res. 31, 3901-3908.
26. Das, R., Kwok, L. W., Millett, I. S., Bai, Y., Mills, T. T., Jacob, J., Maskel, G. S., Seifert, S., Mochrie, S. G. J., Thiyagarajan, P., Doniach, S., Pollack, L., and Herschlag, D. (2003) The Fastest Global Events in RNA Folding: Electrostatic Relaxation and Tertiary Collapse of the Tetrahymena Ribozyme, J. Mol. Biol. 332, 311-319.
27. Ha, B. Y., and Thirumalai, D. (1992) Conformations of a Polyelectrolyte Chain, Phys. Rev. A 46, R3012-R3015.
28. Rouzina, I., and Bloomfield, V. A. (1996) Macroion attraction due to electrostatic correlation between screening counterions 0.1. Mobile surface-adsorbed ions and diffuse ion cloud, J. Phys. Chem. 100, 9977-9989.
29. Cate, J. H., Gooding, A. R., Podell, E., Zhou, K., Golden, B. L., Kundrot, C. E., Cech, T. R., and Doudna, J. A. (1996) Crystal structure of a group I ribozyme domain: principles of RNA packing, Science 273, 1678-1685.
30. Doherty, E. A., Batey, R. T., Masquida, B., and Doudna, J. A. (2001) A universal mode of helix packing in RNA, Nat. Struct. Biol. 8, 339-343.
31. Bokinsky, G., Rueda, D., Misra, V. K., Rhodes, M. M., Gordus, A., Babcock, H. P., Walter, N. G., and Zhuang, X. (2003) Single-molecule transition-state analysis of RNA folding, Proc. Natl. Acad. Sci. U.S.A. 100, 9302-9307.
32. Deras, M. L., Brenowitz, M., Ralston, C. Y., Chance, M. R., and Woodson, S. A. (2000) Folding mechanism of the Tetrahymena ribozyme P4-P6 domain, Biochemistry 39, 10975-10985.
33. Bloomfield, V. A. (1997) DNA condensation by multivalent cations, Biopolymers 44, 269-282.
34. Misra, V. K., and Draper, D. E. (1999) The interpretation of Mg(2+) binding isotherms for nucleic acids using Poisson-Boltz-mann theory, J. Mol. Biol. 294, 1135-1147.
35. Misra, V. K., and Draper, D. E. (2002) The linkage between magnesium binding and RNA folding, J. Mol. Biol. 317, 507-521.
36. Manning, G. S. (1977) A field-dissociation relation for polyelectrolytes with an application to field-induced conformational changes of polynucleotides, Biophys. Chem. 7, 189-192.
37. Bloomfield, V. A., Crothers, D. M., and Tinoco, I. J. (2000) Nucleic Acids: Structures, Properties, and Functions, University Science Books, Sausalito, CA.
38. Pan, J., Thirumalai, D., and Woodson, S. A. (1997) Folding of RNA involves parallel pathways, J. Mol. Biol. 273, 7-13.
39. Pan, J., and Woodson, S. A. (1998) Folding intermediates of a self-splicing RNA: mispairing of the catalytic core, J. Mol. Biol. 280, 597-609.
40. Rook, M. S., Treiber, D. K., and Williamson, J. R. (1998) Fast folding mutants of the Tetrahymena group I ribozyme reveal a rugged folding energy landscape, J. Mol. Biol. 281, 609-620.
41. Russell, R., Zhuang, X., Babcock, H. P., Millett, I. S., Doniach, S., Chu, S., and Herschlag, D. (2002) Exploring the folding landscape of a structured RNA, Proc. Natl. Acad. Sci. U.S.A. 99, 155-160.
42. Thirumalai, D. (1995) From the minimal models to real proteins: time scales for protein folding kinetics, J. Phys. 15, 1457-1467.
43. Damberger, S. H., and Gutell, R. R. (1994) A comparative database of group I intron structures, Nucleic Acids Res. 22, 3508-3510.