Principles of ion recognition in RNA: Insights from the group II intron structures

RNA

Volumn 20, Issue 4, 2014, Pages 516-527

  Marcia, Marco ^a   Pyle, Anna Marie ^a,b  

^a YALE UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

GA imino mismatch; Ribonucleoprotein; Splicing; T loop; Tetraloop receptor; X ray crystallography

Indexed keywords

AMPHOLYTE; ANION; ION; METAL ION; NUCLEOTIDE; POLYCATION; PROTEIN; RIBOSE; RNA;

ARTICLE; BACILLUS; BINDING SITE; CRYSTAL STRUCTURE; CRYSTALLIZATION; HYDROGEN BOND; INTRON; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; OCEANOBACILLUS IHEYENSIS; PRIORITY JOURNAL; RNA STRUCTURE; TETRAHYMENA THERMOPHILA; X RAY CRYSTALLOGRAPHY;

GA IMINO MISMATCH; RIBONUCLEOPROTEIN; SPLICING; T-LOOP; TETRALOOP-RECEPTOR; X-RAY CRYSTALLOGRAPHY;

BACILLALES; BINDING SITES; CATALYTIC DOMAIN; INTRONS; METALS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; RNA SPLICING; RNA, BACTERIAL; RNA, CATALYTIC; RNA-BINDING PROTEINS;

EID: 84896497296     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.043414.113     Document Type: Article

References (88)

1. Abramovitz DL, Friedman RA, Pyle AM. 1996. Catalytic role of 2'-hydroxyl groups within a group II intron active site. Science 271: 1410-1413.
2. Adams PL, Stahley MR, Kosek AB, Wang J, Strobel SA. 2004. Crystal structure of a self-splicing group I intron with both exons. Nature 430: 45-50.
3. Agarwal RC. 1978. A new least-squares refinement technique based on the fast Fourier transform algorithm. Acta Crystallogr A Found Crystallogr 34: 791-809.
4. Auffinger P, Bielecki L, Westhof E. 2004. Anion binding to nucleic acids. Structure 12: 379-388.
5. Auffinger P, Grover N, Westhof E. 2011. Metal ion binding to RNA. Met Ions Life Sci 9: 1-35.
6. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: Application to microtubules and the ribosome. Proc Natl Acad Sci 98: 10037-10041.
7. Banatao DR, Altman RB, Klein TE. 2003. Microenvironment analysis and identification of magnesium binding sites in RNA. Nucleic Acids Res 31: 4450-4460.
8. Basu S, Rambo RP, Strauss-Soukup J, Cate JH, Ferre-D'Amare AR, Strobel SA, Doudna JA. 1998. A specific monovalent metal ion integral to the AA platform of the RNA tetraloop receptor. Nat Struct Biol 5: 986-992.
9. Boudvillain M, Pyle AM. 1998. Defining functional groups, core structural features and inter-domain tertiary contacts essential for group II intron self-splicing: A NAIM analysis. EMBO J 17: 7091-7104.
10. Boudvillain M, de Lencastre A, Pyle AM. 2000. A tertiary interaction that links active-site domains to the 5' splice site of a group II intron. Nature 406: 315-318.
11. Boulanger SC, Belcher SM, Schmidt U, Dib-Hajj SD, Schmidt T, Perlman PS. 1995. Studies of point mutants define three essential paired nucleotides in the domain 5 substructure of a group II intron. Mol Cell Biol 15: 4479-4488.
12. Butcher SE, Pyle AM. 2011. The molecular interactions that stabilize RNA tertiary structure: RNA motifs, patterns, and networks. Acc Chem Res 44: 1302-1311.
13. Cate JH, Doudna JA. 1996. Metal-binding sites in the major groove of a large ribozyme domain. Structure 4: 1221-1229.
14. Chin K, Sharp KA, Honig B, Pyle AM. 1999. Calculating the electrostatic properties of RNA provides new insights into molecular interactions and function. Nat Struct Biol 6: 1055-1061.
15. Conn GL, Gittis AG, Lattman EE, Misra VK, Draper DE. 2002. A compact RNA tertiary structure contains a buried backbone-K+ complex. J Mol Biol 318: 963-973.
16. Costa M, Deme E, Jacquier A, Michel F. 1997. Multiple tertiary interactions involving domain II of group II self-splicing introns. J Mol Biol 267: 520-536.
17. Costa M, Michel F, Westhof E. 2000. A three-dimensional perspective on exon binding by a group II self-splicing intron. EMBO J 19: 5007-5018.
18. Dai L, Chai D, Gu SQ, Gabel J, Noskov SY, Blocker FJ, Lambowitz AM, Zimmerly S. 2008. A three-dimensional model of a group II intron RNA and its interaction with the intron-encoded reverse transcriptase. Mol Cell 30: 472-485.
19. Daniels DL, Michels WJ Jr, Pyle AM. 1996. Two competing pathways for self-splicing by group II introns: A quantitative analysis of in vitro reaction rates and products. J Mol Biol 256: 31-49.
20. 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.
21. de Lencastre A, Pyle AM. 2008. Three essential and conserved regions of the group II intron are proximal to the 5'-splice site. RNA 14: 11-24.
22. de Lencastre A, Hamill S, Pyle AM. 2005. A single active-site region for a group II intron. Nat Struct Mol Biol 12: 626-627.
23. DeLano WL. 2009. PyMOL molecular viewer: Updates and refinements. Abstr Pap Am Chem Soc 238.
24. DeRose VJ. 2003. Metal ion binding to catalytic RNA molecules. Curr Opin Struct Biol 13: 317-324.
25. Ditzler MA, Sponer J, Walter NG. 2009. Molecular dynamics suggest multifunctionality of an adenine imino group in acid-base catalysis of the hairpin ribozyme. RNA 15: 560-575.
26. Dolinsky TJ, Nielsen JE, McCammon JA, Baker NA. 2004. PDB2PQR: An automated pipeline for the setup of Poisson-Boltzmann electrostatics calculations. Nucleic Acids Res 32: (Web Server issue): W665-W667.
27. Donghi D, Pechlaner M, Finazzo C, Knobloch B, Sigel RK. 2013. The structural stabilization of the k three-way junction by Mg(II) represents the first step in the folding of a group II intron. Nucleic Acids Res 41: 2489-2504.
28. Draper DE. 2004. A guide to ions and RNA structure. RNA 10: 335-343.
29. Draper DE. 2013. Folding of RNA tertiary structure: Linkages between backbone phosphates, ions, and water. Biopolymers 99: 1105-1113.
30. Ennifar E, Yusupov M, Walter P, Marquet R, Ehresmann B, Ehresmann C, Dumas P. 1999. The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. Structure 7: 1439-1449.
31. Erat MC, Sigel RK. 2007. Determination of the intrinsic affinities of multiple site-specific Mg2+ ions coordinated to domain 6 of a group II intron ribozyme. Inorg Chem 46: 11224-11234.
32. Erat MC, Sigel RK. 2008. Divalent metal ions tune the self-splicing reaction of the yeast mitochondrial group II intron Sc.ai5y. J Biol Inorg Chem 13: 1025-1036.
33. Feig AL, Uhlenbeck OC. 1999. The role of metal ions in RNA biochemistry. In The RNA world (ed. RF Gestelandet al.), pp. 287-320. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
34. Freisinger E, Sigel RKO. 2007. From nucleotides to ribozymes-a comparison of their metal ion binding properties. Coord Chem Rev 251: 1834-1851.
35. 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.
36. Hamill S, Pyle AM. 2006. The receptor for branch-site docking within a group II intron active site. Mol Cell 23: 831-840.
37. Harding MM. 2001. Geometry of metal-ligand interactions in proteins. Acta Crystallogr D Biol Crystallogr 57 (Pt 3): 401-411.
38. Harding MM. 2002. Metal-ligand geometry relevant to proteins and in proteins: Sodium and potassium. Acta Crystallogr D Biol Crystallogr 58 (Pt 5): 872-874.
39. Hertweck M, Mueller MW. 2001. Mapping divalent metal ion binding sites in a group II intron by Mn2+- and Zn2+-induced site-specific RNA cleavage. Eur J Biochem 268: 4610-4620.
40. Heus HA, Wijmenga SS, Hoppe H, Hilbers CW. 1997. The detailed structure of tandem G.A mismatched base-pair motifs in RNA duplexes is context dependent. J Mol Biol 271: 147-158.
41. Holbrook SR, Sussman JL, Warrant RW, Kim SH. 1978. Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. J Mol Biol 123: 631-660.
42. Jarrell KA, Peebles CL, Dietrich RC, Romiti SL, Perlman PS. 1988. Group II intron self-splicing. Alternative reaction conditions yield novel products. J Biol Chem 263: 3432-3439.
43. Kazantsev AV, Krivenko AA, Pace NR. 2009. Mapping metal-binding sites in the catalytic domain of bacterial RNase P RNA. RNA 15: 266-276.
44. Kieft JS, Chase E, Costantino DA, Golden BL. 2010. Identification and characterization of anion binding sites in RNA. RNA 16: 1118-1123.
45. Klein DJ, Ferre-D'Amare AR. 2006. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313: 1752-1756.
46. Klein DJ, Schmeing TM, Moore PB, Steitz TA. 2001. The kink-turn: A new RNA secondary structure motif. EMBO J 20: 4214-4221.
47. Klein DJ, Moore PB, Steitz TA. 2004. The contribution of metal ions to the structural stability of the large ribosomal subunit. RNA 10: 1366-1379.
48. Korolev N, Lyubartsev AP, Laaksonen A, Nordenskiold L. 2002. On the competition between water, sodium ions, and spermine in binding to DNA: A molecular dynamics computer simulation study. Biophys J 82: 2860-2875.
49. Krasilnikov AS, Mondragon A. 2003. On the occurrence of the T-loop RNA folding motif in large RNA molecules. RNA 9: 640-643.
50. Krasilnikov AS, Yang X, Pan T, Mondragon A. 2003. Crystal structure of the specificity domain of ribonuclease P. Nature 421: 760-764.
51. Kruschel D, Sigel RK. 2008. Divalent metal ions promote the formation of the 5'-splice site recognition complex in a self-splicing group II intron. J Inorg Biochem 102: 2147-2154.
52. Lambert D, Leipply D, Shiman R, Draper DE. 2009. The influence of monovalent cation size on the stability of RNA tertiary structures. J Mol Biol 390: 791-804.
53. Leipply D, Lambert D, Draper DE. 2009. Ion-RNA interactions thermodynamic analysis of the effects of mono- and divalent ions on RNA conformational equilibria. Methods Enzymol 469: 433-463.
54. Leontis NB, Westhof E. 1998. A common motif organizes the structure of multi-helix loops in 16 S and 23 S ribosomal RNAs. J Mol Biol 283: 571-583.
55. Mahler J, Persson I. 2012. A study of the hydration of the alkali metal ions in aqueous solution. Inorg Chem 51: 425-438.
56. Marcia M, Pyle AM. 2012. Visualizing group II intron catalysis through the stages of splicing. Cell 151: 497-507.
57. Marcia M, Humphris-Narayanan E, Keating KS, Somarowthu S, Rajashankar K, Pyle AM. 2013a. Solving nucleic acid structures by molecular replacement: Examples from group II intron studies. Acta Crystallogr D Biol Crystallogr 69 (Pt 11): 2174-2185.
58. Marcia M, Somarowthu S, Pyle AM. 2013b. Now on display: A gallery of group II intron structures at different stages of catalysis. Mob DNA 4: 14.
59. Matsuura M, Noah JW, Lambowitz AM. 2001. Mechanism of maturasepromoted group II intron splicing. EMBO J 20: 7259-7270.
60. Michel F, Ferat JL. 1995. Structure and activities of group II introns. Annu Rev Biochem 64: 435-461.
61. Michel F, Umesono K, Ozeki H. 1989. Comparative and functional anatomy of group II catalytic introns-a review. Gene 82: 5-30.
62. Misra VK, Draper DE. 2001. A thermodynamic framework for Mg2+ binding to RNA. Proc Natl Acad Sci 98: 12456-12461.
63. Pley HW, Flaherty KM, Mckay DB. 1994. Three-dimensional structure of a hammerhead ribozyme. Nature 372: 68-74.
64. Podar M, Perlman PS, Padgett RA. 1995. Stereochemical selectivity of group II intron splicing, reverse splicing, and hydrolysis reactions. Mol Cell Biol 15: 4466-4478.
65. Pyle AM. 2002. Metal ions in the structure and function of RNA. J Biol Inorg Chem 7: 679-690.
66. Pyle AM. 2010. The tertiary structure of group II introns: Implications for biological function and evolution. Crit Rev Biochem Mol Biol 45: 215-232.
67. Pyle AM, Fedorova O, Waldsich C. 2007. Folding of group II introns: A model system for large, multidomain RNAs? Trends Biochem Sci 32: 138-145.
68. Quigley GJ, Teeter MM, Rich A. 1978. Structural analysis of spermine and magnesium ion binding to yeast phenylalanine transfer RNA. Proc Natl Acad Sci 75: 64-68.
69. Rüdisser S, Tinoco I Jr. 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.
70. Schmidt U, Podar M, Stahl U, Perlman PS. 1996. Mutations of the twonucleotide bulge of D5 of a group II intron block splicing in vitro and in vivo: Phenotypes and suppressor mutations. RNA 2: 1161-1172.
71. Schnabl J, Suter P, Sigel RK. 2012. MINAS-a database of Metal Ions in Nucleic AcidS. Nucleic Acids Res 40 (Database issue): D434-D438.
72. Sigel RK, Vaidya A, Pyle AM. 2000. Metal ion binding sites in a group II intron core. Nat Struct Biol 7: 1111-1116.
73. Stahley MR, Adams PL, Wang J, Strobel SA. 2007. Structural metals in the group I intron: A ribozyme with a multiple metal ion core. J Mol Biol 372: 89-102.
74. Stefan LR, Zhang R, Levitan AG, Hendrix DK, Brenner SE, Holbrook SR. 2006. MeRNA: A database of metal ion binding sites in RNA structures. Nucleic Acids Res 34 (Database issue): D131-D134.
75. Strobel SA. 2002. Biochemical identification of A-minor motifs within RNA tertiary structure by interference analysis. Biochem Soc Trans 30 (Pt 6): 1126-1131.
76. Su LJ, Brenowitz M, Pyle AM. 2003. An alternative route for the folding of large RNAs: Apparent two-state folding by a group II intron ribozyme. J Mol Biol 334: 639-652.
77. Su LJ, Waldsich C, Pyle AM. 2005. An obligate intermediate along the slow folding pathway of a group II intron ribozyme. Nucleic Acids Res 33: 6674-6687.
78. Swisher JF, Su LJ, Brenowitz M, Anderson VE, Pyle AM. 2002. Productive folding to the native state by a group II intron ribozyme. J Mol Biol 315: 297-310.
79. Szep S, Wang J, Moore PB. 2003. The crystal structure of a 26-nucleotide RNA containing a hook-turn. RNA 9: 44-51.
80. Ten Eyck LF. 1973. Crystal physics, diffraction, theoretical and general crystallography. Acta Crystallogr A Found Crystallogr 29: 183-191.
81. Toor N, Keating KS, Taylor SD, Pyle AM. 2008a. Crystal structure of a self-spliced group II intron. Science 320: 77-82.
82. Toor N, Rajashankar K, Keating KS, Pyle AM. 2008b. Structural basis for exon recognition by a group II intron. Nat Struct Mol Biol 15: 1221-1222.
83. Toor N, Keating KS, Fedorova O, Rajashankar K, Wang J, Pyle AM. 2010. Tertiary architecture of the Oceanobacillus iheyensis group II intron. RNA 16: 57-69.
84. Traub W, Sussman JL. 1982. Adenine-guanine base pairing ribosomal RNA. Nucleic Acids Res 10: 2701-2708.
85. Villescas-Diaz G, Zacharias M. 2003. Sequence context dependence of tandem guanine:adenine mismatch conformations in RNA: A continuum solvent analysis. Biophys J 85: 416-425.
86. Waldsich C, Pyle AM. 2008. A kinetic intermediate that regulates proper folding of a group II intron RNA. J Mol Biol 375: 572-580.
87. Walter NG, Yang N, Burke JM. 2000. Probing non-selective cation binding in the hairpin ribozyme with Tb(III). J Mol Biol 298: 539-555.
88. Yamada M, Miyawaki R, Nakai I, Izumi F, Nagashima K. 1998. A Rietveld analysis of the crystal structure of ammonioleucite. Mineral J 20: 105-112.