Profiling small RNA reveals multimodal substructural signals in a Boltzmann ensemble

Nucleic Acids Research

Volumn 42, Issue 22, 2014, Pages

  Rogers, Emily ^a   Heitsch, Christine E ^b  

^a Georgia Institute of Technology   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 5S; TRANSFER RNA; BACTERIAL RNA; SMALL UNTRANSLATED RNA;

ARTICLE; BASE PAIRING; BOLTZMANN ENSEMBLE; CONTROLLED STUDY; LOW ENERGY SECONDARY STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RNA ANALYSIS; RNA PROFILING; RNA SEQUENCE; RNA STRUCTURE; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; GENETICS; PROCEDURES; SEQUENCE ANALYSIS; STATISTICAL ANALYSIS; VIBRIO CHOLERAE;

BASE PAIRING; DATA INTERPRETATION, STATISTICAL; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, RNA; VIBRIO CHOLERAE;

EID: 84927606642     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku959     Document Type: Article

References (51)

1. Couzin, J. (2002) Small RNAs make big splash. Science, 298, 2296-2297.
2. Doudna, J. A. (2000) Structural genomics of RNA. Nat. Struct. Biol., 7, 954-956.
3. Breaker, R. R. (1996) Are engineered proteins getting competition from RNA? Curr. Opin. Biotechnol., 7, 442-448.
4. Serganov, A. and Patel, D. J. (2007) Ribozymes, riboswitches and beyond: regulation of gene expression without proteins. Nat. Rev. Genet., 8, 776-790.
5. Tucker, B. J. and Breaker, R. R. (2005) Inventing and improving ribozyme function: rational design versus iterative selection methods. Curr. Opin. Struct. Biol., 15, 342-348.
6. Lenz, D. H., Mok, K. C., Lilley, B. N., Kulkarni, R. V., Wingreen, N. S. and Bassler, B. L. (2004) The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell, 117, 69-82.
7. Tu, K. C. and Bassler, B. L. (2007) Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev., 21, 221-233.
8. Mathews, D. H., Sabina, J., Zuker, M. and Turner, D. H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940.
9. Doshi, K. J., Cannone, J. J., Cobaugh, C. W. and Gutell, R. R. (2004) Evaluation of the suitability of free-energy minimization using nearest-neighbor energy parameters for RNA secondary structure prediction. BMC Bioinformatics, 5, 105.
10. Williams, A. L. Jr and Tinoco, I. Jr (1986) A dynamic programming algorithm for finding alternative RNA secondary structures. Nucleic Acids Res., 14, 299-315.
11. Jaeger, J. A., Turner, D. H. and Zuker, M. (1989) Improved predictions of secondary structures for RNA. Proc. Natl. Acad. Sci. U. S. A., 86, 7706-7710.
12. Zuker, M., Jaeger, J. A. and Turner, D. H. (1991) A comparison of optimal and suboptimal RNA secondary structures predicted by free energy minimization with structures determined by phylogenetic comparison. Nucleic Acids Res., 19, 2707-2714.
13. Jacobson, A. B. and Zuker, M. (1993) Structural analysis by energy dot plot of a large mRNA. J. Mol. Biol., 233, 261-269.
14. Zuker, M. and Jacobson, A. B. (1995) "Well-determined" regions in RNA secondary structure prediction: analysis of small subunit ribosomal RNA. Nucleic Acids Res., 23, 2791-2798.
15. Zuker, M. and Jacobson, A. (1998) Using reliability information to annotate RNA secondary structures. RNA, 4, 669-679.
16. Wuchty, S., Fontana, W., Hofacker, I. L. and Schuster, P. (1999) Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers, 49, 145-165.
17. Zuker, M. (1989) On finding all suboptimal foldings of an RNA molecule. Science, 244, 48-52.
18. Ding, Y. and Lawrence, C. E. (2003) A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res., 31, 7280-7301.
19. Mathews, D. H. (2006) Revolutions in RNA secondary structure prediction. J. Mol. Biol., 359, 526-532.
20. McCaskill, J. S. (1990) The equilibrium partition function and base pair binding probabilities for RNA secondary structure. Biopolymers, 29, 1105-1119.
21. Hofacker, I. L., Fontana, W., Stadler, P. F., Bonhoeffer, L. S., Tacker, M. and Schuster, P. (1994) Fast folding and comparison of RNA secondary structures. Monatsh. Chem., 125, 167-188.
22. Huynen, M., Gutell, R. and Konings, D. (1997) Assessing the reliability of RNA folding using statistical mechanics. J. Mol. Biol., 267, 1104-1112.
23. Mathews, D. H. (2004) Using an RNA secondary structure partition function to determine confidence in base pairs predicted by free energy minimization. RNA, 10, 1178-1190.
24. Ding, Y., Chan, C. Y. and Lawrence, C. E. (2005) RNA secondary structure prediction by centroids in a Boltzmann weighted ensemble. RNA, 11, 1157-1166.
25. Giegerich, R., Voß, B. and Rehmsmeier, M. (2004) Abstract shapes of RNA. Nucleic Acids Res., 32, 4843-4851.
26. Miller, M. B. and Bassler, B. L. (2001) Quorum sensing in bacteria. Annu. Rev. Microbiol., 55, 165-199.
27. Zhu, J., Miller, M. B., Vance, R. E., Dziejman, M., Bassler, B. L. and Mekalanos, J. J. (2002) Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A., 99, 3129-3134.
28. Mutreja, A., Kim, D. W., Thomson, N. R., Connor, T. R., Lee, J. H., Kariuki, S., Croucher, N. J., Choi, S. Y., Harris, S. R., Lebens, M. et al. (2011) Evidence for several waves of global transmission in the seventh cholera pandemic. Nature, 477, 462-465.
29. Bardill, J. P., Zhao, X. and Hammer, B. K. (2011) The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions. Mol. Microbiol., 80, 1381-1394.
30. Miyashiro, T., Wollenberg, M. S., Cao, X., Oehlert, D. and Ruby, E. G. (2010) A single qrr gene is necessary and sufficient for LuxO-mediated regulation in Vibrio fischeri. Mol. Microbiol., 77, 1556-1567.
31. Zuker, M. and Stiegler, P. (1981) Optimal computer folding of large RNA sequences using thermodynamics and auxiliary information. Nucleic Acids Res., 9, 133-148.
32. Turner, D. H. and Mathews, D. H. (2010) NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure. Nucleic Acids Res., 38, D280-D282.
33. Ding, Y., Chan, C. Y. and Lawrence, C. E. (2004) Sfold web server for statistical folding and rational design of nucleic acids. Nucleic Acids Res., 32, W135-W141.
34. Chan, C. Y., Lawrence, C. E. and Ding, Y. (2005) Structure clustering features on the Sfold Web server. Bioinformatics, 21, 3926-3928.
35. Moulton, V., Zuker, M., Steel, M., Pointon, R. and Penny, D. (2000) Metrics on RNA secondary structures. J. Comput. Biol., 7, 277-292.
36. Voß, B., Giegerich, R. and Rehmsmeier, M. (2006) Complete probabilistic analysis of RNA shapes. BMC Biol., 4, 5.
37. Steffen, P., Voß, B., Rehmsmeier, M., Reeder, J. and Giegerich, R. (2006) RNAshapes: an integrated RNA analysis package based on abstract shapes. Bioinformatics, 22, 500-503.
38. Huang, J., Backofen, R. and Voß, B. (2012) Abstract folding space analysis based on helices. RNA, 18, 2135-2147.
39. Huang, J. and Voß, B. (2014) Analysing RNA-kinetics based on folding space abstraction. BMC Bioinformatics, 15, 60.
40. Cannone, J. J., Subramanian, S., Schnare, M. N., Collett, J. R., D'Souza, L. M., Du, Y., Feng, B., Lin, N., Madabusi, L. V., Müller, K. M. et al. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics, 3, 2.
41. Griffiths-Jones, S., Bateman, A., Marshall, M., Khanna, A. and Eddy, S. R. (2003) Rfam: an RNA family database. Nucleic Acids Res., 31, 439-441.
42. Burge, S. W., Daub, J., Eberhardt, R., Tate, J., Barquist, L., Nawrocki, E. P., Eddy, S. R., Gardner, P. P. and Bateman, A. (2013) Rfam 11.0:10 years of RNA families. Nucleic Acids Res., 41, D226-D232.
43. Swenson, M. S., Anderson, J., Ash, A., Gaurav, P., Sükösd, Z., Bader, D. A., Harvey, S. C. and Heitsch, C. E. (2012) GTfold: enabling parallel RNA secondary structure prediction on multi-core desktops. BMC Res. Notes, 5, 341.
44. Hammer, B. K. and Bassler, B. L. (2007) Regulatory small RNAs circumvent the conventional quorum sensing pathway in pandemic Vibrio cholerae. Proc. Natl. Acad. Sci. U. S. A., 104, 11145-11149.
45. Bardill, J. P. and Hammer, B. (2012) Non-coding sRNAs regulate virulence in the bacterial pathogen Vibrio cholerae. RNA Biol., 9, 392-401.
46. Shao, Y. and Bassler, B. L. (2012) Quorum-sensing non-coding small RNAs use unique pairing regions to differentially control mRNA targets. Mol. Microbiol., 83, 599-611.
47. Bardill, J. P., Zhao, X. and Hammer, B. K. (2011) The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions. Mol. Microbiol., 80, 1381-1394.
48. Zhao, X., Koestler, B. J., Waters, C. M. and Hammer, B. K. (2013) Post-transcriptional activation of a diguanylate cyclase by quorum sensing small RNAs promotes biofilm formation in Vibrio cholerae. Mol. Microbiol., 89, 989-1002.
49. Tu, K. C. and Bassler, B. L. (2009) Gene dosage compensation calibrates four regulatory RNAs to control Vibrio cholerae quorum sensing. EMBO, 28, 429-439.
50. Rutherford, S. T., Van Kessel, J. C., Shao, Y. and Bassler, B. L. (2011) AphA and LuxR/HapR reciprocally control quorum sensing in vibrios. Genes Dev., 25, 397-408.
51. Stein, P. and Waterman, M. (1979) On some new sequences generalizing the Catalan and Motzkin numbers. Discrete Math., 26, 261-272.