Unique Biofilm Signature, Drug Susceptibility and Decreased Virulence in Drosophila through the Pseudomonas aeruginosa Two-Component System PprAB

PLoS Pathogens

Volumn 8, Issue 11, 2012, Pages

  de Bentzmann, Sophie ^a   Giraud, Caroline ^a   Bernard, Christophe S ^a   Calderon, Virginie ^b   Ewald, Friederike ^a   Plésiat, Patrick ^c   Nguyen, Cathy ^d   Grunwald, Didier ^e,f,g   Attree, Ina ^e,f,g   Jeannot, Katy ^c   Fauvarque, Marie Odile ^e,f,g   Bordi, Christophe ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UPS   (France)

^c UNIVERSITÉ DE FRANCHE COMTÉ   (France)

^d Aix Marseille university   (France)

^e CEA GRENOBLE   (France)

^f INSERM   (France)

^g UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BACTERIAL PROTEIN; BAPA PROTEIN; CHAPERONE; CIPROFLOXACIN; EXOPOLYSACCHARIDE; FIMBRIA PROTEIN; HELIX LOOP HELIX PROTEIN; OUTER MEMBRANE PROTEIN; PSEUDOMONAS MEMBRANE PERMEABILITY REGULATOR; TOBRAMYCIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM PILUS; BIOFILM; CELL ADHESION; DROSOPHILA; DRUG SENSITIVITY; GEL MOBILITY SHIFT ASSAY; GENE CONTROL; GENE EXPRESSION; HEMOLYMPH; IMMUNODETECTION; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PROTEIN LOCALIZATION; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TYPE I SECRETION SYSTEM; TYPE III SECRETION SYSTEM;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL SECRETION SYSTEMS; BIOFILMS; CELL LINE; DROSOPHILA MELANOGASTER; FIMBRIAE, BACTERIAL; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA;

EID: 84870840401     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003052     Document Type: Article

References (59)

1. Bordi C, de Bentzmann S, (2011) Hacking into bacterial biofilms: a new therapeutic challenge. Ann Intensive Care 1: 19.
2. Lynch AS, Robertson GT, (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59: 415-428.
3. Flemming HC, Wingender J, (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
4. D'Argenio DA, Gallagher LA, Berg CA, Manoil C, (2001) Drosophila as a model host for Pseudomonas aeruginosa infection. J Bacteriol 183: 1466-1471.
5. Fauvarque MO, Bergeret E, Chabert J, Dacheux D, Satre M, et al. (2002) Role and activation of type III secretion system genes in Pseudomonas aeruginosa-induced Drosophila killing. Microb Pathog 32: 287-295.
6. Lau GW, Goumnerov BC, Walendziewicz CL, Hewitson J, Xiao W, et al. (2003) The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect Immun 71: 4059-4066.
7. Mahajan-Miklos S, Rahme LG, Ausubel FM, (2000) Elucidating the molecular mechanisms of bacterial virulence using non-mammalian hosts. Mol Microbiol 37: 981-988.
8. Rodrigue A, Quentin Y, Lazdunski A, Mejean V, Foglino M, (2000) Two-component systems in Pseudomonas aeruginosa: why so many? Trends Microbiol 8: 498-504.
9. He J, Baldini RL, Deziel E, Saucier M, Zhang Q, et al. (2004) The broad host range pathogen Pseudomonas aeruginosa strain PA14 carries two pathogenicity islands harboring plant and animal virulence genes. Proc Natl Acad Sci U S A 101: 2530-2535.
10. Roy PH, Tetu SG, Larouche A, Elbourne L, Tremblay S, et al. (2010) Complete genome sequence of the multiresistant taxonomic outlier Pseudomonas aeruginosa PA7. PLoS One 5: e8842.
11. Ventre I, Goodman AL, Vallet-Gely I, Vasseur P, Soscia C, et al. (2006) Multiple sensors control reciprocal expression of Pseudomonas aeruginosa regulatory RNA and virulence genes. Proc Natl Acad Sci U S A 103: 171-176.
12. Goodman AL, Kulasekara B, Rietsch A, Boyd D, Smith RS, et al. (2004) A signaling network reciprocally regulates genes associated with acute infection and chronic persistence in Pseudomonas aeruginosa. Dev Cell 7: 745-754.
13. Bordi C, Lamy MC, Ventre I, Termine E, Hachani A, et al. (2010) Regulatory RNAs and the HptB/RetS signalling pathways fine-tune Pseudomonas aeruginosa pathogenesis. Mol Microbiol 76: 1427-1443.
14. Petrova OE, Sauer K, (2010) The novel two-component regulatory system BfiSR regulates biofilm development by controlling the small RNA rsmZ through CafA. J Bacteriol 192: 5275-5288.
15. Petrova OE, Sauer K, (2009) A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLoS Pathog 5: e1000668.
16. Kulasekara HD, Ventre I, Kulasekara BR, Lazdunski A, Filloux A, et al. (2005) A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 55: 368-380.
17. Sivaneson M, Mikkelsen H, Ventre I, Bordi C, Filloux A, (2011) Two-component regulatory systems in Pseudomonas aeruginosa: an intricate network mediating fimbrial and efflux pump gene expression. Mol Microbiol 79: 1353-1366.
18. Mikkelsen H, Ball G, Giraud C, Filloux A, (2009) Expression of Pseudomonas aeruginosa CupD fimbrial genes is antagonistically controlled by RcsB and the EAL-containing PvrR response regulators. PLoS One 4: e6018.
19. Giraud C, de Bentzmann S, (2012) Inside the complex regulation of Pseudomonas aeruginosa chaperone usher systems. Environ Microbiol 14: 1805-1816.
20. Wang Y, Ha U, Zeng L, Jin S, (2003) Regulation of membrane permeability by a two-component regulatory system in Pseudomonas aeruginosa. Antimicrob Agents Chemother 47: 95-101.
21. Giraud C, Bernard CS, Ruer S, de Bentzmann S, (2010) Biological "glue" and "Velcro": Molecular tools for adhesion and biofilm formation in the hairy and gluey bug Pseudomonas aeruginosa. Environ Microbiol Rep 2: 343-358.
22. Bernard CS, Bordi C, Termine E, Filloux A, de Bentzmann S, (2009) Organization and PprB-dependent control of the Pseudomonas aeruginosa tad Locus, involved in Flp pilus biology. J Bacteriol 191: 1961-1973.
23. Giraud C, Bernard CS, Calderon V, Yang L, Filloux A, et al. (2011) The PprA-PprB two-component system activates CupE, the first non-archetypal Pseudomonas aeruginosa chaperone-usher pathway system assembling fimbriae. Environ Microbiol 13: 666-683.
24. Mulcahy H, Sibley CD, Surette MG, Lewenza S, (2011) Drosophila melanogaster as an Animal Model for the Study of Pseudomonas aeruginosa Biofilm Infections In Vivo. PLoS Pathog 7: e1002299.
25. Limmer S, Haller S, Drenkard E, Lee J, Yu S, et al. (2011) Pseudomonas aeruginosa RhlR is required to neutralize the cellular immune response in a Drosophila melanogaster oral infection model. Proc Natl Acad Sci U S A 108: 17378-17383.
26. Avet-Rochex A, Bergeret E, Attree I, Meister M, Fauvarque MO, (2005) Suppression of Drosophila cellular immunity by directed expression of the ExoS toxin GAP domain of Pseudomonas aeruginosa. Cell Microbiol 7: 799-810.
27. Apidianakis Y, Mindrinos MN, Xiao W, Lau GW, Baldini RL, et al. (2005) Profiling early infection responses: Pseudomonas aeruginosa eludes host defenses by suppressing antimicrobial peptide gene expression. Proc Natl Acad Sci U S A 102: 2573-2578.
28. Zhang L, Mah TF, (2008) Involvement of a novel efflux system in biofilm-specific resistance to antibiotics. J Bacteriol 190: 4447-4452.
29. Stabb EV, Reich KA, Ruby EG, (2001) Vibrio fischeri genes hvnA and hvnB encode secreted NAD(+)-glycohydrolases. J Bacteriol 183: 309-317.
30. Hinsa SM, Espinosa-Urgel M, Ramos JL, O'Toole GA, (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49: 905-918.
31. Espinosa-Urgel M, Salido A, Ramos JL, (2000) Genetic analysis of functions involved in adhesion of Pseudomonas putida to seeds. J Bacteriol 182: 2363-2369.
32. Martinez-Gil M, Yousef-Coronado F, Espinosa-Urgel M, (2010) LapF, the second largest Pseudomonas putida protein, contributes to plant root colonization and determines biofilm architecture. Mol Microbiol 77: 549-561.
33. Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, et al. (2005) BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 58: 1322-1339.
34. Latasa C, Solano C, Penades JR, Lasa I, (2006) Biofilm-associated proteins. C R Biol 329: 849-857.
35. Fuqua C, (2010) Passing the baton between laps: adhesion and cohesion in Pseudomonas putida biofilms. Mol Microbiol 77: 533-536.
36. Colvin KM, Irie Y, Tart CS, Urbano R, Whitney JC, et al. (2011) The Pel and Psl polysaccharides provide Pseudomonas aeruginosa structural redundancy within the biofilm matrix. Environ Microbiol 14: 1913-28.
37. Allesen-Holm M, Barken KB, Yang L, Klausen M, Webb JS, et al. (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59: 1114-1128.
38. Dominiak DM, Nielsen JL, Nielsen PH, (2011) Extracellular DNA is abundant and important for microcolony strength in mixed microbial biofilms. Environ Microbiol 13: 710-721.
39. Debarbieux L, Wandersman C, (2001) Folded HasA inhibits its own secretion through its ABC exporter. EMBO J 20: 4657-4663.
40. Zakikhany K, Harrington CR, Nimtz M, Hinton JC, Romling U, (2010) Unphosphorylated CsgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol Microbiol 77: 771-786.
41. Romling U, Rohde M, Olsen A, Normark S, Reinkoster J, (2000) AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 36: 10-23.
42. Newell PD, Monds RD, O'Toole GA, (2009) LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci U S A 106: 3461-3466.
43. Kulasakara H, Lee V, Brencic A, Liberati N, Urbach J, et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3′-5′)-cyclic-GMP in virulence. Proc Natl Acad Sci U S A 103: 2839-2844.
44. Borlee BR, Goldman AD, Murakami K, Samudrala R, Wozniak DJ, et al. (2010) Pseudomonas aeruginosa uses a cyclic-di-GMP-regulated adhesin to reinforce the biofilm extracellular matrix. Mol Microbiol 75: 827-842.
45. Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker-Nielsen T, (2009) Pyoverdine and PQS mediated subpopulation interactions involved in Pseudomonas aeruginosa biofilm formation. Mol Microbiol 74: 1380-1392.
46. Santaella C, Schue M, Berge O, Heulin T, Achouak W, (2008) The exopolysaccharide of Rhizobium sp. YAS34 is not necessary for biofilm formation on Arabidopsis thaliana and Brassica napus roots but contributes to root colonization. Environ Microbiol 10: 2150-2163.
47. de Bentzmann S, Plesiat P, (2011) The Pseudomonas aeruginosa opportunistic pathogen and human infections. Environ Microbiol 13: 1655-1665.
48. Singh G, Wu B, Baek MS, Camargo A, Nguyen A, et al. (2010) Secretion of Pseudomonas aeruginosa type III cytotoxins is dependent on pseudomonas quinolone signal concentration. Microb Pathog 49: 196-203.
49. Reich KA, Schoolnik GK, (1996) Halovibrin, secreted from the light organ symbiont Vibrio fischeri, is a member of a new class of ADP-ribosyltransferases. J Bacteriol 178: 209-215.
50. Karasawa T, Yamakawa K, Tanaka D, Gyobu Y, Nakamura S, (1995) NAD(+)-glycohydrolase productivity of haemolytic streptococci assayed by a simple fluorescent method and its relation to T serotype. FEMS Microbiol Lett 128: 289-292.
51. Stewart-Tull DE, Ollar RA, Scobie TS, (1986) Studies on the Vibrio cholerae mucinase complex. I. Enzymic activities associated with the complex. J Med Microbiol 22: 325-333.
52. Bernier SP, Letoffe S, Delepierre M, Ghigo JM, (2011) Biogenic ammonia modifies antibiotic resistance at a distance in physically separated bacteria. Mol Microbiol 81: 705-716.
53. Chattopadhyay MK, Tabor CW, Tabor H, (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci U S A 100: 2261-2265.
54. Yang L, Rau MH, Hoiby N, Molin S, Jelsbak L, (2011) Bacterial adaptation during chronic infection revealed by independent component analysis of transcriptomic data. BMC Microbiol 11: 184.
55. Koch B, Jensen LE, Nybroe O, (2001) A panel of Tn7-based vectors for insertion of the gfp marker gene or for delivery of cloned DNA into Gram-negative bacteria at a neutral chromosomal site. J Microbiol Methods 45: 187-195.
56. Reisner A, Haagensen JA, Schembri MA, Zechner EL, Molin S, (2003) Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol 48: 933-946.
57. Apidianakis Y, Rahme LG, (2011) Drosophila melanogaster as a model for human intestinal infection and pathology. Dis Model Mech 4: 21-30.
58. Goure J, Pastor A, Faudry E, Chabert J, Dessen A, et al. (2004) The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes. Infect Immun 72: 4741-4750.
59. CLSI (2010) Performance standards for antimicrobial susceptibility testing, twentieth Information Supplement. Nat'l Comm Clinical and Laboratory Standards.