Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis

Infection and Immunity

Volumn 72, Issue 12, 2004, Pages 6836-6845

  Liaw, Shwu Jen ^a,b   Lai, Hsin Chih ^a,b   Wang, Won Bo ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; FATTY ACID; HEMOLYSIN; HISTIDINE; LAURIC ACID; MYRISTIC ACID; OLEIC ACID; PALMITIC ACID; PROTEIN RSBA; SATURATED FATTY ACID; STEARIC ACID; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BIOFILM; BODY REGIONS; GENE; GRAM NEGATIVE INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEUS MIRABILIS; RSBA GENE; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; BIOFILMS; FATTY ACIDS; GENE EXPRESSION REGULATION, BACTERIAL; POLYSACCHARIDES, BACTERIAL; PROTEUS MIRABILIS; VIRULENCE FACTORS;

EID: 9244261620     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.72.12.6836-6845.2004     Document Type: Article

References (43)

1. Aguilar, P. S., A. M. Hernandez-Arriaga, L. E. Cybulski, A. C. Erazo, and D. de Mendoza. 2001. Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J. 20:1681-1691.
2. Allison, C., L. Emödy, N. Coleman, and C. Hughes. 1994. The role of swarm cell differentiation and multicellular migration in the uropathogenicity of Proteus mirabilis. J. Infect. Dis. 169:1155-1158.
3. Allison, C., and C. Hughes. 1991. Bacterial swarming: an example of prokaryotic differentiation and multicellular behaviour. Sci. Progress 75:403-422.
4. Allison, C., and C. Hughes. 1991. Closely linked genetic loci required for swarm cell differentiation and multicellular migration by Proteus mirabilis. Mol. Microbiol. 5:1975-1982.
5. Allison, C., H. C. Lai, D. Gygi, and C. Hughes. 1993. Cell differentiation of Proteus mirabilis is initiated by glutamine, a specific chemoattractant for swarming cells. Mol. Microbiol. 8:53-60.
6. Allison, C., H. C. Lai, and C. Hughes. 1992. Coordinate expression of virulence genes during swarm cell differentiation and population migration of Proteus mirabilis. Mol. Microbiol. 6:1583-1591.
7. Belas, R., R. Schneider, and M. Melch. 1998. Characterization of Proteus mirabilis precocious swarming mutants: identification of rsbA, encoding a regulator of swarming behavior. J. Bacteriol. 180:6126-6139.
8. Cronan, J. E. 1997. In vivo evidence that acyl coenzyme A regulates DNA binding by the Escherichia coli FadR global transcription factor. J. Bacteriol. 179:1819-1823.
9. Cybulski, L. E., D. Albanesi, M. C. Mansilla, S. Altabe, P. S. Aguilar, and D. de Mendoza. 2002. Mechanism of membrane fluidity optimization: isothermal control of the Bacillus subtilis acyl-lipid desaturase. Mol. Microbiol. 45:1379-1388.
10. Déziel, E., Y. Comeau, and R. Villemur. 2001. Initiation of biofilm formation by Pseudomonas aeruginosa 57RP correlates with emergence of hyperpiliated and highly adherent phenotypic variants deficient in swimming, swarming, and twitching motilities. J. Bacteriol. 183:1195-1204.
11. Dong, Y. H., L. H. Wang, J. L. Xu, H. B. Zhang, X. F. Zhang, and L. H. Zhang. 2001. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411:813-816.
12. Downard, J., and D. Toal. 1995. Branched-chain fatty acids: the case for a novel form of cell-cell signaling during Myxococcus xanthus development. Mol. Microbiol. 16:171-175.
13. Dufour, A., R. B. Furness, and C. Hughes. 1998. Novel genes that upregulate the Proteus mirabilis flhDC master operon controlling flagellar biogenesis and swarming. Mol. Microbiol. 29:741-751.
14. Eberl, L., M. K. Winson, C. Sternberg, G. S. A. B. Stewart, G. Christiansen, S. R. Chhabra, B. Bycroft, P. Williams, S. Molin, and M. Givskov. 1996. Involvement of N-acyl-L-homoserine lactone autoinducers in controlling the multicellular behavior of Serratia liquefaciens. Mol. Microbiol. 20:127-136.
15. Flavier, A. B., S. J. Clough, M. A. Schell, and T. P. Denny. 1997. Identification of 3-hydroxypalmitic acid methyl ester as a novel autoregulator controlling virulence in Ralstonia solanacearum. Mol. Microbiol. 26:251-259.
16. Flemming, H. C., J. Wingender, C. Griegbe, and C. Mayer. 2000. Physicochemical properties of biofilms, p. 19-34. In L. V. Evans (ed.), Biofilms: recent advances in their study and control. Harwood Academic Publishers, Amsterdam, The Netherlands.
17. Fraser, G. M., and C. Hughes. 1999. Swarming motility. Curr. Opin. Microbiol. 2:630-635.
18. Gaisser, S., and C. Hughes. 1997. A locus coding for putative non-ribosomal peptide/polyketide synthase functions is mutated in a swarming defective Proteus mirabilis strain. Mol. Gen. Genet. 253:415-427.
19. Gygi, D., M. J. Bailey, C. Allison, and C. Hughes. 1995. Requirement for FlhA in flagella assembly and swarm-cell differentiation by Proteus mirabilis. Mol. Microbiol. 15:761-769.
20. Gygi, D., M. M. Rahman, H. C. Lai, R. Carlson, J. Guard-Petter, and C. Hughes. 1995. A cell-surface polysaccharide that facilitates rapid population migration by differentiated swarm cells of Proteus mirabilis. Mol. Microbiol. 17:1167-1175.
21. Harshey, R. M. 1994. Bees aren't the only ones: swarming in gram-negative bacteria. Mol. Microbiol. 13:389-394.
22. Hay, N. A., D. J. Tipper, D. Gygi, and C. Hughes. 1997. A nonswarming mutant of Proteus mirabilis lacks the Lrp global transcriptional regulator. J. Bacteriol. 179:4741-4746.
23. Huber, B., K. Riedel, M. Hentzer, A. Heydorn, A. Gotschlich, M. Givskov, S. Molin, and L. Eberl. 2001. The cep quorum-sensing system of Burkholderia cepacia Hill controls biofilm formation and swarming motility. Microbiology 147:2517-2528.
24. Koronakis, V., M. Cross, B. Senior, E. Koronakis, and C. Hughes. 1987. The secreted hemolysins of Proteus mirabilis, Proteus vulgaris, and Morganella morganii are genetically related to each other and to the alpha-hemolysin of Escherichia coli. J. Bacteriol. 169:1509-1515.
25. Lai, H. C., D. Gygi, G. M. Fraser, and C. Hughes. 1998. A swarming-defective mutant of Proteus mirabilis lacking a putative cation-transporting membrane P-type ATPase. Microbiology 144:1957-1961.
26. Liaw, S. J., H. C. Lai, S. W. Ho, K. T. Luh, and W. B. Wang. 2000. Inhibition of virulence factor expression and swarming differentiation in Proteus mirabilis by p-nitrophenylglycerol. J. Med. Microbiol. 49:725-731.
27. Liaw, S. J., H. C. Lai, S. W. Ho, K. T. Luh, and W. B. Wang. 2001. Characterisation of p-nitrophenylglycerol-resistant Proteus mirabilis super-swarming mutants. J. Med. Microbiol. 50:1039-1048.
28. Liaw, S. J., H. C. Lai, S. W. Ho, K. T. Luh, and W. B. Wang. 2003. Role of RsmA in the regulation of swarming motility and virulence factor expression in Proteus mirabilis. J. Med. Microbiol. 52:19-28.
29. Lucas, R. L., C. P. Lostroh, C. C. DiRusso, M. P. Specter, B. L. Wanner, and C. A. Lee. 2000. Multiple factors independently regulate hilA and invasion gene expression in Salmonella enterica serovar Typhimurium. J. Bacteriol. 182:1872-1882.
30. Mireles, J. R., A. Toguchi, and R. M. Harshey. 2001. Salmonella enterica serovar Typhimurium swarming mutants with altered biofilm-forming abilities: surfactin inhibits biofilm formation. J. Bacteriol. 183:5848-5854.
31. Mobley, H. L., G. R. Chippendale, K. G. Swihart, and R. A. Welch. 1991. Cytotoxicity of HpmA hemolysin and urease of Proteus mirabilis and Proteus vulgaris against cultured human renal proximal tubular epithelial cells. Infect. Immun. 59:2036-2042.
32. More, M. I., L. D. Finger, J. L. Stryker, C. Fuqua, A. Eberhard, and S. C. Winans. 1996. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science 272:1655-1658.
33. O'Toole, G. A., and R. Kolter. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28:449-461.
34. Rauprich, O., M. Matsushita, C. J. Weijer, F. Siegert, S. E. Esipov, and J. A. Shapiro. 1996. Periodic phenomena in Proteus mirabilis swarm colony development. J. Bacteriol. 178:6525-6538.
35. Schaefer, A. L., D. L. Val, B. L. Hanzelka, J. E. Cronan, Jr., and E. P. Greenberg. 1996. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA 93:9505-9509.
36. Slater, H., A. Alvarez-Morales, C. E. Barber, M. J. Daniels, and J. M. Dow. 2000. A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol. Microbiol. 38:986-1003.
37. Soto, M. J., M. Fernández-Pascual, J. Sanjuan, and J. Olivares. 2002. A fadD mutant of Sinorhizobium meliloti shows multicellular swarming migration and is impaired in nodulation efficiency on alfalfa roots. Mol. Microbiol. 43:371-382.
38. Strauch, M. A., D. de Mendoza, and J. A. Hoch. 1992. cis-unsaturated fatty acids specifically inhibit a signal-transducing protein kinase required for initiation of sporulation in Bacillus subtilis. Mol. Microbiol. 6:2909-2917.
39. Takeda, S., Y. Fujisawa, M. Matsubara, H. Aiba, and T. Mizuno. 2001. A novel feature of the multistep phosphorelay in Escherichia coli: a revised model of the RcsC→YojN→RcsB signalling pathway implicated in capsular synthesis and swarming behaviour. Mol. Microbiol. 40:440-450.
40. von Bodman, S. B., D. R. Majerczak, and D. L. Coplin. 1998. A negative regulator mediates quorum-sensing control of exopolysaccharide production in Pantoea stewartii subsp. stewartii. Proc. Natl. Acad. Sci. USA 95:7687-7692.
41. Wang, L. H., Y. He, Y. Gao, J. E. Wu, Y. H. Dong, C. He, S. X. Wang, L. X. Weng, J. L. Xu, L. Tay, R. X. Fang, and L. H. Zhang. 2004. A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol. Microbiol. 51:903-912.
42. Warren, J. W., J. H. Tenney, J. M. Hoopes, H. L. Muncie, and W. C. Anthony. 1982. A prospective microbiologic study of bacteriuria in patients with chronic indwelling urethral catheters. J. Infect. Dis. 146:719-723.
43. Zhang, L. H. 2003. Quorum quenching and proactive host defense. Trends Plant Sci. 8:238-244.