Proteus mirabilis pmrI, an RppA-regulated gene necessary for polymyxin B resistance, biofilm formation, and urothelial cell invasion

Antimicrobial Agents and Chemotherapy

Volumn 54, Issue 4, 2010, Pages 1564-1571

  Jiang, Sin Sien ^a   Liu, Ming Che ^a   Teng, Lee Jene ^a   Wang, Won Bo ^a   Hsueh, Po Ren ^b   Liaw, Shwu Jen ^a,b  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BACTERIUM LIPOPOLYSACCHARIDE; CARBOXYLYASE; CIPROFLOXACIN; GENTAMICIN; IMIPENEM; POLYMYXIN B; TETRACYCLINE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCURONIC ACID DECARBOXYLASE; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GENE; BACTERIUM MUTANT; BIOFILM; CELL INVASION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC CODE; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; KNOCKOUT GENE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHENOTYPE; PRIORITY JOURNAL; PROTEUS MIRABILIS; RPPA GENE; UROTHELIUM; WILD TYPE;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BASE SEQUENCE; BIOFILMS; CARBOXY-LYASES; CELL LINE; DNA PRIMERS; DNA, BACTERIAL; DRUG RESISTANCE, BACTERIAL; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HUMANS; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; OPERON; PHENOTYPE; POLYMYXIN B; PROMOTER REGIONS, GENETIC; PROTEUS MIRABILIS; UROTHELIUM;

EID: 77950170505     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01219-09     Document Type: Article

References (50)

1. Amini, S., H. Goodarzi, and S. Tavazoie. 2009. Genetic dissection of an exogenously induced biofilm in laboratory and clinical isolates of E. coli. PLoS Pathog. 5:e1000432.
2. Augustin, D. K., Y. Song, M. S. Baek, Y. Sawa, G. Singh, B. Taylor, A. Rubio-Mills, J. L. Flanagan, J. P. Wiener-Kronish, and S. V. Lynch. 2007. Presence or absence of lipopolysaccharide O antigens affects type III secretion by Pseudomonas aeruginosa. J. Bacteriol. 189:2203-2209.
3. Bader, M. W., W. W. Navarre, W. Shiau, H. Nikaido, J. G. Frye, M. McClelland, F. C. Fang, and S. I. Miller. 2003. Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol. Microbiol. 50:219-230.
4. Bader, M. W., S. Sanowar, M. E. Daley, A. R. Schneider, U. Cho, W. Xu, R. E. Klevit, H. Le Moual, and S. I. Miller. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472.
5. Belas, R., D. Erskine, and D. Flaherty. 1991. Transposon mutagenesis in Proteus mirabilis. J. Bacteriol. 173:6289-6293.
6. Brodsky, I. E., R. K. Ernst, S. I. Miller, and S. Falkow. 2002. mig-14 is a Salmonella gene that plays a role in bacterial resistance to antimicrobial peptides. J. Bacteriol. 184:3203-3213.
7. Chang, A. C., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
8. Clinical and Laboratory Standards Institute. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard M7-A7, 7th ed. Clinical and Laboratory Standards Institute, Wayne, PA.
9. de Lorenzo, V., M. Herrero, U. Jakubzik, and K. N. Timmis. 1990. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J. Bacteriol. 172:6568-6572.
10. Evans, D., T. Kuo, M. Kwong, R. Van, and S. Fleiszig. 2002. Pseudomonas aeruginosa strains with lipopolysaccharide defects exhibit reduced intracellular viability after invasion of corneal epithelial cells. Exp. Eye Res. 75:635-643.
11. Evans, M. E., D. J. Feola, and R. P. Rapp. 1999. Polymyxin B sulfate and colistin: old antibiotics for emerging multiresistant gram-negative bacteria. Ann. Pharmacother. 33:960-967.
12. Falagas, M. E., and S. K. Kasiakou. 2005. Colistin: the revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections. Clin. Infect. Dis. 40:1333-1341.
13. Geurtsen, J., M. Dzieciatkowska, L. Steeghs, H. J. Hamstra, J. Boleij, K. Broen, G. Akkerman, H. El Hassan, J. Li, J. C. Richards, J. Tommassen, and P. van der Ley. 2009. Identification of a novel lipopolysaccharide core biosynthesis gene cluster in Bordetella pertussis, and influence of core structure and lipid A glucosamine substitution on endotoxic activity. Infect. Immun. 77:2602-2611.
14. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
15. Gunn, J. S. 2001. Bacterial modification of LPS and resistance to antimicrobial peptides. J. Endotoxin Res. 7:57-62.
16. Gunn, J. S. 2008. The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol. 16: 284-290.
17. Gunn, J. S., K. B. Lim, J. Krueger, K. Kim, L. Guo, M. Hackett, and S. I. Miller. 1998. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27:1171-1182.
18. Gunn, J. S., S. S. Ryan, J. C. Van Velkinburgh, R. K. Ernst, and S. I. Miller. 2000. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar typhimurium. Infect. Immun. 68:6139-6146.
19. Gupta, S. K., S. Masinick, M. Garrett, and L. D. Hazlett. 1997. Pseudomonas aeruginosa lipopolysaccharide binds galectin-3 and other human corneal epithelial proteins. Infect. Immun. 65:2747-2753.
20. Hancock, R. E., and M. G. Scott. 2000. The role of antimicrobial peptides in animal defenses. Proc. Natl. Acad. Sci. U. S. A. 97:8856-8861.
21. Hu, R. M., K. J. Huang, L. T. Wu, Y. J. Hsiao, and T. C. Yang. 2008. Induction of L1 and L2 beta-lactamases of Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 52:1198-1200.
22. Kaca, W., J. Radziejewska-Lebrecht, and U. R. Bhat. 1990. Effect of polymyxins on the lipopolysaccharide-defective mutants of Proteus mirabilis. Microbios 61:23-32.
23. Kaiser, D. 2007. Bacterial swarming: a re-examination of cell-movement patterns. Curr. Biol. 17:R561-R570.
24. Kox, L. F., M. M. Wosten, and E. A. Groisman. 2000. A small protein that mediates the activation of a two-component system by another two-component system. EMBO J. 19:1861-1872.
25. Lacour, S., E. Bechet, A. J. Cozzone, I. Mijakovic, and C. Grangeasse. 2008. Tyrosine phosphorylation of the UDP-glucose dehydrogenase of Escherichia coli is at the crossroads of colanic acid synthesis and polymyxin resistance. PLoS One 3:e3053.
26. 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.
27. Liaw, S. J., H. C. Lai, and W. B. Wang. 2004. Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect. Immun. 72:6836-6845.
28. Macfarlane, E. L., A. Kwasnicka, M. M. Ochs, and R. E. Hancock. 1999. PhoP-PhoQ homologues in Pseudomonas aeruginosa regulate expression of the outer-membrane protein OprH and polymyxin B resistance. Mol. Microbiol. 34:305-316.
29. Marceau, M., F. Sebbane, F. Ewann, F. Collyn, B. Lindner, M. A. Campos, J. A. Bengoechea, and M. Simonet. 2004. The pmrF polymyxin-resistance operon of Yersinia pseudotuberculosis is upregulated by the PhoP-PhoQ two-component system but not by PmrA-PmrB, and is not required for virulence. Microbiology 150:3947-3957.
30. McCoy, A. J., H. Liu, T. J. Falla, and J. S. Gunn. 2001. Identification of Proteus mirabilis mutants with increased sensitivity to antimicrobial peptides. Antimicrob. Agents Chemother. 45:2030-2037.
31. Moskowitz, S. M., R. K. Ernst, and S. I. Miller. 2004. PmrAB, a two-component regulatory system of Pseudomonas aeruginosa that modulates resistance to cationic antimicrobial peptides and addition of aminoarabinose to lipid A. J. Bacteriol. 186:575-579.
32. Moss, J. E., P. E. Fisher, B. Vick, E. A. Groisman, and A. Zychlinsky. 2000. The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell. Microbiol. 2:443-452.
33. Mouslim, C., and E. A. Groisman. 2003. Control of the Salmonella ugd gene by three two-component regulatory systems. Mol. Microbiol. 47:335-344.
34. Mouslim, C., T. Latifi, and E. A. Groisman. 2003. Signal-dependent requirement for the co-activator protein RcsA in transcription of the RcsB-regulated ugd gene. J. Biol. Chem. 278:50588-50595.
35. Nakao, R., H. Senpuku, and H. Watanabe. 2006. Porphyromonas gingivalis galE is involved in lipopolysaccharide O-antigen synthesis and biofilm formation. Infect. Immun. 74:6145-6153.
36. Nesper, J., C. M. Lauriano, K. E. Klose, D. Kapfhammer, A. Kraiss, and J. Reidl. 2001. Characterization of Vibrio cholerae O1 El tor galU and galE mutants: influence on lipopolysaccharide structure, colonization, and biofilm formation. Infect. Immun. 69:435-445.
37. Newcombe, J., J. C. Jeynes, E. Mendoza, J. Hinds, G. L. Marsden, R. A. Stabler, M. Marti, and J. J. McFadden. 2005. Phenotypic and transcriptional characterization of the meningococcal PhoPQ system, a magnesium-sensing two-component regulatory system that controls genes involved in remodeling the meningococcal cell surface. J. Bacteriol. 187:4967-4975.
38. Nishino, K., F. F. Hsu, J. Turk, M. J. Cromie, M. M. Wosten, and E. A. Groisman. 2006. Identification of the lipopolysaccharide modifications controlled by the Salmonella PmrA/PmrB system mediating resistance to Fe(III) and Al(III). Mol. Microbiol. 61:645-654.
39. Peschel, A. 2002. How do bacteria resist human antimicrobial peptides? Trends Microbiol. 10:179-186.
40. Raetz, C. R., C. M. Reynolds, M. S. Trent, and R. E. Bishop. 2007. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 76: 295-329.
41. Rebeil, R., R. K. Ernst, B. B. Gowen, S. I. Miller, and B. J. Hinnebusch. 2004. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 52:1363-1373.
42. Rozalski, A., Z. Sidorczyk, and K. Kotelko. 1997. Potential virulence factors of Proteus bacilli. Microbiol. Mol. Biol. Rev. 61:65-89.
43. Toguchi, A., M. Siano, M. Burkart, and R. M. Harshey. 2000. Genetics of swarming motility in Salmonella enterica serovar typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
44. Tran, A. X., M. E. Lester, C. M. Stead, C. R. Raetz, D. J. Maskell, S. C. McGrath, R. J. Cotter, and M. S. Trent. 2005. Resistance to the antimicrobial peptide polymyxin requires myristoylation of Escherichia coli and Salmonella typhimurium lipid A. J. Biol. Chem. 280:28186-28194.
45. Trent, M. S., A. A. Ribeiro, S. Lin, R. J. Cotter, and C. R. Raetz. 2001. An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4-amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor. J. Biol. Chem. 276:43122-43131.
46. Vanderlinde, E. M., A. Muszynski, J. J. Harrison, S. F. Koval, D. L. Foreman, H. Ceri, E. L. Kannenberg, R. W. Carlson, and C. K. Yost. 2009. Rhizobium leguminosarum biovar viciae 3841, deficient in 27-hydroxyoctacosanoate-modified lipopolysaccharide, is impaired in desiccation tolerance, biofilm formation and motility. Microbiology 155:3055-3069.
47. Vilches, S., R. Canals, M. Wilhelms, M. T. Salo, Y. A. Knirel, E. Vinogradov, S. Merino, and J. M. Tomas. 2007. Mesophilic Aeromonas UDP-glucose pyrophosphorylase (GalU) mutants show two types of lipopolysaccharide structures and reduced virulence. Microbiology 153:2393-2404.
48. Wang, W. B., I. C. Chen, S. S. Jiang, H. R. Chen, C. Y. Hsu, P. R. Hsueh, W. B. Hsu, and S. J. Liaw. 2008. Role of RppA in the regulation of polymyxin b susceptibility, swarming, and virulence factor expression in Proteus mirabilis. Infect. Immun. 76:2051-2062.
49. West, N. P., P. Sansonetti, J. Mounier, R. M. Exley, C. Parsot, S. Guadagnini, M. C. Prevost, A. Prochnicka-Chalufour, M. Delepierre, M. Tanguy, and C. M. Tang. 2005. Optimization of virulence functions through glucosylation of Shigella LPS. Science 307:1313-1317.
50. Zaidi, T. S., S. M. Fleiszig, M. J. Preston, J. B. Goldberg, and G. B. Pier. 1996. Lipopolysaccharide outer core is a ligand for corneal cell binding and ingestion of Pseudomonas aeruginosa. Investig. Ophthalmol. Vis. Sci. 37:976-986.