Single-molecule colocalization FRET evidence that spliceosome activation precedes stable approach of 5' splice site and branch site

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 17, 2013, Pages 6783-6788

  Crawford, Daniel J ^a,b,c   Hoskins, Aaron A ^a,b,d   Friedman, Larry J ^b   Gelles, Jeff ^b   Moore, Melissa J ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

RNA dynamics; Single molecule FRET; Splicing mechanism

Indexed keywords

MESSENGER RNA; MESSENGER RNA PRECURSOR; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; ENERGY TRANSFER; EXON; INTRON; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA SPLICING; SPLICEOSOME;

BASE SEQUENCE; DNA PRIMERS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, FLUORESCENCE; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OLIGONUCLEOTIDES; RNA SPLICE SITES; RNA SPLICING; SACCHAROMYCES CEREVISIAE; SPECTRUM ANALYSIS; SPLICEOSOMES;

EID: 84876875040     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1219305110     Document Type: Article

References (30)

1. Nilsen TW (2003) The spliceosome: The most complex macromolecular machine in the cell? Bioessays 25(12):1147-1149.
2. Moore MJ, Sharp PA (1993) Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nature 365(6444):364-368.
3. Wahl MC, Will CL, Lührmann R (2009) The spliceosome: Design principles of a dynamic RNP machine. Cell 136(4):701-718.
4. Hoskins AA, Moore MJ (2012) The spliceosome: A flexible, reversible macromolecular machine. Trends Biochem Sci 37(5):179-188.
5. Brow DA (2002) Allosteric cascade of spliceosome activation. Annu Rev Genet 36: 333-360.
6. Gozani O, Potashkin J, Reed R (1998) A potential role for U2AF-SAP 155 interactions in recruiting U2 snRNP to the branch site. Mol Cell Biol 18(8):4752-4760.
7. Valcárcel J, Gaur RK, Singh R, Green MR (1996) Interaction of U2AF65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA [corrected]. Science 273(5282):1706-1709.
8. Kent OA, MacMillan AM (2002) Early organization of pre-mRNA during spliceosome assembly. Nat Struct Biol 9(8):576-581.
9. MacMillan AM, et al. (1994) Dynamic association of proteins with the pre-mRNA branch region. Genes Dev 8(24):3008-3020.
10. McPheeters DS, Muhlenkamp P (2003) Spatial organization of protein-RNA interactions in the branch site-3′ splice site region during pre-mRNA splicing in yeast. Mol Cell Biol 23(12):4174-4186.
11. Dönmez G, Hartmuth K, Kastner B, Will CL, Lührmann R (2007) The 5′ end of U2 snRNA is in close proximity to U1 and functional sites of the pre-mRNA in early spliceosomal complexes. Mol Cell 25(3):399-411.
12. Abovich N, Liao XC, Rosbash M (1994) The yeast MUD2 protein: An interaction with PRP11 defines a bridge between commitment complexes and U2 snRNP addition. Genes Dev 8(7):843-854.
13. Séraphin B, Rosbash M (1991) The yeast branchpoint sequence is not required for the formation of a stable U1 snRNA-pre-mRNA complex and is recognized in the absence of U2 snRNA. EMBO J 10(5):1209-1216.
14. Friedman LJ, Chung J, Gelles J (2006) Viewing dynamic assembly of molecular complexes by multi-wavelength single-molecule fluorescence. Biophys J 91(3):1023-1031.
15. Hoskins AA, et al. (2011) Ordered and dynamic assembly of single spliceosomes. Science 331(6022):1289-1295.
16. McPheeters DS, Fabrizio P, Abelson J (1989) In vitro reconstitution of functional yeast U2 snRNPs. Genes Dev3(12B):2124-2136.
17. Fabrizio P, McPheeters DS, Abelson J (1989) In vitro assembly of yeast U6 snRNP: A functional assay. Genes Dev3(12B):2137-2150.
18. Fabrizio P, et al. (2009) The evolutionary conserved core design of the catalytic activation step of the yeast spliceosome. Mol Cell 36(4):593-608.
19. dos Remedios CG, Moens PD (1995) Fluorescence resonance energy transfer spectroscopy is a reliable "ruler" for measuring structural changes in proteins. Dispelling the problem of the unknown orientation factor. J Struct Biol 115(2):175-185.
20. Abelson J, et al. (2010) Conformational dynamics of single pre-mRNA molecules during in vitro splicing. Nat Struct Mol Biol 17(4):504-512.
21. Hogg R, McGrail JC, O'Keefe RT (2010) The function of the NineTeen Complex (NTC) in regulating spliceosome conformations and fidelity during pre-mRNA splicing. Bio-chem Soc Trans 38(4):1110-1115.
22. Chan S-P, Cheng S-C (2005) The Prp19-associated complex is required for specifying interactions of U5 and U6 with pre-mRNA during spliceosome activation. J Biol Chem 280(35):31190-31199.
23. Rasche N, et al. (2012) Cwc2 and its human homologue RBM22 promote an active conformation of the spliceosome catalytic centre. EMBO J 31(6):1591-1604.
24. Guo Z, Karunatilaka KS, Rueda D (2009) Single-molecule analysis of protein-free U2-U6 snRNAs. Nat Struct Mol Biol 16(11):1154-1159.
25. Ohrt T, et al. (2012) Prp2-mediated protein rearrangements at the catalytic core of the spliceosome as revealed by dcFCCS. RNA 18(6):1244-1256.
26. Semlow DR, Staley JP (2012) Staying on message: Ensuring fidelity in pre-mRNA splicing. Trends Biochem Sci 37(7):263-273.
27. Tseng C-K, Liu H-L, Cheng S-C (2011) DEAH-box ATPase Prp16 has dual roles in remodeling of the spliceosome in catalytic steps. RNA 17(1):145-154.
28. Liu Y-C, Chen H-C, Wu N-Y, Cheng S-C (2007) A novel splicing factor, Yju2, is associated with NTC and acts after Prp2 in promoting the first catalytic reaction of pre-mRNA splicing. Mol Cell Biol 27(15):5403-5413.
29. Warkocki Z, et al. (2009) Reconstitution of both steps of Saccharomyces cerevisiae splicing with purified spliceosomal components. Nat Struct Mol Biol 16(12):1237-1243.
30. Bronson JE, Fei J, Hofman JM, Gonzalez RL, Jr., Wiggins CH (2009) Learning rates and states from biophysical time series: A Bayesian approach to model selection and single-molecule FRET data. Biophys J 97(12):3196-3205.