An important role of G638 in the cis-cleavage reaction of the Neurospora VS ribozyme revealed by a novel nucleotide analog incorporation method

RNA

Volumn 14, Issue 5, 2008, Pages 938-949

  Jaikaran, Dominic ^a   Smith, M Duane ^a   Mehdizadeh, Reza ^a   Olive, Joan ^a   Collins, Richard A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

General acid base catalysis; Ribozyme mechanism; RNA ligation

Indexed keywords

NUCLEOTIDE DERIVATIVE; PROTON; PURINE DERIVATIVE; RIBOZYME; RNA; FUNGAL RNA; PURINE NUCLEOTIDE; RIBONUCLEASE; VARKUD SATELLITE RIBOZYME;

ARTICLE; CONTROLLED STUDY; GENETIC LINKAGE; ION TRANSPORT; ISOTOPE ANALYSIS; MUTAGENESIS; NEUROSPORA; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; PH; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA CLEAVAGE; RNA STRUCTURE; BINDING SITE; CHEMISTRY; CONFORMATION; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; SITE DIRECTED MUTAGENESIS;

NEUROSPORA;

BASE SEQUENCE; BINDING SITES; ENDORIBONUCLEASES; HYDROGEN-ION CONCENTRATION; KINETICS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NEUROSPORA; NUCLEIC ACID CONFORMATION; PURINE NUCLEOTIDES; RNA, CATALYTIC; RNA, FUNGAL;

EID: 42449110782     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.936508     Document Type: Article

References (57)

1. Andersen, A.A. and Collins, R.A. 2000. Rearrangement of a stable RNA secondary structure during VS ribozyme catalysis. Mol. Cell 5: 469-478.
2. Baum, D.A. and Silverman, S.K. 2007. Deoxyribozyme-catalyzed labeling of RNA. Angew. Chem. Int. Ed. Engl. 46: 3502-3504.
3. Bellon, L., Workman, C., Scherrer, J., Usman, N., and Wincott, F. 1996. Morpholino-linked ribozymes: A convergent synthetic approach. J. Am. Chem. Soc. 118: 3771-3772.
4. Bevilacqua, P.C. 2003. Mechanistic considerations for general acid-base catalysis by RNA: Revisiting the mechanism of the hairpin ribozyme. Biochemistry 42: 2259-2265.
5. Bevilacqua, P.C., Brown, T.S., Nakano, S., and Yajima, R. 2004. Catalytic roles for proton transfer and protonation in ribozymes. Biopolymers 73: 90-109.
6. Cohen, S.B. and Cech, T.R. 1997. Dynamics of thermal motions within a large catalytic RNA investigated by cross-linking with thiol-disulfide interchange. J. Am. Chem. Soc. 119: 6259-6268.
7. Curtis, E.A. and Bartel, D.P. 2001. The hammerhead cleavage reaction in monovalent cations. RNA 7: 546-552.
8. Da Costa, C.P., Fedor, M.J., and Scott, L.G. 2007. 8-Azaguanine reporter of purine ionization states in structured RNAs. J. Am. Chem. Soc. 129: 3426-3432.
9. Das, S.R. and Piccirilli, J.A. 2005. General acid catalysis by the hepatitis delta virus ribozyme. Nat. Chem. Biol. 1: 45-52.
10. Eckstein, F. 1985. Nucleoside phosphorothioates. Annu. Rev. Biochem. 54: 367-402.
11. Fedor, M.J. and Williamson, J.R. 2005. The catalytic diversity of RNAs. Nat. Rev. Mol. Cell Biol. 6: 399-412.
12. Han, J. and Burke, J.M. 2005. Model for general acid-base catalysis by the hammerhead ribozyme: pH-activity relationships of G8 and G12 variants at the putative active site. Biochemistry 44: 7864-7870.
13. Hiley, S.L. and Collins, R.A. 2001. Rapid formation of a solvent-inaccessible core in the Neurospora Varkud satellite ribozyme. EMBO J. 20: 5461-5469.
14. Hiley, S.L., Sood, V.D., Fan, J., and Collins, R.A. 2002. 4-thio-U crosslinking identifies the active site of the VS ribozyme. EMBO J. 21: 4691-4698.
15. Hoffmann, B., Mitchell, G.T., Gendron, P., Major, F., Andersen, A., Collins, R.A., and Legault, P. 2003. NMR structure of the active conformation of the Varkud satellite ribozyme cleavage site. Proc. Natl. Acad. Sci. 100: 7003-7008.
16. Jencks, W. 1969. Catalysis and enzymology: Dover Publications Inc., New York.
17. Jones, F.D. and Strobel, S.A. 2003. Ionization of a critical adenosine residue in the Neurospora Varkud satellite ribozyme active site. Biochemistry 42: 4265-4276.
18. Ke, A., Zhou, K., Ding, F., Cate, J.H., and Doudna, J.A. 2004. A conformational switch controls hepatitis d virus ribozyme catalysis. Nature 429: 201-205.
19. a. Biochemistry 35: 1560-1570.
20. Kuzmin, Y.I., Da Costa, C.P., and Fedor, M.J. 2004. Role of an active site guanine in hairpin ribozyme catalysis probed by exogenous nucleobase rescue. J. Mol. Biol. 340: 233-251.
21. Lafontaine, D.A., Norman, D.G., and Lilley, D.M. 2001a. Structure, folding and activity of the VS ribozyme: Importance of the 2-3-6 helical junction. EMBO J. 20: 1415-1424.
22. Lafontaine, D.A., Wilson, T.J., Norman, D.G., and Lilley, D.M. 2001b. The A730 loop is an important component of the active site of the VS ribozyme. J. Mol. Biol. 312: 663-674.
23. Lafontaine, D.A., Wilson, T.J., Zhao, Z.Y., and Lilley, D.M. 2002. Functional group requirements in the probable active site of the VS ribozyme. J. Mol. Biol. 323: 23-34.
24. Martick, M. and Scott, W.G. 2006. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126: 309-320.
25. Milligan, J.F., Groebe, D.R., Witherell, G.W., and Uhlenbeck, O.C. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 15: 8783-8798. doi: 10.1093/nar/15.21.8783.
26. a shifting. RNA 11: 157-172.
27. Moore, M.J. and Query, C.C. 2000. Joining of RNAs by splinted ligation. Methods Enzymol. 317: 109-123.
28. Moore, M.J. and Sharp, P.A. 1992. Site-specific modification of premRNA: The 2′-hydroxyl groups at the splice sites. Science 256: 992-997.
29. Murray, J.B., Seyhan, A.A., Walter, N.G., Burke, J.M., and Scott, W.G. 1998. The hammerhead, hairpin and VS ribozymes are catalytically proficient in monovalent cations alone. Chem. Biol. 5: 587-595.
30. Nakano, S., Chadalavada, D.M., and Bevilacqua, P.C. 2000. General acid-base catalysis in the mechanism of a hepatitis δ virus ribozyme. Science 287: 1493-1497.
31. Nesbitt, S., Hegg, L.A., and Fedor, M.J. 1997. An unusual pH-independent and metal-ion-independent mechanism for hairpin ribozyme catalysis. Chem. Biol. 4: 619-630.
32. Ogilvie, K.K., Usman, N., Nicoghosian, K., and Cedergren, R.J. 1988. Total chemical synthesis of a 77-nucleotide-long RNA sequence having methionine-acceptance activity. Proc. Natl. Acad. Sci. 85: 5764-5768.
33. O'Rear, J.L., Wang, S., Feig, A.L., Beigelman, L., Uhlenbeck, O.C., and Herschlag, D. 2001. Comparison of the hammerhead cleavage reactions stimulated by monovalent and divalent cations. RNA 7: 537-545.
34. Perrotta, A.T. and Been, M.D. 2006. HDV ribozyme activity in monovalent cations. Biochemistry 45: 11357-11365.
35. Perrotta, A.T., Wadkins, T.S., and Been, M.D. 2006. Chemical rescue, multiple ionizable groups, and general acid-base catalysis in the HDV genomic ribozyme. RNA 12: 1282-1291.
36. Pinard, R., Hampel, K.J., Heckman, J.E., Lambert, D., Chan, P.A., Major, F., and Burke, J.M. 2001. Functional involvement of G8 in the hairpin ribozyme cleavage mechanism. EMBO J. 20: 6434-6442.
37. Poon, A.H., Olive, J.E., McLaren, M., and Collins, R.A. 2006. Identification of separate structural features that affect rate and cation concentration dependence of self-cleavage by the Neurospora VS ribozyme. Biochemistry 45: 13394-13400.
38. Pyle, A.M. 1993. Ribozymes: A distinct class of metalloenzymes. Science 261: 709-714.
39. Rastogi, T. and Collins, R.A. 1998. Smaller, faster ribozymes reveal the catalytic core of Neurospora VS RNA. J. Mol. Biol. 277: 215-224.
40. Rastogi, T., Beattie, T.L., Olive, J.E., and Collins, R.A. 1996. A long-range pseudoknot is required for activity of the Neurospora VS ribozyme. EMBO J. 15: 2820-2825.
41. Saenger, W. 1984. Principles of nucleic acid structure. Springer-Verlag, New York.
42. Scaringe, S.A., Francklyn, C., and Usman, N. 1990. Chemical synthesis of biologically active oligoribonucleotides using β-cyanoethyl protected ribonucleoside phosphoramidites. Nucleic Acids Res. 18: 5433-5441. doi: 10.1093/nar/18.18.5433.
43. Shih, I.H. and Been, M.D. 2001. Involvement of a cytosine side chain in proton transfer in the rate-determining step of ribozyme self-cleavage. Proc. Natl. Acad. Sci. 98: 1489-1494.
44. Siegfried, N.A., Metzger, S.L., and Bevilacqua, P.C. 2007. Folding cooperativity in RNA and DNA is dependent on position in the helix. Biochemistry 46: 172-181.
45. Sigel, R.K. and Pyle, A.M. 2007. Alternative roles for metal ions in enzyme catalysis and the implications for ribozyme chemistry. Chem. Rev. 107: 97-113.
46. Smith, M.D. and Collins, R.A. 2007. Evidence for proton transfer in the rate-limiting step of a fast-cleaving Varkud satellite ribozyme. Proc. Natl. Acad. Sci. 104: 5818-5823.
47. Sood, V.D. and Collins, R.A. 2001. Functional equivalence of the uridine turn and the hairpin as building blocks of tertiary structure in the Neurospora VS ribozyme. J. Mol. Biol. 313: 1013-1019.
48. Sood, V.D. and Collins, R.A. 2002. Identification of the catalytic subdomain of the VS ribozyme and evidence for remarkable sequence tolerance in the active site loop. J. Mol. Biol. 320: 443-454.
49. Strobel, S.A. 1999. A chemogenetic approach to RNA function/structure analysis. Curr. Opin. Struct. Biol. 9: 346-352.
50. as in RNA: On the structural origins and functional roles of protonated nucleotides. J. Mol. Biol. 366: 1475-1496.
51. Thomas, J.M. and Perrin, D.M. 2006. Active site labeling of G8 in the hairpin ribozyme: Implications for structure and mechanism. J. Am. Chem. Soc. 128: 16540-16545.
52. Weiss, J.N. 1997. The Hill equation revisited: Uses and misuses. FASEB J. 11: 835-841.
53. Wilson, T.J., Ouellet, J., Zhao, Z.Y., Harusawa, S., Araki, L., Kurihara, T., and Lilley, D.M. 2006. Nucleobase catalysis in the hairpin ribozyme. RNA 12: 980-987.
54. Wilson, T.J., McLeod, A.C., and Lilley, D.M. 2007. A guanine nucleobase important for catalysis by the VS ribozyme. EMBO J. 26: 2489-2500.
55. Wincott, F., DiRenzo, A., Shaffer, C., Grimm, S., Tracz, D., Workman, C., Sweedler, D., Gonzalez, C., Scaringe, S., and Usman, N. 1995. Synthesis, deprotection, analysis and purification of RNA and ribozymes. Nucleic Acids Res. 23: 2677-2684. doi: 10.1093/nar/23.14.2677.
56. Young, K.J., Gill, F., and Grasby, J.A. 1997. Metal ions play a passive role in the hairpin ribozyme catalysed reaction. Nucleic Acids Res. 25: 3760-3766. doi: 10.1093/nar/25.19.3760.
57. Zamel, R., Poon, A., Jaikaran, D., Andersen, A., Olive, J., De Abreu, D., and Collins, R.A. 2004. Exceptionally fast self-cleavage by a Neurospora Varkud satellite ribozyme. Proc. Natl. Acad. Sci. 101: 1467-1472.