Tightening of active site interactions en route to the transition state revealed by single-atom substitution in the guanosine-binding site of the Tetrahymena group i ribozyme

Journal of the American Chemical Society

Volumn 133, Issue 20, 2011, Pages 7791-7800

  Forconi, Marcello ^a   Porecha, Rishi H ^a   Piccirilli, Joseph A ^b   Herschlag, Daniel ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; AMINO GROUP; BINDING INTERACTION; CHEMICAL TRANSITION STATE; DOUBLE MUTANTS; EN-ROUTE; ENERGETIC PROPERTIES; FUNCTIONAL TEST; GUANOSINES; INFERRED NETWORKS; INTERACTION NETWORKS; MULTIPLE CONTACTS; PRE-STEADY-STATE KINETIC ANALYSIS; REACTIVE ELEMENTS; RIBOZYMES; TETRAHYMENA; TRANSITION STATE;

ACTIVE NETWORKS; BINDING ENERGY; BIOMOLECULES; CATALYSTS; ENZYMES; NUCLEOPHILES; RNA;

BINDING SITES;

AMINO ACID; GUANOSINE; NUCLEOPHILE; RIBOZYME;

ARTICLE; ATOM; CATALYSIS; CILIATE; CRYSTAL STRUCTURE; ENERGY; MUTANT; NONHUMAN; PROTEIN INTERACTION; STEADY STATE; SUBSTITUTION REACTION; TETRAHYMENA;

BINDING SITES; CATALYTIC DOMAIN; GUANOSINE; KINETICS; MODELS, MOLECULAR; RNA, CATALYTIC; TETRAHYMENA;

EID: 79957764695     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja111316y     Document Type: Article

References (61)

1. Hoogstraten, C. G.; Sumita, M. Biopolymers 2007, 87, 317
2. Lilley, D. M. Trends Biochem. Sci. 2003, 28, 495
3. Narlikar, G. J.; Herschlag, D. Annu. Rev. Biochem. 1997, 66, 19
4. Hougland, J. L.; Piccirilli, J. A.; Forconi, M.; Lee, J.; Herschlag, D. In The RNA World; 3rd ed.; Gesteland, R. F.; Cech, T. R.; Atkins, J. F., Eds.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 2006.
5. Narlikar, G. J.; Gopalakrishnan, V.; McConnell, T. S.; Usman, N.; Herschlag, D. Proc. Natl. Acad. Sci.U.S.A. 1995, 92, 3668
6. Hertel, K. J.; Peracchi, A.; Uhlenbeck, O. C.; Herschlag, D. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 8497
7. Sigler, P. B. Annu. Rev. Biophys. Bioeng. 1975, 4, 477
8. Antonioli, A. H.; Cochrane, J. C.; Lipchock, S. V.; Strobel, S. A. RNA 2010, 16, 762
9. Santalucia, J.; Kierzek, R.; Turner, D. H. Science 1992, 256, 217
10. Herschlag, D.; Cech, T. R. Biochemistry 1990, 29, 10159
11. Bevilacqua, P. C.; Turner, D. H. Biochemistry 1991, 30, 10632
12. Herschlag, D. Biochemistry 1992, 31, 1386
13. McConnell, T. S.; Cech, T. R.; Herschlag, D. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 8362
14. Latham, J. A.; Cech, T. R. Science 1989, 245, 276
15. Bass, B. L.; Cech, T. R. Nature 1984, 308, 820
16. Michel, F.; Hanna, M.; Green, R.; Bartel, D. P.; Szostak, J. W. Nature 1989, 342, 391
17. Ortoleva-Donnelly, L.; Szewczak, A. A.; Gutell, R. R.; Strobel, S. A. RNA 1998, 4, 498
18. Yarus, M.; Illangesekare, M.; Christian, E. J. Mol. Biol. 1991, 222, 995
19. Adams, P. L.; Stahley, M. R.; Kosek, A. B.; Wang, J.; Strobel, S. A. Nature 2004, 430, 45
20. Golden, B. L.; Kim, H.; Chase, E. Nature Struct. Mol. Biol. 2005, 12, 82
21. Guo, F.; Gooding, A. R.; Cech, T. R. Mol. Cell 2005, 16, 351
22. Lipchock, S. V.; Strobel, S. A. Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 5699
23. Paukstelis, P. J.; Chen, J. H.; Chase, E.; Lambowitz, A. M.; Golden, B. L. Nature 2008, 451, 94
24. Stahley, M. R.; Strobel, S. A. Science 2005, 309, 1587
25. Dai, Q.; Deb, S. K.; Hougland, J. L.; Piccirilli, J. A. Bioorg. Med. Chem. 2006, 14, 705
26. Forconi, M.; Sengupta, R. N.; Piccirilli, J. A.; Herschlag, D. Biochemistry 2010, 49, 2753
27. Moore, M. J.; Sharp, P. A. Science 1992, 256, 992
28. Mei, R.; Herschlag, D. Biochemistry 1996, 35, 5796
29. Pyle, A. M.; Mcswiggen, J. A.; Cech, T. R. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 8187
30. Knitt, D. S.; Herschlag, D. Biochemistry 1996, 35, 1560
31. Horovitz, A. Folding Des. 1996, 1, R121
32. Strobel, S. A.; Ortoleva-Donnelly, L. Chem. Biol. 1999, 6, 153
33. Szewczak, A. A.; Kosek, A. B.; Piccirilli, J. A.; Strobel, S. A. Biochemistry 2002, 41, 2516
34. Hougland, J. L.; Kravchuk, A. V.; Herschlag, D.; Piccirilli, J. A. PLoS Biol. 2005, 3, 1536
35. Forconi, M.; Lee, J.; Lee, J. K.; Piccirilli, J. A.; Herschlag, D. Biochemistry 2008, 47, 6883
36. Forconi, M.; Sengupta, R. N.; Liu, M. C.; Sartorelli, A. C.; Piccirilli, J. A.; Herschlag, D. Angew. Chem., Int. Ed. 2009, 48, 7171
37. Pitha, P. M.; Huang, W. M.; Ts?o, P. O. Proc. Natl. Acad. Sci. U.S.A. 1968, 61, 332
38. Moran, S.; Kierzek, R.; Turner, D. H. Biochemistry 1993, 32, 5247
39. Russell, R.; Herschlag, D. RNA 1999, 5, 158
40. Narlikar, G. J.; Bartley, L. E.; Koshla, M.; Herschlag, D. Biochemistry 1999, 38, 14192
41. Shi, X.; Mollova, E. T.; Pljevaljcic, G.; Millar, D. P.; Herschlag, D. J. Am. Chem. Soc. 2009, 131, 9571
42. Fersht, A. R.; Shi, J. P.; Knill-Jones, J.; Lowe, D. M.; Wilkinson, A. J.; Blow, D. M.; Brick, P.; Carter, P.; Waye, M. M.; Winter, G. Nature 1985, 314, 235
43. Turner, D. H.; Sugimoto, N.; Kierzek, R.; Dreiker, S. D. J. Am. Chem. Soc. 1987, 109, 3783
44. Seela, F.; Chen, Y. M. Nucleic Acids Res. 1995, 23, 2499
45. Seela, F.; Tranthi, Q. H.; Franzen, D. Biochemistry 1982, 21, 4338
46. Sistare, M. F.; Codden, S. J.; Heimlich, G.; Thorp, H. H. J. Am. Chem. Soc. 2000, 122, 4742
47. Siegfried, N. A.; Kierzek, R.; Bevilacqua, P. C. J. Am. Chem. Soc. 2010, 132, 5342
48. McConnell, T. S.; Cech, T. R. Biochemistry 1995, 34, 4056
49. Shan, S.; Herschlag, D. Biochemistry 1999, 38, 10958
50. Sjogren, A. J.; Petterson, E.; Sjoberg, B. M.; Stromberg, R. Nucleic Acids Res. 1997, 25, 648
51. Shan, S.; Herschlag, D. RNA 2000, 6, 795
52. Buchner, E. F. Ber. Dt. Chem. Ges. 1897, 30, 117
53. McMurry, J.; Begley, T. The Organic Chemistry of Biological Pathways; Roberts & Company: Greenwood Village, CO, 2005.
54. Fersht, A. Structure and Mechanism in Protein Science; W.H. Freeman and Company: New York, 1999.
55. Hedstrom, L.; Szilagyi, L.; Rutter, W. J. Science 1992, 255, 1249
56. Lockless, S. W.; Ranganathan, R. Science 1999, 286, 295
57. Oue, S.; Okamoto, A.; Yano, T.; Kagamiyama, H. J. Biol. Chem. 1999, 274, 2344
58. Patten, P. A.; Gray, N. S.; Yang, P. L.; Marks, C. B.; Wedemayer, G. J.; Boniface, J. J.; Stevens, R. C.; Schultz, P. G. Science 1996, 271, 1086
59. Das, S. R.; Fong, R.; Piccirilli, J. A. Curr. Opin. Chem. Biol. 2005, 9, 585
60. The second hydrogen bond with the 2′-OH of residue A261 that is formed in the closed complex is not formed in the open complex, but the 2.4 kcal/mol loss of binding energy associated with the removal of the exocyclic amino group of G suggests the loss of two hydrogen bonds, as described in ref 26.
61. Wolfenden, R. Mol. Cell. Biochem. 1974, 3, 207