Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1

Infection and Immunity

Volumn 74, Issue 3, 2006, Pages 1673-1682

  Sio, Charles F ^a   Otten, Linda G ^a   Cool, Robbert H ^a   Diggle, Stephen P ^b   Braun, Peter G ^a   Bos, Rein ^a   Daykin, Mavis ^b   Cámara, Miguel ^b   Williams, Paul ^b   Quax, Wim J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

2 HEPTYL 3 HYDROXY 4(1H) QUINOLONE; AMIDASE; ANTIINFECTIVE AGENT; BETA LACTAM ACYLASE; CARBON; ELASTASE; FATTY ACID; GENE PRODUCT; HYDROLASE; LACTONE; N (3 OXODODECANOYL)HOMOSERINE LACTONE; N ACYL HOMOSERINE LACTONE; N ACYL HOMOSERINE LACTONE ACYLASE; N BUTANOYL HOMOSERINE LACTONE; N TERMINAL NUCLEOPHILE HYDROLASE; PA2385 PROTEIN; PYOCYANINE; QUINOLONE DERIVATIVE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIMICROBIAL THERAPY; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BIOASSAY; BIOSYNTHESIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEGRADATION; ENZYME ACTIVITY; GENE FUNCTION; GENE OVEREXPRESSION; HYDROLYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PA2385 GENE; PATHOGENICITY; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN PROCESSING; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

4-BUTYROLACTONE; AMIDOHYDROLASES; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; LACTONES; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; SUBSTRATE SPECIFICITY;

EID: 33644783590     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.3.1673-1682.2006     Document Type: Article

References (58)

1. Arevalo-Ferro, C., M. Hentzer, G. Reil, A. Gorg, S. Kjelleberg, M. Givskov, K. Riedel, and L. Eberl. 2003. Identification of quorum-sensing regulated proteins in the opportunistic pathogen Pseudomonas aeruginosa by proteomics. Environ. Microbiol. 5:1350-1369.
2. Brannigan, J. A., G. Dodson, H. J. Duggleby, P. C. Moody, J. L. Smith, D. R. Tomchick, and A. G. Murzin. 1995. A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378:416-419.
3. Bruggink, A., E. C. Roos, and E. de Vroom. 1998. Penicillin acylase in the industrial production of β-lactam antibiotics. Org. Process Res. Dev. 2:128-133.
4. Chen, W. P., and T. T. Kuo. 1993. A simple and rapid method for the preparation of Gram-negative bacterial genomic DNA. Nucleic Acids Res. 21:2260.
5. Chhabra, S. R., P. Stead, N. J. Bainton, G. P. C. Salmond, G. S. A. B. Stewart, P. Williams, and B. W. Bycroft. 1993. Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogs of N-(3-oxohexanoyl)-L-homoserine lactone. J. Antibiot. 46:441-454.
6. Cornells, P., V. Anjaiah, N. Koedam, P. Delfosse, P. Jacques, P. Thonart, and L. Nelrinckx. 1992. Stability, frequency and multiplicity of transposon insertions in the pyoverdine region in the chromosomes of different fluorescent pseudomonads. J. Gen. Microbiol. 138:1337-1343.
7. de Kievit, T. R., and B. H. Iglewski. 2000. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68:4839-4849.
8. Déziel, E., F. Lépine, S. Milot, J. X. He, M. N. Mindrinos, R. G. Tompkins, and L. G. Rahme. 2004. Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2- heptylquinoline in cell-to-cell communication. Proc. Natl. Acad. Sci. USA 101:1339-1344.
9. Diggle, S. P., K. Winzer, S. R. Chhabra, K. E. Worrall, M. Cámara, and P. Williams. 2003. The Pseudomonas aeruginosa quinolone signal molecule overcomes the cell density-dependency of the quorum sensing hierarchy, regulates rhl-dependent genes at the onset of stationary phase and can be produced in the absence of LasR. Mol. Microbiol. 50:29-43.
10. Dong, Y. H., J. L. Xu, X. Z. Li, and L. H. Zhang. 2000. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA 97:3526-3531.
11. Duggleby, H. J., S. P. Tolley, C. P. Hill, E. J. Dodson, G. Dodson, and P. C. Moody. 1995. Penicillin acylase has a single-amino-acid catalytic centre. Nature 373:264-268.
12. Essar, D. W., L. Eberly, A. Hadero, and I. P. Crawford. 1990. Identification and characterization of genes for a second anthranilate synthase in Pseudomonas aeruginosa: interchangeability of the two anthranilate synthases and evolutionary implications. J. Bacteriol. 172:884-900.
13. Fuchs, R., M. Schafer, V. Geoffroy, and J. M. Meyer. 2001. Siderotyping - a powerful tool for the characterization of pyoverdines. Curr. Top. Med. Chem. 1:31-57.
14. Heeb, S., C. Blumer, and D. Haas. 2002. Regulatory RNA as mediator in GacA/RsmA-dependent global control of exoproduct formation in Pseudomonas fluorescent CHAO. J. Bacteriol. 184:1046-1056.
15. Hentzer, M., H. Wu, J. B. Andersen, K. Riedel, T. B. Rasmussen, N. Bagge, N. Kumar, M. A. Schembri, Z. J. Song, P. Kristoffersen, M. Manefield, J. W. Costerton, S. Molin, L. Eberl, P. Steinberg, S. Kjelleberg, N. Hoiby, and M. Givskov. 2003. Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J. 22:3803-3815.
16. Huang, J. J., J. I. Han, L. H. Zhang, and J. R. Leadbetter. 2003. Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 69:5941-5949.
17. Kim, J. K., I. S. Yang, S. Rhee, Z. Dauter, Y. S. Lee, S. S. Park, and K. H. Kim. 2003. Crystal structures of glutaryl 7-aminocephalosporanic acid acylase: insight into autoproteolytic activation. Biochemistry 42:4084-4093.
18. Kim, S., and Y. Kim. 2001. Active site residues of cephalosporin acylase are Critical not only for enzymatic catalysis but also for post-translational modification. J. Biol. Chem. 276:48376-48381.
19. Kim, Y., K. H. Yoon, Y. Khang, S. Turley, and W. G. J. Hol. 2000. The 2.0 Å crystal structure of cephalosporin acylase. Structure 8:1059-1068.
20. Lamont, I. L., P. A. Beare, U. Ochsner, A. I. Vasil, and M. L. Vasil. 2002. Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 99:7072-7077.
21. Lament, I. L., and L. W. Martin. 2003. Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology 149:833-842.
22. Latifl, A., M. Foglino, K. Tanaka, P. Williams, and A. Lazdunski. 1996. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhlR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol. Microbiol. 21:1137-1146.
23. Leadbetter, J. R., and E. P. Greenberg. 2000. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus. J. Bacteriol. 182:6921-6926.
24. Lee, Y. S., and S. S. Park. 1998. Two-step autocatalytic processing of the glutaryl 7-aminocephalosporanic acid acylase from Pseudomonas sp. strain GK16. J. Bacteriol. 180:4576-4582.
25. Li, Y., J. Chen, W. Jiang, X. Mao, G. Zhao, and E. Wang. 1999. In vivo post-translational processing and subunit reconstitution of cephalosporin acylase from Pseudomonas sp. 130. Eur. J. Biochem. 262:713-719.
26. Lin, Y. H., J. L. Xu, J. Hu, L. H. Wang, S. L. Ong, J. R. Leadbetter, and L. H. Zhang. 2003, Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol. Microbiol. 47:849-860.
27. McClean, K. H., M. K. Winson, L. Fish, A. Taylor, S. R. Chhabra, M. Camara, M. Daykin, J. H. Lamb, S. Swift, B. W. Bycroft, G. S. Stewart, and P. Williams. 1997. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143:3703-3711.
28. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Herjne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
29. Nouwens, A. S., S. A. Beatson, C. B. Whitchurch, B. J. Welsh, H. P. Schweizer, J. S. Mattick, and S. J. Cordwell. 2003. Proteome analysis of extracellular proteins regulated by the las and rhl quorum sensing systems in Pseudomonas aeruginosa PAO1. Microbiology 149:1311-1322.
30. R expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes. Mol. Microbiol. 45:1277-1287.
31. Ohman, D. E., S. J. Cryz, and B. H. Iglewski. 1980, Isolation and characterization of a Pseudomonas aeruginosa PAO mutant that produces altered elastase. J. Bacteriol. 142:836-842.
32. Otten, L. G., C. F. Sio, A. M. van der Sloot, R. H. Cool, and W. J. Quax. 2004. Mutational analysis of a key residue in the substrate specificity of a cephalosporin acylase. Chembiochem 5:820-825.
33. Otten, L. G., C. F. Sio, J. Vrielink, R. H. Cool, and W. J. Quax. 2002. Altering the substrate specificity of cephalosporin acylase by directed evolution of the β-subunit. J. Biol. Chem. 277:42121-42127.
34. Park, S. Y., H. O. Kang, H. S. Jang, J. K. Lee, B. T. Koo, and D. Y. Yum. 2005. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl. Environ. Microbiol. 71:2632-2641.
35. Park, S. Y., S. J. Lee, T. K. Oh, J. W. Oh, B. T. Koo, D. Y. Yum, and J. K. Lee. 2003. AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149:1541-1550.
36. Parsek, M. R., and E. P. Greenberg. 2000. Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc. Natl. Acad. Sci. USA 97:8789-8793.
37. Pearson, J. P., E. C. Pesci, and B. H. Iglewski. 1997. Roles of Pseudomonas aeruginosa las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J. Bacteriol. 179:5756-5767.
38. Pesci, E. C., J. B. Milbank, J. P. Pearson, S. McKnight, A. S. Kende, E. P. Greenberg, and B. H. Iglewski, 1999. Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96:11229-11234.
39. Reyes, F., M. J. Martinez, and J. Soliveri. 1989. Determination of cephalosporin-C amidohydrolase activity with fluorescamine. J. Pharm. Pharmacol. 41:136-137.
40. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
41. Schuster, M., C. P. Lostroh, T. Ogi, and E. P. Greenberg. 2003. Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis. J. Bacteriol. 185:2066-2079.
42. Shirtliff, M. E., J. T. Mader, and A. K. Camper. 2002. Molecular interactions in biofilms. Chem. Biol. 9:859-871.
43. Singh, P. K., M. R. Parsek, E. P. Greenberg, and M. J. Welsh. 2002. A component of innate immunity prevents bacterial biofilm development. Nature 417:552-555.
44. Sio, C. F., and W. J. Quax. 2004. Improved β-lactam acylases and their use as industrial biocatalysts. Curr. Opin. Biotechnol. 15:349-355.
45. Sio, C. F., A. M. Riemens, J. M. van der Laan, R. M. D. Verhaert, and W. J. Quax. 2002. Directed evolution of a glutaryl acylase into an adipyl acylase. Eur. J. Biochem. 269:4495-4504.
46. Smith, A. W., and B. H. Iglewski. 1989. Transformation of Pseudomonas aeruginosa by electroporation. Nucleic Acids Res. 17:10509.
47. Stover, C. K., X. Q. Pham, A. L. Erwin, S. D. Mizoguchi, P. Warrener, M. J. Hickey, F. S. Brinkman, W. O. Hufnagle, D. J. Kowalik, M. Lagrou, R. L. Garber, L. Goltry, E. Tolentino, S. Westbrock-Wadman, Y. Yuan, L. L. Brody, S. N. Coulter, K. R. Folger, A. Kas, K. Larbig, R. Lim, K. Smith, D. Spencer, G. K. Wong, Z. Wu, and I. T. Paulsen. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406:959-964.
48. Swift, S., A. V. Karlyshev, L. Fish, E. L. Durant, M. K. Winson, S. R. Chhabra, P. Williams, S. MacIntyre, and G. S. A. B. Stewart. 1997. 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. 179:5271-5281.
49. Tjalsma, H., A. Bolhuis, J. D. Jongbloed, S. Bron, and J. M. van Dijl. 2000. Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbiol. Mol. Biol. Rev. 64:515-547.
50. Wagner, V. E., D. Bushnell, L. Passador, A. I. Brooks, and B. H. Iglewski. 2003. Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment. J. Bacteriol. 185:2080-2095.
51. Whitehead, N. A., A. M. L. Barnard, H. Slater, N. J. L. Simpson, and G. P. C. Salmond. 2001. Quorum-sensing in gram-negative bacteria. FEMS Microbiol. Rev. 25:365-404.
52. Whiteley, M., K. M. Lee, and E. P. Greenberg. 1999. Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc. Natl. Acad. Sci. USA 96:13904-13909.
53. Williams, P. 2002. Quorum sensing: an emerging target for antibacterial chemotherapy? Expert Opin. Ther. Targets 6:257-274.
54. Winson, M. K., S. Swift, L. Fish, J. P. Throup, F. Jergensen, S. R. Chhabra, B. W. Bycroft, P. Williams, and G. S. A. B. Stewart. 1998. Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol. Lett. 163:185-192.
55. Winzer, K., C. Falconer, N. C. Garber, S. P. Diggle, M. Cámara, and P. Williams. 2000. The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoS. J. Bacteriol. 182:6401-6411.
56. Xu, F., T. Byun, H. J. Dussen, and K. R. Duke. 2003. Degradation of N-acylhomoserine lactones, the bacterial quorum-sensing molecules, by acylase. J. Biotechnol. 101:89-96.
57. Zhang, H.-B., C. Wang, and L. H. Zhang. 2004. The quormone degradation system of Agrobacterium tumefaciens is regulated by starvation signal and stress hormone (p)ppGpp. Mol. Microbiol. 52:1389-1401.
58. Zhang, H. B., L. H. Wang, and L. H. Zhang. 2002. Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens. Proc. Natl. Acad. Sci. USA 99:4638-4643.