Analysis of the networks controlling the antimicrobial-peptide-dependent induction of Klebsiella pneumoniae virulence factors

Infection and Immunity

Volumn 79, Issue 9, 2011, Pages 3718-3732

  Llobet, Enrique ^a,b   Campos, Miguel A ^a   Giménez, Paloma ^a,b   Moranta, David ^a,b   Bengoechea, José A ^a,b,c  

^a Recinto Hospital Joan March   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOARABINOSE; LIPID A; PALMITIC ACID; POLYMYXIN B; POLYPEPTIDE ANTIBIOTIC AGENT; POLYSACCHARIDE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL LOAD; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATION; FEMALE; GENETIC ANALYSIS; KLEBSIELLA PNEUMONIAE; LUNG; MASS SPECTROMETRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMID; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SURFACE PROPERTY; TRACHEA; UPREGULATION;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; ARABINOSE; BACTERIAL CAPSULES; BACTERIAL LOAD; BACTERIAL PROTEINS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; FEMALE; KLEBSIELLA INFECTIONS; KLEBSIELLA PNEUMONIAE; LIPID A; LUNG; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; PALMITIC ACID; POLYMYXINS; TRACHEA; VIRULENCE FACTORS;

EID: 80052326581     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05226-11     Document Type: Article

References (65)

1. Agerberth, B., et al. 1999. Antibacterial components in bronchoalveolar lavage fluid from healthy individuals and sarcoidosis patients. Am. J. Respir. Crit. Care Med. 160:283-290.
2. Appleyard, R. K. 1954. Segregation of new lysogenic types during growth of doubly lysogenic strain derived from Escherichia coli K-12. Genetics 39:440-452.
3. Aussel, L., et al. 2000. Novel variation of lipid A structures in strains of different Yersinia species. FEBS Lett. 465:87-92.
4. Bader, M. W., et al. 2003. Regulation of Salmonella typhimurium virulence gene expression by cationic antimicrobial peptides. Mol. Microbiol. 50:219-230.
5. Bader, M. W., et al. 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472.
6. Behlau, I., and S. I. Miller. 1993. A PhoP-repressed gene promotes Salmonella typhimurium invasion of epithelial cells. J. Bacteriol. 175:4475-4484.
7. Bitter, T., and H. M. Muir. 1962. A modified uronic acid carbazole reaction. Anal. Biochem. 4:330-334.
8. Brogden, K. A. 2005. Antimicrobial peptides: pore formers or metabolic inhibitors in bacteria? Nat. Rev. Microbiol. 3:238-250.
9. Byrappa, S., D. K. Gavin, and K. C. Gupta. 1995. A highly efficient procedure for site-specific mutagenesis of full-length plasmids using Vent DNA polymerase. Genome Res. 5:404-407.
10. Campos, M. A., et al. 2004. Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect. Immun. 72:7107-7114.
11. Clements, A., et al. 2007. Secondary acylation of Klebsiella pneumoniae lipopolysaccharide contributes to sensitivity to antibacterial peptides. J. Biol. Chem. 282:15569-15577.
12. Coats, S. R., et al. 2009. Human Toll-like receptor 4 responses to Porphyromonas gingivalis are regulated by lipid A 1- and 4'-phosphatase activities. Cell Microbiol. 11:1587-1599.
13. Cortes, G., et al. 2002. Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect. Immun. 70:2583-2590.
14. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
15. Detweiler, C. S., D. M. Monack, I. Ealmonel. Brodsky, H. Mathew, and S. Falkow. 2003. virK, somA, and rcsC are important for systemic Sla enterica serovar Typhimurium infection and cationic peptide resistance. Mol. Microbiol. 48:385-400.
16. El, H. A., A. Tirsoaga, A. Novikov, A. Hussein, and M. Caroff. 2005. Microextraction of bacterial lipid A: easy and rapid method for mass spectrometric characterization. J. Lipid Res. 46:1773-1778.
17. 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.
18. Farris, C., S. Sanowar, M. W. Bader, R. Pfuetzner, and S. I. Miller. 2010. Antimicrobial peptides activate the Rcs regulon through the outer membrane lipoprotein RcsF. J. Bacteriol. 192:4894-4903.
19. Favre, D., and J. F. Viret. 2000. Gene replacement in gram-negative bacteria: the pMAKSAC vectors. Biotechniques 28:198-200.
20. Fields, P. I., E. A. Groisman, and F. Heffron. 1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243:1059-1062.
21. Fields, P. I., R. V. Swanson, C. G. Haidaris, and F. Heffron. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. U. S. A. 83:5189-5193.
22. Ganz, T. 1987. Extracellular release of antimicrobial defensins by human polymorphonuclear leukocytes. Infect. Immun. 55:568-571.
23. 2+/α-ketoglutarate-dependent dioxygenase homologue. J. Biol. Chem. 275:32940-32949.
24. Gootz, T. D. 2010. The global problem of antibiotic resistance. Crit. Rev. Immunol. 30:79-93.
25. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
26. Groisman, E. A., C. Parralopez, M. Salcedo, C. J. Lipps, and F. Heffron. 1992. Resistance to host antimicrobial peptides is necessary for Salmonella virulence. Proc. Natl. Acad. Sci. U. S. A. 89:11939-11943.
27. Gunn, J. S. 2008. The Salmonella PmrAB regulon: lipopolysaccharide modifications, antimicrobial peptide resistance and more. Trends Microbiol. 16: 284-290.
28. Gunn, J. S., et al. 1998. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27:1171-1182.
29. Gunn, J. S., and S. I. Miller. 1996. Pho-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J. Bacteriol. 178:6857-6864.
30. 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.
31. Guo, L., et al. 1998. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95:189-198.
32. Hancock, R. E. W., and D. S. Chapple. 1999. Peptide antibiotics. Antimicrob. Agents Chemother. 43:1317-1323.
33. Harder, J., J. Bartels, E. Christophers, and J. M. Schroder. 2001. Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. J. Biol. Chem. 276:5707-5713.
34. Harder, J., et al. 2000. Mucoid Pseudomonas aeruginosa, TNF-α, and IL-1β, but not IL-6, induce human beta-defensin-2 in respiratory epithelia. Am. J. Respir. Cell Mol. Biol. 22:714-721.
35. Hermsen, E. D., C. J. Sullivan, and J. C. Rotschafer. 2003. Polymyxins: pharmacology, pharmacokinetics, pharmacodynamics, and clinical applications. Infect. Dis. Clin. N. Am. 17:545-562.
36. Hiratsuka, T., et al. 1998. Identification of human beta-defensin-2 in respiratory tract and plasma and its increase in bacterial pneumonia. Biochem. Biophys. Res. Commun. 249:943-947.
37. Hoang, T. T., R. R. Karkhoff-Schweizer, A. J. Kutchma, and H. P. Schweizer. 1998. A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212:77-86.
38. Karbarz, M. J., S. R. Kalb, R. J. Cotter, and C. R. Raetz. 2003. Expression cloning and biochemical characterization of a Rhizobium leguminosarum lipid A 1-phosphatase. J. Biol. Chem. 278:39269-39279.
39. Kox, L. F., M. M. Wösten, 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.
40. Lee, H., F. F. Hsu, J. Turk, and E. A. Groisman. 2004. The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J. Bacteriol. 186:4124-4133.
41. Lindner, B. 2000. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry of lipopolysaccharides. Methods Mol. Biol. 145:311-325.
42. Link, A. J., D. Phillips, and G. M. Church. 1997. Methods for generating precise deletions and insertions in the genome of wild-type Escherichia coli: application to open reading frame characterization. J. Bacteriol. 179:6228-6237.
43. Llobet, E., J. M. Tomas, and J. A. Bengoechea. 2008. Capsule polysaccharide is a bacterial decoy for antimicrobial peptides. Microbiology 154:3877-3886.
44. Majdalani, N., and S. Gottesman. 2005. The Rcs phosphorelay: a complex signal transduction system. Annu. Rev. Microbiol. 59:379-405.
45. Matsuzaki, K. 1998. Magainins as paradigm for the mode of action of pore forming polypeptides. Biochim. Biophys. Acta 1376:391-400.
46. McCray, P. B., Jr., and L. Bentley. 1997. Human airway epithelia express a beta-defensin. Am. J. Respir. Cell Mol. Biol. 16:343-349.
47. Mitrophanov, A. Y., M. W. Jewett, T. J. Hadley, and E. A. Groisman. 2008. Evolution and dynamics of regulatory architectures controlling polymyxin B resistance in enteric bacteria. PLoS Genet. 4:e1000233.
48. Moranta, D., et al. 2010. Klebsiella pneumoniae capsule polysaccharide impedes the expression of β-defensins by airway epithelial cells. Infect. Immun. 78:1135-1146.
49. Nassif, X., J. M. Fournier, J. Arondel, and P. J. Sansonetti. 1989. Mucoid phenotype of Klebsiella pneumoniae is a plasmid-encoded virulence factor. Infect. Immun. 57:546-552.
50. Nicolas, P., and A. Mor. 1995. Peptides as weapons against microorganisms in the chemical defense system of vertebrates. Annu. Rev. Microbiol. 49: 277-304.
51. Nizet, V. 2006. Antimicrobial peptide resistance mechanisms of human bacterial pathogens. Curr. Issues Mol. Biol. 8:11-26.
52. Oertelt, C., B. Lindner, M. Skurnik, and O. Holst. 2001. Isolation and structural characterization of an R-form lipopolysaccharide from Yersinia enterocolitica serotype O:8. Eur. J. Biochem. 268:554-564.
53. Perez-Gutierrez, C., E. Llobet, C. M. Llompart, M. Reines, and J. A. Bengoechea. 2010. Role of lipid A acylation in Yersinia enterocolitica virulence. Infect. Immun. 78:2768-2781.
54. Prost, L. R., M. E. Daley, M. W. Bader, R. E. Klevit, and S. I. Miller. 2008. The PhoQ histidine kinases of Salmonella and Pseudomonas spp. are structurally and functionally different: evidence that pH and antimicrobial peptide sensing contribute to mammalian pathogenesis. Mol. Microbiol. 69:503-519.
55. Prost, L. R., et al. 2007. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol. Cell 26:165-174.
56. 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.
57. Rahn, A., and C. Whitfield. 2003. Transcriptional organization and regulation of the Escherichia coli K30 group 1 capsule biosynthesis (cps) gene cluster. Mol. Microbiol. 47:1045-1060.
58. 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.
59. Singh, P. K., et al. 1998. Production of beta-defensins by human airway epithelia. Proc. Natl. Acad. Sci. U. S. A. 95:14961-14966.
60. Soncini, F. C., V. E. Garcia, F. Solomon, and E. A. Groisman. 1996. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J. Bacteriol. 178: 5092-5099.
61. Tran, A. X., et al. 2006. The lipid A 1-phosphatase of Helicobacter pylori is required for resistance to the antimicrobial peptide polymyxin. J. Bacteriol. 188:4531-4541.
62. Vaara, M. 1992. Agents that increase the permeability of the outer membrane. Microbiol. Rev. 56:395-411.
63. Vaara, M. 2010. Polymyxins and their novel derivatives. Curr. Opin. Microbiol. 13:574-581.
64. Wang, X., S. C. McGrath, R. J. Cotter, and C. R. Raetz. 2006. Expression cloning and periplasmic orientation of the Francisella novicida lipid A 4'-phosphatase LpxF. J. Biol. Chem. 281:9321-9330.
65. Wehland, M., and F. Bernhard. 2000. The RcsAB box. Characterization of a new operator essential for the regulation of exopolysaccharide biosynthesis in enteric bacteria. J. Biol. Chem. 275:7013-7020.