Post-transcriptional modifications modulate conformational dynamics in human U2-U6 snRNA complex

RNA

Volumn 20, Issue 1, 2014, Pages 16-23

  Karunatilaka, Krishanthi S ^a   Rueda, David ^a,b  

^a WAYNE STATE UNIVERSITY   (United States)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Human U2 U6 snRNAs; Post transcriptional modifications; Single molecule FRET; Splicing; Structural dynamics

Indexed keywords

MAGNESIUM; MESSENGER RNA PRECURSOR; SMALL NUCLEAR RNA; U2 SMALL NUCLEAR RNA; U6 SMALL NUCLEAR RNA; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; IN VITRO STUDY; PRIORITY JOURNAL; RNA CONFORMATION; RNA SPLICING; RNA STABILITY; RNA STRUCTURE;

EID: 84890678626     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.041806.113     Document Type: Article

References (51)

1. Aleman EA, Lamichhane R, Rueda D. 2008. Exploring RNA folding one molecule at a time. Curr Opin Chem Biol 12: 647-654.
2. Arnez JG, Steitz TA. 1994. Crystal structure of unmodified tRNAGln complexed with glutaminyl-tRNA synthetase and ATP suggests a possible role for pseudo-uridines in stabilization of RNA structure. Biochemistry 33: 7560-7567.
3. Auffinger P, Westhof E. 1997. Rules governing the orientation of the 2-hydroxyl group in RNA. J Mol Biol 274: 54-63.
4. Brow DA, Guthrie C. 1988. Spliceosomal RNA U6 is remarkably conserved from yeast to mammals. Nature 334: 213-218.
5. Burke JE, Sashital DG, Zuo X, Wang YX, Butcher SE. 2012. Structure of the yeast U2/U6 snRNA complex. RNA 18: 673-683.
6. Butcher SE. 2011. The spliceosome and its metal ions. Met Ions Life Sci 9: 235-251.
7. Davis DR. 1995. Stabilization of RNA stacking by pseudouridine. Nucleic Acids Res 23: 5020-5026.
8. Donmez G, Hartmuth K, Luhrmann R. 2004. Modified nucleotides at the 5 end of human U2 snRNA are required for spliceosomal E-complex formation. RNA 10: 1925-1933.
9. Efron B, Gong G. 1983. A leisurely look at the bootstrap, the jackknife, and cross-validation. Am Stat 37: 36-48.
10. Galej WP, Oubridge C, Newman AJ, Nagai K. 2013. Crystal structure of Prp8 reveals active site cavity of the spliceosome. Nature 493: 638-643.
11. Gordon PM, Sontheimer EJ, Piccirilli JA. 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.
12. Guo Z, Karunatilaka KS, Rueda D. 2009. Single-molecule analysis of protein-free U2-U6 snRNAs. Nat Struct Mol Biol 16: 1154-1159.
13. Helm M. 2006. Post-transcriptional nucleotide modification and alternative folding of RNA. Nucleic Acids Res 34: 721-733.
14. Hilliker AK, Staley JP. 2004. Multiple functions for the invariant AGC triad of U6 snRNA. RNA 10: 921-928.
15. Huppler A, Nikstad LJ, Allmann AM, Brow DA, Butcher SE. 2002. Metal binding and base ionization in the U6 RNA intramolecular stemloop structure. Nat Struct Biol 9: 431-435.
16. Kalnina Z, Zayakin P, Silina K, Line A. 2005. Alterations of pre-mRNA splicing in cancer. Genes Chromosomes Cancer 42: 342-357.
17. Karijolich J, Yu YT. 2010. Spliceosomal snRNA modifications and their function. RNA Biol 7: 192-204.
18. Karunatilaka KS, Rueda D. 2009. Single-molecule fluorescence studies of RNA: A decade's progress. Chem Phys Lett 476: 1-10.
19. Lesser CF, Guthrie C. 1993. Mutations in U6 snRNA that alter splice site specificity: Implications for the active site. Science 262: 1982-1988.
20. Licatalosi DD, Darnell RB. 2006. Splicing regulation in neurologic disease. Neuron 52: 93-101.
21. Madhani HD, 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.
22. Massenet S, Mougin A, Branlant C. 1998. Posttranscriptional modifications in the U small nuclear RNAs. In The modification and editing of RNA. (ed. Grosjean H, Benne R), pp. 201-228. ASM Press, Washington, DC.
23. McKinney SA, Freeman AD, Lilley DM, Ha T. 2005. Observing spontaneous branch migration of Holliday junctions one step at a time. Proc Natl Acad Sci 102: 5715-5720.
24. Mefford MA, Staley JP. 2009. Evidence that U2/U6 helix I promotes both catalytic steps of pre-mRNA splicing and rearranges in between these steps. RNA 15: 1386-1397.
25. Newby MI, Greenbaum NL. 2002a. Investigation of Overhauser effects between pseudouridine and water protons in RNA helices. Proc Natl Acad Sci 99: 12697-12702.
26. Newby MI, Greenbaum NL. 2002b. Sculpting of the spliceosomal branch site recognition motif by a conserved pseudouridine. Nat Struct Biol 9: 958-965.
27. Newman A. 1998. RNA splicing. Curr Biol 8: R903-R905.
28. O'Keefe RT, Norman C, Newman AJ. 1996. The invariant U5 snRNA loop 1 sequence is dispensable for the first catalytic step of premRNA splicing in yeast. Cell 86: 679-689.
29. Parker R, Siliciano PG, Guthrie C. 1987. Recognition of the TACTAAC box during mRNA splicing in yeast involves base pairing to the U2-like snRNA. Cell 49: 229-239.
30. Pettigrew CA, Brown MA. 2008. Pre-mRNA splicing aberrations and cancer. Front Biosci 13: 1090-1105.
31. Rhode BM, Hartmuth K, Westhof E, Luhrmann R. 2006. Proximity of conserved U6 and U2 snRNA elements to the 5 splice site region in activated spliceosomes. EMBO J 25: 2475-2486.
32. Ritchie DB, Schellenberg MJ, MacMillan AM. 2009. Spliceosome structure: Piece by piece. Biochim Biophys Acta 1789: 624-633.
33. Rueda D, Walter NG. 2005. Single molecule fluorescence control for nanotechnology. J Nanosci Nanotechnol 5: 1990-2000.
34. Saltzman AL, Pan Q, Blencowe BJ. 2011. Regulation of alternative splicing by the core spliceosomal machinery. Genes Dev 25: 373-384.
35. Sashital DG, Cornilescu G, McManus CJ, Brow DA, Butcher SE. 2004. U2-U6 RNA folding reveals a group II intron-like domain and a four-helix junction. Nat Struct Mol Biol 11: 1237-1242.
36. Sashital DG, Venditti V, Angers CG, Cornilescu G, Butcher SE. 2007. Structure and thermodynamics of a conserved U2 snRNA domain from yeast and human. RNA 13: 328-338.
37. Segault V, Will CL, Polycarpou-Schwarz M, Mattaj IW, Branlant C, Luhrmann R. 1999. Conserved loop I of U5 small nuclear RNA is dispensable for both catalytic steps of pre-mRNA splicing in HeLa nuclear extracts. Mol Cell Biol 19: 2782-2790.
38. Sontheimer EJ, Gordon PM, Piccirilli JA. 1999. Metal ion catalysis during group II intron self-splicing: Parallels with the spliceosome. Genes Dev 13: 1729-1741.
39. Stark H, Luhrmann R. 2006. Cryo-electron microscopy of spliceosomal components. Annu Rev Biophys Biomol Struct 35: 435-457.
40. Steiner M, Karunatilaka KS, Sigel RK, Rueda D. 2008. Single-molecule studies of group II intron ribozymes. Proc Natl Acad Sci 105: 13853-13858.
41. Sun JS, Manley JL. 1995. A novel U2-U6 snRNA structure is necessary for mammalian mRNA splicing. Genes Dev 9: 843-854.
42. Valadkhan S, Manley JL. 2001. Splicing-related catalysis by protein-free snRNAs. Nature 413: 701-707.
43. Valadkhan S, Manley JL. 2003. Characterization of the catalytic activity of U2 and U6 snRNAs. RNA 9: 892-904.
44. Valadkhan S, Mohammadi A, Jaladat Y, Geisler S. 2009. Protein-free small nuclear RNAs catalyze a two-step splicing reaction. Proc Natl Acad Sci 106: 11901-11906.
45. Wahl MC, Will CL, Luhrmann R. 2009. The spliceosome: Design principles of a dynamic RNP machine. Cell 136: 701-718.
46. Will CL, Luhrmann R. 2011. Spliceosome structure and function. Cold Spring Harb Perspect Biol 3: A003707.
47. Wolff T, Bindereif A. 1993. Conformational changes of U6 RNA during the spliceosome cycle: An intramolecular helix is essential both for initiating the U4-U6 interaction and for the first step of slicing. Genes Dev 7: 1377-1389.
48. Yean SL, Wuenschell G, Termini J, Lin RJ. 2000. Metal-ion coordination by U6 small nuclear RNA contributes to catalysis in the spliceosome. Nature 408: 881-884.
49. Yu YT, Shu MD, Steitz JA. 1998. Modifications of U2 snRNA are required for snRNP assembly and pre-mRNA splicing. EMBO J 17: 5783-5795.
50. Zhao R, Rueda D. 2009. RNA folding dynamics by single-molecule fluorescence resonance energy transfer. Methods 49: 112-117.
51. Zhao C, Bachu R, Popovic M, Devany M, Brenowitz M, Schlatterer JC, Greenbaum NL. 2013. Conformational heterogeneity of the proteinfree human spliceosomal U2-U6 snRNA complex. RNA 19: 561-573.