Reducing virulence of the human pathogen Burkholderia by altering the substrate specificity of the quorum-quenching acylase PvdQ

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 4, 2014, Pages 1568-1573

  Koch, Gudrun ^a,b   Nadal Jimenez, Pol ^a,c   Reis, Carlos R ^a,d   Muntendam, Remco ^a   Bokhove, Marcel ^a,e   Melillo, Elena ^a   Dijkstra, Bauke W ^a   Cool, Robbert H ^a   Quax, Wim J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Antibiotic; Computational design; Cystic fibrosis; Enzyme engineering

Indexed keywords

AMIDASE; ANTIBIOTIC AGENT; C8 HSL MOLECULE; ENZYME VARIANT; MICROBIAL PRODUCTS NOT CLASSIFIED ELSEWHERE; PSEUDOMONAS AERUGINOSA QUORUM QUENCHING ACYLASE; UNCLASSIFIED DRUG;

ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL MUTATION; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA INFECTION; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GALLERIA MELLONELLA; HYDROLYSIS; IN VIVO CULTURE; LARVA; MICROBIAL COMMUNITY; MOLECULAR DOCKING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

ANTIBIOTIC; COMPUTATIONAL DESIGN; CYSTIC FIBROSIS; ENZYME ENGINEERING;

AMIDOHYDROLASES; ANIMALS; BURKHOLDERIA CENOCEPACIA; KINETICS; LARVA; MODELS, MOLECULAR; MOTHS; QUORUM SENSING; SUBSTRATE SPECIFICITY; VIRULENCE;

EID: 84893403769     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1311263111     Document Type: Article

References (52)

1. Mahenthiralingam E, Urban TA, Goldberg JB (2005) The multifarious, multireplicon Burkholderia cepacia complex. Nat Rev Microbiol 3(2):144-156.
2. Goldmann DA, Klinger JD (1986) Pseudomonas cepacia: Biology, mechanisms of virulence, epidemiology. J Pediatr 108(5 Pt 2):806-812.
3. Isles A, et al. (1984) Pseudomonas cepacia infection in cystic fibrosis: An emerging problem. J Pediatr 104(2):206-210.
4. Jones AM, et al. (2004) Burkholderia cenocepacia and Burkholderia multivorans: Influence on survival in cystic fibrosis. Thorax 59(11):948-951.
5. Coenye T, LiPuma JJ (2003) Molecular epidemiology of Burkholderia species. Front Biosci 8:e55-e67.
6. Gotschlich A, et al. (2001) Synthesis of multiple N-acylhomoserine lactones is wide-spread among the members of the Burkholderia cepacia complex. Syst Appl Microbiol 24(1):1-14.
7. Govan JR, Deretic V (1996) Microbial pathogenesis in cystic fibrosis: Mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol Rev 60(3):539-574.
8. Govan JR, Hughes JE, Vandamme P (1996) Burkholderia cepacia: Medical, taxonomic and ecological issues. J Med Microbiol 45(6):395-407.
9. Lewenza S, Conway B, Greenberg EP, Sokol PA (1999) Quorum sensing in Burkholderia cepacia: Identification of the LuxRI homologs CepRI. J Bacteriol 181(3):748-756.
10. Davies JC, Rubin BK (2007) Emerging and unusual Gram-negative infections in cystic fibrosis. Semin Respir Crit Care Med 28(3):312-321.
11. Njoroge J, Sperandio V (2009) Jamming bacterial communication: New approaches for the treatment of infectious diseases. EMBO Mol Med 1(4):201-210.
12. Fuqua WC, Winans SC, Greenberg EP (1994) Quorum sensing in bacteria: The LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol 176(2):269-275.
13. Antunes LC, Ferreira RB, Buckner MM, Finlay BB (2010) Quorum sensing in bacterial virulence. Microbiology 156(Pt 8):2271-2282.
14. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197-222.
15. Rasmussen TB, Givskov M (2006) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296(2-3):149-161.
16. Rasmussen TB, Givskov M (2006) Quorum sensing inhibitors: A bargain of effects. Microbiology 152(Pt 4):895-904.
17. Sokol PA, Malott RJ, Riedel K, Eberl L (2007) Communication systems in the genus Burkholderia: Global regulators and targets for novel antipathogenic drugs. Future Microbiol 2(5):555-563.
18. Dong YH, Wang LY, Zhang LH (2007) Quorum-quenching microbial infections: Mechanisms and implications. Philos Trans R Soc Lond B Biol Sci 362(1483):1201-1211.
19. Dong YH, Zhang LH (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43(1):101-109.
20. Uroz S, Dessaux Y, Oger P (2009) Quorum sensing and quorum quenching: The yin and yang of bacterial communication. ChemBioChem 10(2):205-216.
21. Sio CF, et al. (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun 74(3):1673-1682.
22. Dong YH, et al. (2001) Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature 411(6839):813-817.
23. Papaioannou E, et al. (2009) Quorum-quenching acylase reduces the virulence of Pseudomonas aeruginosa in a Caenorhabditis elegans infection model. Antimicrob Agents Chemother 53(11):4891-4897.
24. Reimmann C, et al. (2002) Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148(Pt 4):923-932.
25. Uroz S, et al. (2003) Novel bacteria degrading N-acylhomoserine lactones and their use as quenchers of quorum-sensing-regulated functions of plant-pathogenic bacteria. Microbiology 149(Pt 8):1981-1989.
26. Huang JJ, Han JI, Zhang LH, Leadbetter JR (2003) Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 69(10):5941-5949.
27. Koch G, et al. (2010) The acylase PvdQ has a conserved function among fluorescent Pseudomonas spp. Environ Microbiol Rep 2(3):433-439.
28. Bokhove M, Nadal Jimenez P, Quax WJ, Dijkstra BW (2010) The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate- binding pocket. Proc Natl Acad Sci USA 107(2):686-691.
29. Uehlinger S, et al. (2009) Identification of specific and universal virulence factors in Burkholderia cenocepacia strains by using multiple infection hosts. Infect Immun 77(9):4102-4110.
30. Kooi C, Subsin B, Chen R, Pohorelic B, Sokol PA (2006) Burkholderia cenocepacia ZmpB is a broad-specificity zinc metalloprotease involved in virulence. Infect Immun 74(7): 4083-4093.
31. McClean S, Callaghan M (2009) Burkholderia cepacia complex: Epithelial cell-pathogen confrontations and potential for therapeutic intervention. J Med Microbiol 58(Pt 1):1-12.
32. Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859-904.
33. Sekirov I, Finlay BB (2009) The role of the intestinal microbiota in enteric infection. J Physiol 587(Pt 17):4159-4167.
34. Erickson JA, Jalaie M, Robertson DH, Lewis RA, Vieth M (2004) Lessons in molecular recognition: The effects of ligand and protein flexibility on molecular docking accuracy. J Med Chem 47(1):45-55.
35. Wu G, Robertson DH, Brooks CL III, Vieth M (2003) Detailed analysis of grid-based molecular docking: A case study of CDOCKER-A CHARMm-based MD docking algorithm. J Comput Chem 24(13):1549-1562.
36. MacKerell ADJ, et al. (1998) CHARMM: The energy function and its parameterization with an overview of the program. Encyclopedia of Computational Chemistry, ed Schleyer PV (John Wiley, Chichester, UK), pp 271-277.
37. Miyazaki K, Takenouchi M (2002) Creating random mutagenesis libraries using megaprimer PCR of whole plasmid. Biotechniques 33(5):1033-1034, 1036-1038.
38. Sambrook J, Fritsch EF, Maniatis T (2008) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor, NY).
39. Steidle A, et al. (2001) Visualization of N-acylhomoserine lactone-mediated cell-cell communication between bacteria colonizing the tomato rhizosphere. Appl Environ Microbiol 67(12):5761-5770.
40. Nadal Jimenez P, et al. (2010) Role of PvdQ in Pseudomonas aeruginosa virulence under iron-limiting conditions. Microbiology 156(Pt 1):49-59.
41. Winson MK, et al. (1998) Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing. FEMS Microbiol Lett 163(2):185-192.
42. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26(Pt 6):795-800.
43. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62(Pt 1):72-82.
44. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: Programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50(Pt 5):760-763.
45. McCoy AJ, Grosse-Kunstleve RW, Storoni LC, Read RJ (2005) Likelihood-enhanced fast translation functions. Acta Crystallogr D Biol Crystallogr 61(Pt 4):458-464.
46. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66(Pt 4):486-501.
47. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53(Pt 3):240-255.
48. Winn MD, Murshudov GN, Papiz MZ (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions. Methods Enzymol 374:300-321.
49. Davis IW, et al. (2007) MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35(Web Server issue):W375-W383.
50. Römling U, et al. (1994) Epidemiology of chronic Pseudomonas aeruginosa infections in cystic fibrosis. J Infect Dis 170(6):1616-1621.
51. Huber B, et al. (2001) The cep quorum-sensing system of Burkholderia cepacia H111 controls biofilm formation and swarming motility. Microbiology 147(Pt 9):2517-2528.
52. Wahjudi M, et al. (2011) PA0305 of Pseudomonas aeruginosa is a quorum quenching acylhomoserine lactone acylase belonging to the Ntn hydrolase superfamily. Microbiology 157(Pt 7):2042-2055.