Tobramycin at subinhibitory concentration inhibits the RhlI/R quorum sensing system in a Pseudomonas aeruginosa environmental isolate

BMC Infectious Diseases

Volumn 10, Issue , 2010, Pages

  Babić, Fedora ^a,b   Venturi, Vittorio ^b   Maravić Vlahoviček, Gordana ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; ANTIBIOTIC AGENT; CHLORAMPHENICOL; GENTAMICIN; KANAMYCIN; N ACYLHOMOSERINE LACTONE; PROTEIN RHLI; PROTEIN RHLR; RIBOSOME PROTEIN; TETRAMYCIN; TOBRAMYCIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; LIGASE; RHLI PROTEIN, PSEUDOMONAS AERUGINOSA; RHLR PROTEIN, PSEUDOMONAS AERUGINOSA;

ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM ISOLATE; CONTROLLED STUDY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PHENOTYPE; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SIGNAL TRANSDUCTION; STREPTOMYCES; DRUG EFFECT; GENE EXPRESSION REGULATION; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; ENVIRONMENTAL MICROBIOLOGY; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LIGASES; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; SIGNAL TRANSDUCTION; TOBRAMYCIN; TRANSCRIPTION FACTORS;

EID: 77952798899     PISSN: None     EISSN: 14712334     Source Type: Journal    
DOI: 10.1186/1471-2334-10-148     Document Type: Article

References (52)

1. Borovinskaya MA, Pai RD, Zhang W, Schuwirth BS, Holton JM, Hirokawa G, Kaji H, Kaji A, Cate JHD. Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat Struct Mol Biol 2007, 14(8):727-732. 10.1038/nsmb1271, 17660832.
2. Fourmy D, Recht MI, Blanchard SC, Puglisi JD. Structure of the A Site of Escherichia coli 16 S Ribosomal RNA Complexed with an Aminoglycoside Antibiotic. Science 1996, 274(5291):1367-1371. 10.1126/science.274.5291.1367, 8910275.
3. Smith RS, Iglewski BH. P. aeruginosa quorum-sensing systems and virulence. Current Opinion in Microbiology 2003, 6(1):56-60. 10.1016/S1369-5274(03)00008-0, 12615220.
4. Vicens Q, Westhof E. Crystal Structure of a Complex between the Aminoglycoside Tobramycin and an Oligonucleotide Containing the Ribosomal Decoding A Site. Chemistry & Biology 2002, 9(6):747-755. 10.1016/S1074-5521(02)00153-9, 12079787.
5. Kotra LP, Haddad J, Mobashery S. Aminoglycosides: Perspectives on Mechanisms of Action and Resistance and Strategies to Counter Resistance. Antimicrob Agents Chemother 2000, 44(12):3249-3256. 10.1128/AAC.44.12.3249-3256.2000, 90188, 11083623.
6. Davies J. Microbes have the last word. A drastic re-evaluation of antimicrobial treatment is needed to overcome the threat of antibiotic-resistant bacteria. EMBO reports 2007, 8(7):616-621. 10.1038/sj.embor.7401022, 1905906, 17603533.
7. Davies J, Spiegelman GB, Yim G. The world of subinhibitory antibiotic concentrations. Current Opinion in Microbiology 2006, 9(5):445-453. 10.1016/j.mib.2006.08.006, 16942902.
8. Ryan RP, Dow JM. Diffusible signals and interspecies communication in bacteria. Microbiology 2008, 154(7):1845-1858. 10.1099/mic.0.2008/017871-0, 18599814.
9. Yim G, Huimi Wang H, Davies Frs J. Antibiotics as signalling molecules. Philosophical Transactions of the Royal Society B: Biological Sciences 2007, 362(1483):1195-1200.
10. Goh E-B, Yim G, Tsui W, McClure J, Surette MG, Davies J. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proceedings of the National Academy of Sciences of the United States of America 2002, 99(26):17025-17030. 10.1073/pnas.252607699, 139263, 12482953.
11. Linares JF, Gustafsson I, Baquero F, Martinez JL. Antibiotics as intermicrobial signaling agents instead of weapons. Proceedings of the National Academy of Sciences 2006, 103(51):19484-19489.
12. Skindersoe ME, Alhede M, Phipps R, Yang L, Jensen PO, Rasmussen TB, Bjarnsholt T, Tolker-Nielsen T, Hoiby N, Givskov M. Effects of Antibiotics on Quorum Sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2008, 52(10):3648-3663. 10.1128/AAC.01230-07, 2565867, 18644954.
13. Tanaka M, Hasegawa T, Okamoto A, Torii K, Ohta M. Effect of Antibiotics on Group A Streptococcus Exoprotein Production Analyzed by Two-Dimensional Gel Electrophoresis. Antimicrob Agents Chemother 2005, 49(1):88-96. 10.1128/AAC.49.1.88-96.2005, 538853, 15616280.
14. Hoffman LR, D'Argenio DA, MacCoss MJ, Zhang Z, Jones RA, Miller SI. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005, 436(7054):1171-1175. 10.1038/nature03912, 16121184.
15. Juhas M, Eberl L, Tümmler B. Quorum sensing: the power of cooperation in the world of Pseudomonas. Environmental Microbiology 2005, 7(4):459-471. 10.1111/j.1462-2920.2005.00769.x, 15816912.
16. Venturi V. Regulation of quorum sensing in Pseudomonas. FEMS Microbiology Reviews 2006, 30(2):274-291. 10.1111/j.1574-6976.2005.00012.x, 16472307.
17. Nalca Y, Jansch L, Bredenbruch F, Geffers R, Buer J, Haussler S. Quorum-Sensing Antagonistic Activities of Azithromycin in Pseudomonas aeruginosa PAO1: a Global Approach. Antimicrob Agents Chemother 2006, 50(5):1680-1688. 10.1128/AAC.50.5.1680-1688.2006, 1472232, 16641435.
18. Tateda K, Comte R, Pechere J-C, Kohler T, Yamaguchi K, Van Delden C. Azithromycin Inhibits Quorum Sensing in Pseudomonas aeruginosa. Antimicrob Agents Chemother 2001, 45(6):1930-1933. 10.1128/AAC.45.6.1930-1933.2001, 90577, 11353657.
19. Kumar RS, Ayyadurai N, Pandiaraja P, Reddy AV, Venkateswarlu Y, Prakash O, Sakthivel N. Characterization of antifungal metabolite produced by a new strain Pseudomonas aeruginosa PUPa3 that exhibits broad-spectrum antifungal activity and biofertilizing traits. Journal of Applied Microbiology 2005, 98(1):145-154. 10.1111/j.1365-2672.2004.02435.x, 15610427.
20. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 1983, 166:557-580. 10.1016/S0022-2836(83)80284-8, 6345791.
21. Figurski DH, Helinski DR. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proceedings of the National Academy of Sciences of the United States of America 1979, 76(4):1648-1652. 10.1073/pnas.76.4.1648, 383447, 377280.
22. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 1989, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 2.
23. Wachino J, Shibayama K, Kurokawa H, Kimura K, Yamane K, Suzuki S, Shibata N, Ike Y, Arakawa Y. Novel Plasmid-Mediated 16 S rRNA m1A1408 Methyltransferase, NpmA, Found in a Clinically Isolated Escherichia coli Strain Resistant to Structurally Diverse Aminoglycosides. Antimicrob Agents Chemother 2007, 51(12):4401-4409. 10.1128/AAC.00926-07, 2168023, 17875999.
24. Maravic-Vlahovicek G, Cubrilo S, Tkaczuk KL, Bujnicki JM. Modeling and experimental analyses reveal a two-domain structure and amino acids important for the activity of aminoglycoside resistance methyltransferase Sgm. Biochimica et Biophysica Acta (BBA) - Proteins & Proteomics 2008, 1784(4):582-590.
25. Bradford M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254. 10.1016/0003-2697(76)90527-3, 942051.
26. Steindler L, Bertani I, De Sordi L, Schwager S, Eberl L, Venturi V. LasI/R and RhlI/R Quorum Sensing in a Strain of Pseudomonas aeruginosa Beneficial to Plants. Appl Environ Microbiol 2009, 75(15):5131-5140. 10.1128/AEM.02914-08, 2725484, 19525275.
27. Huber B, Riedel K, Hentzer M, Heydorn A, Gotschlich A, Givskov M, Molin S, Eberl L. The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 2001, 147(9):2517-2528.
28. Winson MK, Swift S, Fish L, Throup JP, Jørgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart G, S AB. Construction and analysis of luxCDABE based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiology Letters 1998, 163(2):185-192. 10.1111/j.1574-6968.1998.tb13044.x, 9673021.
29. Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK, Chhabra SR, Williams P, Macintyre S, Stewart GS. Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 1997, 179(17):5271-5281. 179392, 9286976.
30. Rampioni G, Polticelli F, Bertani I, Righetti K, Venturi V, Zennaro E, Leoni L. The Pseudomonas Quorum-Sensing Regulator RsaL Belongs to the Tetrahelical Superclass of H-T-H Proteins. J Bacteriol 2007, 189(5):1922-1930. 10.1128/JB.01552-06, 1855778, 17172347.
31. Essar DW, Eberly L, Hadero A, Crawford IP. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J Bacteriol 1990, 172(2):884-900. 208517, 2153661.
32. Brint JM, Ohman DE. Synthesis of multiple exoproducts in Pseudomonas aeruginosa is under the control of RhlR-RhlI, another set of regulators in strain PAO1 with homology to the autoinducer-responsive LuxR-LuxI family. J Bacteriol 1995, 177(24):7155-7163. 177595, 8522523.
33. Wachino J, Yamane K, Shibayama K, Kurokawa H, Shibata N, Suzuki S, Doi Y, Kimura K, Ike Y, Arakawa Y. Novel Plasmid-Mediated 16 S rRNA Methylase, RmtC, Found in a Proteus mirabilis Isolate Demonstrating Extraordinary High-Level Resistance against Various Aminoglycosides. Antimicrob Agents Chemother 2006, 50(1):178-184. 10.1128/AAC.50.1.178-184.2006, 1346777, 16377684.
34. Yokoyama K, Doi Y, Yamane K, Kurokawa H, Shibata N, Shibayama K, Yagi T, Kato H, Arakawa Y. Acquisition of 16 S rRNA methylase gene in Pseudomonas aeruginosa. The Lancet 2003, 362(9399):1888-1893.
35. Barclay ML. Adaptive resistance to tobramycin in Pseudomonas aeruginosa lung infection in cystic fibrosis. J Antimicrob Chemother 1996, 37:1155-1164. 10.1093/jac/37.6.1155, 8836818.
36. Luke A, Beatson SA, Leech AJ, Walsh SL, Bell SC. Sub-inhibitory concentrations of ceftazidime and tobramycin reduce the quorum sensing signals of Pseudomonas aeruginosa. Pathology 2004, 36:571-575. 10.1080/00313020400011300, 15841693.
37. Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol 1996, 21(6):1137-1146. 10.1046/j.1365-2958.1996.00063.x, 8898383.
38. Kai T, Tateda K, Kimura S, Ishii Y, Ito H, Yoshida H, Kimura T, Yamaguchi K. A low concentration of azithromycin inhibits the mRNA expression of N-acyl homoserine lactone synthesis enzymes, upstream of lasI or rhlI, in Pseudomonas aeruginosa. Pulmonary Pharmacology & Therapeutics 2009, 22(6):483-486. 10.1016/j.pupt.2009.04.004, 19393329.
39. Kohler T, Dumas J-L, Van Delden C. Ribosome Protection Prevents Azithromycin-Mediated Quorum-Sensing Modulation and Stationary-Phase Killing of Pseudomonas aeruginosa. Antimicrob Agents Chemother 2007, 51(12):4243-4248. 10.1128/AAC.00613-07, 2167979, 17876004.
40. Gupta R, Gobble TR, Schuster M. GidA posttranscriptionally regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 2009, 191(18):5785-5792. 10.1128/JB.00335-09, 2737955, 19592591.
41. Pearson JP, Van Delden C, Iglewski BH. Active efflux and diffusion are involved in transport of Pseudomonas aeruginosa cell-to-cell signals. J Bacteriol 1999, 181(4):1203-1210. 93498, 9973347.
42. Kumar RS, Ayyadurai N, Pandiaraja P, Reddy AV, Venkateswarlu Y, Prakash O, Sakthivel N. Characterization of antifungal metabolite produced by a new strain Pseudomonas aeruginosa PUPa3 that exhibits broad-spectrum antifungal activity and biofertilizing traits. J Appl Microbiol 2005, 98(1):145-154. 10.1111/j.1365-2672.2004.02435.x, 15610427.
43. Steindler L, Bertani I, De Sordi L, Schwager S, Eberl L, Venturi V. LasI/R and RhlI/R quorum sensing in a strain of Pseudomonas aeruginosa beneficial to plants. Appl Environ Microbiol 2009, 75(15):5131-5140. 10.1128/AEM.02914-08, 2725484, 19525275.
44. Sambrook J, Fritsch EF, Maniatis T. Molecular cloning: a laboratory manual. 1989, Cold Spring Harbor, N.Y., 2.
45. Spaink HP, Okker RJH, Wijffelmann CA, Pees E, Lugtemberg BJJ. Promoter in the nodulation region of the Rhizobium leguminosarum Sym plasmid pRL1JI. Plant Mol Biol 1987, 9:27-39.
46. Kovach ME, Elzer PH, Hill DS, Robertson GT, Farris MA, Roop RM, Peterson KM. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 1995, 166(1):175-176. 10.1016/0378-1119(95)00584-1, 8529885.
47. Bertani I, Venturi V. Regulation of the N-Acyl Homoserine Lactone-Dependent Quorum-Sensing System in Rhizosphere Pseudomonas putida WCS358 and Cross-Talk with the Stationary-Phase RpoS Sigma Factor and the Global Regulator GacA. Appl Environ Microbiol 2004, 70(9):5493-5502. 10.1128/AEM.70.9.5493-5502.2004, 520884, 15345437.
48. Winson MK, Swift S, Fish L, Throup JP, Jorgensen F, Chhabra SR, Bycroft BW, Williams P, Stewart GS. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 1998, 163(2):185-192. 10.1111/j.1574-6968.1998.tb13044.x, 9673021.
49. Swift S, Karlyshev AV, Fish L, Durant EL, Winson MK, Chhabra SR, Williams P, Macintyre S, Stewart GS. Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules. J Bacteriol 1997, 179(17):5271-5281. 179392, 9286976.
50. Figurski DH, Helinski DR. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc Natl Acad Sci USA 1979, 76(4):1648-1652. 10.1073/pnas.76.4.1648, 383447, 377280.
51. Kojic M, Venturi V. Regulation of rpoS gene expression in Pseudomonas: involvement of a TetR family regulator. J Bacteriol 2001, 183(12):3712-3720. 10.1128/JB.183.12.3712-3720.2001, 95248, 11371535.
52. Rampioni G, Bertani I, Zennaro E, Polticelli F, Venturi V, Leoni L. The quorum-sensing negative regulator RsaL of Pseudomonas aeruginosa binds to the lasI promoter. J Bacteriol 2006, 188(2):815-819. 10.1128/JB.188.2.815-819.2006, 1347304, 16385073.