Hfq and Hfq-dependent small RNAs are major contributors to multicellular development in Salmonella enterica serovar typhimurium

RNA Biology

Volumn 9, Issue 4, 2012, Pages 489-502

  Monteiro, Claudia ^a,c   Papenfort, Kai ^b   Hentrich, Karina ^a   Ahmad, Irfan ^a   Le Guyon, Soazig ^a   Reimann, Romy ^a   Grantcharova, Nina ^a   Römling, Ute ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c INEB INSTITUTO DE ENGENHARIA BIOMÉDICA   (Portugal)

Author keywords

ArcZ; CsgD; Curli fimbriae; Flagella; RyeB; SdsR; Type 1 fimbriae

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; MESSENGER RNA; PROTEIN HFQ; SIGMA FACTOR RPOS; SMALL UNTRANSLATED RNA; UNCLASSIFIED DRUG;

ARTICLE; BIOFILM; CELL MATURATION; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; FIMBRIA; GENETIC TRANSCRIPTION; MORPHOTYPE; MUTANT; NONHUMAN; PROTEIN EXPRESSION; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 84858865125     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.19682     Document Type: Article

References (67)

1. Römling U. Characterization of the rdar morphotype, a multicellular behaviour in Enterobacteriaceae. Cell Mol Life Sci 2005; 62:1234-46; PMID:15818467; http:// dx.doi.org/10.1007/s00018-005-4557-x.
2. Römling U, Sierralta WD, Eriksson K, Normark S. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 1998; 28:249-64; PMID:9622351; http://dx.doi.org/10.1046/j.1365- 2958.1998.00791.x.
3. Zakikhany K, Harrington CR, Nimtz M, Hinton JCD, Römling U. Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar typhimurium. Mol Microbiol 2010; 77:771-86; PMID:20545866; http://dx.doi.org/10. 1111/j.1365-2958.2010.07247.x.
4. Simm R, Morr M, Kader A, Nimtz M, Römling U. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 2004; 53:1123-34; PMID:15306016; http://dx.doi.org/10. 1111/j.1365-2958.2004.04206.x.
5. Kader A, Simm R, Gerstel U, Morr M, Römling U. Hierarchical involvement of various GGDEF domain proteins in rdar morphotype development of Salmonella enterica serovar typhimurium. Mol Microbiol 2006; 60:602-16; PMID:16629664; http:// dx.doi.org/10.1111/j.1365-2958.2006.05123.x.
6. Gerstel U, Römling U. The csgD promoter, a control unit for biofilm formation in Salmonella typhimurium. Res Microbiol 2003; 154:659-67; PMID:14643403; http://dx.doi.org/10.1016/j.resmic.2003.08.005.
7. Ishihama A. Prokaryotic genome regulation: multifactor promoters, multitarget regulators and hierarchic networks. FEMS Microbiol Rev 2010; 34:628-45; PMID:20491932.
8. Robbe-Saule V, Jaumouillé V, Prévost MC, Guadagnini S, Talhouarne C, Mathout H, et al. Crl activates transcription initiation of RpoS-regulated genes involved in the multicellular behavior of Salmonella enterica serovar typhimurium. J Bacteriol 2006; 188:3983-94; PMID:16707690; http://dx.doi.org/10.1128/JB.00033-06.
9. Mika F, Hengge R. A two-component phosphotransfer network involving ArcB, ArcA and RssB coordinates synthesis and proteolysis of sigma S (RpoS) in E. coli. Genes Dev 2005; 19:2770-81; PMID:16291649; http://dx.doi.org/10.1101/gad. 353705.
10. Lange R, Hengge-Aronis R. The cellular concentration of the sigma S subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation and protein stability. Genes Dev 1994; 8:1600-12; PMID:7525405; http://dx.doi. org/10.1101/gad.8.13.1600.
11. Hommais F, Krin E, Coppée JY, Lacroix C, Yeramian E, Danchin A, et al. GadE (YhiE): a novel activator involved in the response to acid environment in Escherichia coli. Microbiology 2004; 150:61-72; PMID:14702398; http://dx.doi.org/10.1099/mic.0.26659-0.
12. Hoerter JD, Arnold AA, Ward CS, Sauer M, Johnson S, Fleming T, et al. Reduced hydroperoxidase (HPI and HPII) activity in the Deltafur mutant contributes to increased sensitivity to UVA radiation in Escherichia coli. J Photochem Photobiol B 2005; 79:151-7; PMID:15878120; http://dx.doi.org/10.1016/ j.jphotobiol.2005.01.003.
13. Hengge R. Proteolysis of sigma S (RpoS) and the general stress response in Escherichia coli. Res Microbiol 2009; 160:667-76; PMID:19765651; http://dx.doi. org/10.1016/j.resmic.2009.08.014.
14. Battesti A, Majdalani N, Gottesman S. The RpoS-mediated general stress response in Escherichia coli. Annu Rev Microbiol 2011; 65:189-213; PMID:21639793; http://dx.doi.org/10.1146/annurevmicro-090110-102946.
15. Altuvia S, Weinstein-Fischer D, Zhang A, Postow L, Storz G. A small, stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 1997; 90:43-53; PMID:9230301; http://dx.doi. org/10.1016/S0092-8674(00)80312-8.
16. Majdalani N, Chen S, Murrow J, St. John K, Gottesman S. Regulation of RpoS by a novel small RNA: the characterization of RprA. Mol Microbiol 2001; 39:1382-94; PMID:11251852; http://dx.doi. org/10.1111/j.1365-2958.2001.02329.x.
17. Papenfort K, Said N, Welsink T, Lucchini S, Hinton JC, Vogel J. Specific and pleiotropic patterns of mRNA regulation by ArcZ, a conserved, Hfq-dependent small RNA. Mol Microbiol 2009; 74:139-58; PMID:19732340; http://dx.doi.org/10. 1111/j.1365-2958.2009.06857.x.
18. Sledjeski DD, Gupta A, 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; PMID:8670904.
19. Soper T, Mandin P, Majdalani N, Gottesman S, Woodson SA. Positive regulation by small RNAs and the role of Hfq. Proc Natl Acad Sci USA 2010; 107:9602-7; PMID:20457943; http://dx.doi.org/10.1073/pnas.1004435107.
20. Mandin P, Gottesman S. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 2010; 29:3094-107; PMID:20683441; http://dx.doi.org/10.1038/emboj.2010.179.
21. McCullen CA, Benhammou JN, Majdalani N, Gottesman S. Mechanism of positive regulation by DsrA and RprA small noncoding RNAs: pairing increases translation and protects rpoS mRNA from degradation. J Bacteriol 2010; 192:5559-71; PMID:20802038; http://dx.doi.org/10.1128/JB.00464-10.
22. Brown L, Elliott T. Efficient translation of the RpoS sigma factor in Salmonella typhimurium requires host factor I, an RNA-binding protein encoded by the hfq gene. J Bacteriol 1996; 178:3763-70; PMID:8682778.
23. Sittka A, Lucchini S, Papenfort K, Sharma CM, Rolle K, Binnewies TT, et al. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 2008; 4:1000163; PMID:18725932; http://dx.doi. org/10.1371/journal.pgen.1000163.
24. Jones AM, Goodwill A, Elliott T. Limited role for the DsrA and RprA regulatory RNAs in rpoS regulation in Salmonella enterica. J Bacteriol 2006; 188:5077-88; PMID:16816180; http://dx.doi.org/10.1128/JB.00206-06.
25. Weber H, Pesavento C, Possling A, Tischendorf G, Hengge R. Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 2006; 62:1014-34; PMID:17010156; http://dx.doi. org/10.1111/j.1365-2958.2006.05440.x.
26. Holmqvist E, Reimegård J, Sterk M, Grantcharova N, Römling U, Wagner EGH. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J 2010; 29:1840-50; PMID:20407422; http://dx.doi.org/10.1038/emboj.2010.73.
27. Valentin-Hansen P, Eriksen M, Udesen C. The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 2004; 51:1525-33; PMID:15009882; http://dx.doi.org/10.1111/j.1365-2958.2003.03935.x.
28. Römling U. Genetic and phenotypic analysis of multicellular behavior in Salmonella typhimurium. Methods Enzymol 2001; 336:48-59; PMID:11398418; http:// dx.doi.org/10.1016/S0076-6879(01)36577-1.
29. Römling U, Bian Z, Hammar M, Sierralta WD, Normark S. Curli fibers are highly conserved between Salmonella typhimurium and Escherichia coli with respect to operon structure and regulation. J Bacteriol 1998; 180:722-31; PMID:9457880.
30. Urban JH, Vogel J. Translational control and target recognition by Escherichia coli small RNAs in vivo. Nucleic Acids Res 2007; 35:1018-37; PMID:17264113; http:// dx.doi.org/10.1093/nar/gkl1040.
31. Römling U, Pesen D, Yaron S. Biofilms of Salmonella enterica. In: Rhen M, Maskell D, Mastroeni P, Threlfall J, Ed. Salmonella Molecular Biology and Pathogenesis. Norfolk: Horizon Press 2007; 127-45.
32. Boddicker JD, Ledeboer NA, Jagnow J, Jones BD, Clegg S. Differential binding to and biofilm formation on, HEp-2 cells by Salmonella enterica serovar typhimurium is dependent upon allelic variation in the fimH gene of the fim gene cluster. Mol Microbiol 2002; 45:1255-65; PMID:12207694; http://dx.doi. org/10.1046/j.1365-2958.2002.03121.x.
33. Crawford RW, Reeve KE, Gunn JS. Flagellated but not hyperfimbriated Salmonella enterica serovar typhimurium attaches to and forms biofilms on cholesterol- coated surfaces. J Bacteriol 2010; 192:2981- 90; PMID:20118264; http://dx.doi.org/10.1128/ JB.01620-09.
34. Fang FC, Libby SJ, Buchmeier NA, Loewen PC, Switala J, Harwood J, et al. The alternative sigma factor katF (rpoS) regulates Salmonella virulence. Proc Natl Acad Sci USA 1992; 89:11978-82; PMID:1465428; http://dx.doi.org/10.1073/ pnas.89.24.11978.
35. Gualdi L, Tagliabue L, Landini P. Biofilm formationgene expression relay system in Escherichia coli: modulation of sigma S-dependent gene expression by the CsgD regulatory protein via sigma S protein stabilization. J Bacteriol 2007; 189:8034-43; PMID:17873038; http://dx.doi.org/10.1128/JB.00900-07.
36. Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar typhimurium. J Bacteriol 2010; 192:456-66; PMID:19897646; http://dx.doi.org/10.1128/JB.01826-08.
37. Majdalani N, Cunning C, Sledjeski D, Elliott T, Gottesman S. 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 USA 1998; 95:12462-7; PMID:9770508; http://dx.doi.org/10.1073/pnas.95.21. 12462.
38. Papenfort K, Pfeiffer V, Lucchini S, Sonawane A, Hinton JC, Vogel J. Systematic deletion of Salmonella small RNA genes identifies CyaR, a conserved CRP-dependent riboregulator of OmpX synthesis. Mol Microbiol 2008; 68:890-906; PMID:18399940; http://dx.doi.org/10.1111/j.1365-2958.2008.06189.x.
39. Argaman L, Hershberg R, Vogel J, Bejerano G, Wagner EG, Margalit H, et al. Novel small RNA-encoding genes in the intergenic regions of Escherichia coli. Curr Biol 2001; 11:941-50; PMID:11448770; http:// dx.doi.org/10.1016/ S0960-9822(01)00270-6.
40. Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S. Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev 2001; 15:1637-51; PMID:11445539; http://dx.doi. org/10.1101/gad.901001.
41. Fröhlich KS, Papenfort K, Berger AA, Vogel J. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res 2011; In press; PMID:22180532; http://dx.doi.org/10.1093/ nar/gkr1156.
42. Römling U, Rohde M, Olsén A, Normark S, Reinköster J. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 2000; 36:10-23; PMID:10760159; http:// dx.doi.org/10.1046/j.1365-2958.2000.01822.x.
43. Simm R, Lusch A, Kader A, Andersson M, Römling U. Role of EAL-containing proteins in multicellular behavior of Salmonella enterica serovar typhimurium. J Bacteriol 2007; 189:3613-23; PMID:17322315; http://dx.doi.org/ 10.1128/JB.01719-06.
44. Pratt LA, Kolter R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 1998; 30:285-93; PMID:9791174; http://dx.doi.org/10.1046/j.1365- 2958.1998.01061.x.
45. Korea CG, Badouraly R, Prevost MC, Ghigo JM, Beloin C. Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol 2010; 12:1957-77; PMID:20345943; http://dx.doi. org/10.1111/j.1462-2920.2010.02202.x.
46. Zogaj X, Nimtz M, Rohde M, Bokranz W, Römling U. The multicellular morphotypes of Salmonella typhimurium and Escherichia coli produce cellulose as the second component of the extracellular matrix. Mol Microbiol 2001; 39:1452-63; PMID:11260463; http://dx.doi.org/10.1046/j.1365-2958.2001.02337.x.
47. Ogasawara H, Yamada K, Kori A, Yamamoto K, Ishihama A. Regulation of the Escherichia coli csgD promoter: interplay between five transcription factors. Microbiology 2010; 156:2470-83; PMID:20466769; http://dx.doi.org/10.1099/mic.0. 039131-0.
48. Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, Lejeune P, et al. CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 2005; 187:2038- 49; PMID:15743952; http://dx.doi.org/10.1128/ JB.187.6.2038-49.2005.
49. Brown PK, Dozois CM, Nickerson CA, Zuppardo A, Terlonge J, Curtiss R, 3rd. MlrA, a novel regulator of curli (AgF) and extracellular matrix synthesis by Escherichia coli and Salmonella enterica serovar typhimurium. Mol Microbiol 2001; 41:349-63; PMID:11489123; http://dx.doi.org/10.1046/j.1365- 2958.2001.02529.x.
50. Brennan RG, Link TM. Hfq structure, function and ligand binding. Curr Opin Microbiol 2007; 10:125- 33; PMID:17395525; http://dx.doi.org/10.1016/j.mib. 2007.03.015.
51. Ansong C, Yoon H, Porwollik S, Mottaz-Brewer H, Petritis BO, Jaitly N, et al. Global systems-level analysis of Hfq and SmpB deletion mutants in Salmonella: implications for virulence and global protein translation. PLoS One 2009; 4:4809; PMID:19277208; http://dx.doi.org/10.1371/journal.pone.0004809.
52. Sittka A, Pfeiffer V, Tedin K, Vogel J. The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 2007; 63:193-217; PMID:17163975; http://dx.doi.org/10.1111/j.1365- 2958.2006.05489.x.
53. Hammar M, Arnqvist A, Bian Z, Olsén A, Normark S. Expression of two csg operons is required for production of fibronectin- and congo red-binding curli polymers in Escherichia coli K-12. Mol Microbiol 1995; 18:661-70; PMID:8817489; http://dx.doi. org/10.1111/j.1365-2958.1995.mmi-18040661.x.
54. Papenfort K, Vogel J. Regulatory RNA in bacterial pathogens. Cell Host Microbe 2010; 8:116-27; PMID:20638647; http://dx.doi.org/10.1016/j. chom.2010.06.008.
55. Waters LS, Storz G. Regulatory RNAs in bacteria. Cell 2009; 136:615-28; PMID:19239884; http://dx.doi. org/10.1016/j.cell.2009.01.043.
56. Thomason MK, Fontaine F, De Lay N, Storz G. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 2012; In press; PMID:22289118; http://dx.doi.org/10.1111/j.1365- 2958.2012.07965.x.
57. Jørgensen MG, Nielsen JS, Boysen A, Franch T, Møller-Jensen J, Valentin-Hansen P. Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol 2012; In press; PMID:22250746; http://dx.doi.org/10.1111/j.1365-2958.2012.07976.x.
58. Vogel J, Bartels V, Tang TH, Churakov G, Slagter- Jäger JG, Hüttenhofer A, et al. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res 2003; 31:6435-43; PMID:14602901; http://dx.doi. org/10.1093/nar/gkg867.
59. Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A, et al. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev 2008; 22:2434- 46; PMID:18765794; http://dx.doi.org/10.1101/gad.475808.
60. Jonas K, Tomenius H, Kader A, Normark S, Römling U, Belova LM, et al. Roles of curli, cellulose and BapA in Salmonella biofilm morphology studied by atomic force microscopy. BMC Microbiol 2007; 7:70; PMID:17650335; http://dx.doi.org/10.1186/1471- 2180-7-70.
61. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, et al. Current Protocols in Molecular Biology. Washington, DC: John Wiley & Sons 1994.
62. Datsenko KA, Wanner BL. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 2000; 97:6640- 5; PMID:10829079; http://dx.doi.org/10.1073/ pnas.120163297.
63. Crawford RW, Reeve KE, Gunn JS. Flagellated but not hyperfimbriated Salmonella enterica serovar typhimurium attaches to and forms biofilms on cholesterol- coated surfaces. J Bacteriol 2010; 192:2981- 90; PMID:20118264; http://dx.doi.org/10.1128/JB.01620-09.
64. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi. org/10.1006/meth.2001.1262.
65. Lamprokostopoulou A, Monteiro C, Rhen M, Römling U. Cyclic di-GMP signalling controls virulence properties of Salmonella enterica serovar typhimurium at the mucosal lining. Environ Microbiol 2010; 12:40-53; PMID:19691499; http://dx.doi.org/10.1111/j.1462- 2920.2009.02032.x.
66. Guzman LM, Belin D, Carson MJ, Beckwith J. Tight regulation, modulation and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 1995; 177:4121-30; PMID:7608087.
67. Volkert MR, Hajec LI, Matijasevic Z, Fang FC, Prince R. Induction of the Escherichia coli aidB gene under oxygen-limiting conditions requires a functional rpoS (katF) gene. J Bacteriol 1994; 176:7638-45; PMID:8002588.