Two Distinct Binding Modes of a Protein Cofactor with its Target RNA

Journal of Molecular Biology

Volumn 361, Issue 4, 2006, Pages 771-784

  Bokinsky, Gregory ^a,b   Nivón, Lucas G ^a   Liu, Shixin ^a,b   Chai, Geqing ^d   Hong, Minh ^a,b   Weeks, Kevin M ^d   Zhuang, Xiaowei ^a,b,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c HARVARD UNIVERSITY   (United States)

^d University of North Carolina at Chapel Hill   (United States)

Author keywords

FRET; group I intron; ribonucleoprotein; RNA folding; RNA protein interaction

Indexed keywords

PROTEIN; PROTEIN COFACTOR CB2; RNA; UNCLASSIFIED DRUG;

ARTICLE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN RNA BINDING; RNA STRUCTURE;

EID: 33746793263     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.06.048     Document Type: Article

References (42)

1. Gesteland R.F., Cech T.R., and Atkins J.F. The RNA world. 2nd edit (1999), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
2. Pan J., and Woodson S.A. Folding intermediates of a self-splicing RNA: Mispairing of the catalytic core. J. Mol. Biol. 280 (1998) 597-609
3. Pan T., and Sosnick T.R. Intermediates and kinetics traps in the folding of a large ribozyme revealed by circular dichroism and UV absorbance spectroscopies and catalytic activity. Nature Struct. Biol. 4 (1997) 931-938
4. Russell R., and Herschlag D. New pathways in folding of the Tetrahymena group I RNA enzyme. J. Mol. Biol. 291 (1999) 1155-1167
5. Treiber D.K., Rook M.S., Zarrinkar P.P., and Williamson J.R. Kinetic intermediates trapped by native interactions in RNA folding. Science 279 (1998) 1943-1946
6. Zhuang X., Bartley L., Babcock H., Russell R., Ha T., Herschlag D., and Chu S. A single molecule study of RNA catalysis and folding. Science 288 (2000) 2048-2051
7. Onoa B., Dumont S., Liphardt J., Smith S.B., Tinoco I., and Bustamante C. Identifying kinetic barriers to mechanical unfolding of the T. thermophila ribozyme. Science 299 (2003) 1892-1895
8. Sclavi B., Sullivan M., Chance M.R., Brenowitz M., and Woodson S.A. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science 279 (1998) 1940-1943
9. Treiber D.K., and Williamson J.R. Beyond kinetic traps in RNA folding. Curr. Opin. Struc. Biol. 11 (2001) 309-314
10. Weeks K.M., and Cech T.R. Protein facilitation of group I intron splicing by assembly of the catalytic core and the 5′-splice-site domain. Cell 82 (1995) 221-230
11. Caprara M.G., Lehnert V., Lambowitz A.M., and Westhof E. A tyrosyl-tRNA synthetase recognizes a conserved tRNA-like structural motif in the group I intron catalytic core. Cell 87 (1996) 1135-1145
12. Weeks K.M. Protein-facilitated RNA folding. Curr. Opin. Struct. Biol. 7 (1997) 336-342
13. Schroeder R., Grossberger R., Pichler A., and Waldsich C. RNA folding in vivo. Curr. Opin. Struc. Biol. 12 (2002) 296-300
14. Hsien J., Andrews A.J., and Fierke C.A. Roles of protein subunit in RNA-protein complexes: Lessons from Ribonuclease P. Biopolymers 73 (2004) 79-89
15. Dreyfuss G., Kim V.N., and Kataoka N. Messenger-RNA-binding proteins and the messages they carry. Nat. Rev. Mol. Cell Biol. 3 (2002) 195-205
16. Coetzee T., Herschlag D., and Belfort M. Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Dev. 8 (1994) 1575-1588
17. Herschlag D. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270 (1995) 20871-20874
18. Caprara M.G., Mohr G., and Lambowitz A.M. A tyrosyl-tRNA synthetase protein induces tertiary folding of the group I intron catalytic core. J. Mol. Biol. 257 (1996) 512-531
19. Weeks K.M., and Cech T.R. Assembly of a ribonucleoprotein catalyst by tertiary structure capture. Science 271 (1996) 345-348
20. Garcia I., and Weeks K.M. Structural basis for the self-chaperoning function of an RNA collapsed state. Biochemistry 43 (2004) 15179-15186
21. Geese W.J., and Waring R.B. A comprehensive characterization of a group IB intron and its encoded maturase reveals that protein-assisted splicing requires an almost intact intron RNA. J. Mol. Biol. 308 (2001) 609-622
22. Solem A., Chatterjee P., and Caprara M.G. A novel mechanism for protein-assisted group I intron splicing. RNA 8 (2002) 412-425
23. Mohr S., Stryker J.M., and Lambowitz A.M. A DEAD-box protein functions as an ATP-dependent RNA chaperone in group I intron splicing. Cell 109 (2002) 769-779
24. Selvin P.R. Fluorescence resonance energy-transfer. Methods Enzymol. 246 (1995) 300-334
25. Weiss S. Measuring conformational dynamics of biomolecules by single molecule fluorescence spectroscopy. Nature Struct. Biol. 7 (2000) 724-729
26. Ha T., Zhuang X., Kim H., Orr J.W., Williamson J.R., and Chu S. Ligand-induced conformational changes observed in single RNA molecules. Proc. Natl Acad. Sci. USA 96 (1999) 9077-9082
27. Cosa G., Zeng Y.N., Liu H.W., Landes C.F., Makarov D.E., Musier-Forsyth K., and Barbara P.F. Evidence for non-two-state kinetics in the nucleocapsid protein chaperoned opening of DNA hairpins. J. Phys. Chem. B 110 (2006) 2419-2426
28. Zhuang X., Kim H., Pereira M., Babcock H., Walter N., and Chu S. Correlating structural dynamics and function in single ribozyme molecules. Science 296 (2002) 1473-1476
29. Tan E., Wilson T.J., Nahas M.K., Clegg R.M., Lilley D.M.J., and Ha T. A four-way junction accelerates hairpin ribozyme folding via a discrete intermediate. Proc. Natl Acad. Sci. USA 100 (2003) 9308-9313
30. Xie Z., Srividya N., Sosnick T.R., Pan T., and Scherer N.F. Single-molecule studies highlight conformational heterogeneity in the early folding steps of a large ribozyme. Proc. Natl Acad. Sci. USA 101 (2004) 534-539
31. Lipman E.A., Schuler B., Bakajin O., and Eaton W.A. Single-molecule measurement of protein folding kinetics. Science 301 (2003) 1233-1235
32. Gampel A., and Tzagoloff A. In vitro splicing of the terminal intervening sequence of Saccharomyces cerevisiae cytochrome-B pre-mRNA. Mol. Cell. Biol. 7 (1987) 2545-2551
33. Weeks K.M., and Cech T.R. Efficient protein-facilitated splicing of the Yeast mitochondrial bI5 intron. Biochemistry 34 (1995) 7728-7738
34. Shaw L.C., and Lewin A.S. Protein-induced folding of a group I intron in cytochrome b pre-mRNA. J. Biol. Chem. 270 (1995) 21552-21562
35. Buchmueller K.L., Webb A.E., Richardson D.A., and Weeks K.M. A collapsed non-native RNA folding state. Nature Struct. Biol. 7 (2000) 362-366
36. Mrksich M., and Whitesides G.M. Using self-assembled monolayers that present oligo(ethylene glycol) groups to control the interactions of proteins with surfaces. ACS Symposium Series 680 (1997) 361-373
37. Knitt D.S., Narlikar G.J., and Herschlag D. Dissection of the role of the conserved GU pair in group I RNA self-splicing. Biochemistry 33 (1994) 13864-13879
38. Chamberlin S.I., and Weeks K.M. 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 (2003) 901-909
39. Buchmueller K.L., and Weeks K.M. Near native structure in an RNA collapsed state. Biochemistry 42 (2003) 13869-13878
40. Webb A.E., and Weeks K.M. A collapsed state functions to self-chaperone RNA folding into a native ribonucleoprotein complex. Nature Struct. Biol. 8 (2001) 135-140
41. Webb A.E., Rose M.A., Westhof E., and Weeks K.M. Protein-dependent transition states for ribonucleoprotein assembly. J. Mol. Biol. 309 (2001) 1087-1100
42. Tirupati H.K., Shaw L.C., and Lewin A.S. An RNA binding motif in the Cbp2 protein required for protein-stimulated RNA catalysis. J. Biol. Chem. 274 (1999) 30393-30401