Discovery and validation of novel and distinct RNA regulators for ribosomal protein S15 in diverse bacterial phyla

详细信息    查看全文

• 作者：Betty L Slinger (5)
  Kaila Deiorio-Haggar (5)
  Jon S Anthony (5)
  Molly M Gilligan (5)
  Michelle M Meyer (5)
  
  5. Biology Department ; Boston College ; Chestnut Hill ; MA ; 02135 ; USA
  
• 刊名：BMC Genomics
• 出版年：2014
• 出版时间：December 2014
• 年：2014
• 卷：15
• 期：1
• 全文大小：1,230 KB
• 参考文献：1. Amaral, PP, Mattick, JS (2008) Noncoding RNA in development. Mamm Genome 19: pp. 454-492 CrossRef
  2. Johansson, J, Cossart, P (2003) RNA-mediated control of virulence gene expression in bacterial pathogens. Trends Microbiol 11: pp. 280-285 CrossRef
  3. Dambach, M, Winkler, W (2009) Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12: pp. 161-169 CrossRef
  4. Waters, LS, Storz, G (2009) Regulatory RNAs in bacteria. Cell 136: pp. 615-628 CrossRef
  5. Fabian, MR, Sonenberg, N, Filipowicz, W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79: pp. 351-379 CrossRef
  6. Storz, G, Vogel, J, Wassarman, KM (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43: pp. 880-891 CrossRef
  7. Wilusz, JE, Sunwoo, H, Spector, DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Gene Dev 23: pp. 1494-1504 CrossRef
  8. Gilbert, SD, Rambo, RP, Van Tyne, D, Batey, RT (2008) Structure of the SAM-II riboswitch bound to S-adenosylmethionine. Nat Struct Mol Biol 15: pp. 177-182 CrossRef
  9. Montange, RK, Batey, RT (2006) Structure of the S-adenosylmethionine riboswitch regulatory mRNA element. Nature 441: pp. 1172-1175 CrossRef
  10. Lu, C, Smith, AM, Fuchs, RT, Ding, F, Rajashankar, K, Henkin, TM, Ke, A (2008) Crystal structures of the SAM-III/S(MK) riboswitch reveal the SAM-dependent translation inhibition mechanism. Nat Struct Mol Biol 15: pp. 1076-1083 CrossRef
  11. Wang, JX, Breaker, RR (2008) Riboswitches that sense S-adenosylmethionine and S-adenosylhomocysteine. Biochem Cell Biol 86: pp. 157-168 CrossRef
  12. Winkler, W, Nahvi, A, Roth, A, Collins, J, Breaker, R (2004) Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428: pp. 281-286 CrossRef
  13. Urban, J, Papenfort, K, Thomsen, J, Schmitz, R, Vogel, J (2007) A conserved small RNA promotes discoordinate expression of the glmUS operon mRNA to activate GlmS synthesis. J Mol Biol 373: pp. 521-528 CrossRef
  14. Dean, D, Nomura, M (1980) Feedback regulation of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci USA 77: pp. 3590-3594 CrossRef
  15. Zengel, JM, Lindahl, L (1994) Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. Prog Nucleic Acid Res Mol Biol 47: pp. 331-370 CrossRef
  16. Harvey, RJ (1970) Regulation of ribosomal protein synthesis in Escherichia coli. J Bacteriol 101: pp. 574-583
  17. Fu, Y, Deiorio-Haggar, K, Anthony, J, Meyer, MM (2013) Most RNAs regulating ribosomal protein biosynthesis in Escherichia coli are narrowly distributed to Gammaproteobacteria. Nucleic Acids Res 41: pp. 3491-3503 CrossRef
  18. Deiorio-Haggar, K, Anthony, J, Meyer, MM (2013) RNA structures regulating ribosomal protein biosynthesis in bacilli. RNA Biol 10: pp. 1180-1184 CrossRef
  19. Grundy, F, Henkin, T (1992) Characterization of the bacillus subtilis rpsD regulatory target site. J Bacteriol 174: pp. 6763-6770
  20. Guillier, M, Allemand, F, Raibaud, S, Dardel, F, Springer, M, Chairuttini, C (2002) Translational feedback regulation of the gene for L35 in Escherichia coli requires binding of ribosomal protein L20 to two sites in its leader mRNA: a possible case of ribosomal RNA-messenger RNA molecular mimicry. RNA 8: pp. 878-889 CrossRef
  21. Choonee, N, Even, S, Zig, L, Putzer, H (2007) Ribosomal protein L20 controls expression of the bacillus subtilis infC operon via a transcription attenuation mechanism. Nucleic Acids Res 35: pp. 1578-1588 CrossRef
  22. Philippe, C, Portier, C, Mougel, M, Grunberg-Manago, M, Ebel, J, Ehresmann, B, Ehresmann, C (1990) Target site of Escherichia coli ribosomal protein S15 on its messenger RNA* 1: conformation and interaction with the protein. J Mol Biol 211: pp. 415-426 CrossRef
  23. Scott, LG, Williamson, JR (2001) Interaction of the bacillus stearothermophilus ribosomal protein S15 with its 5鈥?translational operator mRNA1. J Mol Biol 314: pp. 413-422 CrossRef
  24. Serganov, A, Polonskaia, A, Ehresmann, B, Ehresmann, C, Patel, D (2003) Ribosomal protein S15 represses its own translation via adaptation of an rRNA-like fold within its mRNA. EMBO J 22: pp. 1898-1908 CrossRef
  25. Mathy, N, Pellegrini, O, Serganov, A, Patel, DJ, Ehresmann, C, Portier, C (2004) Specific recognition of rpsO mRNA and 16S rRNA by Escherichia coli ribosomal protein S15 relies on both mimicry and site differentiation. Mol Microbiol 52: pp. 661-675 CrossRef
  26. Scott, L, Williamson, J (2005) The binding interface between bacillus stearothermophilus ribosomal protein S15 and its 5鈥?translational operator mRNA. J Mol Biol 351: pp. 280-290 CrossRef
  27. Yao, Z, Barrick, J, Weinberg, Z, Neph, S, Breaker, R, Tompa, M, Ruzzo, WL (2007) A computational pipeline for high-throughput discovery of cis-regulatory noncoding RNA in prokaryotes. PLoS Comput Biol 3: pp. e126 CrossRef
  28. Weinberg, Z, Wang, JX, Bogue, J, Yang, J, Corbino, K, Moy, RH, Breaker, RR (2010) Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11: pp. 1-17 CrossRef
  29. Weinberg, Z, Barrick, JE, Yao, Z, Roth, A, Kim, JN, Gore, J, Wang, JX, Lee, ER, Block, KF, Sudarsan, N, Neph, S, Tompa, M, Ruzzo, WL, Breaker, RR (2007) Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35: pp. 4809-4819 CrossRef
  30. Yao, Z, Weinberg, Z, Ruzzo, WL (2005) CMfinder鈥揳 covariance model based RNA motif finding algorithm. Bioinformatics 22: pp. 445-452 CrossRef
  31. Nawrocki, EP, Eddy, SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29: pp. 2933-2935 CrossRef
  32. Staple, DW, Butcher, SE (2005) Pseudoknots: RNA structures with diverse functions. PLoS Biol 3: pp. e213 CrossRef
  33. Merhej, V, Raoult, D (2011) Rickettsial evolution in the light of comparative genomics. Bio Rev Camb Philos Soc 86: pp. 379-405 CrossRef
  34. Giannoukos, G, Ciulla, DM, Huang, K, Haas, BJ, Izard, J, Levin, JZ, Livny, J, Earl, AM, Gevers, D, Ward, DV, Nusbaum, C, Birren, BW, Gnirke, A (2012) Efficient and robust RNA-seq process for cultured bacteria and complex community transcriptomes. Genome Biol 13: pp. R23 CrossRef
  35. Serganov, A, Ennifar, E, Portier, C, Ehresmann, B, Ehresmann, C (2002) Do mRNA and rRNA binding sites of E. coli ribosomal protein S15 share common structural determinants?. J Mol Biol 320: pp. 963-978 CrossRef
  36. Philippe, C, Eyermann, F, Benard, L, Portier, C, Ehresmann, B, Ehresmann, C (1993) Ribosomal protein S15 from Escherichia coli modulates its own translation by trapping the ribosome on the mRNA initiation loading site. Proc Natl Acad Sci USA 90: pp. 4394-4298 CrossRef
  37. Albrecht, M, Sharma, CM, Reinhardt, R, Vogel, J, Rudel, T (2010) Deep sequencing-based discovery of the Chlamydia trachomatis transcriptome. Nucleic Acids Res 38: pp. 868-877 CrossRef
  38. Gardner, P, Daub, J, Tate, J, Moore, B, Osuch, I, Griffiths-Jones, S, Finn, R, Nawrocki, E, Kolbe, D, Eddy, S (2011) Rfam: Wikipedia, clans and the 鈥渄ecimal鈥?release. Nucleic Acids Res 39: pp. D141 CrossRef
  39. Lu, X, Goodrich-Blair, H, Tjaden, B (2011) Assessing computational tools for the discovery of small RNA genes in bacteria. RNA 17: pp. 1635-1647 CrossRef
  40. Hall, K, Kranz, J (1999) Nitrocellulose filter binding for determination of dissociation constants. Methods Mol Biol 118: pp. 105-114
  41. Weinberg, Z, Regulski, EE, Hammond, MC, Barrick, JE, Yao, Z, Ruzzo, WL, Breaker, RR (2008) The aptamer core of SAM-IV riboswitches mimics the ligand-binding site of SAM-I riboswitches. RNA 14: pp. 822-828 CrossRef
  42. Poiata, E, Meyer, MM, Ames, TD, Breaker, RR (2009) A variant riboswitch aptamer class for S-adenosylmethionine common in marine bacteria. RNA 15: pp. 2046-2056 CrossRef
  43. Nevskaya, N, Tishchenko, S, Gabdoulkhakov, A, Nikonova, E, Nikonov, O, Nikulin, A, Platonova, O, Garner, M, Nikonov, S, Piendl, W (2005) Ribosomal protein L1 recognizes the same specific structural motif in its target sites on the autoregulatory mRNA and 23S rRNA. Nucleic Acids Res 33: pp. 478-485 CrossRef
  44. Pruitt, KD, Tatusova, T, Brown, GR, Maglott, DR (2011) NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 40: pp. D130-D135 CrossRef
  45. Altschul, S, Gish, W, Miller, W, Myers, E, Lipman, D (1990) Basic local alignment search tool. J Mol Biol 215: pp. 403-410 CrossRef
  46. Arnvig, KB, Comas, I, Thomson, NR, Houghton, J, Boshoff, HI, Croucher, NJ, Rose, G, Perkins, TT, Parkhill, J, Dougan, G, Young, DB (2011) Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis. PLoS Pathog 7: pp. e1002342 CrossRef
  47. Weinberg, Z, Breaker, RR (2011) R2R鈥搒oftware to speed the depiction of aesthetic consensus RNA secondary structures. BMC Bioinformatics 12: pp. 3 CrossRef
  48. Milligan, J, Groebe, D, Witherell, G, Uhlenbeck, O (1987) Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res 15: pp. 8783 CrossRef
  49. Regulski, E, Breaker, R (2008) In-line probing analysis of riboswitches. Meth Mol Biol 419: pp. 53-67 CrossRef
  50. Block, KF, Puerta-Fernandez, E, Wallace, JG, Breaker, RR (2011) Association of OLE RNA with bacterial membranes via an RNA-protein interaction. Mol Microbiol 79: pp. 21-34 CrossRef
  51. Philippe, C, Benard, L, Eyermann, F, Cachia, C, Kirillov, SV, Portier, C, Ehresmann, B, Ehresmann, C (1994) Structural elements of rps0 mRNA involved in the modulation of translational initiation and regulation of E. coli ribosomal protein S15. Nucleic Acids Res 22: pp. 2538-2546 CrossRef
  52. Culver, G, Noller, H (1999) Efficient reconstitution of functional Escherichia coli 30S ribosomal subunits from a complete set of recombinant small subunit ribosomal proteins. RNA 5: pp. 832 CrossRef
  53. Muranaka, N, Sharma, V, Nomura, Y, Yokobayashi, Y (2009) An efficient platform for genetic selection and screening of gene switches in Escherichia coli. Nucleic Acids Res 37: pp. e39-e39 CrossRef
  
• 刊物主题：Life Sciences, general; Microarrays; Proteomics; Animal Genetics and Genomics; Microbial Genetics and Genomics; Plant Genetics & Genomics;
• 出版者：BioMed Central
• ISSN：1471-2164

文摘

Background Autogenous cis-regulators of ribosomal protein synthesis play a critical role in maintaining the stoichiometry of ribosome components. Structured portions within an mRNA transcript typically interact with specific ribosomal proteins to prevent expression of the entire operon, thus balancing levels of ribosomal proteins across transcriptional units. Three distinct RNA structures from different bacterial phyla have demonstrated interactions with S15 to regulate gene expression; however, these RNAs are distributed across a small fraction of bacterial diversity. Results We used comparative genomics in combination with analysis of existing transcriptomic data to identify three novel putative RNA structures associated with the S15 coding region in microbial genomes. These structures are completely distinct from those previously published and encompass potential regulatory regions including ribosome-binding sites. To validate the biological relevance of our findings, we demonstrate that an example of the Alphaproteobacterial RNA from Rhizobium radiobacter specifically interacts with S15 in vitro, and allows in vivo regulation of gene expression in an E. coli reporter system. In addition, structural probing and nuclease protection assays confirm the predicted secondary structure and indicate nucleotides required for protein interaction. Conclusions This work illustrates the importance of integrating comparative genomic and transcriptomic approaches during de novo ncRNA identification and reveals a diversity of distinct natural RNA regulators that support analogous biological functions. Furthermore, this work indicates that many additional uncharacterized RNA regulators likely exist within bacterial genomes and that the plasticity of RNA structure allows unique, and likely independently derived, solutions to the same biological problem.