Use of a novel Förster resonance energy transfer method to identify locations of site-bound metal ions in the U2-U6 snRNA complex

Nucleic Acids Research

Volumn 35, Issue 9, 2007, Pages 2833-2845

  Yuan, Faqing ^a   Griffin, Laura ^a   Phelps, Laura Jane ^a   Buschmann, Volker ^a,b   Weston, Kenneth ^a   Greenbaum, Nancy L ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b PICOQUANT GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; GUANINE; LANTHANIDE; SMALL NUCLEAR RNA; CARBOCYANINE; CYANINE DYE 3; FLUORESCENT DYE; ION; TERBIUM; U2 SMALL NUCLEAR RNA; U6 SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; COMPLEX FORMATION; CONSENSUS SEQUENCE; COVALENT BOND; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; NUCLEAR MAGNETIC RESONANCE; PH; PRIORITY JOURNAL; RNA SPLICING; STOICHIOMETRY; BASE PAIRING; CHEMISTRY; CONFORMATION; METABOLISM; METHODOLOGY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE;

BASE PAIRING; BASE SEQUENCE; BINDING SITES; CARBOCYANINES; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT DYES; HUMANS; HYDROGEN-ION CONCENTRATION; IONS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEIC ACID CONFORMATION; RNA, SMALL NUCLEAR; TERBIUM;

EID: 34250674526     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm134     Document Type: Article

References (47)

1. Brow,D.A. (2002) Allosteric cascade of spliceosome activation. Annu. Rev. Genet., 36, 333-360.
2. Datta,B. and Weiner,A.M. (1991) Genetic evidence for base pairing between U2 and U6 snRNA in mammalian mRNA splicing. Nature, 352 821-824.
3. Wu,J.A. and Manley,J.L. (1991) Base pairing between U2 and U6 snRNAs is necessary for splicing of a mammalian pre-mRNA. Nature, 352, 818-821.
4. Madhani,H.D. and Guthrie,C. (1992) A novel base-pairing interaction between U2 and U6 snRNAs suggests a mechanism for the catalytic activation of the spliceosome. Cell, 71, 803-817.
5. Madhani,H.D. and Guthrie,C. (1994) Randomization-selection analysis of snRNAs in vivo: Evidence for a tertiary interaction in the spliceosome. Genes. Dev., 8, 1071-1086.
6. Sun,J. and Manley,J. (1995) A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev., 9, 843-854.
7. Valadkhan,S. and Manley,J.L. (2003) Characterization of the catalytic activity of U2 and U6 snRNAs. RNA, 9, 892-904.
8. Valadkhan,S. and Manley,J.L. (2001) Splicing-related catalysis by protein-free snRNAs. Nature, 413, 701-707.
9. Fedor,M.J. (2002) The role of metal ions in RNA catalysis. Curr. Opin. Struct. Biol., 12, 289-295.
10. Fabrizio,P. and Abelson,J. (1992) Thiophosphates in yeast U6 snRNA specifically affect pre-mRNA splicing in vitro. Nucleic Acids Res. 20, 3659-3664.
11. Yu,Y.T., Maroney,P.A., Darzynkiwicz,E. and Nilsen,T.W. (1995) U6 snRNA function in nuclear pre-mRNA splicing: A phosphorothioate interference analysis of the U6 phosphate back-bone. RNA, 1, 46-54.
12. Gordon,P.M., Sontheimer,E.J. and Piccirilli,J.A. (2000) Metal ion catalysis during the exon-ligation step of nuclear pre-mRNA splicing: extending the parallels between the spliceosome and group II introns. RNA, 6, 199-205.
13. Valadkhan,S. and Manley,J.L. (2000) A tertiary interaction detected in a human U2-U6 snRNA complex assembled in vitro resembles a genetically proven interaction in yeast. RNA, 6, 206-219.
14. Huppler,A., Nikstad,L.J., Allmann,A.M., Brow,D.A. and Butcher,S.E. (2002) Metal binding and base ionization in the U6 RNA intramolecular stem-loop structure. Nat. Struct. Biol., 9, 431-435.
15. Evans,C.H. (1990) Biochemistry of the Lanthanides. Plenum Press, New York.
16. Horrocks,W.D. Jr., Schmidt,G.F., Sudnick,D.R., Kittrell,C. and Bernheim,R.A. (1977) Laser-induced lanthanide ion luminescence lifetime measurements by direct excitation of metal ion levels. A new class of structural probe for calcium-binding proteins and nucleic acids. J. Am. Chem. Soc., 99, 2378-2380.
17. Horrocks,W.D. Jr. and Sudnick,D.R. (1979) Lanthanide ion probes of structure in biology. Laser induced luminescence decay constants provide a direct measure of the number of metal coordinated water molecules. J. Am. Chem. Soc., 334-340.
18. Jack,A., Ladner,J.E., Rhodes,D., Brown,R.S. and Klug,A. (1977) A crystallographic study of metal-binding to yeast phenylalanine transfer RNA. J. Mol. Biol., 111, 315-328.
19. Greenbaum,N.L., Mundoma,C. and Peterman,D.R. (2001) Probing of metal-binding domains of RNA hairpin loops by laser-induced lanthanide(III) luminescence. Biochemistry, 40, 1124-1134.
20. Draper,D.E. (1985) On the coordination properties of Eu3+ bound to tRNA. Biophys. Chem., 21, 91-101.
21. Feig,A.L., Scott,W.G. and Uhlenbeck,O.C. (1998) Inhibition of the hammerhead ribozyme cleavage reaction by site-specific binding of Tb. Science, 279, 81-84.
22. Selvin,P.R. and Hearst,J.E. (1994) Luminescence energy transfer using a terbium chelate: Improvements on fluorescence energy transfer. Proc. Natl. Acad. Sci. USA, 91, 10024-10028.
23. Selvin,P.R. (2002) Principles and biophysical applications of lanthanide-based probes. Annu. Rev. Biophys. Biomol. Struct., 31, 275-302.
24. Periasamy,A. and Day, N.R. (eds), (2005) Molecular Imaging: FRET Microscopy and Spectroscopy. Oxford University Press, New York, Oxford.
25. Clegg,R. (1992) Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol., 211, 352-388.
26. Burmeister Getz,E., Cooke,R. and Selvin,P.R. (1998) Luminescence resonance energy transfer measurements in myosin. Biophys J., 74, 2451-2458.
27. Ha,T., Rasnik,I., Cheng,W., Babcock,H.P., Gauss,G.H., Lohman,T.M. and Chu,S. (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature, 419, 638-641.
28. Xiao,M. and Selvin,P. (2001) Quantum yields of luminescent lanthanide chelates and far-red dyes measured by resonance energy transfer. J. Am. Chem. Soc., 123, 7067-7073.
29. He,B., Rong,M., Lyakhov,D., Gartenstein,H., Diaz,G., Castagna,R., McAllister,W.T. and Durbin,R.K. (1997) Rapid mutagenesis and purification of phage RNA polymerases. Protein Expr. Purif., 9 142-151.
30. Matsumura,K. and Komiyama,M. (1997) Enormously fast RNA hydrolysis by lanthanide(III) ions under physiological conditions: Eminent candidates for novel tools of biotechnology. J. Biochem. (Tokyo), 122, 387-394.
31. Costa,D., Burrows,H.D. and da Graca Miguel,M. (2005) Changes in hydration of lanthanide ions on binding to DNA in aqueous solution. Langmuir, 21, 10492-10496.
32. Huang,C.Y. (1982) Determination of binding stoichiometry by the continuous variation method: The Job plot. Methods Enzymol., 87 509-525.
33. Thomas,D.D., Carlsen,W.F. and Stryer,L. (1978) Fluorescence energy transfer in the rapid-diffusion limit. Proc. Natl. Acad. Sci. USA, 75, 5746-5750.
34. Norman,D.G., Grainger,R.J., Uhrin,D. and Lilley,D.M. (2000) Location of cyanine-3 on double-stranded DNA: Importance for fluorescence resonance energy transfer studies. Biochemistry, 39, 6317-6324.
35. Xu,D., Greenbaum,N.L. and Fenley,M.O. (2005) Recognition of the spliceosomal branch site RNA helix on the basis of surface and electrostatic features. Nucleic Acids Res., 33, 1154-1161.
36. Chen,X., McDowell,J.A., Kierzek,R., Krugh,T.R. and Turner,D.H. (2000) Nuclear magnetic resonance spectroscopy and molecular modeling reveal that different hydrogen bonding patterns are possible for G.U pairs: One hydrogen bond for each G.U pair in r(GGCGUGCC)(2) and two for each G.U pair in r(GAGUGCUC)(2). Biochemistry, 39, 8970-8982.
37. Wolfson,J.M. and Kearns,D.R. (1975) Europium as a fluorescent probe of transfer RNA structure. Biochemistry, 14, 1436-1444.
38. Marciniec,T., Ciesiolka,J., Wrzesinski,J. and Krzyzosiak,W.J. (1989) Identification of the magnesium, europium and lead binding sites in E. coli and lupine tRNAPhe by specific metal ion-induced cleavages. FEBS Lett., 243, 293-298.
39. Hargittai,M.R. and Musier-Forsyth,K. (2000) Use of terbium as a probe of tRNA tertiary structure and folding. RNA, 6, 1672-1680.
40. Mundoma,C. and Greenbaum,N.L. (2002) Sequestering of Eu(III) by a GAAA RNA tetraloop. J. Am. Chem. Soc., 124, 3525-3532.
41. Feig,A.L., Panek,M., Horrocks,W.D. Jr. and Uhlenbeck,O.C. (1999) Probing the binding of Tb(III) and Eu(III) to the hammerhead ribozyme using luminescence spectroscopy. Chem. Biol., 6, 801-810.
42. Misra,V.K. and Draper,D.E. (1998) On the role of magnesium ions in RNA stability. Biopolymers, 48, 113-135.
43. 2+ binding sites of the 5S rRNA loop E motif as investigated by molecular dynamics simulations. Chem. Biol., 10, 551-561.
44. Blad,H., Reiter,N.J., Abildgaard,F., Markley,J.L. and Butcher,S.E. (2005) Dynamics and metal ion binding in the U6 RNA intramolecular stem-loop as analyzed by NMR. J. Mol. Biol., 353, 540-555.
45. Newby,M.I. and Greenbaum,N.L. (2002) Sculpting of the spliceosomal branch site recognition motif by a conserved pseudouridine. Nat. Struct. Biol., 9, 958-965.
46. Sashital,D.G., Cornilescu,G., McManus,C.J., Brow,D.A. and Butcher,S.E. (2004) U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat. Struct. Mol. Biol., 11, 1237-1242.
47. Butcher,S.E. (2001) Structure and function of the small ribozymes. Curr. Opin. Struct. Biol., 11, 315-320.