Distinct sites of phosphorothioate substitution interfere with folding and splicing of the Anabaena group I intron

Nucleic Acids Research

Volumn 32, Issue 7, 2004, Pages 2272-2280

  Lupták, Andrej ^a,c   Doudna, Jennifer A ^a,b  

^a YALE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; GUANIDINE; HELIX LOOP HELIX PROTEIN; MAGNESIUM ION; PHOSPHATE; PHOSPHOROTHIOIC ACID DERIVATIVE; RNA; THYMINE; LEUCINE TRANSFER RNA; NUCLEOTIDE; RIBOZYME; RNA PRECURSOR;

ANABAENA; ARTICLE; AZOARCUS; BINDING SITE; CATALYSIS; CONTROLLED STUDY; GENETIC CONSERVATION; GENETIC VARIABILITY; INTRON; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN STABILITY; RNA INTERFERENCE; RNA STRUCTURE; TETRAHYMENA; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA SPLICING;

ANABAENA; AZOARCUS; TETRAHYMENA;

ANABAENA; BASE SEQUENCE; BINDING SITES; INTRONS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA PRECURSORS; RNA SPLICING; RNA, CATALYTIC; RNA, TRANSFER, LEU; THIONUCLEOTIDES;

EID: 2342522611     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkh548     Document Type: Article

References (41)

1. Strauss-Soukup,J.K. and Strobel,S.A. (2000) A chemical phylogeny of group I introns based upon interference mapping of a bacterial ribozyme. J. Mol. Biol., 302, 339-358.
2. 2+ binding in the group I intron core. J. Mol. Biol., 329, 229-238.
3. Xu,M.Q., Kathe,S.D., Goodrich-Blair,H., Nierzwicki-Bauer,S.A. and Shub,D.A. (1990) Bacterial origin of a chloroplast intron: conserved self-splicing group I introns in cyanobacteria. Science, 250, 1566-1570.
4. Zaug,A.J., McEnvoy,M.M. and Cech,T.R. (1993) Self-splicing of the group I intron from Anabaena pre-tRNA: requirement for base-pairing of the exons in the anticodon stem. Biochemistry, 32, 7946-7953.
5. Engelhardt,M.A., Doherty,E.A., Knitt,D.S., Doudna,J.A. and Herschlag,D. (2000) The P5abc peripheral element facilitates preorganization of the Tetrahymena group I ribozyme for catalysis. Biochemistry, 39, 2639-2651.
6. Lehnert,V., Jaeger,L., Michel,F. and Westhof,E. (1996) New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem Biol., 3, 993-1009.
7. Doudna,J.A. and Szostak,J.W. (1989) Miniribozymes, small derivatives of the sunY intron, are catalytically active. Mol. Cell. Biol., 9, 5480-5483.
8. leu. Biochemistry, 33, 14935-14947.
9. Ryder,S.P. and Strobel,S.A. (1999) Nucleotide analog interference mapping. Methods, 18, 38-50.
10. Bruce,A.G. and Uhlenbeck,O.C. (1978) Reactions at the termini of tRNA with T4 RNA ligase. Nucleic Acids Res., 5, 3665-3677.
11. Gish,G. and Eckstein,F. (1988) DNA and RNA sequence determination based on phophorothioate chemistry. Science, 240, 1520-1522.
12. Tanner,M.A. and Cech,T.R. (1996) Activity and thermostability of the small self-splicing group I intron in the pre-tRNAile of the purple bacterium Azoarcus. RNA, 2, 74-83.
13. 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. USA, 100, 1574-1579.
14. Reinhold-Hurek,B. and Shub,D.A. (1992) Self-splicing introns in tRNA genes of widely divergent bacteria. Nature, 357, 173-176.
15. Buchemueller,K.L., Webb,A.E., Richardson,D.A, and Weeks,K.M. (2000) A collapsed non-native RNA folding state. Nature Struct. Biol., 7, 362-366.
16. Cate,J.H., Hanna,R.L. and Doudna,J.A. (1997) A magnesium ion core at the heart of a ribozyme domain. Nature Struct. Biol., 4, 553-558.
17. Tanner,M.A. and Cech,T.R. (1997) Joining the two domains of a group I ribozyme to form the catalytic core. Science, 275, 847-849.
18. Cannone,J.J., Subramanian,S., Schnare,M.N., Collett,J.R., D'Souza,L.M., Du,Y., Feng,B., Lin,N., Madabusi,L.V., Muller,K.M. et al. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron and other RNAs. BMC Bioinformatics, 3, 2.
19. Golden,B.L., Gooding,A.R., Podell,E.R. and Cech,T.R. (1998) A preorganized active site in the crystal structure of the Tetrahymena ribozyme. Science, 282, 259-264.
20. Waldsich,C., Masquida,B., Westhof,E. and Schroeder,R. (2002) Monitoring intermediate folding states of the td group I intron in vivo. EMBO J., 21, 5281-5291.
21. Jaeger,L., Michel,F. and Westhof,E. (1994) Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J. Mol. Biol., 236, 1271-1276.
22. Rüdisser,S. and Tinoco,I.J. (2000) Solution structure of cobalt(III) hexammine complexed to the GAAA tetraloop and metal-ion binding to G.A mismatches. J. Mol. Biol., 295, 1211-1223.
23. 31 P NMR and phosphorothioate substitutions. Biochemistry, 39, 8193-8200.
24. Horton,T.E., Maderia,M. and DeRose,V.J. (2000) Impact of phosphorothioate substitutions on the thermodynamic stability of an RNA GAAA tertraloop: an unexpected stabilization. Biochemistry, 39, 8201-8207.
25. Costa,M. and Michel,F. (1995) Frequent use of the same tertiary motif by self-folding RNAs. EMBO J., 14, 1276-1285.
26. Tanner,M.A. and Cech,T.R. (1995) An important RNA tertiary interaction of group I and group II introns is implicated in gram-positive RNase P RNAs. RNA, 1, 349-350.
27. Proctor,D.J., Schaak,J.E., Bevilacqua,J.M., Falzone,C.J. and Bevilacqua,P.C. (2002) Isolation and characterization of a family of stable RNA tetraloops with the motif YNMG that participate in tertiary interactions. Biochemistry, 41, 12062-12075.
28. Wimberly,B.T., Brodersen,D.E., Clemons,W.M., Jr., Morgan-Warren,R.J., Carter,A.P., Vonrhein,C., Hartsch,T. and Ramakrishnan,V. (2000) Structure of the 30S ribosomal subunit. Nature, 407, 327-339.
29. Lippard,S.J. and Berg,J.M. (1994) Principles of Bioinorganic Chemistry. University Science Books, Mill Valley, CA.
30. Frey,P.A. and Sammons,R.D. (1985) Bond order and charge localization in nucleoside phosphorothioates. Science, 228, 541-545.
31. Brautigam,C.A. and Steitz,T.A. (1998) Structural principles for the inhibition of the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I by phosphorothioates. J. Mol. Biol., 277, 363-377.
32. Smith,J.S. and Nikonowicz,E.P. (2000) Phosphorothioate substitution can substantially alter RNA conformation. Biochemistry, 39, 5642-5652.
33. Schwans,J.P., Cortez,C.N., Olvera,J.M. and Piccirilli,J.A. (2003) 2′-Mercaptonucleotide interference reveals regions of close packing within folded RNA molecules. J. Am. Chem. Soc., 125, 10012-10018.
34. Basu,S. and Strobel,S.A. (1999) Thiophilic metal ion rescue of phosphorothioate interference within the Tetrahymena ribozyme P4-P6 domain. RNA, 5, 1399-1407.
35. 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 intron ribozyme domain: principles of RNA packing. Science, 273, 1678-1685.
36. Basu,S., Rambo,R.P., Strauss-Soukup,J., Cate,J.H., Ferré D'Amaré,A.R., Strobel,S.A. and Doudna,J.A. (1998) A specific monovalent metal ion integral to the AA platform of the RNA tetraloop receptor. Nature Struct. Biol., 5, 986-992.
37. Christian,E.L. and Yarus,M. (1992) Analysis of the role of phosphate oxygens in the group I intron from Tetrahymena. J. Mol. Biol., 228, 743-758.
38. Christian,E.L. and Yarus,M. (1993) Metal coordination sites that contribute to structure and catalysis in the group I intron from Tetrahymena. Biochemistry, 32, 4475-4480.
39. Zarrinkar,P.P. and Williamson,J.R. (1994) Kinetic intermediates in RNA folding. Science, 265, 918-924.
40. Sclavi,B., Sullivan,M., Chance,M.R., Brenowitz,M. and Woodson,S. (1998) RNA folding at milisecond intervals by synchrotron hydroxyl radical footprinting. Science, 279, 1940-1943.
41. Doherty,E.A., Herschlag,D. and Doudna,J.A. (1999) Assembly of an exceptionally stable RNA tertiary interface in a group I ribozyme. Biochemistry, 38, 2982-2990.