Solution structure of the K-turn and specifier loop domains from the bacillus subtilis tyrs T-box leader RNA

Journal of Molecular Biology

Volumn 408, Issue 1, 2011, Pages 99-117

  Wang, Jiachen ^a   Nikonowicz, Edward P ^a  

^a RICE UNIVERSITY   (United States)

Author keywords

hairpin; heteronuclear; riboswitch; transcription regulation; TRNA

Indexed keywords

BACTERIAL PROTEIN; MAGNESIUM; NUCLEOTIDE; SPECIFIER LOOP DOMAIN; T BOX TRANSCRIPTION FACTOR; TRANSFER RNA; UNCLASSIFIED DRUG;

ANTICODON; ARTICLE; BACILLUS SUBTILIS; GENE EXPRESSION; ISOTHERMAL TITRATION CALORIMETRY; KINK TURN; NONHUMAN; PRIORITY JOURNAL; RIBOSWITCH; RNA STRUCTURE; TRANSCRIPTION REGULATION;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 79953233677     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.02.014     Document Type: Article

References (69)

1. Henkin T.M. Transcription termination control in bacteria Curr. Opin. Microbiol. 3 2000 149 153 (Pubitemid 30180065)
2. Henkin T.M. Riboswitch RNAs: using RNA to sense cellular metabolism Genes Dev. 22 2008 3383 3390
3. Grundy F.J., and Henkin T.M. tRNA as a positive regulator of transcription antitermination in B. subtilis Cell 74 1993 475 482 (Pubitemid 23244613)
4. Grundy F.J., Rollins S.M., and Henkin T.M. Interaction between the acceptor end of tRNA and the T box stimulates antitermination in the Bacillus subtilis tyrS gene: a new role for the discriminator base J. Bacteriol. 176 1994 4518 4526 (Pubitemid 24237953)
5. Grundy F.J., Hodil S.E., Rollins S.M., and Henkin T.M. Specificity of tRNA-mRNA interactions in Bacillus subtilis tyrS antitermination J. Bacteriol. 179 1997 2587 2594 (Pubitemid 27164558)
6. Grundy F.J., Moir T.R., Haldeman M.T., and Henkin T.M. Sequence requirements for terminators and antiterminators in the T box transcription antitermination system: disparity between conservation and functional requirements Nucleic Acids Res. 30 2002 1646 1655 (Pubitemid 34679740)
7. Vitreschak A.G., Mironov A.A., Lyubetsky V.A., and Gelfand M.S. Comparative genomic analysis of T-box regulatory systems in bacteria RNA 14 2008 717 735 (Pubitemid 351480884)
8. Yousef M.R., Grundy F.J., and Henkin T.M. Structural transitions induced by the interaction between tRNA(Gly) and the Bacillus subtilis glyQS T box leader RNA J. Mol. Biol. 349 2005 273 287 (Pubitemid 40693749)
9. Grundy F.J., and Henkin T.M. Conservation of a transcription antitermination mechanism in aminoacyl-tRNA synthetase and amino acid biosynthesis genes in gram-positive bacteria J. Mol. Biol. 235 1994 798 804
10. Grundy F.J., Winkler W.C., and Henkin T.M. tRNA-mediated transcription antitermination in vitro: codon-anticodon pairing independent of the ribosome Proc. Natl Acad. Sci. USA 99 2002 11121 11126 (Pubitemid 34920889)
11. Winkler W.C., Grundy F.J., Murphy B.A., and Henkin T.M. The GA motif: an RNA element common to bacterial antitermination systems, rRNA, and eukaryotic RNAs RNA 7 2001 1165 1172 (Pubitemid 32726914)
12. Schroeder K.T., McPhee S.A., Ouellet J., and Lilley D.M. A structural database for k-turn motifs in RNA RNA 16 2010 1463 1468
13. Klein D.J., Schmeing T.M., Moore P.B., and Steitz T.A. The kink-turn: a new RNA secondary structure motif EMBO J. 20 2001 4214 4221 (Pubitemid 32751837)
14. Lescoute A., Leontis N.B., Massire C., and Westhof E. Recurrent structural RNA motifs, isostericity matrices and sequence alignments Nucleic Acids Res. 33 2005 2395 2409 (Pubitemid 41511259)
15. Vidovic I., Nottrott S., Hartmuth K., Luhrmann R., and Ficner R. Crystal structure of the spliceosomal 15.5kD protein bound to a U4 snRNA fragment Mol. Cell 6 2000 1331 1342 (Pubitemid 32045926)
16. Schultz A., Nottrott S., Hartmuth K., and Luhrmann R. RNA structural requirements for the association of the spliceosomal hPrp31 protein with the U4 and U4atac small nuclear ribonucleoproteins J. Biol. Chem. 281 2006 28278 28286 (Pubitemid 44414541)
17. Omer A.D., Zago M., Chang A., and Dennis P.P. Probing the structure and function of an archaeal C/D-box methylation guide sRNA RNA 12 2006 1708 1720 (Pubitemid 44316035)
18. Adams P.L., Stahley M.R., Kosek A.B., Wang J., and Strobel S.A. Crystal structure of a self-splicing group I intron with both exons Nature 430 2004 45 50 (Pubitemid 38915218)
19. Blouin S., and Lafontaine D.A. A loop loop interaction and a K-turn motif located in the lysine aptamer domain are important for the riboswitch gene regulation control RNA 13 2007 1256 1267 (Pubitemid 47080471)
20. Montange R.K., and Batey R.T. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element Nature 441 2006 1172 1175 (Pubitemid 43990740)
21. Chao J.A., and Williamson J.R. Joint X-ray and NMR refinement of the yeast L30e-mRNA complex Structure 12 2004 1165 1176 (Pubitemid 38900759)
22. Strobel S.A., Adams P.L., Stahley M.R., and Wang J. RNA kink turns to the left and to the right RNA 10 2004 1852 1854 (Pubitemid 39557822)
23. Antonioli A.H., Cochrane J.C., Lipchock S.V., and Strobel S.A. Plasticity of the RNA kink turn structural motif RNA 16 2010 762 768
24. Szewczak L.B., Gabrielsen J.S., Degregorio S.J., Strobel S.A., and Steitz J.A. Molecular basis for RNA kink-turn recognition by the h15.5K small RNP protein RNA 11 2005 1407 1419 (Pubitemid 41215443)
25. 15N-labeled RNA J. Am. Chem. Soc. 118 1996 5316 5317
26. Pardi A. Multidimensional heteronuclear NMR experiments for structure determination of isotopically labeled RNA Methods Enzymol. 261 1995 350 380
27. Dieckmann T., and Feigon J. Assignment methodology for larger RNA oligonucleotides: application to an ATP-binding RNA aptamer J. Biomol. NMR 9 1997 259 272 (Pubitemid 127505387)
28. 15N labeled nucleic acids J. Mol. Biol. 232 1993 1141 1156 (Pubitemid 23276427)
29. 31P) and two-dimensional hetero TOCSY J. Am. Chem. Soc. 116 1994 4983 4984
30. 31P-driven NMR procedures for complete assignment of backbone resonances in oligodeoxyribonucleotides J. Biomol. NMR 3 1993 577 595
31. Allain F.H., and Varani G. Structure of the P1 helix from group I self-splicing introns J. Mol. Biol. 250 1995 333 353
32. Gorenstein D.G. Phosphorus-31 NMR: Principles and Applications 1984 Academic Press New York
33. Goody T.A., Melcher S.E., Norman D.G., and Lilley D.M. The kink-turn motif in RNA is dimorphic, and metal ion-dependent RNA 10 2004 254 264 (Pubitemid 38129830)
34. Schroeder K.T., and Lilley D.M. Ion-induced folding of a kink turn that departs from the conventional sequence Nucleic Acids Res. 37 2009 7281 7289
35. Serra M.J., Baird J.D., Dale T., Fey B.L., Retatagos K., and Westhof E. Effects of magnesium ions on the stabilization of RNA oligomers of defined structures RNA 8 2002 307 323 (Pubitemid 34311181)
36. Rupert P.B., and Ferre-D'Amare A.R. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis Nature 410 2001 780 786 (Pubitemid 32303769)
37. Finger L.D., Trantirek L., Johansson C., and Feigon J. Solution structures of stem-loop RNAs that bind to the two N-terminal RNA-binding domains of nucleolin Nucleic Acids Res. 31 2003 6461 6472 (Pubitemid 37508750)
38. Correll C.C., Freeborn B., Moore P.B., and Steitz T.A. Metals, motifs, and recognition in the crystal structure of a 5S rRNA domain Cell 91 1997 705 712 (Pubitemid 27513661)
39. Wimberly B.T., Brodersen D.E., Clemons W.M. Jr., Morgan-Warren R.J., Carter A.P., and Vonrhein C. Structure of the 30S ribosomal subunit Nature 407 2000 327 339
40. Misra V.K., and Draper D.E. The linkage between magnesium binding and RNA folding J. Mol. Biol. 317 2002 507 521 (Pubitemid 34722166)
41. Phe Biochemistry 43 2004 55 66 (Pubitemid 38055942)
42. Wang J., Henkin T.M., and Nikonowicz E.P. NMR structure and dynamics of the Specifier Loop domain from the Bacillus subtilis tyrS T box leader RNA Nucleic Acids Res. 38 2010 3388 3398
43. Dallas A., and Moore P.B. The loop E-loop D region of Escherichia coli 5S rRNA: the solution structure reveals an unusual loop that may be important for binding ribosomal proteins Structure 5 1997 1639 1653 (Pubitemid 28051977)
44. Leontis N.B., and Westhof E. A common motif organizes the structure of multi-helix loops in 16S and 23S ribosomal RNAs J. Mol. Biol. 283 1998 571 583 (Pubitemid 28486721)
45. Butcher S.E., and Burke J.M. Structure-mapping of the hairpin ribozyme. Magnesium-dependent folding and evidence for tertiary interactions within the ribozyme-substrate complex J. Mol. Biol. 244 1994 52 63
46. Johansson C., Finger L.D., Trantirek L., Mueller T.D., Kim S., Laird-Offringa I.A., and Feigon J. Solution structure of the complex formed by the two N-terminal RNA-binding domains of nucleolin and a pre-rRNA target J. Mol. Biol. 337 2004 799 816 (Pubitemid 38368926)
47. Falb M., Amata I., Gabel F., Simon B., and Carlomagno T. Structure of the K-turn U4 RNA: a combined NMR and SANS study Nucleic Acids Res. 38 2010 6274 6285
48. 2: probing the structural features that shape the thermodynamic stability of GA pairs Biochemistry 46 2007 1511 1522
49. Juhling F., Morl M., Hartmann R.K., Sprinzl M., Stadler P.F., and Putz J. tRNAdb 2009: compilation of tRNA sequences and tRNA genes Nucleic Acids Res. 37 2009 D159 162
50. Nelson A.R., Henkin T.M., and Agris P.F. tRNA regulation of gene expression: interactions of an mRNA 5′-UTR with a regulatory tRNA RNA 12 2006 1254 1261 (Pubitemid 43990550)
51. Rollins S.M., Grundy F.J., and Henkin T.M. Analysis of cis-acting sequence and structural elements required for antitermination of the Bacillus subtilis tyrS gene Mol. Microbiol. 25 1997 411 421 (Pubitemid 27351591)
52. Diener J.L., and Moore P.B. Solution structure of a substrate for the archaeal pre-tRNA splicing endonucleases: the bulge-helix-bulge motif Mol. Cell 1 1998 883 894 (Pubitemid 128379072)
53. Hermann T., and Patel D.J. RNA bulges as architectural and recognition motifs Structure 8 2000 R47 54
54. Mao H., and Williamson J.R. Assignment of the L30-mRNA complex using selective isotopic labeling and RNA mutants Nucleic Acids Res. 27 1999 4059 4070 (Pubitemid 29479033)
55. Matsumura S., Ikawa Y., and Inoue T. Biochemical characterization of the kink-turn RNA motif Nucleic Acids Res. 31 2003 5544 5551 (Pubitemid 37441924)
56. Clore G.M., and Kuszewski J. Improving the accuracy of NMR structures of RNA by means of conformational database potentials of mean force as assessed by complete dipolar coupling cross-validation J. Am. Chem. Soc. 125 2003 1518 1525 (Pubitemid 36206232)
57. Owens R.A., and Baumstark T. Structural differences within the loop E motif imply alternative mechanisms of viroid processing RNA 13 2007 824 834 (Pubitemid 46799816)
58. Davanloo P., Rosenberg A.H., Dunn J.J., and Sturdier F.W. Cloning and expression of the gene for bacteriophage T7 RNA polymerase Proc. Natl Acad. Sci. USA 81 1984 2035 2039 (Pubitemid 14146599)
59. Milligan J.F., Groebe D.R., Witherell G.W., and Uhlenbeck O.C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates Nucleic Acids Res. 15 1987 8783 8798
60. 15N labelled RNAs for heteronuclear multi-dimensional NMR studies Nucleic Acids Res. 20 1992 4507 4513
61. Hansen M.R., Mueller L., and Pardi A. Tunable alignment of macromolecules by filamentous phage yields dipolar coupling interactions Nat. Struct. Biol. 5 1998 1065 1074 (Pubitemid 28546270)
62. Legault P., Farmer B.T., Mueller L., and Pardi A. Through-bond correlation of adenine protons in a 13C-labeled ribozyme J. Am. Chem. Soc. 116 1994 2203 2204
63. 13C-labeled RNA J. Am. Chem. Soc. 119 1997 7361 7366 (Pubitemid 27348593)
64. Majumdar A., Kettani A., Skripkin E., and Patel D.J. Pulse sequences for detection of NH2...N hydrogen bonds in sheared G.A mismatches via remote, non-exchangeable protons J. Biomol. NMR 19 2001 103 113 (Pubitemid 32184439)
65. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR molecular structure determination package J. Magn. Reson. 160 2003 65 73
66. 31P J coupling constants in isotopically labeled RNA FEBS Lett. 362 1995 156 160
67. NN couplings J. Am. Chem. Soc. 120 1998 8293 8297 (Pubitemid 28420452)
68. Varani G., Aboul-ela F., and Allain F.H.T. NMR investigation of RNA structure Prog. Nucl. Magn. Reson. Spectrosc. 29 1996 51 127 (Pubitemid 126381972)
69. Salim N.N., and Feig A.L. Isothermal titration calorimetry of RNA Methods 47 2009 198 205