The effect of hfq on global gene expression and virulence in Neisseria gonorrhoeae

FEBS Journal

Volumn 276, Issue 19, 2009, Pages 5507-5520

  Dietrich, Manuela ^a   Munke, Rebekka ^a   Gottschald, Marion ^a   Ziska, Elke ^a   Boettcher, Jan Peter ^a   Mollenkopf, Hans ^a   Friedrich, Alexandra ^a  

^a MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

Gene expression; Hfq; Neisseria gonorrhoeae; RNA chaperone; Virulence

Indexed keywords

BACTERIAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN HFQ; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL ADHESION; CELL MOTILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME REGULATION; GENE MUTATION; NEISSERIA GONORRHOEAE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

BACTERIAL ADHESION; CELL LINE; EPITHELIAL CELLS; GENE EXPRESSION; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HOST FACTOR 1 PROTEIN; HUMANS; INTERLEUKIN-8; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENESIS; MUTATION; NEISSERIA GONORRHOEAE; RECOMBINANT PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, BACTERIAL; VIRULENCE;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

EID: 70349241915     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2009.07234.x     Document Type: Article

References (60)

1. Merz AJ So M (2000) Interactions of pathogenic neisseriae with epithelial cell membranes. Annu Rev Cell Dev Biol 16, 423 457.
2. Nassif X, Pujol C, Morand P Eugene E (1999) Interactions of pathogenic Neisseria with host cells. Is it possible to assemble the puzzle? Mol Microbiol 32, 1124 1132. (Pubitemid 29286653)
3. Gray-Owen SD (2003) Neisserial Opa proteins: impact on colonization, dissemination and immunity. Scand J Infect Dis 35, 614 618.
4. Hauck CR Meyer TF (2003) 'Small' talk: Opa proteins as mediators of Neisseria-host-cell communication. Curr Opin Microbiol 6, 43 49.
5. Mattick JS (2002) Type IV pili and twitching motility. Annu Rev Microbiol 56, 289 314.
6. Varga JJ, Nguyen V, O'Brien DK, Rodgers K, Walker RA Melville SB (2006) Type IV pili-dependent gliding motility in the Gram-positive pathogen Clostridium perfringens and other Clostridia. Mol Microbiol 62, 680 694.
7. Wall D Kaiser D (1999) Type IV pili and cell motility. Mol Microbiol 32, 1 10.
8. Chen I Dubnau D (2003) DNA transport during transformation. Front Biosci 8, s544 s556.
9. Howie HL, Glogauer M So M (2005) The N. gonorrhoeae type IV pilus stimulates mechanosensitive pathways and cytoprotection through a pilT-dependent mechanism. PLoS Biol 3, e100.
10. Naumann M, Wessler S, Bartsch C, Wieland B Meyer TF (1997) Neisseria gonorrhoeae epithelial cell interaction leads to the activation of the transcription factors nuclear factor kappaB and activator protein 1 and the induction of inflammatory cytokines. J Exp Med 186, 247 258.
11. Taylor CT, Fueki N, Agah A, Hershberg RM Colgan SP (1999) Critical role of cAMP response element binding protein expression in hypoxia-elicited induction of epithelial tumor necrosis factor-alpha. J Biol Chem 274, 19447 19454.
12. Li JD (2003) Exploitation of host epithelial signaling networks by respiratory bacterial pathogens. J Pharmacol Sci 91, 1 7.
13. Bruder JT Kovesdi I (1997) Adenovirus infection stimulates the Raf/MAPK signaling pathway and induces interleukin-8 expression. J Virol 71, 398 404.
14. Baggiolini M Clark-Lewis I (1992) Interleukin-8, a chemotactic and inflammatory cytokine. FEBS Lett 307, 97 101.
15. Agarwal S, King CA, Klein EK, Soper DE, Rice PA, Wetzler LM Genco CA (2005) The gonococcal Fur-regulated tbpA and tbpB genes are expressed during natural mucosal gonococcal infection. Infect Immun 73, 4281 4287.
16. Warner DM, Folster JP, Shafer WM Jerse AE (2007) Regulation of the MtrC-MtrD-MtrE efflux-pump system modulates the in vivo fitness of Neisseria gonorrhoeae. J Infect Dis 196, 1804 1812.
17. Pichon C Felden B (2007) Proteins that interact with bacterial small RNA regulators. FEMS Microbiol Rev 31, 614 625.
18. Toledo-Arana A, Repoila F Cossart P (2007) Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10, 182 188.
19. Mellin JR, Goswami S, Grogan S, Tjaden B Genco CA (2007) A novel fur- and iron-regulated small RNA, NrrF, is required for indirect fur-mediated regulation of the sdhA and sdhC genes in Neisseria meningitidis. J Bacteriol 189, 3686 3694.
20. Metruccio MM, Fantappie L, Serruto D, Muzzi A, Roncarati D, Donati C, Scarlato V Delany I (2009) The Hfq-dependent small noncoding RNA NrrF directly mediates Fur-dependent positive regulation of succinate dehydrogenase in Neisseria meningitidis. J Bacteriol 191, 1330 1342.
21. Aiba H (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10, 134 139.
22. Brennan RG Link TM (2007) Hfq structure, function and ligand binding. Curr Opin Microbiol 10, 125 133.
23. Valentin-Hansen P, Eriksen M Udesen C (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 51, 1525 1533.
24. Kulesus RR, Diaz-Perez K, Slechta ES, Eto DS Mulvey MA (2008) Impact of the RNA chaperone Hfq on the fitness and virulence potential of uropathogenic Escherichia coli. Infect Immun 76, 3019 3026.
25. McNealy TL, Forsbach-Birk V, Shi C Marre R (2005) The Hfq homolog in Legionella pneumophila demonstrates regulation by LetA and RpoS and interacts with the global regulator CsrA. J Bacteriol 187, 1527 1532.
26. Christiansen JK, Larsen MH, Ingmer H, Sogaard-Andersen L Kallipolitis BH (2004) The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J Bacteriol 186, 3355 3362.
27. Ding Y, Davis BM Waldor MK (2004) Hfq is essential for Vibrio cholerae virulence and downregulates sigma expression. Mol Microbiol 53, 345 354.
28. Roop RM 2nd., Gee JM, Robertson GT, Richardson JM, Ng WL Winkler ME (2003) Brucella stationary-phase gene expression and virulence. Annu Rev Microbiol 57, 57 76.
29. Sonnleitner E, Hagens S, Rosenau F, Wilhelm S, Habel A, Jager KE Blasi U (2003) Reduced virulence of a hfq mutant of Pseudomonas aeruginosa O1. Microb Pathog 35, 217 228.
30. Sittka A, Pfeiffer V, Tedin K Vogel J (2007) The RNA chaperone Hfq is essential for the virulence of Salmonella typhimurium. Mol Microbiol 63, 193 217.
31. Wilson JW, Ott CM, Honer zu Bentrup K, Ramamurthy R, Quick L, Porwollik S, Cheng P, McClelland M, Tsaprailis G, Radabaugh T et al. (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci USA 104, 16299 16304.
32. Pannekoek Y, Huis In 't Veld R, Hopman CT, Langerak AA, Speijer D van der Ende A (2009) Molecular characterization and identification of proteins regulated by Hfq in Neisseria meningitidis. FEMS Microbiol Lett 294, 216 224.
33. Hamilton HL, Dominguez NM, Schwartz KJ, Hackett KT Dillard JP (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol Microbiol 55, 1704 1721.
34. Fantappie L, Metruccio MM, Seib KL, Oriente F, Cartocci E, Ferlicca F, Giuliani MM, Scarlato V Delany I (2009) The RNA chaperone Hfq is involved in stress response and virulence in Neisseria meningitidis and is a pleiotropic regulator of protein expression. Infect Immun 77, 1842 1853.
35. Bohn C, Rigoulay C Bouloc P (2007) No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC Microbiol 7, 10.
36. Park HS, Wolfgang M Koomey M (2002) Modification of type IV pilus-associated epithelial cell adherence and multicellular behavior by the PilU protein of Neisseria gonorrhoeae. Infect Immun 70, 3891 3903.
37. Merz AJ So M (1997) Attachment of piliated, Opa- and Opc- gonococci and meningococci to epithelial cells elicits cortical actin rearrangements and clustering of tyrosine-phosphorylated proteins. Infect Immun 65, 4341 4349.
38. Dietrich M, Mollenkopf H, So M Friedrich A (2009) Pilin regulation in the pilT mutant of Neisseria gonorrhoeae strain MS11. FEMS Microbiol Lett 296, 248 256.
39. Higashi DL, Lee SW, Snyder A, Weyand NJ, Bakke A So M (2007) Dynamics of Neisseria gonorrhoeae attachment: microcolony development, cortical plaque formation, and cytoprotection. Infect Immun 75, 4743 4753.
40. Edgar R, Domrachev M Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30, 207 210.
41. Veal WL, Nicholas RA Shafer WM (2002) Overexpression of the MtrC-MtrD-MtrE efflux pump due to an mtrR mutation is required for chromosomally mediated penicillin resistance in Neisseria gonorrhoeae. J Bacteriol 184, 5619 5624.
42. Lee EH, Rouquette-Loughlin C, Folster JP Shafer WM (2003) FarR regulates the farAB-encoded efflux pump of Neisseria gonorrhoeae via an MtrR regulatory mechanism. J Bacteriol 185, 7145 7152.
43. Dillard JP Seifert HS (2001) A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 41, 263 277.
44. Urban JH Vogel J (2008) Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation. PLoS Biol 6, e64.
45. Muffler A, Fischer D Hengge-Aronis R (1996) The RNA-binding protein HF-I, known as a host factor for phage Qbeta RNA replication, is essential for rpoS translation in Escherichia coli. Genes Dev 10, 1143 1151.
46. Brown L Elliott T (1996) 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 178, 3763 3770.
47. Tsui HC, Leung HC Winkler ME (1994) Characterization of broadly pleiotropic phenotypes caused by an hfq insertion mutation in Escherichia coli K-12. Mol Microbiol 13, 35 49.
48. Gunesekere IC, Kahler CM, Ryan CS, Snyder LA, Saunders NJ, Rood JI Davies JK (2006) Ecf, an alternative sigma factor from Neisseria gonorrhoeae, controls expression of msrAB, which encodes methionine sulfoxide reductase. J Bacteriol 188, 3463 3469.
49. Testerman TL, Vazquez-Torres A, Xu Y, Jones-Carson J, Libby SJ Fang FC (2002) The alternative sigma factor sigmaE controls antioxidant defences required for Salmonella virulence and stationary-phase survival. Mol Microbiol 43, 771 782.
50. Rolhion N, Carvalho FA Darfeuille-Michaud A (2007) OmpC and the sigma(E) regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82. Mol Microbiol 63, 1684 1700.
51. Kovacikova G Skorupski K (2002) The alternative sigma factor sigma(E) plays an important role in intestinal survival and virulence in Vibrio cholerae. Infect Immun 70, 5355 5362.
52. Cano DA, Martinez-Moya M, Pucciarelli MG, Groisman EA, Casadesus J Garcia-Del Portillo F (2001) Salmonella enterica serovar Typhimurium response involved in attenuation of pathogen intracellular proliferation. Infect Immun 69, 6463 6474.
53. Du Y, Lenz J Arvidson CG (2005) Global gene expression and the role of sigma factors in Neisseria gonorrhoeae in interactions with epithelial cells. Infect Immun 73, 4834 4845.
54. Folster JP, Johnson PJ, Jackson L, Dhulipali V, Dyer DW Shafer WM (2009) MtrR modulates rpoH expression and levels of antimicrobial resistance in Neisseria gonorrhoeae. J Bacteriol 191, 287 297.
55. Gunesekere IC, Kahler CM, Powell DR, Snyder LA, Saunders NJ, Rood JI Davies JK (2006) Comparison of the RpoH-dependent regulon and general stress response in Neisseria gonorrhoeae. J Bacteriol 188, 4769 4776.
56. Arvidson CG, Kirkpatrick R, Witkamp MT, Larson JA, Schipper CA, Waldbeser LS, O'Gaora P, Cooper M So M (1999) Neisseria gonorrhoeae mutants altered in toxicity to human fallopian tubes and molecular characterization of the genetic locus involved. Infect Immun 67, 643 652.
57. Mitobe J, Morita-Ishihara T, Ishihama A Watanabe H (2008) Involvement of RNA-binding protein Hfq in the post-transcriptional regulation of invE gene expression in Shigella sonnei. J Biol Chem 283, 5738 5747.
58. Haas R, Kahrs AF, Facius D, Allmeier H, Schmitt R Meyer TF (1993) TnMax - a versatile mini-transposon for the analysis of cloned genes and shuttle mutagenesis. Gene 130, 23 31.
59. Friedrich A, Arvidson CG, Shafer WM, Lee EH So M (2007) Two ABC transporter operons and the antimicrobial resistance gene mtrF are pilT responsive in Neisseria gonorrhoeae. J Bacteriol 189, 5399 5402.
60. Lee SW, Higashi DL, Snyder A, Merz AJ, Potter L So M (2005) PilT is required for PI(3,4,5)P3-mediated crosstalk between Neisseria gonorrhoeae and epithelial cells. Cell Microbiol 7, 1271 1284. (Pubitemid 41179420)