The K-turn motif in riboswitches and other RNA species

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1839, Issue 10, 2014, Pages 995-1004

  Lilley, David M J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

Kink turn; RNA folding; RNA structure; Tertiary interaction

Indexed keywords

L7AE PROTEIN; RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

BINDING AFFINITY; HUMAN; KINK TURN MOTIF; NONHUMAN; NUCLEOTIDE BINDING SITE; NUCLEOTIDE MOTIF; PROTEIN FAMILY; PROTEIN RNA BINDING; REVIEW; RIBOSOME SUBUNIT; RIBOSWITCH; RNA ANALYSIS; RNA FOLDING; RNA STRUCTURE;

EID: 84908326089     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2014.04.020     Document Type: Review

References (60)

1. Winkler W.C., Grundy F.J., Murphy B.A., Henkin T.M. The GA motif: an RNA element common to bacterial antitermination systems, rRNA, and eukaryotic RNAs. RNA 2001, 7:1165-1172.
2. Vidovic I., Nottrott S., Hartmuth K., Luhrmann R., Ficner R. Crystal structure of the spliceosomal 15.5 kD protein bound to a U4 snRNA fragment. Mol. Cell 2000, 6:1331-1342.
3. Klein D.J., Schmeing T.M., Moore P.B., Steitz T.A. The kink-turn: a new RNA secondary structure motif. EMBO J. 2001, 20:4214-4221.
4. Montange R.K., Batey R.T. Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 2006, 441:1172-1175.
5. Smith K.D., Lipchock S.V., Ames T.D., Wang J., Breaker R.R., Strobel S.A. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat. Struct. Mol. Biol. 2009, 16:1218-1223.
6. Smith K.D., Shanahan C.A., Moore E.L., Simon A.C., Strobel S.A. Structural basis of differential ligand recognition by two classes of bis-(3'-5')-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:7757-7762.
7. 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.
8. Zhang J., Ferre-D'Amare A.R. Co-crystal structure of a T-box riboswitch stem I domain in complex with its cognate tRNA. Nature 2013, 500:363-366.
9. Blouin S., 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 2007, 13:1256-12567.
10. Baird N.J., Ferre-D'Amare A.R. Modulation of quaternary structure and enhancement of ligand binding by the K-turn of tandem glycine riboswitches. RNA 2013, 19:167-176.
11. Thore S., Leibundgut M., Ban N. Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 2006, 312:1208-1211.
12. Serganov A., Polonskaia A., Phan A.T., Breaker R.R., Patel D.J. Structural basis for gene regulation by a thiamine pyrophosphate-sensing riboswitch. Nature 2006, 441:1167-1171.
13. Wang J., Huang L., Lilley D.M.J. The k-junction motif in RNA structure. Nucleic Acids Res. 2014, 42:5322-5331.
14. Moore T., Zhang Y., Fenley M.O., Li H. Molecular basis of box C/D RNA-protein interactions; cocrystal structure of archaeal L7Ae and a box C/D RNA. Structure 2004, 12:807-818.
15. Hamma T., Ferré-D'Amaré A.R. Structure of protein L7Ae bound to a K-turn derived from an archaeal box H/ACA sRNA at 1.8Å resolution. Structure 2004, 12:893-903.
16. Szewczak L.B., Gabrielsen J.S., Degregorio S.J., Strobel S.A., Steitz J.A. Molecular basis for RNA kink-turn recognition by the h15.5K small RNP protein. RNA 2005, 11:1407-1419.
17. Youssef O.A., Terns R.M., Terns M.P. Dynamic interactions within sub-complexes of the H/ACA pseudouridylation guide RNP. Nucleic Acids Res. 2007, 35:6196-6206.
18. Wozniak A.K., Nottrott S., Kuhn-Holsken E., Schroder G.F., Grubmuller H., Luhrmann R., Seidel C.A., Oesterhelt F. Detecting protein-induced folding of the U4 snRNA kink-turn by single-molecule multiparameter FRET measurements. RNA 2005, 11:1545-1554.
19. Mao H., White S.A., Williamson J.R. A novel loop-loop recognition motif in the yeast ribosomal protein L30 autoregulatory RNA complex. Nat. Struct. Biol. 1999, 6:1139-1147.
20. White S.A., Hoeger M., Schweppe J.J., Shillingford A., Shipilov V., Zarutskie J. Internal loop mutations in the ribosomal protein L30 binding site of the yeast L30 RNA transcript. RNA 2004, 10:369-377.
21. Andersen E.S., Rosenblad M.A., Larsen N., Westergaard J.C., Burks J., Wower I.K., Wower J., Gorodkin J., Samuelsson T., Zwieb C. The tmRDB and SRPDB resources. Nucleic Acids Res. 2006, 34:D163-D168.
22. Reiter N.J., Osterman A., Torres-Larios A., Swinger K.K., Pan T., Mondragon A. Structure of a bacterial ribonuclease P holoenzyme in complex with tRNA. Nature 2010, 468:784-789.
23. Schroeder K.T., McPhee S.A., Ouellet J., Lilley D.M.J. A structural database for k-turn motifs in RNA. RNA 2010, 16:1463-1468.
24. Liu J., Lilley D.M.J. The role of specific 2'-hydroxyl groups in the stabilization of the folded conformation of kink-turn RNA. RNA 2007, 13:200-210.
25. Schroeder K.T., Lilley D.M.J. Ion-induced folding of a kink turn that departs from the conventional sequence. Nucleic Acids Res. 2009, 37:7281-7289.
26. Schroeder K.T., Daldrop P., McPhee S.A., Lilley D.M.J. Structure and folding of a rare, natural kink turn in RNA with an A*A pair at the 2b*2n position. RNA 2012, 18:1257-1266.
27. Meyer M., Westhof E., Masquida B. A structural module in RNase P expands the variety of RNA kinks. RNA Biol. 2012, 9:254-260.
28. Daldrop P., Masquida B., Lilley D.M.J. The functional exchangeability of pk- and k-turns in RNA structure. RNA Biol. 2013, 10:445-452.
29. Garst A.D., Heroux A., Rambo R.P., Batey R.T. Crystal structure of the lysine riboswitch regulatory mRNA element. J. Biol. Chem. 2008, 283:22347-22351.
30. Serganov A., Huang L., Patel D.J. Structural insights into amino acid binding and gene control by a lysine riboswitch. Nature 2008, 455:1263-1267.
31. Turner B., Lilley D.M.J. The importance of G·A hydrogen bonding in the metal ion- and protein-induced folding of a kink turn RNA. J. Mol. Biol. 2008, 381:431-442.
32. Lescoute A., Leontis N.B., Massire C., Westhof E. Recurrent structural RNA motifs, isostericity matrices and sequence alignments. Nucleic Acids Res. 2005, 33:2395-2409.
33. Daldrop P., Lilley D.M.J. The plasticity of a structural motif in RNA: structural polymorphism of a kink turn as a function of its environment. RNA 2013, 19:357-364.
34. Nissen P., Ippolito J.A., Ban N., Moore P.B., Steitz T.A. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:4899-4903.
35. Ban N., Nissen P., Hansen J., Moore P.B., Steitz T.A. The complete atomic structure of the large ribosomal subunit at 2.4Å resolution. Science 2000, 289:905-920.
36. Wimberly B.T., Brodersen D.E., Clemons W.M., Morgan-Warren R.J., Carter A.P., Vonrhein C., Hartsch T., Ramakrishnan V. Structure of the 30S ribosomal subunit. Nature 2000, 407:327-339.
37. Chao J.A., Williamson J.R. Joint X-ray and NMR refinement of the yeast L30e-mRNA complex. Structure 2004, 12:1165-1176.
38. Schroeder K.T., Daldrop P., Lilley D.M.J. RNA tertiary interactions in a riboswitch stabilize the structure of a kink turn. Structure 2011, 19:1233-1240.
39. Huang L., Lilley D.M.J. The molecular recognition of kink turn structure by the L7Ae class of proteins. RNA 2013, 19:1703-1710.
40. Huang L., Lilley D.M.J. Structure of a rare, non-standard sequence k-turn bound by L7Ae protein. Nucleic Acids Res. 2014, 42:4734-4740.
41. Reblova K., Sponer J.E., Spackova N., Besseova I., Sponer J. A-minor tertiary interactions in RNA kink-turns. Molecular dynamics and quantum chemical analysis. J. Phys. Chem. B 2011, 115:13897-13910.
42. Goody T.A., Melcher S.E., Norman D.G., Lilley D.M.J. The kink-turn motif in RNA is dimorphic, and metal ion dependent. RNA 2004, 10:254-264.
43. Matsumura S., Ikawa Y., Inoue T. Biochemical characterization of the kink-turn RNA motif. Nucleic Acids Res. 2003, 31:5544-5551.
44. Heppell B., Lafontaine D.A. Folding of the SAM aptamer is determined by the formation of a K-turn-dependent pseudoknot. Biochemistry 2008, 47:1490-1499.
45. Turner B., Melcher S.E., Wilson T.J., Norman D.G., Lilley D.M.J. Induced fit of RNA on binding the L7Ae protein to the kink-turn motif. RNA 2005, 11:1192-1200.
46. Koonin E.V., Bork P., Sander C. A novel RNA-binding motif in omnipotent suppressors of translation termination, ribosomal proteins and a ribosome modification enzyme?. Nucleic Acids Res. 1994, 22:2166-2167.
47. Nottrott S., Hartmuth K., Fabrizio P., Urlaub H., Vidovic I., Ficner R., Luhrmann R. Functional interaction of a novel 15.5kD [U4/U6.U5] tri-snRNP protein with the 5' stem-loop of U4 snRNA. EMBO J. 1999, 18:6119-6133.
48. Baird N.J., Zhang J., Hamma T., Ferré-D'Amaré A.R. YbxF and YlxQ are bacterial homologs of L7Ae, and bind K-turns but not K-loops. RNA 2012, 18:759-770.
49. Rozhdestvensky T.S., Tang T.H., Tchirkova I.V., Brosius J., Bachellerie J.-P., Hüttenhofer A. Binding of L7Ae protein to the K-turn of archaeal snoRNAs: a shared RNA binding motif for C/D and H/ACA box snoRNAs in Archaea. Nucleic Acids Res. 2003, 31:869-877.
50. Kiss-Laszlo Z., Henry Y., Bachellerie J.P., Caizergues-Ferrer M., Kiss T. Site-specific ribose methylation of preribosomal RNA: a novel function for small nucleolar RNAs. Cell 1996, 85:1077-1088.
51. Ganot P., Bortolin M.L., Kiss T. Site-specific pseudouridine formation in preribosomal RNA is guided by small nucleolar RNAs. Cell 1997, 89:799-809.
52. Trahan C., Dragon F. Dyskeratosis congenita mutations in the H/ACA domain of human telomerase RNA affect its assembly into a pre-RNP. RNA 2009, 15:235-243.
53. Marmier-Gourrier N., Clery A., Senty-Segault V., Charpentier B., Schlotter F., Leclerc F., Fournier R., Branlant C. A structural, phylogenetic, and functional study of 15.5-kD/Snu13 protein binding on U3 small nucleolar RNA. RNA 2003, 9:821-838.
54. Cho I.M., Lai L.B., Susanti D., Mukhopadhyay B., Gopalan V. Ribosomal protein L7Ae is a subunit of archaeal RNase P. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14573-14578.
55. Tsai C.J., Ma B., Sham Y.Y., Kumar S., Nussinov R. Structured disorder and conformational selection. Proteins 2001, 44:418-427.
56. Koshland D.E. Application of a theory of enzyme specificity to protein synthesis. Proc. Natl. Acad. Sci. U. S. A. 1958, 44:98-104.
57. Wang J., Fessl T., Schroeder K.T., Ouellet J., Liu Y., Freeman A.D., Lilley D.M.J. Single-molecule observation of the induction of k-turn RNA structure on binding L7Ae protein. Biophys. J. 2012, 103:2541-2548.
58. Kulshina N., Baird N.J., Ferre-D'Amare A.R. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat. Struct. Mol. Biol. 2009, 16:1212-1217.
59. Rohl R., Nierhaus K.H. Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc. Natl. Acad. Sci. U. S. A. 1982, 79:729-733.
60. Herold M., Nierhaus K.H. Incorporation of six additional proteins to complete the assembly map of the 50S subunit from Escherichia coli ribosomes. J. Biol. Chem. 1987, 262:8826-8833.