Exploiting preQ1 riboswitches to regulate ribosomal frameshifting

ACS Chemical Biology

Volumn 8, Issue 4, 2013, Pages 733-740

  Yu, Chien Hung ^a   Luo, Jinghui ^a   Iwata Reuyl, Dirk ^b   Olsthoorn, René C L ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b PORTLAND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APTAMER; GUANINE;

ARTICLE; CONTROLLED STUDY; CRYSTALLOGRAPHY; FUSOBACTERIUM NUCLEATUM; IN VITRO STUDY; LIGAND BINDING; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; RIBOSOMAL FRAMESHIFTING; RIBOSWITCH;

APTAMERS, NUCLEOTIDE; BASE SEQUENCE; FRAMESHIFTING, RIBOSOMAL; NUCLEIC ACID CONFORMATION; RIBOSWITCH;

BACTERIA (MICROORGANISMS); EUKARYOTA; FUSOBACTERIUM NUCLEATUM;

EID: 84876532777     PISSN: 15548929     EISSN: 15548937     Source Type: Journal    
DOI: 10.1021/cb300629b     Document Type: Article

References (53)

1. Farabaugh, P. J. (2000) Translational frameshifting: implications for the mechanism of translational frame maintenance Prog. Nucleic Acid Res. Mol. Biol. 64, 131-170
2. Baranov, P. V., Gesteland, R. F., and Atkins, J. F. (2002) Recoding: translational bifurcations in gene expression Gene 286, 187-201
3. Namy, O., Rousset, J. P., Napthine, S., and Brierley, I. (2004) Reprogrammed genetic decoding in cellular gene expression Mol. Cell 13, 157-168
4. Brierley, I., Jenner, A. J., and Inglis, S. C. (1992) Mutational analysis of the "slippery-sequence" component of a coronavirus ribosomal frameshifting signal J. Mol. Biol. 227, 463-479
5. Brierley, I. and Pennell, S. (2001) Structure and function of the stimulatory RNAs involved in programmed eukaryotic-1 ribosomal frameshifting Cold Spring Harbor Symp. Quant. Biol. 66, 233-248
6. Giedroc, D. P. and Cornish, P. V. (2009) Frameshifting RNA pseudoknots: structure and mechanism Virus Res. 139, 193-208
7. Namy, O., Moran, S. J., Stuart, D. I., Gilbert, R. J. C., and Brierley, I. (2006) A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting Nature 441, 244-247
8. Lin, Z., Gilbert, R. J. C., and Brierley, I. (2012) Spacer-length dependence of programmed -1 or -2 ribosomal frameshifting on a U6A heptamer supports a role for messenger RNA (mRNA) tension in frameshifting Nucleic Acids Res. 40, 8674-8689
9. Brierley, I., Pennell, S., and Gilbert, R. J. (2007) Viral RNA pseudoknots: versatile motifs in gene expression and replication Nat. Rev. Microbiol. 5, 598-610
10. Baranov, P. V., Fayet, O., Hendrix, R. W., and Atkins, J. F. (2006) Recoding in bacteriophages and bacterial IS elements Trends Genet. 22, 174-181
11. Larsen, B., Gesteland, R. F., and Atkins, J. F. (1997) Structural probing and mutagenic analysis of the stem-loop required for Escherichia coli dnaX ribosomal frameshifting: programmed efficiency of 50% J. Mol. Biol. 271, 47-60
12. Baranov, P. V., Wills, N. M., Barriscale, K. A., Firth, A. E., Jud, M. C., Letsou, A., Manning, G., and Atkins, J. F. (2011) Programmed ribosomal frameshifting in the expression of the regulator of intestinal stem cell proliferation, adenomatous polyposis coli (APC) RNA Biol. 8, 637-647
13. Manktelow, E., Shigemoto, K., and Brierley, I. (2005) Characterization of the frameshift signal of Edr, a mammalian example of programmed- 1 ribosomal frameshifting Nucleic Acids Res. 33, 1553-1563
14. Wills, N. M. (2006) A functionaL-1 ribosomal frameshift signal in the human paraneoplastic Ma3 gene J. Biol. Chem. 281, 7082-7088
15. Clark, M. B., Janicke, M., Gottesbuhren, U., Kleffmann, T., Legge, M., Poole, E. S., and Tate, W. P. (2007) Mammalian gene PEG10 expresses two reading frames by high efficiency -1 frameshifting in embryonic-Associated tissues J. Biol. Chem. 282, 37359-37369
16. Shehu-Xhilaga, M., Crowe, S. M., and Mak, J. (2001) Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type-1 RNA dimerization and viral infectivity J. Virol. 75, 1834-1841
17. Park, S.-J., Kim, Y.-G., and Park, H.-J. (2011) Identification of RNA pseudoknot-binding ligand that inhibits the -1 ribosomal frameshifting of SARS-Coronavirus by structure-based virtual screening J. Am. Chem. Soc. 133, 10094-10100
18. Hansen, T. M., Reihani, S. N. S., Oddershede, L. B., and Sørensen, M. A. (2007) Correlation between mechanical strength of messenger RNA pseudoknots and ribosomal frameshifting Proc. Natl. Acad. Sci. U.S.A. 104, 5830-5835
19. Green, L., Kim, C.-H., Bustamante, C., and Tinoco, I., Jr. (2008) Characterization of the mechanical unfolding of RNA pseudoknots J. Mol. Biol. 375, 511-528
20. Chen, G., Chang, K.-Y., Chou, M.-Y., Bustamante, C., and Tinoco, I., Jr. (2009) Triplex structures in an RNA pseudoknot enhance mechanical stability and increase efficiency of -1 ribosomal frameshifting Proc. Natl. Acad. Sci. U.S.A. 106, 12706-12711
21. Yu, C.-H., Noteborn, M. H. M., and Olsthoorn, R. C. L. (2010) Stimulation of ribosomal frameshifting by antisense LNA Nucleic Acids Res. 38, 8277-8283
22. Yu, C.-H., Noteborn, M. H., Pleij, C. W. A., and Olsthoorn, R. C. L. (2011) Stem-loop structures can effectively substitute for an RNA pseudoknot in -1 ribosomal frameshifting Nucleic Acids Res. 39, 8952-8959
23. Bidou, L., Stahl, G., Grima, B., Liu, H., and Cassan, M. (1997) In vivo HIV-1 frameshifting efficiency is directly related to the stability of the stem-loop stimulatory signal RNA 3, 1153-1158
24. Cornish, P. V., Stammler, S. N., and Giedroc, D. P. (2006) The global structures of a wild-type and poorly functional plant luteoviral mRNA pseudoknot are essentially identical RNA 12, 1959-1969
25. Su, L., Chen, L., Egli, M., Berger, J. M., and Rich, A. (1999) Minor groove RNA triplex in the crystal structure of a ribosomal frameshifting viral pseudoknot Nat. Struct. Mol. Biol. 6, 285-292
26. Michiels, P. J., Versleijen, A. A., Verlaan, P. W., Pleij, C. W., Hilbers, C. W., and Heus, H. A. (2001) Solution structure of the pseudoknot of SRV-1 RNA involved in ribosomal frameshifting J. Mol. Biol. 310, 1109-1123
27. Cornish, P. V., Hennig, M., and Giedroc, D. P. (2005) A loop 2 cytidine-stem 1 minor groove interaction as a positive determinant for pseudoknot-stimulated -1 ribosomal frameshifting Proc. Natl. Acad. Sci. U.S.A. 102, 12694-12699
28. Olsthoorn, R. C. L., Reumerman, R., Hilbers, C. W., Pleij, C. W. A., and Heus, H. A. (2010) Functional analysis of the SRV-1 RNA frameshifting pseudoknot Nucleic Acids Res. 38, 7665-7672
29. Kim, Y. G., Maas, S., Wang, S. C., and Rich, A. (2000) Mutational study reveals that tertiary interactions are conserved in ribosomal frameshifting pseudoknots of two luteoviruses RNA 6, 1157-1165
30. Chou, M.-Y. and Chang, K.-Y. (2010) An intermolecular RNA triplex provides insight into structural determinants for the pseudoknot stimulator of -1 ribosomal frameshifting Nucleic Acids Res. 38, 1676-1685
31. Roth, A. and Breaker, R. R. (2009) The structural and functional diversity of metabolite-binding riboswitches Annu. Rev. Biochem. 78, 305-334
32. Deigan, K. E. and Ferré-D'Amaré, A. R. (2011) Riboswitches: discovery of drugs that target bacterial gene-regulatory RNAs Acc. Chem. Res. 44, 1329-1338
33. Chou, M.-Y., Lin, S.-C., and Chang, K.-Y. (2010) Stimulation of -1 programmed ribosomal frameshifting by a metabolite-responsive RNA pseudoknot RNA 16, 1236-1244
34. Edwards, A. L., Reyes, F. E., Héroux, A., and Batey, R. T. (2010) Structural basis for recognition of S-Adenosylhomocysteine by riboswitches RNA 16, 2144-2155
35. Roth, A., Winkler, W. C., Regulski, E. E., Lee, B. W. K., Lim, J., Jona, I., Barrick, J. E., Ritwik, A., Kim, J. N., Welz, R., Iwata-Reuyl, D., and Breaker, R. R. (2007) A riboswitch selective for the queuosine precursor preQ1 contains an unusually small aptamer domain Nat. Struct. Mol. Biol. 14, 308-317
36. Iwata-Reuyl, D. (2008) An embarrassment of riches: the enzymology of RNA modification Curr. Opin. Chem. Biol. 12, 126-133
37. Kang, M., Peterson, R., and Feigon, J. (2009) Structural Insights into riboswitch control of the biosynthesis of queuosine, a modified nucleotide found in the anticodon of tRNA Mol. Cell 33, 784-790
38. Klein, D. J., Edwards, T. E., and Ferré D'Amaré, A. R. (2009) Cocrystal structure of a class I preQ1 riboswitch reveals a pseudoknot recognizing an essential hypermodified nucleobase Nat. Struct. Mol. Biol. 16, 343-344
39. Jenkins, J. L., Krucinska, J., McCarty, R. M., Bandarian, V., and Wedekind, J. E. (2011) Comparison of a preQ1 riboswitch aptamer in metabolite-bound and free states with implications for gene regulation J. Biol. Chem. 286, 24626-24637
40. Rieder, U., Lang, K., Kreutz, C., Polacek, N., and Micura, R. (2009) Evidence for pseudoknot formation of class I preQ1 riboswitch aptamers ChembBioChem 10, 1141-1144
41. ten Dam, E. B., Verlaan, P. W., and Pleij, C. W. (1995) Analysis of the role of the pseudoknot component in the SRV-1 gag-pro ribosomal frameshift signal: loop lengths and stability of the stem regions RNA 1, 146-154
42. Egli, M., Minasov, G., Su, L., and Rich, A. (2002) Metal ions and flexibility in a viral RNA pseudoknot at atomic resolution Proc. Natl. Acad. Sci. U.S.A. 99, 4302-4307
43. Pallan, P. S., Marshall, W. S., Harp, J., Jewett, F. C., 3rd, Wawrzak, Z., Brown, B. A., 2nd, Rich, A., and Egli, M. (2005) Crystal structure of a luteoviral RNA pseudoknot and model for a minimal ribosomal frameshifting motif Biochemistry 44, 11315-11322
44. Breaker, R. R. (2011) Prospects for riboswitch discovery and analysis Mol. Cell 43, 867-879
45. Mandal, M., Boese, B., Barrick, J. E., Winkler, W. C., and Breaker, R. R. (2003) Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria Cell 113, 577-586
46. Gilbert, S. D., Stoddard, C. D., Wise, S. J., and Batey, R. T. (2006) Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain J. Mol. Biol. 359, 754-768
47. Wickiser, J. K., Winkler, W. C., Breaker, R. R., and Crothers, D. M. (2005) The speed of RNA transcription and metabolite binding kinetics operate an FMN riboswitch Mol. Cell 18, 49-60
48. Plant, E. P. and Dinman, J. D. (2005) Torsional restraint: a new twist on frameshifting pseudoknots Nucleic Acids Res. 33, 1825-1833
49. Franch, T., Petersen, M., Wagner, E. G., Jacobsen, J. P., and Gerdes, K. (1999) Antisense RNA regulation in prokaryotes: rapid RNA/RNA interaction facilitated by a general U-turn loop structure J. Mol. Biol. 294, 1115-1125
50. Pennell, S., Manktelow, E., Flatt, A., Kelly, G., Smerdon, S. J., and Brierley, I. (2008) The stimulatory RNA of the Visna-Maedi retrovirus ribosomal frameshifting signal is an unusual pseudoknot with an interstem element RNA 14, 1366-1377
51. Nissen, P., Ippolito, J. A., Ban, N., Moore, P. B., and Steitz, T. A. (2001) RNA tertiary interactions in the large ribosomal subunit: the A-minor motif Proc. Natl. Acad. Sci. U.S.A. 98, 4899-4903
52. Rieder, U., Kreutz, C., and Micura, R. (2010) Folding of a transcriptionally acting preQ1 riboswitch Proc. Natl. Acad. Sci. U.S.A. 107, 10804-10809
53. Iwata-Reuyl, D. (2003) Biosynthesis of the 7-deazaguanosine hypermodified nucleosides of transfer RNA Bioorg. Chem. 31, 24-43