Metal binding and substrate positioning by evolutionarily invariant U6 sequences in catalytically active protein-free snRNAs

RNA

Volumn 16, Issue 11, 2010, Pages 2226-2238

  Lee, Caroline ^a   Jaladat, Yasaman ^a   Mohammadi, Afshin ^a   Sharifi, Armin ^a   Geisler, Sarah ^a   Valadkhan, Saba ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Catalysis; Ribozyme; snRNA; Spliceosome; U6

Indexed keywords

ENZYME; SMALL NUCLEAR RNA; TERBIUM;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; CATALYSIS; ENZYME ACTIVE SITE; ENZYME MECHANISM; EVOLUTION; INTRON; METAL BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; RNA SEQUENCE; SPLICEOSOME;

BASE SEQUENCE; EXONS; HUMANS; MAGNESIUM; MOLECULAR SEQUENCE DATA; RNA SPLICING; RNA, CATALYTIC; RNA, SMALL NUCLEAR; SUBSTRATE SPECIFICITY;

EID: 78149354420     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.2170910     Document Type: Article

References (63)

1. Abelson J. 2008. Is the spliceosome a ribonucleoprotein enzyme? Nat Struct Mol Biol 15: 1235-1237.
2. Butcher SE. 2009. The spliceosome as ribozyme hypothesis takes a second step. Proc Natl Acad Sci 106: 12211-12212.
3. Cech TR. 1986. The generality of self-splicing RNA: Relationship to nuclear mRNA splicing. Cell 44: 207-210.
4. Chu VT, Liu Q, Podar M, Perlman PS, Pyle AM. 1998. More than one way to splice an RNA: Branching without a bulge and splicing without branching in group II introns. RNA 4: 1186-1202.
5. Cochrane JC, Strobel SA. 2008. Catalytic strategies of self-cleaving ribozymes. Acc Chem Res 41: 1027-1035.
6. Collins CA, Guthrie C. 2000. The question remains: Is the spliceosome a ribozyme? Nat Struct Biol 7: 850-854.
7. Collins CA, Guthrie C. 2001. Genetic interactions between the 5′ and 3′ splice site consensus sequences and U6 snRNA during the second catalytic step of pre-mRNA splicing. RNA 7: 1845-1854.
8. Datta B, Weiner AM. 1993. The phylogenetically invariant ACAGAGA and AGC sequences of U6 small nuclear RNA are more tolerant of mutation in human cells than in Saccharomyces cerevisiae. Mol Cell Biol 13: 5377-5382.
9. Davis JH, Foster TR, Tonelli M, Butcher SE. 2007. Role of metal ions in the tetraloop-receptor complex as analyzed by NMR. RNA 13: 76-86. (Pubitemid 46026182)
10. Dayie KT, Padgett RA. 2008. A glimpse into the active site of a group II intron and maybe the spliceosome, too. RNA 14: 1697-1703.
11. Fabrizio P, Abelson J. 1990. Two domains of yeast U6 small nuclear RNA required for both steps of nuclear precursor messenger RNA splicing. Science 250: 404-409.
12. Fabrizio P, Abelson J. 1992. Thiophosphates in yeast U6 snRNA specifically affect pre-mRNA splicing in vitro. Nucleic Acids Res 20: 3659-3664.
13. Fedor MJ, Williamson JR. 2005. The catalytic diversity of RNAs. Nat Rev Mol Cell Biol 6: 399-412.
14. Forconi M, Lee J, Lee JK, Piccirilli JA, Herschlag D. 2008. Functional identification of ligands for a catalytic metal ion in group I introns. Biochemistry 47: 6883-6894.
15. Frederiksen JK, Piccirilli JA. 2009. Identification of catalytic metal ion ligands in ribozymes. Methods 49: 148-166.
16. Gordon PM, Piccirilli JA. 2001. Metal ion coordination by the AGC triad in domain 5 contributes to group II intron catalysis. Nat Struct Biol 8: 893-898.
17. 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.
18. Harris DA, Walter NG. 2003. Probing RNA structure and metalbinding sites using terbium(III) footprinting. Curr Protoc Nucleic Acid Chem Chapter 6: Unit 6.8.
19. Heilman-Miller SL, Pan J, Thirumalai D, Woodson SA. 2001. Role of counterion condensation in folding of the Tetrahymena ribozyme. II. Counterion-dependence of folding kinetics. J Mol Biol 309: 57-68. (Pubitemid 32553507)
20. Hilliker AK, Staley JP. 2004. Multiple functions for the invariant AGC triad of U6 snRNA. RNA 10: 921-928.
21. Hougland JL, Kravchuk AV, Herschlag D, Piccirilli JA. 2005. Functional identification of catalytic metal ion binding sites within RNA. PLoS Biol 3: e277. doi: 10.1371/journal.pbio.0030277.
22. Huppler A, Nikstad LJ, Allmann AM, Brow DA, Butcher SE. 2002. Metal binding and base ionization in the U6 RNA intramolecular stem-loop structure. Nat Struct Biol 9: 431-435.
23. Kandels-Lewis S, Séraphin B. 1993. Involvement of U6 snRNA in 5′ splice site selection. Science 262: 2035-2039. (Pubitemid 124000645)
24. Keating KS, Toor N, Perlman PS, Pyle AM. 2010. A structural analysis of the group II intron active site and implications for the spliceosome. RNA 16: 1-9.
25. Konarska MM, Vilardell J, Query CC. 2006. Repositioning of the reaction intermediate within the catalytic center of the spliceosome. Mol Cell 21: 543-553.
26. Lehmann K, Schmidt U. 2003. Group II introns: Structure and catalytic versatility of large natural ribozymes. Crit Rev Biochem Mol Biol 38: 249-303.
27. Lesser CF, Guthrie C. 1993. Mutations in U6 snRNA that alter splice site specificity: Implications for the active site. Science 262: 1982-1988.
28. Luukkonen BG, Séraphin B. 1998. Genetic interaction between U6 snRNA and the first intron nucleotide in Saccharomyces cerevisiae. RNA 4: 167-180.
29. 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.
30. Madhani HD, Bordonné R, Guthrie C. 1990. Multiple roles for U6 snRNA in the splicing pathway. Genes Dev 4: 2264-2277.
31. McPheeters DS. 1996. Interactions of the yeast U6 RNA with the pre-mRNA branch site. RNA 2: 1110-1123.
32. Michel F, Costa M, Westhof E. 2009. The ribozyme core of group II introns: A structure in want of partners. Trends Biochem Sci 34: 189-199.
33. Moore MJ, Sharp PA. 1993. Evidence for two active sites in the spliceosome provided by stereochemistry of pre-mRNA splicing. Nature 365: 364-368.
34. Narlikar GJ, Herschlag D. 1997. Mechanistic aspects of enzymatic catalysis: Lessons from comparison of RNA and protein enzymes. Annu Rev Biochem 66: 19-59. (Pubitemid 27274651)
35. Newman AJ, Nagai K. 2010. Structural studies of the spliceosome: Blind men and an elephant. Curr Opin Struct Biol 20: 82-89.
36. Nilsen TW. 1998. RNA-RNA interactions in nuclear pre-mRNA splicing. In RNA structure and function (eds. RW Simons and M Grunberg-Manago), pp. 279-307. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
37. Podar M, Chu VT, Pyle AM, Perlman PS. 1998. Group II intron splicing in vivo by first-step hydrolysis. Nature 391: 915-918.
38. Pyle AM, Green JB. 1994. Building a kinetic framework for group II intron ribozyme activity: Quantitation of interdomain binding and reaction rate. Biochemistry 33: 2716-2725.
39. Pyle AM, Lambowitz AM. 2006. Group II introns: Ribozymes that splice RNA and invade DNA. In The RNA world (eds. RF Gesteland, TR Cech, and JF Atkins), pp. 469-506. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Reiter NJ, Nikstad LJ, Allmann AM, Johnson RJ, Butcher SE. 2003. Structure of the U6 RNA intramolecular stem-loop harboring an S(P)-phosphorothioate modification. RNA 9: 533-542.
41. Roychowdhury-Saha M, Burke DH. 2007. Distinct reaction pathway promoted by non-divalent-metal cations in a tertiary stabilized hammerhead ribozyme. RNA 13: 841-848.
42. Shan SO, Yoshida A, Sun S, Piccirilli JA, Herschlag D. 1999. Three metal ions at the active site of the Tetrahymena group I ribozyme. Proc Natl Acad Sci 96: 12299-12304.
43. Sharp PA. 1985. On the origin of RNA splicing and introns. Cell 42: 397-400.
44. Sigel RKO, Pyle AM. 2003. Lanthanide ions as probes for metal ions in the structure and catalytic mechanism of ribozymes. Met Ions Biol Syst 40: 477-512.
45. Sigel RKO, Pyle AM. 2007. Alternative roles for metal ions in enzyme catalysis and the implications for ribozyme chemistry. Chem Rev 107: 97-113.
46. Sigel RK, Vaidya A, Pyle AM. 2000. Metal ion binding sites in a group II intron core. Nat Struct Biol 7: 1111-1116.
47. Sontheimer EJ, Steitz JA. 1993. The U5 and U6 small nuclear RNAs as active site components of the spliceosome. Science 262: 1989-1996.
48. Sontheimer EJ, Sun S, Piccirilli JA. 1997. Metal ion catalysis during splicing of premessenger RNA. Nature 388: 801-805.
49. Toor N, Keating KS, Taylor SD, Pyle AM. 2008. Crystal structure of a self-spliced group II intron. Science 320: 77-82.
50. Valadkhan S. 2007. The spliceosome: A ribozyme at heart? Biol Chem 388: 693-697.
51. Valadkhan S, Manley JL. 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.
52. Valadkhan S, Manley JL. 2001. Splicing-related catalysis by protein-free snRNAs. Nature 413: 701-707.
53. Valadkhan S, Manley JL. 2002. Intrinsic metal binding by a spliceosomal RNA. Nat Struct Biol 9: 498-499.
54. Valadkhan S, Manley JL. 2003. Characterization of the catalytic activity of U2 and U6 snRNAs. RNA 9: 892-904.
55. Valadkhan S, Mohammadi A, Wachtel C, Manley JL. 2007. Protein-free spliceosomal snRNAs catalyze a reaction that resembles the first step of splicing. RNA 13: 2300-2311.
56. 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.
57. Wilkinson KA, Merino EJ, Weeks KM. 2006. Selective 2′-hydroxyl acylation analyzed by primer extension (SHAPE): Quantitative RNA structure analysis at single nucleotide resolution. Nat Protoc 1: 1610-1616.
58. Wilson TJ, Lilley DMJ. 2009. Biochemistry. The evolution of ribozyme chemistry. Science 323: 1436-1438.
59. Wolff T, Menssen R, Hammel J, Bindereif A. 1994. Splicing function of mammalian U6 small nuclear RNA: Conserved positions in central domain and helix I are essential during the first and second step of pre-mRNA splicing. Proc Natl Acad Sci 91: 903-907.
60. Woodson SA. 2005. Metal ions and RNA folding: A highly charged topic with a dynamic future. Curr Opin Chem Biol 9: 104-109.
61. 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.
62. Yu YT, Maroney PA, Darzynkiwicz E, Nilsen TW. 1995. U6 snRNA function in nuclear pre-mRNA splicing: A phosphorothioate interference analysis of the U6 phosphate backbone. RNA 1: 46-54.
63. Yuan F, Griffin L, Phelps L, Buschmann V, Weston K, Greenbaum NL. 2007. 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 Res 35: 2833-2845.