Clove bud oil reduces kynurenine and inhibits pqs A gene expression in P. aeruginosa

详细信息    查看全文

• 作者：Jayalekshmi H. ; Athira Omanakuttan…
• 关键词：Quorum sensing ; P. aeruginosa ; Biofilm ; Clove bud oil
• 刊名：Applied Microbiology and Biotechnology
• 出版年：2016
• 出版时间：April 2016
• 年：2016
• 卷：100
• 期：8
• 页码：3681-3692
• 全文大小：853 KB
• 参考文献：Adonizio AL, Kong KF, Mathee K (2008) Inhibition of quorum sensing controlled virulence factor production in P. aeruginosa by South Florida plant extract. Antimicrob Agents Chemother 52:198–203. doi:10.​1128/​AAC.​00612-0 CrossRef PubMed PubMedCentral
  Aliaga L, Mediavilla JD, Cobo F (2002) A clinical index predicting mortality with P.aeruginosa bacteraemia. J Med Microbiol 51:615–661. doi:10.​1099/​0022-1317-51-7-615 CrossRef PubMed
  Bacalso M, Xu T, Yeung K, Zheng D (2011) Biofilm formation of P. aeruginosa PA14 required lasI and was stimulated by the Pseudomonas quinolone signal although salicylic acid inhibition is independent of the PQS pathway. J Exp Microbiol Immun 15:84–89
  Bhowmik D, Sampathkumar KP, Yadav A, Srivastava S, Paswan S, Dutta A (2012) Recent trends in Indian traditional herb Syzygium aromaticum and its health benefits. J Pharmacogn Phytochem 1(1):13–22
  Cady NC, McKean KA, Behnke J, Kubec R, Mosier AP, Stephen H, Kasper SH, Burz DS, Musah RA (2012) Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds. PLoS One 7(6):e38492. doi:10.​1371/​journal.​pone.​0038492 CrossRef PubMed PubMedCentral
  Calfee MW, Coleman JP, Pesci EC (2001) Interference with Pseudomonas quinolone signal synthesis inhibits virulence factor expression by P. aeruginosa. Proc Natl Acad Sci U S A 98:11633–11637. doi:10.​1073/​pnas.​201328498 CrossRef PubMed PubMedCentral
  Chaieb K, Hajlaoui H, Zmantar T, Kahla-Nakbi AB, Rouabhia M, Mahdouani K, Bakhrouf A (2007) The chemical composition and biological activity of clove essential oil, Eugenia caryophyllata (Syzigium aromaticum L. Myrtaceae): a short review. Phyother Res 21:501–506. doi:10.​1002/​ptr 2124 CrossRef
  Das T, Manefield M (2012) Pyocyanin promotes extracellular DNA release in P. aeruginosa. PLoS ONE 7(10):e46718. doi:10.​1371/​journal.​pone.​0046718 CrossRef PubMed PubMedCentral
  Das T, Kutty SK, Kumar N, Manefield M (2013) Pyocyanin facilitates extracellular DNA binding to P. aeruginosa influencing cell surface properties and aggregation. PLoS ONE 8(3):e58299. doi:10.​1371/​journal.​pone.​0058299 CrossRef PubMed PubMedCentral
  Farrow JM III, Pesci EC (2007) Two distinct pathways supply anthranilate as a precursor of the Pseudomonas quinolone signal. J Bacteriol 189(9):3425–3433. doi:10.​1128/​JB.​00209-07 CrossRef PubMed PubMedCentral
  Genestet C, Gouellec AL, Chaker H, Polack B, Guery B, Toussaint B, Stasia MJ (2014) Scavenging of reactive oxygen species by tryptophan metabolites help P. aeruginosa escape neutrophil killing. Free Radic Biol Med 73:400–410. doi:10.​1016/​j.​freeradbiomed.​2014.​06.​003 CrossRef PubMed
  Gloag ES, TurnbullL HA, Vallotton P, Wang H, Nolan M, Mililli L, Hunt C, Lu J, Osvath SR, Monahan LG, Cavaliere R, Charles GI, Wand MP, Gee ML, Prabhakar R, Whitchurch CB (2013) Self-organization of bacterial biofilms is facilitated by extracellular DNA. Proc Natl Acad Sci U S A 110(28):11541–11546. doi:10.​1073/​pnas.​1218898110 CrossRef PubMed PubMedCentral
  Heeb S, Fletcher MP, Chhabra SR, Diggle SP, Williams P, Cámara M (2011) Quinolones from antibiotics to autoinducers. FEMS Microbiol Rev 35:247–274. doi:10.​1111/​j.​1574-6976.​2010.​00247 CrossRef PubMed PubMedCentral
  Jimenez PN, Koch G, Thompson JA, Xavier KB, Cool RH (2012) The multiple signalling systems regulating virulence in Pseudomonas aeruginosa. Microbiol Mol Biol Rev 76:46–65. doi:10.​1128/​MMBR.​05007-11 CrossRef PubMed
  Johnansson EM, Cruz SA, Kolomiets E, Buts L, Kadam RU, Cacciarini M, Bartels KM, Diggle SP, Camara M, Williams P, Loris R, Nativi C, Rosenau F, Jaeger KE, Darbre T, Reymond JL (2008) Inhibition and dispersion of P.aeruginosa biofilm by glycopeptide dendrimers targeting the fucose—specific lectin LecB. Chem Biol 15:1249–1257. doi:10.​1016/​j.​chembiol.​2008.​10.​009 CrossRef
  Kay E, Humair B, De’nervaud V, Riedel K, Spahr S, Eberl L, Valverde C, Haas D (2006) Two GacA-dependent small RNAs modulate the quorum sensing response in P. aeruginosa. J Bacteriol 188:6026–6033. doi:10.​1128/​JB.​00409-06 CrossRef PubMed PubMedCentral
  Kim HS, Lee SH, Byun Y, Park HD (2015) 6-Gingerol reduces P. aeruginosa biofilm formation and virulence via quorum sensing inhibition. Sci Rep 5:8656. doi:10.​1038/​srep08656/​srep08656 CrossRef PubMed PubMedCentral
  Klausen M, Heydorn A, Ragas P, Lambertsen L, Aaes-Jørgensen A, Molin S, Tolker-Nielsen T (2003) Biofilm formation by P. aeruginosa wild type, flagella and type IV pili mutants. Mol Microbiol 48:1511–1524. doi:10.​1046/​j.​1365-2958.​2003.​03525 CrossRef PubMed
  Kruczek C, Qaisar U, Colmer-Hamood JA, Hamood AN (2014) Serum influences the expression of P.aeruginosa quorum sensing genes and QS-controlled virulence genes during early and late stages of growth. MicrobiologyOpen 3(1):64–79. doi:10.​1002/​mbo3.​147 CrossRef PubMed PubMedCentral
  Köhler T, Curty LK, Barja F, van Delden C, Pechère J-C (2000) Swarming of P. aeruginosa is dependent on cell-to-cell signalling and requires flagella and pili. J Bacteriol 182(21):5990–5996. doi:10.​1128/​JB.​182.​21.​5990-5996.​2000 CrossRef PubMed PubMedCentral
  Liang H, Duan J, Sibley CD, Surette MG, Duan K (2011) Identification of mutants with altered phenazine production in P. aeruginosa. J Med Microbiol 60(1):22–34. doi:10.​1099/​jmm.​0.​022350-0 CrossRef PubMed
  Mahady GB (2005) Medicinal plants for the prevention and treatment of bacterial infections. Curr Pharm Des 11:2405–2427CrossRef PubMed
  Marketon MM, Glenn SA, Eberhard A, González JE (2003) Quorum sensing controls exopolysaccharide production in Sinorhizobium mliloti. J Bacteriol 185(1):325–331. doi:10.​1128/​JB CrossRef PubMed PubMedCentral
  Matsukawa M, Greenberg EP (2004) Putative exopolysaccharide synthesis genes influence P. aeruginosa biofilm development. J Bacteriol 186(14):4449–4456. doi:10.​1128/​JB.​186.​14.​4449-4456.​2004 CrossRef PubMed PubMedCentral
  Mavrodi DV, Bonsall RF, Delaney SM, Soule MJ, Phillips G, Thomashow LS (2001) Functional analysis of genes for biosynthesis of pyocyanin and phenazine-1-carboxamide from P. aeruginosa PAO1. J Bacteriol 183:6454–6465. doi:10.​1128/​JB.​183.​21.​6454-6465.​2001 CrossRef PubMed PubMedCentral
  Meynard JL, Barbut F, Guiguet M, Batisse D, Lalande V, Lesage D, Guiard-Schmid JB, Petit JC, Frottier J, Meyohas MC (1999) Pseudomonas aeruginosa infection in human immunodeficiency virus infected patients. J Infect 38:176–181CrossRef PubMed
  Myska K, Czaczk K (2009) Characterization of adhesive exopolysacchride (EPS) produced by P. aeruginosa under starvation conditions. Current Microbiol 58(6):541–546. doi:10.​1007/​s00284-009-9365-3 CrossRef
  Nanjan P, Nambiar J, Nair BG, Banerji (2015) Synthesis and discovery of (I-3, II-3) -biacacetin as a novel non-zinc binding inhibitor of MMP-2 and MMP-9. Bioorg Med Chem 23:3781–3787. doi:10.​1016/​j.​bmc.​2015.​03.​084 CrossRef PubMed
  Nataraj N, Anjusree GS, Madhavan AA, Priyanka P, Sankar D, Nisha N, Lakshmi SV, Jayakumar R, Balakrishnan A, Biswas R (2013) Synthesis and anti-staphylococcal activity of TiO2 nanoparticles and nanowires in ex vivo porcine skin model. J Biomed Nanotechnol 9:1–7. doi:10.​1166/​jbn.​2013.​1756 CrossRef
  Oh J, Lee NR, Jo W, Jung WK, Lim JS (2009) Effects of substrates on biofilm formation observed by atomic force microscopy. Ultramicroscopy 109:874–880. doi:10.​1016/​j.​ultramic.​2009.​03.​042 CrossRef PubMed
  Oncul O, Ulkur E, Acar A (2009) Prospective analysis of nosocomial infections in a burn care unit, Turkey. Indian J Med Res 130:758–764PubMed
  Pesci EC, Pearson JP, Seed PC (1997) Regulation of las and rhl quorum sensing in P. aeruginosa. J Bacteriol 179:3127–3132PubMed PubMedCentral
  Quave CL, Planto LR, Pantuso T, Bennet BL (2008) Effect of Italian medicinal plants on planktonic growth, biofilm formation and adherence of methicillin resistant S. aureus. J Ethanopharmacol 118(3):418–428. doi:10.​1016/​j.​jep.​2008.​05.​005 CrossRef
  Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of P. aeruginosa. Proc Natl Acad Sci USA 97:4885–4890. doi:10.​1073/​pnas.​060030097 CrossRef PubMed PubMedCentral
  Rumbaugh KP, Griswold JA, Hamood AN (2000) The role of quorum sensing in in vivo virulence of Pseudomonas aeruginosa. Microbes Infect 2(14):1721–1731. doi:10.​1016/​S1286-4579(00)01327-7 CrossRef PubMed
  Sanlin JR, Lemos M, Klein-Junior LC, Machado ID, Costa P, de Oliveira AP, Tilia C, de Souza JP, Bastos JK, de Andrade SF (2011) Gatroprotective activity of essential oil of Syzygium aromaticum and its major component eugenol in different animal models. Naunyn Schmiedeberg’s Arch Pharmacol 383(2):149–159. doi:10.​1007/​ 5002-010-2582 CrossRef
  Serate J, Roberts GP, Berg O, Youn H (2011) Ligand responses of Vfr, the virulence factor regulator from P. aeruginosa. J Bacteriol 193:4859–4868. doi:10.​1128/​JB.​00352-11 CrossRef PubMed PubMedCentral
  Shaaban HAE, Ei-Ghorab AH, Shibamoto T (2012) Bioactivity of essential oils and their volatile aroma compounds: review. J Essent Oil Res 24(2):203–212CrossRef
  Stintzi A, Evans K, Meyer JM, Poole K (1998) Quorum-sensing and siderophore biosynthesis in P. aeruginosa lasR/lasI mutants exhibit reduced pyoverdine biosynthesis. FEMS Microbiol Lett 166:341–345CrossRef PubMed
  Szabó MA, Varga GZ, Hohmann J, Schelz Z, Szegedi E, Amaral L, Molnár J (2010) Inhibition of quorum-sensing signals by essential oils. Phytother Res 24:782–786. doi:10.​1002/​ptr.​3010 CrossRef PubMed
  Tamma PD, Cosgrove SE, Maragakis LL (2012) Combination therapy for treatment of infections with Gram-negative bacteria. Clin Microbiol Rev 25(3):450–470. doi:10.​1128/​CMR.​05041-11 CrossRef PubMed PubMedCentral
  Thenmozhi R, Nithyanand P, Rathna J, Pandian SK (2009) Antibiofilm activity of coral associated bacteria against different clinical M serotypes of Streptococcus pyogenes. FEMS Immunol Med Microbiol 57:284–294. doi:10.​1111/​j.​1574-695X.​2009.​00613.​x CrossRef PubMed
  Venturi V (2006) Regulation of quorum sensing in Pseudomonas. FEMS Microbiol Rev 30:274–291CrossRef PubMed
  Wei Q, Tarighi S, Dötsch A, Häussler S, Müsken M, Wright VJ, Cámara M, Williams P, Haenen S, Boerjan B, Bogaerts A, Vierstraete E, Verleyen P, Schoofs L, Willaert R, De Groote VN, Michiels J, Vercammen K, Crabbé A, Cornelis P (2011) Phenotypic and genome-wide analysis of an antibiotic-resistant small colony variant (SCV) of P. aeruginosa. PLoS One 6(12):e29276. doi:10.​1371/​journal.​pone.​0029276 CrossRef PubMed PubMedCentral
  Wei Q, Ma LZ (2013) Biofilm matrix and its regulation in P. aeruginosa. Int J Mol Sci 14(10):20983–21005. doi:10.​3390/​ijms141020983 CrossRef PubMed PubMedCentral
  Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen (2007) Effect of iron on DNA release and biofilm development in P. aeruginosa. Microbiology 153:1318–1328. doi:10.​1099/​mic.​0.​2006/​004911-0 CrossRef PubMed
  Yang L, Nilsson M, Gjermansen M, Givskov M, Tolker-Nielsen T (2009) Pyoverdine and PQS mediated subpopulation interactions involved in P. aeruginosa biofilm. Mol Microbiol 74(6):1380–1392. doi:10.​1111/​j.​1365-2958.​2009.​06934.​x CrossRef PubMed
  Yang Q, Phillips PL, Sampson EM, Progulske-Fox A, Jin S, Antonelli P, Schultz GS (2013) Development of a novel ex vivo porcine skin explant model for the assessment of mature bacterial biofilms. Wound Repair Regen 21:704–714. doi:10.​1111/​wrr.​12074 CrossRef PubMed
  Yildis HF, Schoolnik GK (1999) Vibrio cholerae O1 El Tor: identification of a gene cluster required for the rugose colony type, exopolysaccharide production, chlorine resistance, and biofilm formation. Proc Natl Acad Sci U S A 96:4028–4033CrossRef
  Zhang YM, Frank MW, Zhu K, Mayasundari A, Rock CO (2008) PqsD is responsible for the synthesis of 2, 4-dihydroxyquinoline, an extracellular metabolite produced by P. aeruginosa. J Biol Chem 283:28788–28794. doi:10.​1074/​jbc.​M804555200 CrossRef PubMed PubMedCentral
  
• 作者单位：Jayalekshmi H. (1)
  Athira Omanakuttan (1)
  N. Pandurangan (1)
  Vidhu S. Vargis (2)
  M. Maneesh (3)
  Bipin G. Nair (1)
  Geetha B. Kumar (1)
  
  1. Amrita School of Biotechnology, Amrita Vishwa Vidyapeetham, Clappana P. O, Kollam, Kerala, 690525, India
  2. Department of Sciences, Amrita Vishwa Vidyapeetham, Amritanagar P. O, Coimbatore, 641112, India
  3. Pushpagiri Institute of Medical Sciences and Research Centre, Tiruvalla, Kerala, 689101, India
  
• 刊物类别：Chemistry and Materials Science
• 刊物主题：Chemistry
  Biotechnology
  Microbiology
  Microbial Genetics and Genomics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0614

文摘

Quorum sensing (QS), a communication system involved in virulence of pathogenic bacteria like Pseudomonas aeruginosa is a promising target to combat multiple drug resistance. In vitro studies using clove bud oil (CBO) in P. aeruginosa revealed a concentration dependent attenuation of a variety of virulence factors including motility, extracellular DNA, exopolysaccharides and pigment production. Furthermore, treatment with CBO demonstrated a distinct dose-dependent reduction in biofilm formation as well as promoting dispersion of already formed biofilm, observations that were also supported by porcine skin ex vivo studies. Expression studies of genes involved in signalling systems of P. aeruginosa indicated a specific decrease in transcription of pqsA, but not in the lasI or rhlI levels. Additionally, the expression of vfr and gacA genes, involved in regulation, was also not affected by CBO treatment. CBO also influenced the PQS signalling pathway by decreasing the levels of kynurenine, an effect which was reversed by the addition of exogenous kynurenine. Though the synthesis of the signalling molecules of the Las and Rhl pathways was not affected by CBO, their activity was significantly affected, as observed by decrease in levels of their various effectors. Molecular modelling studies demonstrated that eugenol, the major component of CBO, favourably binds to the QS receptor by hydrophobic interactions as well as by hydrogen bonding with Arg61 and Tyr41 which are key amino acid residues of the LasR receptor. These results thus elucidate the molecular mechanism underlying the action of CBO and provide the basis for the identification of an attractive QS inhibitor.