A multicopy sRNA of Listeria monocytogenes regulates expression of the virulence adhesin LapB

Nucleic Acids Research

Volumn 42, Issue 14, 2014, Pages 9383-9398

  Sievers, Susanne ^a,b   Lillebaek, Eva Maria Sternkopf ^a   Jacobsen, Kirstine ^a   Lund, Anja ^a   Mollerup, Maria Storm ^a   Nielsen, Pia Kiil ^a,c   Kallipolitis, Birgitte Haahr ^a  

^a UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c ORBICON   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; CHAPERONE; LAPB PROTEIN; MESSENGER RNA; RNA CHAPERONE; TRANSFER RNA; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BACTERIAL CELL WALL; BACTERIAL MEMBRANE; BACTERIAL VIRULENCE; BINDING AFFINITY; BINDING SITE; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; GENE DOSAGE; GENE EXPRESSION REGULATION; GENE INTERACTION; GENE REARRANGEMENT; GENE TARGETING; GENE TECHNOLOGY; GENETIC STABILITY; HFQ GENE; LAPB GENE; LHRC1 GENE; LHRC2 GENE; LHRC3 GENE; LHRC4 GENE; LHRC5 GENE; LISTERIA MONOCYTOGENES; NONHUMAN; PRIORITY JOURNAL; RNA BINDING; RNA SEQUENCE; TWO COMPONENT SYSTEM LISRK;

ADHESINS, BACTERIAL; GENE DOSAGE; GENE EXPRESSION REGULATION, BACTERIAL; LISTERIA MONOCYTOGENES; RNA, BACTERIAL; RNA, MESSENGER; RNA, SMALL UNTRANSLATED; STRESS, PHYSIOLOGICAL; VIRULENCE;

EID: 84906267816     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku630     Document Type: Article

References (79)

1. Waters, L.S. and Storz, G. (2009) Regulatory RNAs in bacteria. Cell, 136, 615-628.
2. Storz, G., Vogel, J. and Wassarman, K.M. (2011) Regulation by small RNAs in bacteria: expanding frontiers. Mol. Cell, 43, 880-891.
3. Chao, Y. and Vogel, J. (2010) The role of Hfq in bacterial pathogens. Curr. Opin. Microbiol., 13, 24-33.
4. Papenfort, K. and Vogel, J. (2010) Regulatory RNA in bacterial pathogens. Cell Host. Microbe, 8, 116-127.
5. Felden, B., Vandenesch, F., Bouloc, P. and Romby, P. (2011) The Staphylococcus aureus RNome and its commitment to virulence. PLoS. Pathog., 7, e1002006.
6. Toledo-Arana, A., Dussurget, O., Nikitas, G., Sesto, N., Guet-Revillet, H., Balestrino, D., Loh, E., Gripenland, J., Tiensuu, T., Vaitkevicius, K. et al. (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature, 459, 950-956.
7. Sharma, C.M., Hoffmann, S., Darfeuille, F., Reignier, J., Findeiss, S., Sittka, A., Chabas, S., Reiche, K., Hackermuller, J., Reinhardt, R. et al. (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature, 464, 250-255.
8. Acebo, P., Martin-Galiano, A.J., Navarro, S., Zaballos, A. and Amblar, M. (2012) Identification of 88 regulatory small RNAs in the TIGR4 strain of the human pathogen Streptococcus pneumoniae. RNA., 18, 530-546.
9. Christiansen, J.K., Nielsen, J.S., Ebersbach, T., Valentin-Hansen, P., Sogaard-Andersen, L. and Kallipolitis, B.H. (2006) Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA., 12, 1383-1396.
10. Mandin, P., Repoila, F., Vergassola, M., Geissmann, T. and Cossart, P. (2007) Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res., 35, 962-974.
11. Mraheil, M.A., Billion, A., Mohamed, W., Mukherjee, K., Kuenne, C., Pischimarov, J., Krawitz, C., Retey, J., Hartsch, T., Chakraborty, T. et al. (2011) The intracellular sRNA transcriptome of Listeria monocytogenes during growth in macrophages. Nucleic Acids Res., 39, 4235-4248.
12. Mellin, J.R. and Cossart, P. (2012) The non-coding RNA world of the bacterial pathogen Listeria monocytogenes. RNA. Biol., 9, 372-378.
13. Ramaswamy, V., Cresence, V.M., Rejitha, J.S., Lekshmi, M.U., Dharsana, K.S., Prasad, S.P. and Vijila, H.M. (2007) Listeria-review of epidemiology and pathogenesis. J. Microbiol. Immunol. Infect., 40, 4-13.
14. Valentin-Hansen, P., Eriksen, M. and Udesen, C. (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol. Microbiol., 51, 1525-1533.
15. Silvaggi, J.M., Perkins, J.B. and Losick, R. (2006) Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. J. Bacteriol., 188, 532-541.
16. Gaballa, A., Antelmann, H., Aguilar, C., Khakh, S.K., Song, K.B., Smaldone, G.T. and Helmann, J.D. (2008) The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc. Natl. Acad. Sci. U.S.A, 105, 11927-11932.
17. Heidrich, N., Moll, I. and Brantl, S. (2007) In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. Nucleic Acids Res., 35, 4331-4346.
18. Jahn, N., Preis, H., Wiedemann, C. and Brantl, S. (2012) BsrG/SR4 from Bacillus subtilis-the first temperature-dependent type I toxin-antitoxin system. Mol. Microbiol., 83, 579-598.
19. Dambach, M., Irnov, I. and Winkler, W.C. (2013) Association of RNAs with Bacillus subtilis Hfq. PLoS. One., 8, e55156.
20. Smaldone, G.T., Antelmann, H., Gaballa, A. and Helmann, J.D. (2012) The FsrA sRNA and FbpB protein mediate the iron-dependent induction of the Bacillus subtilis lutABC iron-sulfur-containing oxidases. J. Bacteriol., 194, 2586-2593.
21. Romby, P. and Charpentier, E. (2010) An overview of RNAs with regulatory functions in gram-positive bacteria. Cell Mol. Life Sci., 67, 217-237.
22. Bohn, C., Rigoulay, C. and Bouloc, P. (2007) No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC. Microbiol., 7, 10.
23. Liu, Y., Wu, N., Dong, J., Gao, Y., Zhang, X., Mu, C., Shao, N. and Yang, G. (2010) Hfq is a global regulator that controls the pathogenicity of Staphylococcus aureus. PLoS. One., 5, e13069.
24. Christiansen, J.K., Larsen, M.H., Ingmer, H., Sogaard-Andersen, L. and Kallipolitis, B.H. (2004) The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J. Bacteriol., 186, 3355-3362.
25. Nielsen, J.S., Lei, L.K., Ebersbach, T., Olsen, A.S., Klitgaard, J.K., Valentin-Hansen, P. and Kallipolitis, B.H. (2010) Defining a role for Hfq in Gram-positive bacteria: evidence for Hfq-dependent antisense regulation in Listeria monocytogenes. Nucleic Acids Res., 38, 907-919.
26. Nielsen, J.S., Larsen, M.H., Lillebaek, E.M., Bergholz, T.M., Christiansen, M.H., Boor, K.J., Wiedmann, M. and Kallipolitis, B.H. (2011) A small RNA controls expression of the chitinase ChiA in Listeria monocytogenes. PLoS. One., 6, e19019.
27. Vazquez-Boland, J.A., Kocks, C., Dramsi, S., Ohayon, H., Geoffroy, C., Mengaud, J. and Cossart, P. (1992) Nucleotide sequence of the lecithinase operon of Listeria monocytogenes and possible role of lecithinase in cell-to-cell spread. Infect. Immun., 60, 219-230.
28. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res., 29, e45.
29. Pfaffl, M.W., Horgan, G.W. and Dempfle, L. (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res., 30, e36.
30. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
31. Eggenhofer, F., Tafer, H., Stadler, P.F. and Hofacker, I.L. (2011) RNApredator: fast accessibility-based prediction of sRNA targets. Nucleic Acids Res., 39, W149-W154.
32. Poyart, C. and Trieu-Cuot, P. (1997) A broad-host-range mobilizable shuttle vector for the construction of transcriptional fusions to beta-galactosidase in gram-positive bacteria. FEMS Microbiol. Lett., 156, 193-198.
33. Boysen, A., Moller-Jensen, J., Kallipolitis, B., Valentin-Hansen, P. and Overgaard, M. (2010) Translational regulation of gene expression by an anaerobically induced small non-coding RNA in Escherichia coli. J. Biol. Chem., 285, 10690-10702.
34. 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.
35. Gotfredsen, M. and Gerdes, K. (1998) The Escherichia coli relBE genes belong to a new toxin-antitoxin gene family. Mol. Microbiol., 29, 1065-1076.
36. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
37. Reis, O., Sousa, S., Camejo, A., Villiers, V., Gouin, E., Cossart, P. and Cabanes, D. (2010) LapB, a novel Listeria monocytogenes LPXTG surface adhesin, required for entry into eukaryotic cells and virulence. J. Infect. Dis., 202, 551-562.
38. Cotter, P.D., Emerson, N., Gahan, C.G. and Hill, C. (1999) Identification and disruption of lisRK, a genetic locus encoding a two-component signal transduction system involved in stress tolerance and virulence in Listeria monocytogenes. J. Bacteriol., 181, 6840-6843.
39. Kallipolitis, B.H. and Ingmer, H. (2001) Listeria monocytogenes response regulators important for stress tolerance and pathogenesis. FEMS Microbiol. Lett., 204, 111-115.
40. Cotter, P.D., Guinane, C.M. and Hill, C. (2002) The LisRK signal transduction system determines the sensitivity of Listeria monocytogenes to nisin and cephalosporins. Antimicrob. Agents Chemother., 46, 2784-2790.
41. Kallipolitis, B.H., Ingmer, H., Gahan, C.G., Hill, C. and Sogaard-Andersen, L. (2003) CesRK, a two-component signal transduction system in Listeria monocytogenes, responds to the presence of cell wall-acting antibiotics and affects beta-lactam resistance. Antimicrob. Agents Chemother., 47, 3421-3429.
42. Nielsen, P.K., Andersen, A.Z., Mols, M., van,d.V., Abee, T. and Kallipolitis, B.H. (2012) Genome-wide transcriptional profiling of the cell envelope stress response and the role of LisRK and CesRK in Listeria monocytogenes. Microbiology, 158, 963-974.
43. Gopel, Y. and Gorke, B. (2012) Rewiring two-component signal transduction with small RNAs. Curr. Opin. Microbiol., 15, 132-139.
44. Shimizu, T., Yaguchi, H., Ohtani, K., Banu, S. and Hayashi, H. (2002) Clostridial VirR/VirS regulon involves a regulatory RNA molecule for expression of toxins. Mol. Microbiol., 43, 257-265.
45. Koenig, R.L., Ray, J.L., Maleki, S.J., Smeltzer, M.S. and Hurlburt, B.K. (2004) Staphylococcus aureus AgrA binding to the RNAIII-agr regulatory region. J. Bacteriol., 186, 7549-7555.
46. Halfmann, A., Kovacs, M., Hakenbeck, R. and Bruckner, R. (2007) Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol. Microbiol., 66, 110-126.
47. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics., 23, 2947-2948.
48. Simons, R.W. and Kleckner, N. (1988) Biological regulation by antisense RNA in prokaryotes. Annu. Rev. Genet., 22, 567-600.
49. Eguchi, Y., Itoh, T. and Tomizawa, J. (1991) Antisense RNA. Annu. Rev. Biochem., 60, 631-652.
50. Brunel, C., Marquet, R., Romby, P. and Ehresmann, C. (2002) RNA loop-loop interactions as dynamic functional motifs. Biochimie, 84, 925-944.
51. Geissmann, T., Chevalier, C., Cros, M.J., Boisset, S., Fechter, P., Noirot, C., Schrenzel, J., Francois, P., Vandenesch, F., Gaspin, C. et al. (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res., 37, 7239-7257.
52. Guillier, M., Gottesman, S. and Storz, G. (2006) Modulating the outer membrane with small RNAs. Genes Dev., 20, 2338-2348.
53. Jordan, S., Hutchings, M.I. and Mascher, T. (2008) Cell envelope stress response in Gram-positive bacteria. FEMS Microbiol. Rev., 32, 107-146.
54. Vogel, J. and Papenfort, K. (2006) Small non-coding RNAs and the bacterial outer membrane. Curr. Opin. Microbiol., 9, 605-611.
55. Valentin-Hansen, P., Johansen, J. and Rasmussen, A.A. (2007) Small RNAs controlling outer membrane porins. Curr. Opin. Microbiol., 10, 152-155.
56. Sleator, R.D. and Hill, C. (2005) A novel role for the LisRK two-component regulatory system in listerial osmotolerance. Clin. Microbiol. Infect., 11, 599-601.
57. Brencic, A., McFarland, K.A., McManus, H.R., Castang, S., Mogno, I., Dove, S.L. and Lory, S. (2009) The GacS/GacA signal transduction system of Pseudomonas aeruginosa acts exclusively through its control over the transcription of the RsmY and RsmZ regulatory small RNAs. Mol. Microbiol., 73, 434-445.
58. Raengpradub, S., Wiedmann, M. and Boor, K.J. (2008) Comparative analysis of the sigma B-dependent stress responses in Listeria monocytogenes and Listeria innocua strains exposed to selected stress conditions. Appl. Environ. Microbiol., 74, 158-171.
59. Milohanic, E., Glaser, P., Coppee, J.Y., Frangeul, L., Vega, Y., Vazquez-Boland, J.A., Kunst, F., Cossart, P. and Buchrieser, C. (2003) Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol. Microbiol., 47, 1613-1625.
60. Quillin, S.J., Schwartz, K.T. and Leber, J.H. (2011) The novel Listeria monocytogenes bile sensor BrtA controls expression of the cholic acid efflux pump MdrT. Mol. Microbiol., 81, 129-142.
61. Toledo-Arana, A., Repoila, F. and Cossart, P. (2007) Small noncoding RNAs controlling pathogenesis. Curr. Opin. Microbiol., 10, 182-188.
62. Loh, E., Dussurget, O., Gripenland, J., Vaitkevicius, K., Tiensuu, T., Mandin, P., Repoila, F., Buchrieser, C., Cossart, P. and Johansson, J. (2009) A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell, 139, 770-779.
63. Chaudhuri, S., Gantner, B.N., Ye, R.D., Cianciotto, N.P. and Freitag, N.E. (2013) The Listeria monocytogenes ChiA chitinase enhances virulence through suppression of host innate immunity. MBio., 4, e00617-12.
64. 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.
65. 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.
66. Shao, Y., Feng, L., Rutherford, S.T., Papenfort, K. and Bassler, B.L. (2013) Functional determinants of the quorum-sensing non-coding RNAs and their roles in target regulation. EMBO J., 32, 2158-2171.
67. Reichenbach, B., Maes, A., Kalamorz, F., Hajnsdorf, E. and Gorke, B. (2008) The small RNA GlmY acts upstream of the sRNA GlmZ in the activation of glmS expression and is subject to regulation by polyadenylation in Escherichia coli. Nucleic Acids Res., 36, 2570-2580.
68. Urban, J.H. and Vogel, J. (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS. Biol., 6, e64.
69. Schnorpfeil, A., Kranz, M., Kovacs, M., Kirsch, C., Gartmann, J., Brunner, I., Bittmann, S. and Bruckner, R. (2013) Target evaluation of the non-coding csRNAs reveals a link of the two-component regulatory system CiaRH to competence control in Streptococcus pneumoniae R6. Mol. Microbiol., 89, 334-349.
70. Bordi, C., Lamy, M.C., Ventre, I., Termine, E., Hachani, A., Fillet, S., Roche, B., Bleves, S., Mejean, V., Lazdunski, A. et al. (2010) Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. Mol. Microbiol., 76, 1427-1443.
71. Romeo, T., Vakulskas, C.A. and Babitzke, P. (2013) Post-transcriptional regulation on a global scale: form and function of Csr/Rsm systems. Environ. Microbiol., 15, 313-324.
72. Liu, M.Y., Gui, G., Wei, B., Preston, J.F. III, Oakford, L., Yuksel, U., Giedroc, D.P. and Romeo, T. (1997) The RNA molecule CsrB binds to the global regulatory protein CsrA and antagonizes its activity in Escherichia coli. J. Biol. Chem., 272, 17502-17510.
73. Moll, S., Schneider, D.J., Stodghill, P., Myers, C.R., Cartinhour, S.W. and Filiatrault, M.J. (2010) Construction of an rsmX co-variance model and identification of five rsmX non-coding RNAs in Pseudomonas syringae pv. tomato DC3000. RNA. Biol., 7, 508-516.
74. Jorgensen, M.G., Thomason, M.K., Havelund, J., Valentin-Hansen, P. and Storz, G. (2013) Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev., 27, 1132-1145.
75. Geissmann, T., Marzi, S. and Romby, P. (2009) The role of mRNA structure in translational control in bacteria. RNA. Biol., 6, 153-160.
76. Boisset, S., Geissmann, T., Huntzinger, E., Fechter, P., Bendridi, N., Possedko, M., Chevalier, C., Helfer, A.C., Benito, Y., Jacquier, A. et al. (2007) Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev., 21, 1353-1366.
77. Chabelskaya, S., Gaillot, O. and Felden, B. (2010) A Staphylococcus aureus small RNA is required for bacterial virulence and regulates the expression of an immune-evasion molecule. PLoS. Pathog., 6, e1000927.
78. Koraimann, G., Teferle, K., Markolin, G., Woger, W. and Hogenauer, G. (1996) The FinOP repressor system of plasmid R1: analysis of the antisense RNA control of traJ expression and conjugative DNA transfer. Mol. Microbiol., 21, 811-821.
79. Wagner, E.G. and Simons, R.W. (1994) Antisense RNA control in bacteria, phages, and plasmids. Annu. Rev. Microbiol., 48, 713-742.