Large-scale mapping of sequence-function relations in small regulatory RNAs reveals plasticity and modularity

Nucleic Acids Research

Volumn 42, Issue 19, 2014, Pages 12177-12188

  Peterman, Neil ^a   Lavi Itzkovitz, Anat ^a   Levine, Erel ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; DSRA RNA; NUCLEOTIDE DERIVATIVE; RYHB RNA; SMALL REGULATORY RNA; UNCLASSIFIED DRUG; DSRA RNA, E COLI; SMALL UNTRANSLATED RNA;

ACCURACY; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE LIBRARY; GENE MAPPING; GENE REPRESSION; GENE TARGETING; GENETIC STABILITY; MOLECULAR INTERACTION; NONHUMAN; PLASTICITY; PRIORITY JOURNAL; PROMOTER REGION; QUANTITATIVE ANALYSIS; RNA BINDING; RNA SEQUENCE; RNA STRUCTURE; BIOLOGICAL MODEL; CHEMISTRY; CONFORMATION; FLOW CYTOMETRY; METABOLISM; MUTATION; SEQUENCE ANALYSIS;

FLOW CYTOMETRY; MODELS, BIOLOGICAL; MUTATION; NUCLEIC ACID CONFORMATION; RNA, SMALL UNTRANSLATED; SEQUENCE ANALYSIS, RNA;

EID: 84925283037     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku863     Document Type: Article

References (57)

1. Waters, L.S. and Storz, G. (2009) Regulatory RNAs in bacteria. Cell, 136, 615-628.
2. Gottesman, S. and Storz, G. (2011) Bacterial small RNA regulators: Versatile roles and rapidly evolving variations. Cold Spring Harb. Perspect. Biol., 3, a003798.
3. Storz, G., Vogel, J. and Wassarman, K.M. (2011) Regulation by small RNAs in bacteria: Expanding frontiers. Mol. Cell, 43, 880-891.
4. Jost, D., Nowojewski, A. and Levine, E. (2011) Small RNA biology is systems biology. BMB Rep., 44, 11-21.
5. Argaman, L., Hershberg, R., Vogel, J., Bejerano, G., Wagner, E.G., Margalit, H. and Altuvia, S. (2001) Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr. Biol., 11, 941-950.
6. Wassarman, K.M., Repoila, F., Rosenow, C., Storz, G. and Gottesman, S. (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev., 15, 1637-1651.
7. Massé, E. and Gottesman, S. (2002) A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 99, 4620-4625.
8. Massé, E., Escorcia, F.E. and Gottesman, S. (2003) Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev., 17, 2374-2383.
9. Guillier, M. and Gottesman, S. (2008) The 5' end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res., 36, 6781-6794.
10. Bandyra, K.J., Said, N., Pfeiffer, V., Górna, M.W., Vogel, J. and Luisi, B.F. (2012) The seed region of a small RNA drives the controlled destruction of the target mRNA by the endoribonuclease RNase E. Mol. Cell, 47, 943-953.
11. Andrade, J.M., Pobre, V. and Arraiano, C.M. (2013) Small RNA modules confer different stabilities and interact differently with multiple targets. PLoS ONE, 8, e52866.
12. Majdalani, N., Cunning, C., Sledjeski, D., Elliott, T. and Gottesman, S. (1998) DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc. Natl. Acad. Sci. U.S.A., 95, 12462-12467.
13. Lease, R.A. and Belfort, M. (2000) A trans-acting RNA as a control switch in Escherichia coli: DsrA modulates function by forming alternative structures. Proc. Natl. Acad. Sci. U.S.A., 97, 9919-9924.
14. Prévost, K., Salvail, H., Desnoyers, G., Jacques, J.F., Phaneuf, E. and Massé, E. (2007) The small RNA RyhB activates the translation of shiA mRNA encoding a permease of shikimate, a compound involved in siderophore synthesis. Mol. Microbiol., 64, 1260-1273.
15. Zhang, A., Wassarman, K.M., Ortega, J., Steven, A.C. and Storz, G. (2002) The Sm-like Hfq protein increases OxyS RNA interaction with target mRNAs. Mol. Cell, 9, 11-22.
16. Geissmann, T.A. and Touati, D. (2004) Hfq, a new chaperoning role: Binding to messenger RNA determines access for small RNA regulator. EMBO J., 23, 396-405.
17. 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, 118, 69-82.
18. Aiba, H. (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr. Opin. Microbiol., 10, 134-139.
19. Vogel, J. and Luisi, B.F. (2011) Hfq and its constellation of RNA. Nat. Rev. Microbiol., 9, 578-589.
20. Liu, J.M., Bittker, J.A., Lonshteyn, M. and Liu, D.R. (2005) Functional dissection of sRNA translational regulators by nonhomologous random recombination and in vivo selection. Chem. Biol., 12, 757-767.
21. Hao, Y., Zhang, Z.J., Erickson, D.W., Huang, M., Huang, Y., Li, J., Hwa, T. and Shi, H. (2011) Quantifying the sequence-function relation in gene silencing by bacterial small RNAs. Proc. Natl. Acad. Sci. U.S.A., 108, 12473-12478.
22. Beisel, C.L., Updegrove, T.B., Janson, B.J. and Storz, G. (2012) Multiple factors dictate target selection by Hfq-binding small RNAs. EMBO J., 31, 1961-1974.
23. Ishikawa, H., Otaka, H., Maki, K., Morita, T. and Aiba, H. (2012) The functional Hfq-binding module of bacterial sRNAs consists of a double or single hairpin preceded by a U-rich sequence and followed by a 3- poly(U) tail. RNA, 18, 1062-1074.
24. Rice, J.B., Balasubramanian, D. and Vanderpool, C.K. (2012) Small RNA binding-site multiplicity involved in translational regulation of a polycistronic mRNA. Proc. Natl. Acad. Sci. U.S.A., 109, E2691-E2698.
25. Vogel, J. and Wagner, E.G.H. (2007) Target identification of small noncoding RNAs in bacteria. Curr. Opin. Microbiol., 10, 262-270.
26. Backofen, R. and Hess, W.R. (2010) Computational prediction of sRNAs and their targets in bacteria. RNA Biol., 7, 33-42.
27. Jin, Y., Wu, J., Li, Y., Cai, Z. and Huang, J.-D. (2013) Modification of the RpoS network with a synthetic small RNA. Nucleic Acids Res., 41, 8332-8340.
28. Park, H., Bak, G., Kim, S.C. and Lee, Y. (2013) Exploring sRNA-mediated gene silencing mechanisms using artificial small RNAs derived from a natural RNA scaffold in Escherichia coli. Nucleic Acids Res., 41, 3787-3804.
29. Skippington, E. and Ragan, M.A. (2012) Evolutionary dynamics of small RNAs in 27 Escherichia coli and Shigella genomes. Genome Biol. Evol., 4, 330-345.
30. Cheng, S.W., Lynch, E.C., Leason, K.R., Court, D.L., Shapiro, B.A. and Friedman, D.I. (1991) Functional importance of sequence in the stem-loop of a transcription terminator. Science, 254, 1205-1207.
31. Wilson, K.S. and von Hippel, P.H. (1995) Transcription termination at intrinsic terminators: The role of the RNA hairpin. Proc. Natl. Acad. Sci. U.S.A., 92, 8793-8797.
32. Valentin-Hansen, P., Eriksen, M. and Udesen, C. (2004) MicroReview: The bacterial Sm-like protein Hfq: A key player in RNA transactions. Mol. Microbiol., 51, 1525-1533.
33. Sauer, E., Schmidt, S. and Weichenrieder, O. (2012) Small RNA binding to the lateral surface of Hfq hexamers and structural rearrangements upon mRNA target recognition. Proc. Natl. Acad. Sci. U.S.A., 109, 9396-9401.
34. Otaka, H., Ishikawa, H., Morita, T. and Aiba, H. (2011) PolyU tail of rho-independent terminator of bacterial small RNAs is essential for Hfq action. Proc. Natl. Acad. Sci. U.S.A., 108, 13059-13064.
35. Chen, S., Zhang, A., Blyn, L.B. and Storz, G. (2004) MicC, a second small-RNA regulator of Omp protein expression in Escherichia coli. J. Bacteriol., 186, 6689-6697.
36. Kawamoto, H., Koide, Y., Morita, T. and Aiba, H. (2006) Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq. Mol. Microbiol., 61, 1013-1022.
37. Richter, A.S. and Backofen, R. (2012) Accessibility and conservation: General features of bacterial small RNA-mRNA interactions? RNA Biol., 9, 954-965.
38. Wright, P.R., Richter, A.S., Papenfort, K., Mann, M., Vogel, J., Hess, W.R., Backofen, R. and Georg, J. (2013) Comparative genomics boosts target prediction for bacterial small RNAs. Proc. Natl. Acad. Sci. U.S.A., 110, E3487-E3496.
39. Kinney, J.B., Murugan, A., Callan, C.G. and Cox, E.C. (2010) Using deep sequencing to characterize the biophysical mechanism of a transcriptional regulatory sequence. Proc. Natl. Acad. Sci. U.S.A., 107, 9158-9163.
40. Sharon, E., Kalma, Y., Sharp, A., Raveh-Sadka, T., Levo, M., Zeevi, D., Keren, L., Yakhini, Z., Weinberger, A. and Segal, E. (2012) Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters. Nat. Biotechnol., 30, 521-530.
41. McLaughlin, R.N. Jr, Poelwijk, F.J., Raman, A., Gosal, W.S. and Ranganathan, R. (2012) The spatial architecture of protein function and adaptation. Nature, 491, 138-142.
42. Holmqvist, E., Reimegård, J. and Wagner, E.G.H. (2013) Massive functional mapping of a 5-UTR by saturation mutagenesis, phenotypic sorting and deep sequencing. Nucleic Acids Res., 41, e122.
43. Kosuri, S., Goodman, D.B., Cambray, G., Mutalik, V.K., Gao, Y., Arkin, A.P., Endy, D. and Church, G.M. (2013) Composability of regulatory sequences controlling transcription and translation in Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 110, 14024-14029.
44. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A., 97, 6640-6645.
45. Levine, E., Zhang, Z., Kuhlman, T. and Hwa, T. (2007) Quantitative characteristics of gene regulation by small RNA. PLoS Biol., 5, e229.
46. Pédelacq, J.-D., Cabantous, S., Tran, T., Terwilliger, T.C. and Waldo, G.S. (2006) Engineering and characterization of a superfolder green fluorescent protein. J. Mol. Biol., 24, 79-88.
47. Lutz, R. and Bujard, H. (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res., 25, 1203-1210.
48. Massé, E., Vanderpool, C.K. and Gottesman, S. (2005) Effect of RyhB small RNA on global iron use in Escherichia coli. J. Bacteriol., 187, 6962-6971.
49. Urban, J.H. and Vogel, J. (2007) Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res., 35, 1018-1037.
50. Soper, T., Mandin, P., Majdalani, N., Gottesman, S. and Woodson, S.A. (2010) Positive regulation by small RNAs and the role of Hfq. Proc. Natl. Acad. Sci. U.S.A., 107, 9602-9607.
51. Lorenz, R., Bernhart, S.H., Siederdissen, C.H., Tafer, H., Flamm, C., Stadler, P.F. and Hofacker, I.L. (2011) ViennaRNA Package 2.0. Algorithms Mol. Biol., 6, 26.
52. Lehner, B. (2011) Molecular mechanisms of epistasis within and between genes. Trends Genet., 27, 323-331.
53. Tafer, H., Ameres, S.L., Obernosterer, G., Gebeshuber, C.A., Schroeder, R., Martinez, J. and Hofacker, I.L. (2008) The impact of target site accessibility on the design of effective siRNAs. Nat. Biotechnol., 26, 578-583.
54. Li, X., Quon, G., Lipshitz, H.D. and Morris, Q. (2010) Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure. RNA, 16, 1096-1107.
55. Sarkar, K., Nguyen, D.A. and Gruebele, M. (2010) Loop and stem dynamics during RNA hairpin folding and unfolding. RNA, 16, 2427-2434.
56. Bartel, D.P. (2009) MicroRNAs: Target recognition and regulatory functions. Cell, 136, 215-233.
57. Maki, K., Morita, T., Otaka, H. and Aiba, H. (2010) A minimal base-pairing region of a bacterial small RNA SgrS required for translational repression of ptsG mRNA. Mol. Microbiol., 76, 782-792.