Pitfalls associated with evaluating enzymatic quorum quenching activity: The case of MomL and its effect on Pseudomonas aeruginosa and Acinetobacter baumannii biofilms

PeerJ

Volumn 2017, Issue 4, 2017, Pages

  Zhang, Yunhui ^a   Brackman, Gilles ^a   Coenye, Tom ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Acinetobacter baumannii; Biofilm; MomL; Pseudomonas aeruginosa; Quorum quenching; Quorum sensing; Quorum sensing inhibition

Indexed keywords

CIPROFLOXACIN; COLISTIN; MEROPENEM; TOBRAMYCIN;

ACINETOBACTER; ACINETOBACTER BAUMANNII; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BIOFILM; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENZYMATIC DEGRADATION; FLUORESCENCE MICROSCOPY; GENE EXPRESSION PROFILING; NONHUMAN; PROTEIN PURIFICATION; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; ULTRASOUND;

EID: 85018160589     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.3251     Document Type: Article

References (42)

1. Aybey A, Demirkan E. 2016. Inhibition of quorum sensing-controlled virulence factors in Pseudomonas aeruginosa by human serum paraoxonase. Journal of Medical Microbiology 65:105-113 DOI 10.1099/jmm.0.000206.
2. Bassler BL, Losick R. 2006. Bacterially speaking. Cell 125:237-246 DOI 10.1016/j.cell.2006.04.001.
3. Bhargava N, Sharma P, Capalash N. 2010. Quorum sensing in Acinetobacter: an emerg-ing pathogen. Critical Reviews in Microbiology 36:349-360 DOI 10.3109/1040841X.2010.512269.
4. Bhargava N, Singh SP, Sharma A, Sharma P, Capalash N. 2015. Attenuation of quorum sensing-mediated virulence of Acinetobacter baumannii by Glycyrrhiza glabra flavonoids. Future Microbiology 10:1953-1968 DOI 10.2217/fmb.15.107.
5. Brackman G, Coenye T. 2015. Quorum sensing inhibitors as anti-biofilm agents. Current Pharmaceutical Design 21:5-11.
6. Brackman G, Cos P, Maes L, Nelis HJ, Coenye T. 2011. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrobial Agents and Chemotherapy 55:2655-2661 DOI 10.1128/AAC.00045-11.
7. Brackman G, Garcia-Fernandez MJ, Lenoir J, De Meyer L, Remon JP, De Beer T, Concheiro A, Alvarez-Lorenzo C, Coenye T. 2016. Dressings loaded with cyclodextrin-hamamelitannin complexes increase Staphylococcus aureus suscep-tibility toward antibiotics both in single as well as in mixed biofilm communities. Macromolecular Bioscience 16(6):859-869 DOI 10.1002/mabi.201500437.
8. Bzdrenga J, Daudé D, Rémy B, Jacquet P, Plener L, Elias M, Chabrière E. 2016. Biotechnological applications of quorum quenching enzymes. Chemico-Biological Interactions 267:104-115 DOI 10.1016/j.cbi.2016.05.028.
9. Chow JY, Yang Y, Tay SB, Chua KL, Yew WS. 2014. Disruption of biofilm formation by the human pathogen Acinetobacter baumannii using engineered quorum-quenching lactonases. Antimicrobial Agents and Chemotherapy 58:1802-1805 DOI 10.1128/AAC.02410-13.
10. Donlan RM, Costerton JW. 2002. Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews 15:167-193 DOI 10.1128/CMR.15.2.167-193.2002.
11. Fetzner S. 2015. Quorum quenching enzymes. Journal of Biotechnology 201:2-14 DOI 10.1016/j.jbiotec.2014.09.001.
12. Furiga A, Lajoie B, El Hage S, Baziard G, Roques C. 2016. Impairment of Pseudomonas aeruginosa biofilm resistance to antibiotics by bombining the drugs with a new quorum-sensing inhibitor. Antimicrobial Agents and Chemotherapy 60:1676-1686 DOI 10.1128/AAC.02533-15.
13. González R, Dijkshoorn L, Van den Barselaar M, Nudel C. 2009. Quorum sensing signal profile of Acinetobacter strains from nosocomial and environmental sources. Revista Argentina De Microbiologia 41:73-78.
14. Gonzalez-Villoria AM, Valverde-Garduno V. 2016. Antibiotic-resistant Acinetobacter baumannii increasing success remains a challenge as a nosocomial pathogen. Journal of Pathogens 2016: Epub ahead of print Feb 04 2016 DOI 10.1155/2016/7318075.
15. Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the nat-ural environment to infectious diseases. Nature Reviews Microbiology 2:95-108 DOI 10.1038/nrmicro821.
16. Hentzer M, Givskov M. 2003. Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. The Journal of Clinical Investigation 112:1300-1307 DOI 10.1172/JCI20074.
17. Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N. 2002. Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148:87-102 DOI 10.1099/00221287-148-1-87.
18. Hentzer M, Wu H, Andersen JB, Riedel K, Rasmussen TB, Bagge N, Kumar N, Schembri MA, Song Z, Kristoffersen P. 2003. Attenuation of Pseudomonas aerug-inosa virulence by quorum sensing inhibitors. The EMBO Journal 22:3803-3815 DOI 10.1093/emboj/cdg366.
19. Hraiech S, Hiblot J, Lafleur J, Lepidi H, Papazian L, Rolain J-M, Raoult D, Elias M, Silby MW, Bzdrenga J. 2014. Inhaled lactonase reduces Pseudomonas aerugi-nosa quorum sensing and mortality in rat pneumonia. PLOS ONE 9:e107125 DOI 10.1371/journal.pone.0107125.
20. Ivanova K, Fernandes MM, Francesko A, Mendoza E, Guezguez J, Burnet M, Tzanov T. 2015. Quorum-quenching and matrix-degrading enzymes in multilayer coatings synergistically prevent bacterial biofilm formation on urinary catheters. ACS Applied Materials & Interfaces 7:27066-27077 DOI 10.1021/acsami.5b09489.
21. LaSarre B, Federle MJ. 2013. Exploiting quorum sensing to confuse bacterial pathogens. Microbiology and Molecular Biology Reviews 77:73-111 DOI 10.1128/MMBR.00046-12.
22. Longo F, Vuotto C, Donelli G. 2014. Biofilm formation in Acinetobacter baumannii. New Microbiologica 37:119-127.
23. Migiyama Y, Kaneko Y, Yanagihara K, Morohoshi T, Morinaga Y, Nakamura S, Miyazaki T, Hasegawa H, Izumikawa K, Kakeya H. 2013. Efficacy of AiiM, an N-acylhomoserine lactonase, against Pseudomonas aeruginosa in a mouse model of acute pneumonia. Antimicrobial Agents and Chemotherapy 57:3653-3658 DOI 10.1128/AAC.00456-13.
24. Niu C, Clemmer KM, Bonomo RA, Rather PN. 2008. Isolation and characterization of an autoinducer synthase from Acinetobacter baumannii. Journal of Bacteriology 190:3386-3392 DOI 10.1128/JB.01929-07.
25. O'Loughlin CT, Miller LC, Siryaporn A, Drescher K, Semmelhack MF, Bassler BL. 2013. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proceedings of the National Academy of Sciences of the United States of America 110:17981-17986 DOI 10.1073/pnas.1316981110.
26. Peeters E, Nelis HJ, Coenye T. 2008. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods 72:157-165 DOI 10.1016/j.mimet.2007.11.010.
27. Peleg AY, Jara S, Monga D, Eliopoulos GM, Moellering RC, Mylonakis E. 2009. Galleria mellonella as a model system to study Acinetobacter baumannii patho-genesis and therapeutics. Antimicrobial Agents and Chemotherapy 53:2605-2609 DOI 10.1128/AAC.01533-08.
28. Peleg AY, Seifert H, Paterson DL. 2008. Acinetobacter baumannii: emergence of a suc-cessful pathogen. Clinical Microbiology Reviews 21:538-582 DOI 10.1128/CMR.00058-07.
29. Pesci EC, Pearson JP, Seed PC, Iglewski BH. 1997. Regulation of las and rhl quo-rum sensing in Pseudomonas aeruginosa. Journal of Bacteriology 179:3127-3132 DOI 10.1128/jb.179.10.3127-3132.1997.
30. Potron A, Poirel L, Nordmann P. 2015. Emerging broad-spectrum resistance in Pseudomonas aeruginosa and Acinetobacter baumannii: mechanisms and epidemiology. International Journal of Antimicrobial Agents 45:568-585 DOI 10.1016/j.ijantimicag.2015.03.001.
31. Rasmussen TB, Givskov M. 2006. Quorum sensing inhibitors: a bargain of effects. Microbiology 152:895-904 DOI 10.1099/mic.0.28601-0.
32. Rutherford ST, Bassler BL. 2012. Bacterial quorum sensing: its role in virulence and possibilities for its control. Cold Spring Harbor Perspectives in Medicine 2:a012427.
33. Saroj SD, Rather PN. 2013. Streptomycin inhibits quorum sensing in Acineto-bacter baumannii. Antimicrobial Agents and Chemotherapy 57:1926-1929 DOI 10.1128/AAC.02161-12.
34. Stiernagle T. 1999. Maintenance of C. elegans. C Elegans 2:51-67.
35. Tang K, Su Y, Brackman G, Cui F, Zhang Y, Shi X, Coenye T, Zhang X-H. 2015. MomL, a novel marine-derived N-acyl homoserine lactonase from Muricauda olearia. Applied and Environmental Microbiology 81:774-782 DOI 10.1128/AEM.02805-14.
36. Tang K, Zhang X-H. 2014. Quorum quenching agents: resources for antivirulence therapy. Marine Drugs 12:3245-3282 DOI 10.3390/md12063245.
37. Tang K, Zhang Y, Yu M, Shi X, Coenye T, Bossier P, Zhang X-H. 2013. Evaluation of a new high-throughput method for identifying quorum quenching bacteria. Scientific Reports 3:2935.
38. Tempé J, Petit A, Holsters M, Van Montagu M, Schell J. 1977. Thermosensitive step associated with transfer of the Ti plasmid during conjugation: possible relation to transformation in crown gall. Proceedings of the National Academy of Sciences of the United States of America 74:2848-2849 DOI 10.1073/pnas.74.7.2848.
39. Williams P, Winzer K, Chan WC, Camara M. 2007. Look who's talking: communication and quorum sensing in the bacterial world. Philosophical Transactions of the Royal Society B: Biological Sciences 362:1119-1134 DOI 10.1098/rstb.2007.2039.
40. Wu H, Song Z, Hentzer M, Andersen JB, Molin S, Givskov M, Høiby N. 2004. Syn-thetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseu-domonas aeruginosa lung infection in mice. Journal of Antimicrobial Chemotherapy 53:1054-1061 DOI 10.1093/jac/dkh223.
41. Yin H, Deng Y, Wang H, Liu W, Zhuang X, Chu W. 2015. Tea polyphenols as an antivir-ulence compound disrupt quorum-sensing regulated pathogenicity of Pseudomonas aeruginosa. Scientific Reports 5:16158 DOI 10.1038/srep16158.
42. Zhu J, Beaber JW, Moré MI, Fuqua C, Eberhard A, Winans SC. 1998. Analogs of the autoinducer 3-oxooctanoyl-homoserine lactone strongly inhibit activity of the TraR protein of Agrobacterium tumefaciens. Journal of Bacteriology 180:5398-5405.