Transcription analysis and small non-protein coding RNAs associated with bacterial ribosomal protein operons

Current Medicinal Chemistry

Volumn 19, Issue 30, 2012, Pages 5187-5198

  Khayrullina, G A ^a,b   Raabe, C A ^b   Hoe, C H ^c   Becker, K ^d   Reinhardt, R ^e   Tang, T H ^c   Rozhdestvensky, T S ^b   Kopylov, A M ^a  

^a MOSCOW STATE UNIVERSITY   (Russian Federation)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c ADVANCED MEDICAL AND DENTAL INSTITUTE   (Malaysia)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^e Max Planck Genome Centre Cologne   (Germany)

Author keywords

Bacterial pathogens; Non protein coding RNA (ncRNA); Operons; Regulation; Ribosomal proteins; Transcription

Indexed keywords

BACTERIAL PROTEIN; RIBOSOME PROTEIN; RNA; SMALL NON PROTEIN CODING RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; FEEDBACK SYSTEM; GENETIC TRANSCRIPTION; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PROTEIN SECONDARY STRUCTURE; REAL TIME POLYMERASE CHAIN REACTION; SALMONELLA TYPHI; STAPHYLOCOCCUS AUREUS; TRANSLATION REGULATION; VIBRIO CHOLERAE;

BACTERIA; BACTERIAL PROTEINS; OPERON; RIBOSOMAL PROTEINS; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; TRANSCRIPTION, GENETIC;

EID: 84870471077     PISSN: 09298673     EISSN: 1875533X     Source Type: Journal    
DOI: 10.2174/092986712803530485     Document Type: Article

References (71)

1. Pommier, Y., and Marchand, C. Interfacial inhibitors: targeting macromolecular complexes, Nat Rev Drug Discov, 2012, 11, 25-36.
2. Nomura, M. Regulation of ribosome biosynthesis in Escherichia coli and Saccharomyces cerevisiae: diversity and common principles, J Bacteriol, 1999, 181, 6857-6864.
3. Altuvia, S., Weinstein-Fischer, D., Zhang, A., Postow, L., and Storz, G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator, Cell, 1997, 90, 43-53.
4. Sledjeski, D. D., Gupta, A., and Gottesman, S. The small RNA, DsrA, is essential for the low temperature expression of RpoS during exponential growth in Escherichia coli, Embo J, 1996, 15, 3993-4000.
5. Steglich, C., Futschik, M. E., Lindell, D., Voss, B., Chisholm, S. W., and Hess, W. R. The challenge of regulation in a minimal photoautotroph: noncoding RNAs in Prochlorococcus, PLoS Genet, 2008, 4, e1000173.
6. Wagner, E. G., and Simons, R. W. Antisense RNA control in bacteria, phages, and plasmids, Annu Rev Microbiol, 1994, 48, 713-742.
7. Sittka, A., Pfeiffer, V., Tedin, K., and Vogel, J. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium, Mol Microbiol, 2007, 63, 193-217.
8. Kawamoto, H., Koide, Y., Morita, T., and Aiba, H. Base-pairing requirement for RNA silencing by a bacterial small RNA and acceleration of duplex formation by Hfq, Mol Microbiol, 2006, 61, 1013-1022.
9. Romby, P., Vandenesch, F., and Wagner, E. G. The role of RNAs in the regulation of virulence-gene expression, Curr Opin Microbiol, 2006, 9, 229-236.
10. Vogel, J., and Papenfort, K. Small non-coding RNAs and the bacterial outer membrane, Curr Opin Microbiol, 2006, 9, 605-611.
11. Gottesman, S. The small RNA regulators of Escherichia coli: roles and mechanisms*, Annu Rev Microbiol, 2004, 58, 303-328.
12. Gottesman, S. Micros for microbes: non-coding regulatory RNAs in bacteria, Trends Genet, 2005, 21, 399-404.
13. Montange, R. K., and Batey, R. T. Riboswitches: emerging themes in RNA structure and function, Annu Rev Biophys, 2008, 37, 117-133.
14. Sharma, C. M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiss, S., Sittka, A., Chabas, S., Reiche, K., Hackermuller, J., Reinhardt, R., Stadler, P. F., and Vogel, J. The primary transcriptome of the major human pathogen Helicobacter pylori, Nature, 2010, 464, 250-255.
15. Arnvig, K. B., Comas, I., Thomson, N. R., Houghton, J., Boshoff, H. I., Croucher, N. J., Rose, G., Perkins, T. T., Parkhill, J., Dougan, G., and Young, D. B. Sequence-based analysis uncovers an abundance of non-coding RNA in the total transcriptome of Mycobacterium tuberculosis, PLoS Pathog, 2011, 7, e1002342.
16. Raabe, C. A., Hoe, C. H., Randau, G., Brosius, J., Tang, T. H., and Rozhdestvensky, T. S. The rocks and shallows of deep RNA sequencing: Examples in the Vibrio cholerae RNome, Rna, 2011, 17, 1357-1366.
17. Abu-Qatouseh, L. F., Chinni, S. V., Seggewiss, J., Proctor, R. A., Brosius, J., Rozhdestvensky, T. S., Peters, G., von Eiff, C., and Becker, K. Identification of differentially expressed small non-protein-coding RNAs in Staphylococcus aureus displaying both the normal and the small-colony variant phenotype, J Mol Med (Berl), 2010, 88, 565-575.
18. Chinni, S. V., Raabe, C. A., Zakaria, R., Randau, G., Hoe, C. H., Zemann, A., Brosius, J., Tang, T. H., and Rozhdestvensky, T. S. Experimental identification and characterization of 97 novel npcRNA candidates in Salmonella enterica serovar Typhi, Nucleic Acids Res, 2010, 38, 5893-5908.
19. An, G., Lee, J. S., and Friesen, J. D. Evidence for an internal promoter preceding tufA in the str operon of Escherichia coli, J Bacteriol, 1982, 149, 548-553.
20. Zengel, J. M., and Lindahl, L. Mapping of two promoters for elongation factor Tu within the structural gene for elongation factor G, Biochim Biophys Acta, 1990, 1050, 317-322.
21. Nierhaus, K. H., and Wilson, D. N., (Eds.) Protein Synthesis and Ribosome Structure: Translating the Genome, WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim, 2004.
22. Ding, Y., Davis, B. M., and Waldor, M. K. Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression, Mol Microbiol, 2004, 53, 345-354.
23. DeChiara, T. M., and Brosius, J. Neural BC1 RNA: cDNA clones reveal nonrepetitive sequence content, Proc Natl Acad Sci U S A, 1987, 84, 2624-2628.
24. Raabe, C. A., Sanchez, C. P., Randau, G., Robeck, T., Skryabin, B. V., Chinni, S. V., Kube, M., Reinhardt, R., Ng, G. H., Manickam, R., Kuryshev, V. Y., Lanzer, M., Brosius, J., Tang, T. H., and Rozhdestvensky, T. S. A global view of the nonprotein-coding transcriptome in Plasmodium falciparum, Nucleic Acids Res, 2010, 38, 608-617.
25. Rood, I. G., Pettersson, A., Savelkoul, P. H., and de Korte, D. Development of a reverse transcription-polymerase chain reaction assay for eubacterial RNA detection in platelet concentrates, Transfusion, 2010, 50, 1352-1358.
26. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction, Nucleic Acids Res, 2003, 31, 3406-3415.
27. Tjaden, B. TargetRNA: a tool for predicting targets of small RNA action in bacteria, Nucleic Acids Res, 2008, 36, W109-113.
28. Saito, K., and Nomura, M. Post-transcriptional regulation of the str operon in Escherichia coli. Structural and mutational analysis of the target site for translational repressor S7, J Mol Biol, 1994, 235, 125-139.
29. Saito, K., Mattheakis, L. C., and Nomura, M. Post-transcriptional regulation of the str operon in Escherichia coli. Ribosomal protein S7 inhibits coupled translation of S7 but not its independent translation, J Mol Biol, 1994, 235, 111-124.
30. Spiridonova, V. A., Rozhdestvensky, T. S., and Kopylov, A. M. A study of the thermophilic ribosomal protein S7 binding to the truncated S12-S7 intercistronic region provides more insight into the mechanism of regulation of the str operon of E. coli(1), FEBS Lett, 1999, 460, 353-356.
31. Guell, M., Yus, E., Lluch-Senar, M., and Serrano, L. Bacterial transcriptomics: what is beyond the RNA horiz-ome?, Nat Rev Microbiol, 2011, 9, 658-669.
32. Saint Girons, I., and Margarita, D. Evidence for an internal promoter in the Escherichia coli threonine operon, J Bacteriol, 1985, 161, 461-462.
33. Ely, B., and Ciesla, Z. Internal promoter P2 of the histidine operon of Salmonella typhimurium, J Bacteriol, 1974, 120, 984-986.
34. Guell, M., van Noort, V., Yus, E., Chen, W. H., Leigh-Bell, J., Michalodimitrakis, K., Yamada, T., Arumugam, M., Doerks, T., Kuhner, S., Rode, M., Suyama, M., Schmidt, S., Gavin, A. C., Bork, P., and Serrano, L. Transcriptome complexity in a genome-reduced bacterium, Science, 2009, 326, 1268-1271.
35. Zengel, J. M., and Lindahl, L. A secondary promoter for elongation factor Tu synthesis in the str ribosomal protein operon of Escherichia coli, Mol Gen Genet, 1982, 185, 487-492.
36. Furano, A. V. Content of elongation factor Tu in Escherichia coli, Proc Natl Acad Sci U S A, 1975, 72, 4780-4784.
37. Krasny, L., Vacik, T., Fucik, V., and Jonak, J. Cloning and characterization of the str operon and elongation factor Tu expression in Bacillus stearothermophilus, J Bacteriol, 2000, 182, 6114-6122.
38. Kawano, M., Storz, G., Rao, B. S., Rosner, L. J., and Martin, G. R. Detection of low-level promoter activity within open reading frame sequences of Escherichia coli, Nucleic Acids Research, 2005, 33(19), 6268-6276.
39. Rezuchova, B., Miticka, H., Homerova, D., Roberts, M., and Kormanec, J. New members of the Escherichia coli sigmaE regulon identified by a twoplasmid system, FEMS Microbiol Lett, 2003, 225, 1-7.
40. Rhodius, V. A., Suh, W. C., Nonaka, G., West, J., and Gross, C. A. Conserved and variable functions of the sigmaE stress response in related genomes, PLoS Biol, 2006, 4, e2.
41. Nakano, M., Takahashi, A., Su, Z., Harada, N., Mawatari, K., and Nakaya, Y. Hfq regulates the expression of the thermostable direct hemolysin gene in Vibrio parahaemolyticus, BMC Microbiol, 2008, 8, 155.
42. Dienst, D., Duhring, U., Mollenkopf, H. J., Vogel, J., Golecki, J., Hess, W. R., and Wilde, A. The cyanobacterial homologue of the RNA chaperone Hfq is essential for motility of Synechocystis sp. PCC 6803, Microbiology, 2008, 154, 3134-3143.
43. Sonnleitner, E., Hagens, S., Rosenau, F., Wilhelm, S., Habel, A., Jager, K. E., and Blasi, U. Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1, Microb Pathog, 2003, 35, 217-228.
44. Roop, R. M., 2nd, Gee, J. M., Robertson, G. T., Richardson, J. M., Ng, W. L., and Winkler, M. E. Brucella stationary-phase gene expression and virulence, Annu Rev Microbiol, 2003, 57, 57-76.
45. Christiansen, J. K., Larsen, M. H., Ingmer, H., Sogaard-Andersen, L., and Kallipolitis, B. H. The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence, J Bacteriol, 2004, 186, 3355-3362.
46. McNealy, T. L., Forsbach-Birk, V., Shi, C., and Marre, R. The Hfq homolog in Legionella pneumophila demonstrates regulation by LetA and RpoS and interacts with the global regulator CsrA, J Bacteriol, 2005, 187, 1527-1532.
47. Kulesus, R. R., Diaz-Perez, K., Slechta, E. S., Eto, D. S., and Mulvey, M. A. Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli, Infect Immun, 2008, 76, 3019-3026.
48. Iben, J. R., and Draper, D. E. Specific interactions of the L10(L12)4 ribosomal protein complex with mRNA, rRNA, and L11, Biochemistry, 2008, 47, 2721-2731.
49. Diaconu, M., Kothe, U., Schlunzen, F., Fischer, N., Harms, J. M., Tonevitsky, A. G., Stark, H., Rodnina, M. V., and Wahl, M. C. Structural basis for the function of the ribosomal L7/12 stalk in factor binding and GTPase activation, Cell, 2005, 121, 991-1004.
50. Klein, D. J., Schmeing, T. M., Moore, P. B., and Steitz, T. A. The kink-turn: a new RNA secondary structure motif, Embo J, 2001, 20, 4214-4221.
51. Proctor, R. A., von Eiff, C., Kahl, B. C., Becker, K., McNamara, P., Herrmann, M., and Peters, G. Small colony variants: a pathogenic form of bacteria that facilitates persistent and recurrent infections, Nat Rev Microbiol, 2006, 4, 295-305.
52. von Eiff, C., Becker, K., Metze, D., Lubritz, G., Hockmann, J., Schwarz, T., and Peters, G. Intracellular persistence of Staphylococcus aureus smallcolony variants within keratinocytes: a cause for antibiotic treatment failure in a patient with darier's disease, Clin Infect Dis, 2001, 32, 1643-1647.
53. Vaudaux, P., Kelley, W. L., and Lew, D. P. Staphylococcus aureus small colony variants: difficult to diagnose and difficult to treat, Clin Infect Dis, 2006, 43, 968-970.
54. Christensen, T., Johnsen, M., Fiil, N. P., and Friesen, J. D. RNA secondary structure and translation inhibition: analysis of mutants in the rplJ leader, Embo J, 1984, 3, 1609-1612.
55. Fiil, N. P., Friesen, J. D., Downing, W. L., and Dennis, P. P. Posttranscriptional regulatory mutants in a ribosomal protein-RNA polymerase operon of E. coli, Cell, 1980, 19, 837-844.
56. Friesen, J. D., Tropak, M., and An, G. Mutations in the rpIJ leader of Escherichia coli that abolish feedback regulation, Cell, 1983, 32, 361-369.
57. Tang, C. K., and Draper, D. E. Unusual mRNA pseudoknot structure is recognized by a protein translational repressor, Cell, 1989, 57, 531-536.
58. Spedding, G., and Draper, D. E. Allosteric mechanism for translational repression in the Escherichia coli alpha operon, Proc Natl Acad Sci U S A, 1993, 90, 4399-4403.
59. Schlax, P. J., Xavier, K. A., Gluick, T. C., and Draper, D. E. Translational repression of the Escherichia coli alpha operon mRNA: importance of an mRNA conformational switch and a ternary entrapment complex, J Biol Chem, 2001, 276, 38494-38501.
60. Takebe, Y., Miura, A., Bedwell, D. M., Tam, M., and Nomura, M. Increased expression of ribosomal genes during inhibition of ribosome assembly in Escherichia coli, J Mol Biol, 1985, 184, 23-30.
61. Torres, M., Condon, C., Balada, J. M., Squires, C., and Squires, C. L. Ribosomal protein S4 is a transcription factor with properties remarkably similar to NusA, a protein involved in both non-ribosomal and ribosomal RNA antitermination, Embo J, 2001, 20, 3811-3820.
62. Condon, C., Squires, C., and Squires, C. L. Control of rRNA transcription in Escherichia coli, Microbiol Rev, 1995, 59, 623-645.
63. Jin, D. J., Cagliero, C., and Zhou, Y. N. Growth rate regulation in Escherichia coli, FEMS Microbiol Rev, 2012, 36, 269-287.
64. Lasa, I., Toledo-Arana, A., Dobin, A., Villanueva, M., de los Mozos, I. R., Vergara-Irigaray, M., Segura, V., Fagegaltier, D., Penades, J. R., Valle, J., Solano, C., and Gingeras, T. R. Genome-wide antisense transcription drives mRNA processing in bacteria, Proc Natl Acad Sci U S A, 2011, 108, 20172-20177.
65. Kawano, M., Reynolds, A. A., Miranda-Rios, J., and Storz, G. Detection of 5'- and 3'-UTR-derived small RNAs and cis-encoded antisense RNAs in Escherichia coli, Nucleic Acids Research, 2005, 33 (3), 1040-1050.
66. Krinke, L., and Wulff, D. L. RNase III-dependent hydrolysis of lambda cII-O gene mRNA mediated by lambda OOP antisense RNA, Genes Dev, 1990, 4, 2223-2233.
67. Krinke, L., and Wulff, D. L. OOP RNA, produced from multicopy plasmids, inhibits lambda cII gene expression through an RNase III-dependent mechanism, Genes Dev, 1987, 1, 1005-1013.
68. Han, J., Pedersen, J. S., Kwon, S. C., Belair, C. D., Kim, Y. K., Yeom, K. H., Yang, W. Y., Haussler, D., Blelloch, R., and Kim, V. N. Posttranscriptional crossregulation between Drosha and DGCR8, Cell, 2009, 136, 75-84.
69. Ono, M., Scott, M. S., Yamada, K., Avolio, F., Barton, G. J., and Lamond, A. I. Identification of human miRNA precursors that resemble box C/D snoRNAs, Nucleic Acids Res, 2011, 39, 3879-3891.
70. Scott, M. S., Avolio, F., Ono, M., Lamond, A. I., and Barton, G. J. Human miRNA precursors with box H/ACA snoRNA features, PLoS Comput Biol, 2009, 5, e1000507.
71. Bachellerie, J. P., Cavaille, J., and Huttenhofer, A. The expanding snoRNA world, Biochimie, 2002, 84, 775-790.