Detection of small RNAs in Bordetella pertussis and identification of a novel repeated genetic element

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Hot, David ^a,b,c,d,e   Slupek, Stéphanie ^a,b,c,d,e   Wulbrecht, Bérénice ^a,b,c,d,e   D'Hondt, Anthony ^a,b,c,d,e   Hubans, Christine ^a,e   Antoine, Rudy ^a,b,c,d,e   Locht, Camille ^a,b,c,d,e   Lemoine, Yves ^a,b,c,d,e  

^a INSTITUT PASTEUR DE LILLE   (France)

^b INSERM   (France)

^c CNRS   (France)

^d UNIV LILLE   (France)

^e Molecular and Cellular Medicine   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; SMALL RNA; UNCLASSIFIED DRUG; SMALL UNTRANSLATED RNA; SPACER DNA;

ARTICLE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BETAPROTEOBACTERIA; BORDETELLA AVIUM; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; BVGA SYSTEM; BVGS SYSTEM; COMPUTER MODEL; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION; GENE SEQUENCE; GENOME SIZE; MOLECULAR PHYLOGENY; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PREDICTION; REGULATORY SEQUENCE; RIBOSWITCH; RNA ANALYSIS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TRANSPOSON; GENETIC TRANSCRIPTION; GENETICS; GENOMICS; METHODOLOGY; MOLECULAR GENETICS; NUCLEOTIDE REPEAT; PATHOGENICITY; PHENOTYPE; REPRODUCIBILITY;

BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; BORDETELLA; BORDETELLA AVIUM; BORDETELLA BRONCHISEPTICA; BORDETELLA PARAPERTUSSIS; BORDETELLA PERTUSSIS; PROKARYOTA;

BASE SEQUENCE; BLOTTING, NORTHERN; BORDETELLA PERTUSSIS; DNA, INTERGENIC; GENOME, BACTERIAL; GENOMICS; MOLECULAR SEQUENCE DATA; PHENOTYPE; REPETITIVE SEQUENCES, NUCLEIC ACID; REPRODUCIBILITY OF RESULTS; RNA, BACTERIAL; RNA, SMALL UNTRANSLATED; TRANSCRIPTION, GENETIC;

EID: 79955146850     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-207     Document Type: Article

References (78)

1. Dennis PP, Omer A. Small non-coding RNAs in Archaea. Curr Opin Microbiol 2005, 8(6):685-694.
2. Gottesman S. Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 2005, 21(7):399-404.
3. Livny J, Waldor MK. Identification of small RNAs in diverse bacterial species. Curr Opin Microbiol 2007, 10(2):96-101.
4. Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009, 136(4):615-628.
5. Gottesman S. The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 2004, 58:303-328.
6. Moller T, Franch T, Hojrup P, Keene DR, Bachinger HP, Brennan RG, Valentin-Hansen P. Hfq: a bacterial Sm-like protein that mediates RNA-RNA interaction. Mol Cell 2002, 9(1):23-30.
7. Storz G, Opdyke JA, Zhang A. Controlling mRNA stability and translation with small, noncoding RNAs. Curr Opin Microbiol 2004, 7(2):140-144.
8. Babitzke P, Romeo T. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 2007, 10(2):156-163.
9. Wassarman KM. 6S RNA: a small RNA regulator of transcription. Curr Opin Microbiol 2007, 10(2):164-168.
10. Toledo-Arana A, Repoila F, Cossart P. Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 2007, 10(2):182-188.
11. Boisset S, Geissmann T, Huntzinger E, Fechter P, Bendridi N, Possedko M, Chevalier C, Helfer AC, Benito Y, Jacquier A, et al. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 2007, 21(11):1353-1366.
12. Heroven AK, Bohme K, Rohde M, Dersch P. A Csr-type regulatory system, including small non-coding RNAs, regulates the global virulence regulator RovA of Yersinia pseudotuberculosis through RovM. Mol Microbiol 2008, 68(5):1179-1195.
13. Johansson J, Mandin P, Renzoni A, Chiaruttini C, Springer M, Cossart P. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 2002, 110(5):551-561.
14. Murphy ER, Payne SM. RyhB, an iron-responsive small RNA molecule, regulates Shigella dysenteriae virulence. Infect Immun 2007, 75(7):3470-3477.
15. Padalon-Brauch G, Hershberg R, Elgrably-Weiss M, Baruch K, Rosenshine I, Margalit H, Altuvia S. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 2008, 36(6):1913-1927.
16. Romby P, Vandenesch F, Wagner EG. The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 2006, 9(2):229-236.
17. Novick RP, Ross HF, Projan SJ, Kornblum J, Kreiswirth B, Moghazeh S. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. Embo J 1993, 12(10):3967-3975.
18. WHO Pertussis vaccines--WHO position paper. Wkly Epidemiol Rec 2005, 80(4):31-39. WHO.
19. Crowcroft NS, Pebody RG. Recent developments in pertussis. Lancet 2006, 367(9526):1926-1936.
20. de Melker HE, Schellekens JF, Neppelenbroek SE, Mooi FR, Rumke HC, Conyn-van Spaendonck MA. Reemergence of pertussis in the highly vaccinated population of the Netherlands: observations on surveillance data. Emerg Infect Dis 2000, 6(4):348-357.
21. Guris D, Strebel PM, Bardenheier B, Brennan M, Tachdjian R, Finch E, Wharton M, Livengood JR. Changing epidemiology of pertussis in the United States: increasing reported incidence among adolescents and adults, 1990-1996. Clin Infect Dis 1999, 28(6):1230-1237.
22. Mooi FR, van Loo IH, King AJ. Adaptation of Bordetella pertussis to vaccination: a cause for its reemergence?. Emerg Infect Dis 2001, 7(3 Suppl):526-528.
23. Cummings CA, Bootsma HJ, Relman DA, Miller JF. Speciesand strain-specific control of a complex, flexible regulon by Bordetella BvgAS. J Bacteriol 2006, 188(5):1775-1785.
24. Hot D, Antoine R, Renauld-Mongenie G, Caro V, Hennuy B, Levillain E, Huot L, Wittmann G, Poncet D, Jacob-Dubuisson F, et al. Differential modulation of Bordetella pertussis virulence genes as evidenced by DNA microarray analysis. Mol Genet Genomics 2003, 269(4):475-486.
25. Jones AM, Boucher PE, Williams CL, Stibitz S, Cotter PA. Role of BvgA phosphorylation and DNA binding affinity in control of Bvg-mediated phenotypic phase transition in Bordetella pertussis. Mol Microbiol 2005, 58(3):700-713.
26. Stibitz S. The bvg regulon. Bordetella Molecular Microbiology 2007, Norfolk (UK): Horizon Bioscience, Locht C.
27. Prugnola A, Arico B, Manetti R, Rappuoli R, Scarlato V. Response of the bvg regulon of Bordetella pertussis to different temperatures and short-term temperature shifts. Microbiology 1995, 141(Pt 10):2529-2534.
28. Scarlato V, Arico B, Prugnola A, Rappuoli R. Sequential activation and environmental regulation of virulence genes in Bordetella pertussis. Embo J 1991, 10(12):3971-3975.
29. Trotochaud AE, Wassarman KM. A highly conserved 6S RNA structure is required for regulation of transcription. Nat Struct Mol Biol 2005, 12(4):313-319.
30. Felden B, Massire C, Westhof E, Atkins JF, Gesteland RF. Phylogenetic analysis of tmRNA genes within a bacterial subgroup reveals a specific structural signature. Nucleic Acids Res 2001, 29(7):1602-1607.
31. Scarlato V, Prugnola A, Arico B, Rappuoli R. Positive transcriptional feedback at the bvg locus controls expression of virulence factors in Bordetella pertussis. Proc Natl Acad Sci USA 1990, 87(17):6753-6757.
32. Scarlato V, Rappuoli R. Differential response of the bvg virulence regulon of Bordetella pertussis to MgSO4 modulation. J Bacteriol 1991, 173(22):7401-7404.
33. Washietl S, Hofacker IL, Stadler PF. Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci USA 2005, 102(7):2454-2459.
34. Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall K, et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 2003, 35(1):32-40.
35. Sebaihia M, Preston A, Maskell DJ, Kuzmiak H, Connell TD, King ND, Orndorff PE, Miyamoto DM, Thomson NR, Harris D, et al. Comparison of the genome sequence of the poultry pathogen Bordetella avium with those of B. bronchiseptica, B. pertussis, and B. parapertussis reveals extensive diversity in surface structures associated with host interaction. J Bacteriol 2006, 188(16):6002-6015.
36. Menozzi FD, Mutombo R, Renauld G, Gantiez C, Hannah JH, Leininger E, Brennan MJ, Locht C. Heparin-inhibitable lectin activity of the filamentous hemagglutinin adhesin of Bordetella pertussis. Infect Immun 1994, 62(3):769-778.
37. Antoine R, Alonso S, Raze D, Coutte L, Lesjean S, Willery E, Locht C, Jacob-Dubuisson F. New virulence-activated and virulence-repressed genes identified by systematic gene inactivation and generation of transcriptional fusions in Bordetella pertussis. J Bacteriol 2000, 182(20):5902-5905.
38. NCBI ftp - Genomes Bacteria. , ftp://ftp.ncbi.nih.gov/genomes/Bacteria/
39. Wellcome Trust Sanger Institute - Bacterial genomes. , http://www.sanger.ac.uk/Projects/Micr.bes/
40. RNAz - predicting structural noncoding RNAs. , http://www.tbi.univie.ac.at/~wash/RNAz/
41. FastPCR. , http://www.biocenter.helsinki.fi/bi/Programs/fastpcr.htm
42. Noe L, Kucherov G. YASS: enhancing the sensitivity of DNA similarity search. Nucleic Acids Res 2005, (33 Web Server):W540-543.
43. YASS: DNA pairwise alignment tool.
44. Wellcome Trust Sanger Institute - Rfam. , http://rfam.sanger.ac.uk/
45. Mandal M, Lee M, Barrick JE, Weinberg Z, Emilsson GM, Ruzzo WL, Breaker RR. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 2004, 306(5694):275-279.
46. Winkler WC, Cohen-Chalamish S, Breaker RR. An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci USA 2002, 99(25):15908-15913.
47. Livny J, Brencic A, Lory S, Waldor MK. Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res 2006, 34(12):3484-3493.
48. Vogel J, Argaman L, Wagner EG, Altuvia S. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 2004, 14(24):2271-2276.
49. Grundy FJ, Henkin TM. From ribosome to riboswitch: control of gene expression in bacteria by RNA structural rearrangements. Crit Rev Biochem Mol Biol 2006, 41(6):329-338.
50. Nudler E, Mironov AS. The riboswitch control of bacterial metabolism. Trends Biochem Sci 2004, 29(1):11-17.
51. Kaczanowska M, Ryden-Aulin M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 2007, 71(3):477-494.
52. Meyer MM, Ames TD, Smith DP, Weinberg Z, Schwalbach MS, Giovannoni SJ, Breaker RR. Identification of candidate structured RNAs in the marine organism 'Candidatus Pelagibacter ubique'. BMC Genomics 2009, 10:268.
53. Lindahl L, Archer R, Zengel JM. Transcription of the S10 ribosomal protein operon is regulated by an attenuator in the leader. Cell 1983, 33(1):241-248.
54. Zengel JM, Mueckl D, Lindahl L. Protein L4 of the E. coli ribosome regulates an eleven gene r protein operon. Cell 1980, 21(2):523-535.
55. NCBI - ORF Finder (Open Reading Frame Finder). , http://www.ncbi.nlm.nih.gov/gorf/gorf.html
56. Nielsen P, Krogh A. Large-scale prokaryotic gene prediction and comparison to genome annotation. Bioinformatics 2005, 21(24):4322-4329.
57. Hershberg R, Altuvia S, Margalit H. A survey of small RNA-encoding genes in Escherichia coli. Nucleic Acids Res 2003, 31(7):1813-1820.
58. Tjaden B. TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 2008, (36 Web Server):W109-113.
59. Diwa A, Bricker AL, Jain C, Belasco JG. An evolutionarily conserved RNA stem-loop functions as a sensor that directs feedback regulation of RNase E gene expression. Genes Dev 2000, 14(10):1249-1260.
60. Melton AR, Weiss AA. Environmental regulation of expression of virulence determinants in Bordetella pertussis. J Bacteriol 1989, 171(11):6206-6212.
61. Miller JF, Johnson SA, Black WJ, Beattie DT, Mekalanos JJ, Falkow S. Constitutive sensory transduction mutations in the Bordetella pertussis bvgS gene. J Bacteriol 1992, 174(3):970-979.
62. Knapp S, Mekalanos JJ. Two trans-acting regulatory genes (vir and mod) control antigenic modulation in Bordetella pertussis. J Bacteriol 1988, 170(11):5059-5066.
63. Hulton CS, Higgins CF, Sharp PM. ERIC sequences: a novel family of repetitive elements in the genomes of Escherichia coli, Salmonella typhimurium and other enterobacteria. Mol Microbiol 1991, 5(4):825-834.
64. Sharples GJ, Lloyd RG. A novel repeated DNA sequence located in the intergenic regions of bacterial chromosomes. Nucleic Acids Res 1990, 18(22):6503-6508.
65. Stern MJ, Ames GF, Smith NH, Robinson EC, Higgins CF. Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell 1984, 37(3):1015-1026.
66. Buisine N, Tang CM, Chalmers R. Transposon-like Correia elements: structure, distribution and genetic exchange between pathogenic Neisseria sp. FEBS Lett 2002, 522(1-3):52-58.
67. Correia FF, Inouye S, Inouye M. A family of small repeated elements with some transposon-like properties in the genome of Neisseria gonorrhoeae. J Biol Chem 1988, 263(25):12194-12198.
68. Mazzone M, De Gregorio E, Lavitola A, Pagliarulo C, Alifano P, Di Nocera PP. Whole-genome organization and functional properties of miniature DNA insertion sequences conserved in pathogenic Neisseriae. Gene 2001, 278(1-2):211-222.
69. Knutsen E, Johnsborg O, Quentin Y, Claverys JP, Havarstein LS. BOX elements modulate gene expression in Streptococcus pneumoniae: impact on the fine-tuning of competence development. J Bacteriol 2006, 188(23):8307-8312.
70. Martin B, Humbert O, Camara M, Guenzi E, Walker J, Mitchell T, Andrew P, Prudhomme M, Alloing G, Hakenbeck R, et al. A highly conserved repeated DNA element located in the chromosome of Streptococcus pneumoniae. Nucleic Acids Res 1992, 20(13):3479-3483.
71. Oggioni MR, Claverys JP. Repeated extragenic sequences in prokaryotic genomes: a proposal for the origin and dynamics of the RUP element in Streptococcus pneumoniae. Microbiology 1999, 145(Pt 10):2647-2653.
72. Supply P, Magdalena J, Himpens S, Locht C. Identification of novel intergenic repetitive units in a mycobacterial two-component system operon. Mol Microbiol 1997, 26(5):991-1003.
73. Klevan A, Tourasse NJ, Stabell FB, Kolsto AB, Okstad OA. Exploring the evolution of the Bacillus cereus group repeat element bcr1 by comparative genome analysis of closely related strains. Microbiology 2007, 153(Pt 11):3894-3908.
74. Okstad OA, Tourasse NJ, Stabell FB, Sundfaer CK, Egge-Jacobsen W, Risoen PA, Read TD, Kolsto AB. The bcr1 DNA repeat element is specific to the Bacillus cereus group and exhibits mobile element characteristics. J Bacteriol 2004, 186(22):7714-7725.
75. Denoeud F, Vergnaud G. Identification of polymorphic tandem repeats by direct comparison of genome sequence from different bacterial strains: a web-based resource. BMC Bioinformatics 2004, 5:4.
76. Cummings CA, Brinig MM, Lepp PW, van de Pas S, Relman DA. Bordetella species are distinguished by patterns of substantial gene loss and host adaptation. J Bacteriol 2004, 186(5):1484-1492.
77. Diavatopoulos DA, Cummings CA, Schouls LM, Brinig MM, Relman DA, Mooi FR. Bordetella pertussis, the causative agent of whooping cough, evolved from a distinct, human-associated lineage of B. bronchiseptica. PLoS Pathog 2005, 1(4):e45.
78. Preston A. Bordetella pertussis: the intersection of genomics and pathobiology. Cmaj 2005, 173(1):55-62.