Structure and function of the T-loop structural motif in noncoding RNAs

Wiley Interdisciplinary Reviews: RNA

Volumn 4, Issue 5, 2013, Pages 507-522

  Chan, Clarence W ^a   Chetnani, Bhaskar ^a   Mondragón, Alfonso ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RIBONUCLEASE P; RIBOSOME RNA; SELF SPLICING RIBOSOMAL RNA; TRANSFER RNA; UNTRANSLATED RNA;

BASE PAIRING; CONFORMATIONAL TRANSITION; CONSENSUS SEQUENCE; CRYSTAL STRUCTURE; CRYSTALLIZATION; GENE EXPRESSION; HYDROGEN BOND; INTRON; LIGAND BINDING; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE MOTIF; PRIORITY JOURNAL; REVIEW; RIBOSOME; RIBOSWITCH; RNA STRUCTURE; TRANSESTERIFICATION;

NUCLEIC ACID CONFORMATION; RNA STABILITY; RNA, UNTRANSLATED;

EID: 84881664828     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1175     Document Type: Review

References (95)

1. Lee JT. Epigenetic regulation by long noncoding RNAs. Science 2012, 338:1435-1439.
2. Wery M, Kwapisz M, Morillon A. Noncoding RNAs in gene regulation. Wiley Interdiscip Rev Syst Biol Med 2011, 3:728-738.
3. Eddy SR. Non-coding RNA genes and the modern RNA world. Nat Rev Genet 2001, 2:919-929.
4. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem 2012, 81:145-166.
5. Hogg JR, Collins K. Structured non-coding RNAs and the RNP Renaissance. Curr Opin Chem Biol 2008, 12:684-689.
6. Holbrook SR. Structural principles from large RNAs. Annu Rev Biophys 2008, 37:445-464.
7. Leontis NB, Lescoute A, Westhof E. The building blocks and motifs of RNA architecture. Curr Opin Struct Biol 2006, 16:279-287.
8. Hendrix DK, Brenner SE, Holbrook SR. RNA structural motifs: building blocks of a modular biomolecule. Q Rev Biophys 2005, 38:221-243.
9. Holbrook SR. RNA structure: the long and the short of it. Curr Opin Struct Biol 2005, 15:302-308.
10. Leontis NB, Westhof E. Analysis of RNA motifs. Curr Opin Struct Biol 2003, 13:300-308.
11. Batey RT, Rambo RP, Doudna JA. Tertiary motifs in RNA structure and folding. Angew Chem Int Ed Engl 1999, 38:2326-2343.
12. Moore PB. Structural motifs in RNA. Annu Rev Biochem 1999, 68:287-300.
13. Nissen P, Ippolito JA, Ban N, Moore PB, Steitz TA. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc Natl Acad Sci USA 2001, 98:4899-4903.
14. Cate JH, Gooding AR, Podell E, Zhou K, Golden BL, Szewczak AA, Kundrot CE, Cech TR, Doudna JA. RNA tertiary structure mediation by adenosine platforms. Science 1996, 273:1696-1699.
15. Schroeder KT, McPhee SA, Ouellet J, Lilley DM. A structural database for k-turn motifs in RNA. RNA 2010, 16:1463-1468.
16. Klein DJ, Schmeing TM, Moore PB, Steitz TA. The kink-turn: a new RNA secondary structure motif. EMBO J 2001, 20:4214-4221.
17. Mujeeb A, Clever JL, Billeci TM, James TL, Parslow TG. Structure of the dimer initiation complex of HIV-1 genomic RNA. Nat Struct Biol 1998, 5:432-436.
18. Wyatt JR, Puglisi JD, Tinoco I Jr. RNA folding: pseudoknots, loops and bulges. Bioessays 1989, 11:100-106.
19. Szewczak AA, Moore PB, Chang YL, Wool IG. The conformation of the sarcin/ricin loop from 28S ribosomal RNA. Proc Natl Acad Sci USA 1993, 90:9581-9585.
20. Krasilnikov AS, Mondragon A. On the occurrence of the T-loop RNA folding motif in large RNA molecules. RNA 2003, 9:640-643.
21. Nagaswamy U, Fox GE. Frequent occurrence of the T-loop RNA folding motif in ribosomal RNAs. RNA 2002, 8:1112-1119.
22. Costa M, Michel F. Frequent use of the same tertiary motif by self-folding RNAs. EMBO J 1995, 14:1276-1285.
23. Pley HW, Flaherty KM, McKay DB. Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature 1994, 372:111-113.
24. Abu Almakarem AS, Petrov AI, Stombaugh J, Zirbel CL, Leontis NB. Comprehensive survey and geometric classification of base triples in RNA structures. Nucleic Acids Res 2012, 40:1407-1423.
25. Reiter NJ, Chan CW, Mondragon A. Emerging structural themes in large RNA molecules. Curr Opin Struct Biol 2011, 21:319-326.
26. Robertus JD, Ladner JE, Finch JT, Rhodes D, Brown RS, Clark BF, Klug A. Structure of yeast phenylalanine tRNA at 3 A resolution. Nature 1974, 250:546-551.
27. Kim SH, Suddath FL, Quigley GJ, McPherson A, Sussman JL, Wang AH, Seeman NC, Rich A. Three-dimensional tertiary structure of yeast phenylalanine transfer RNA. Science 1974, 185:435-440.
28. Bessho Y, Shibata R, Sekine S, Murayama K, Higas-hijima K, Hori-Takemoto C, Shirouzu M, Kuramitsu S, Yokoyama S. Structural basis for functional mimicry of long-variable-arm tRNA by transfer-messenger RNA. Proc Natl Acad Sci USA 2007, 104:8293-8298.
29. Gutmann S, Haebel PW, Metzinger L, Sutter M, Felden B, Ban N. Crystal structure of the transfer-RNA domain of transfer-messenger RNA in complex with SmpB. Nature 2003, 424:699-703.
30. Torres-Larios A, Swinger KK, Krasilnikov AS, Pan T, Mondragon A. Crystal structure of the RNA component of bacterial ribonuclease P. Nature 2005, 437:584-587.
31. Krasilnikov AS, Xiao Y, Pan T, Mondragon A. Basis for structural diversity in homologous RNAs. Science 2004, 306:104-107.
32. Krasilnikov AS, Yang X, Pan T, Mondragon A. Crystal structure of the specificity domain of ribonuclease P. Nature 2003, 421:760-764.
33. Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. The structure of the eukaryotic ribosome at 3.0 A resolution. Science 2011, 334:1524-1529.
34. Ben-Shem A, Jenner L, Yusupova G, Yusupov M. Crystal structure of the eukaryotic ribosome. Science 2010, 330:1203-1209.
35. Brodersen DE, Clemons WM Jr, Carter AP, Wimberly BT, Ramakrishnan V. Crystal structure of the 30S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16S RNA. J Mol Biol 2002, 316:725-768.
36. Carter AP, Clemons WM Jr, Brodersen DE, Morgan-Warren RJ, Hartsch T, Wimberly BT, Ramakrishnan V. Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 2001, 291:498-501.
37. Clemons WM Jr, Brodersen DE, McCutcheon JP, May JL, Carter AP, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. Crystal structure of the 30S ribosomal subunit from Thermus thermophilus: purification, crystallization and structure determination. J Mol Biol 2001, 310:827-843.
38. Harms J, Schluenzen F, Zarivach R, Bashan A, Gat S, Agmon I, Bartels H, Franceschi F, Yonath A. High resolution structure of the large ribosomal subunit from a mesophilic eubacterium. Cell 2001, 107:679-688.
39. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF. Crystal structure of the ribosome at 5.5 A resolution. Science 2001, 292:883-896.
40. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 2000, 289:905-920.
41. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT, Ramakrishnan V. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 2000, 407:340-348.
42. Schluenzen F, Tocilj A, Zarivach R, Harms J, Gluehmann M, Janell D, Bashan A, Bartels H, Agmon I, Franceschi F, et al. Structure of functionally activated small ribosomal subunit at 3.3 angstroms resolution. Cell 2000, 102:615-623.
43. Wimberly BT, Brodersen DE, Clemons WM Jr, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature 2000, 407:327-339.
44. Clemons WM Jr, May JL, Wimberly BT, McCutcheon JP, Capel MS, Ramakrishnan V. Structure of a bacterial 30S ribosomal subunit at 5.5 A resolution. Nature 1999, 400:833-840.
45. Cate JH, Yusupov MM, Yusupova GZ, Earnest TN, Noller HF. X-ray crystal structures of 70S ribosome functional complexes. Science 1999, 285:2095-2104.
46. Peselis A, Serganov A. Structural insights into ligand binding and gene expression control by an adenosylcobalamin riboswitch. Nat Struct Mol Biol 2012, 19:1182-1184.
47. Johnson JE Jr, Reyes FE, Polaski JT, Batey RT. B12 cofactors directly stabilize an mRNA regulatory switch. Nature 2012, 492:133-137.
48. Vicens Q, Mondragon E, Batey RT. Molecular sensing by the aptamer domain of the FMN riboswitch: a general model for ligand binding by conformational selection. Nucleic Acids Res 2011, 39:8586-8598.
49. Serganov A, Huang L, Patel DJ. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 2009, 458:233-237.
50. Thore S, Frick C, Ban N. Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch. J Am Chem Soc 2008, 130:8116-8117.
51. Edwards TE, Ferre-D'Amare AR. Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 2006, 14:1459-1468.
52. Serganov A, Polonskaia A, Phan AT, Breaker RR, Patel DJ. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 2006, 441:1167-1171.
53. Thore S, Leibundgut M, Ban N. Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 2006, 312:1208-1211.
54. Reiter NJ, Osterman A, Torres-Larios A, Swinger KK, Pan T, Mondragon A. Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature 2010, 468:784-789.
55. Lee JC, Cannone JJ, Gutell RR. The lonepair triloop: a new motif in RNA structure. J Mol Biol 2003, 325:65-83.
56. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The Protein Data Bank. Nucleic Acids Res 2000, 28:235-242.
57. Ito T, Yokoyama S. Two enzymes bound to one transfer RNA assume alternative conformations for consecutive reactions. Nature 2010, 467:612-616.
58. Nakanishi K, Bonnefond L, Kimura S, Suzuki T, Ishitani R, Nureki O. Structural basis for translational fidelity ensured by transfer RNA lysidine synthetase. Nature 2009, 461:1144-1148.
59. Palencia A, Crepin T, Vu MT, Lincecum TL Jr, Martinis SA, Cusack S. Structural dynamics of the aminoacylation and proofreading functional cycle of bacterial leucyl-tRNA synthetase. Nat Struct Mol Biol 2012, 19:677-684.
60. Gao YG, Selmer M, Dunham CM, Weixlbaumer A, Kelley AC, Ramakrishnan V. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science 2009, 326:694-699.
61. Jin H, Kelley AC, Loakes D, Ramakrishnan V. Structure of the 70S ribosome bound to release factor 2 and a substrate analog provides insights into catalysis of peptide release. Proc Natl Acad Sci USA 2010, 107:8593-8598.
62. Korostelev A, Trakhanov S, Laurberg M, Noller HF. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 2006, 126:1065-1077.
63. Neubauer C, Gillet R, Kelley AC, Ramakrishnan V. Decoding in the absence of a codon by tmRNA and SmpB in the ribosome. Science 2012, 335:1366-1369.
64. Petry S, Brodersen DE, FVt M, Dunham CM, Selmer M, Tarry MJ, Kelley AC, Ramakrishnan V. Crystal structures of the ribosome in complex with release factors RF1 and RF2 bound to a cognate stop codon. Cell 2005, 123:1255-1266.
65. Schmeing TM, Voorhees RM, Kelley AC, Gao YG, Murphy FV, Weir JR, Ramakrishnan V. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science 2009, 326:688-694.
66. Selmer M, Dunham CM, FVt M, Weixlbaumer A, Petry S, Kelley AC, Weir JR, Ramakrishnan V. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006, 313:1935-1942.
67. Kazantsev AV, Krivenko AA, Harrington DJ, Holbrook SR, Adams PD, Pace NR. Crystal structure of a bacterial ribonuclease P RNA. Proc Natl Acad Sci USA 2005, 102:13392-13397.
68. Adams PL, Stahley MR, Kosek AB, Wang J, Strobel SA. Crystal structure of a self-splicing group I intron with both exons. Nature 2004, 430:45-50.
69. Golden BL, Kim H, Chase E. Crystal structure of a phage Twort group I ribozyme-product complex. Nat Struct Mol Biol 2005, 12:82-89.
70. Guo F, Gooding AR, Cech TR. Structure of the Tetrahymena ribozyme: base triple sandwich and metal ion at the active site. Mol Cell 2004, 16:351-362.
71. Toor N, Keating KS, Taylor SD, Pyle AM. Crystal structure of a self-spliced group II intron. Science 2008, 320:77-82.
72. Montange RK, Batey RT. Riboswitches: emerging themes in RNA structure and function. Annu Rev Biophys 2008, 37:117-133.
73. Shi H, Moore PB. The crystal structure of yeast phenylalanine tRNA at 1.93 A resolution: a classic structure revisited. RNA 2000, 6:1091-1105.
74. Collaborative Computational Project 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 1994, 50:760-763.
75. Leontis N, Westhof E, eds. RNA 3D structure analysis and prediction. Berlin, Heidelberg: Springer; 2012, 281-298.
76. Abe T, Ikemura T, Sugahara J, Kanai A, Ohara Y, Uehara H, Kinouchi M, Kanaya S, Yamada Y, Muto A, et al. tRNADB-CE 2011: tRNA gene database curated manually by experts. Nucleic Acids Res 2011, 39:D210-D213.
77. Sampson JR, Uhlenbeck OC. Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro. Proc Natl Acad Sci USA 1988, 85:1033-1037.
78. 2+-dependent tRNA folding. Nucleic Acids Res 2002, 30:4751-4760.
79. Moore SD, Sauer RT. The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 2007, 76:101-124.
80. Gillet R, Felden B. Transfer RNA(Ala) recognizes transfer-messenger RNA with specificity; a functional complex prior to entering the ribosome? EMBO J 2001, 20:2966-2976.
81. Moore PB. The three-dimensional structure of the ribosome and its components. Annu Rev Biophys Biomol Struct 1998, 27:35-58.
82. Moore PB, Steitz TA. The roles of RNA in the synthesis of protein. Cold Spring Harb Perspect Biol 2011, 3:a003780.
83. Torres-Larios A, Swinger KK, Pan T, Mondragon A. Structure of ribonuclease P-a universal ribozyme. Curr Opin Struct Biol 2006, 16:327-335.
84. Kazantsev AV, Krivenko AA, Pace NR. Mapping metal-binding sites in the catalytic domain of bacterial RNase P RNA. RNA 2009, 15:266-276.
85. Brown JW. The Ribonuclease P Database. Nucleic Acids Res 1999, 27:314.
86. Lancelot G, Helene C. Phosphate-guanosine interactions. A model for the involvement of guanine derivatives in autocatalytic reactions of ribonucleic acids. J Biol Chem 1984, 259:15046-15050.
87. Serganov A, Patel DJ. Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat Rev Genet 2007, 8:776-790.
88. Chan RT, Robart AR, Rajashankar KR, Pyle AM, Toor N. Crystal structure of a group II intron in the pre-catalytic state. Nat Struct Mol Biol 2012, 19:555-557.
89. Toor N, Rajashankar K, Keating KS, Pyle AM. Structural basis for exon recognition by a group II intron. Nat Struct Mol Biol 2008, 15:1221-1222.
90. Zhang L, Doudna JA. Structural insights into group II intron catalysis and branch-site selection. Science 2002, 295:2084-2088.
91. Pomeranz Krummel DA, Oubridge C, Leung AK, Li J, Nagai K. Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 2009, 458:475-480.
92. Ferre-D'Amare AR, Zhou K, Doudna JA. Crystal structure of a hepatitis delta virus ribozyme. Nature 1998, 395:567-574.
93. Koldobskaya Y, Duguid EM, Shechner DM, Suslov NB, Ye J, Sidhu SS, Bartel DP, Koide S, Kossiakoff AA, Piccirilli JA. A portable RNA sequence whose recognition by a synthetic antibody facilitates structural determination. Nat Struct Mol Biol 2011, 18:100-106.
94. Toor N, Keating KS, Fedorova O, Rajashankar K, Wang J, Pyle AM. Tertiary architecture of the Oceanobacillus iheyensis group II intron. RNA 2010, 16:57-69.
95. Serganov A, Patel DJ. Metabolite recognition principles and molecular mechanisms underlying riboswitch function. Annu Rev Biophys 2012, 41:343-370.