Proteomic approach to pseudomonas aeruginosa adaptive resistance to benzalkonium chloride

Journal of Proteomics

Volumn 89, Issue , 2013, Pages 273-279

  Machado, Idalina ^a   Coquet, Laurent ^b   Jouenne, Thierry ^b   Pereira, Maria Olívia ^a  

^a UNIVERSITY OF MINHO   (Portugal)

^b UNIVERSITÉ DE ROUEN   (France)

Author keywords

Chemical adaptation; P. aeruginosa; Proteome

Indexed keywords

BENZALKONIUM CHLORIDE; LIPOPROTEIN; OUTER MEMBRANE PROTEIN; PORIN; BACTERIAL PROTEIN; BENZALKONIUM; TOPICAL ANTIINFECTIVE AGENT;

ADAPTATION; ANTIBIOTIC RESISTANCE; ARTICLE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEOMICS; PSEUDOMONAS AERUGINOSA; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

ANTI-INFECTIVE AGENTS, LOCAL; BACTERIAL PROTEINS; BENZALKONIUM COMPOUNDS; DRUG RESISTANCE, BACTERIAL; GENE EXPRESSION REGULATION, BACTERIAL; LIPOPROTEINS; PORINS; PROTEOMICS; PSEUDOMONAS AERUGINOSA;

EID: 84881544973     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2013.04.030     Document Type: Article

References (55)

1. Nikaido H. Prevention of drug access to bacterial targets - permeability barriers and active efflux. Science 1994, 264:382-388.
2. Levy S.B. Active efflux mechanisms for antimicrobial resistance antimicrob agents. Chemotherapy 1992, 36:695-703.
3. Fernandez L., Breidenstein E.B., Hancock R.E. Creeping baselines and adaptive resistance to antibiotics. Drug Resist Updat 2011, 14:1-21.
4. Mawer S.L., Greenwood D. Specific and non-specific resistance to aminoglycosides in Escherichia coli. J Clin Pathol 1978, 31:12-15.
5. Adair F.W., Geftic S.G., Gelzer J. Resistance of Pseudomonas to quaternary ammonium compounds 8. Appl Microbiol 1969, 18:299-&.
6. Loughlin M.F., Jones M.V., Lambert P.A. Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J Antimicrob Chemother 2002, 49:631-639.
7. Russell A.D. Biocides and pharmacologically active drugs as residues and in the environment: is there a correlation with antibiotic resistance?. Am J Infect Control 2002, 30:495-498.
8. Chapman J.S. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeterior Biodegrad 2003, 51:271-276.
9. Rabilloud T. Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 2009, 30:S174-S180.
10. Santoni V., Molloy M., Rabilloud T. Membrane proteins and proteomics: un amour impossible?. Electrophoresis 2000, 21:1054-1070.
11. Machado I., Graca J., Sousa A.M., Lopes S.P., Pereira M.O. Effect of antimicrobial residues on early adhesion and biofilm formation by wild-type and benzalkonium chloride-adapted Pseudomonas aeruginosa. Biofouling 2011, 27:1151-1159.
12. Mizuno T., Kageyama M. Separation and characterization of the outer membrane of Pseudomonas aeruginosa. J Biochem 1978, 84:179-191.
13. Vilain S., Cosette P., Hubert M., Lange C., Junter G.A., Jouenne T. Comparative proteomic analysis of planktonic and immobilized Pseudomonas aeruginosa cells: a multivariate statistical approach. Anal Biochem 2004, 329:120-130.
14. Collet A., Cosette P., Beloin C., Ghigo J.M., Rihouey C., Lerouge P., et al. Impact of rpoS deletion on the proteome of Escherichia coli grown planktonically and as biofilm. J Proteome Res 2008, 7(11):4659-4669.
15. Vilain S., Cosette P., Charlionet R., Hubert M., Lange C., Junter G.A., et al. Substituting Coomassie Brilliant Blue for bromophenol blue in two-dimensional electrophoresis buffers improves the resolution of focusing patterns. Electrophoresis 2001, 22:4368-4374.
16. Rabilloud T., C S Detection of proteins on two-dimensional electrophoresis gels. Proteome research: two-dimensional gel electrophoresis and identification methods 2000, 107-126. Springer-Verlag, Berlin, Heidelberg. T. Rabilloud (Ed.).
17. Joynson J.A., Forbes B., Lambert R.J.W. Adaptive resistance to benzalkonium chloride, amikacin and tobramycin: the effect on susceptibility to other antimicrobials. J Appl Microbiol 2002, 93:96-107.
18. Gilleland L.B., Gilleland H.E., Gibson J.A., Champlin F.R. Adaptive resistance to aminoglycoside antibiotics in Pseudomonas aeruginosa. J Med Microbiol 1989, 29:41-50.
19. Seyer D., Cosette P., Siroy A., Eacute E., Lenz C., Vaudry H., et al. Proteomic comparison of outer membrane protein patterns of sessile and planktonic Pseudomonas aeruginosa cells. Biofilms 2005, 2:27-36.
20. Wagner S., Baars L., Ytterberg A., Klussmeier A., Wagner C., Nord O., et al. Consequences of membrane protein overexpression in Escherichia coli. Mol Cell Proteomics 2007, 6:1527.
21. Molloy M., Herbert B., Slade M., Rabilloud T., Nouwens A., Williams K., et al. Proteomic analysis of the Escherichia coli outer membrane. Eur J Biochem 2000, 267:2871-2881.
22. Chevallet M., Santoni V., Poinas A., Rouquié D., Fuchs A., Kieffer S., et al. New zwitterionic detergents improve the analysis of membrane proteins by two-dimensional electrophoresis. Electrophoresis 1998, 19:1901-1909.
23. To M.S., Favrin S., Romanova N., Griffiths M.W. Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl Environ Microbiol 2002, 68:5258-5264.
24. Jungblut P.R., Holzhütter H.G., Apweiler R., Schlüter H. The speciation of the proteome. Chem Cent J 2008, 2:16.
25. Woodruff W., Hancock R. Pseudomonas aeruginosa outer membrane protein F: structural role and relationship to the Escherichia coli OmpA protein. J Bacteriol 1989, 171:3304.
26. Saint N., El Hamel C., Dé E., Molle G. Ion channel formation by N-terminal domain: a common feature of OprFs of Pseudomonas and OmpA of Escherichia coli. FEMS Microbiol Lett 2000, 190:261-265.
27. Wagner V., Frelinger J., Barth R., Iglewski B. Quorum sensing: dynamic response of Pseudomonas aeruginosa to external signals. Trends Microbiol 2006, 14:55-58.
28. Guyard-Nicodeỳme M., Bazire A., Hémery G., Meylheuc T., Mollé D., Orange N., et al. Outer membrane modifications of Pseudomonas fluorescens MF37 in response to hyperosmolarity. J Proteome Res 2008, 7:1218-1225.
29. Bratu S., Landman D., Gupta J., Quale J. Role of AmpD, OprF and penicillin-binding proteins in {beta}-lactam resistance in clinical isolates of Pseudomonas aeruginosa. J Med Microbiol 2007, 56:809.
30. Piddock L., Hall M., Bellido F., Bains M., Hancock R. A pleiotropic, posttherapy, enoxacin-resistant mutant of Pseudomonas aeruginosa. Antimicrob Agents Chemother 1992, 36:1057.
31. Pumbwe L., Everett M., Hancock R. Role of gyrA mutation and loss of OprF in the multiple antibiotic resistance phenotype of Pseudomonas aeruginosa G49. FEMS Microbiol Lett 1996, 143:25-28.
32. Firoved A., Wood S., Ornatowski W., Deretic V., Timmins G. Microarray analysis and functional characterization of the nitrosative stress response in nonmucoid and mucoid Pseudomonas aeruginosa. J Bacteriol 2004, 186:4046.
33. Remans K., Vercammen K., Bodilis J., Cornelis P. Genome-wide analysis and literature-based survey of lipoproteins in Pseudomonas aeruginosa. Microbiology 2010, 156:2597.
34. Lloubès R., Cascales E., Walburger A., Bouveret E., Lazdunski C., Bernadac A., et al. The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity?. Res Microbiol 2001, 152:523-529.
35. Cascales E., Bernadac A., Gavioli M., Lazzaroni J., Lloubes R. Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 2002, 184:754.
36. Rodriguez-Herva J., Ramos J. Characterization of an OprL null mutant of Pseudomonas putida. J Bacteriol 1996, 178:5836.
37. Rodriguez-Herva J., Ramos-Gonzalez M., Ramos J. The Pseudomonas putida peptidoglycan-associated outer membrane lipoprotein is involved in maintenance of the integrity of the cell cell envelope. J Bacteriol 1996, 178:1699.
38. Llamas M., Ramos J., Rodriguez-Herva J. Transcriptional organization of the Pseudomonas putida tol-oprL genes. J Bacteriol 2003, 185:184.
39. De Vos D., Bouton C., Sarniguet A., De Vos P., Vauterin M., Cornelis P. Sequence diversity of the oprI gene, coding for major outer membrane lipoprotein I, among rRNA group I pseudomonads. J Bacteriol 1998, 180:6551.
40. Rau H., Revets H., Cornelis P., Titzmann A., Ruggli N., McCullough K.C., et al. Efficacy and functionality of lipoprotein OprI from Pseudomonas aeruginosa as adjuvant for a subunit vaccine against classical swine fever. Vaccine 2006 May 29, 24(22):4757-4768. [Electronic publication ahead of print 2006 Mar 31].
41. Qin X., Emerson J., Stapp J., Stapp L., Abe P., Burns J. Use of real-time PCR with multiple targets to identify Pseudomonas aeruginosa and other nonfermenting gram-negative bacilli from patients with cystic fibrosis. J Clin Microbiol 2003, 41:4312.
42. Linares J., Gustafsson I., Baquero F., Martinez J. Antibiotics as intermicrobial signaling agents instead of weapons. Proc Natl Acad Sci U S A 2006, 103:19484-19489.
43. Peng X., Xu C., Ren H., Lin X., Wu L., Wang S. Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Pseudomonas aeruginosa responding to ampicilin, kanamycin, and tetracycline resistance. J Proteome Res 2005, 4:2257-2265.
44. Hancock R., Siehnel R., Martin N. Outer membrane proteins of Pseudomonas. Mol Microbiol 1990.
45. Yates J.M., Morris G., Brown M.R.W. Effect of iron concentration and growth rate on the expression of protein G in Pseudomonas aeruginosa. FEMS Microbiol Lett 1989, 58:259-262.
46. Gensberg K., Smith A.W., Brinkman F.S.L., Hancock R.E.W. Identification of oprG, a gene encoding a major outer membrane protein of Pseudomonas aeruginosa. J Antimicrob Chemother 1999, 43:607.
47. Cirz R.T., O'Neill B.M., Hammond J.A., Head S.R., Romesberg F.E. Defining the Pseudomonas aeruginosa SOS response and its role in the global response to the antibiotic ciprofloxacin. J Bacteriol 2006, 188:7101-7110.
48. Yamano Y., Nishikawa T., Komatsu Y. Cloning and nucleotide sequence of anaerobically induced porin protein E1 (OprE) of Pseudomonas aeruginosa PAO1. Mol Microbiol 1993, 8:993-1004.
49. Paju S., Goulhen F., Asikainen S., Grenier D., Mayrand D., Uitto V.J. Localization of heat shock proteins in clinical Actinobacillus actinomycetemcomitans strains and their effects on epithelial cell proliferation. FEMS Microbiol Lett 2000, 182:231-235.
50. Coquet L., Cosette P., De E., Galas L., Vaudry H., Rihouey C., et al. Immobilization induces alterations in the outer membrane protein pattern of Yersinia ruckeri. J Proteome Res 2005, 4:1988-1998.
51. Nouwens A.S., Willcox M.D.P., Walsh B.J., Cordwell S.J. Proteomic comparison of membrane and extracellular proteins from invasive (PAO1) and cytotoxic (6206) strains of Pseudomonas aeruginosa. Proteomics 2002, 2:1325-1346.
52. Hennequin C., Porcheray F., Waligora-Dupriet A.J., Collignon A., Barc M.C., Bourlioux P., et al. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 2001, 147:87.
53. Sauer K., Camper A.K. Characterization of phenotypic changes in Pseudomonas putida in response to surface-associated growth. J Bacteriol 2001, 183:6579-6589.
54. Boucher J.C., Martinez-Salazar J., Schurr M.J., Mudd M.H., Yu H., Deretic V. Two distinct loci affecting conversion to mucoidy in Pseudomonas aeruginosa in cystic fibrosis encode homologs of the serine protease HtrA. J Bacteriol 1996, 178:511-523.
55. Pallen M.J., Wren B.W. The HtrA family of serine proteases. Mol Microbiol 1997, 26:209-221.