Human probiotic bacteria attenuate Pseudomonas aeruginosa biofilm and virulence by quorum-sensing inhibition

References

• Alexandre Y, Le Berre R, Barbier G, Le Blay G. 2014. Screening of Lactobacillus spp. for the prevention of Pseudomonas aeruginosa pulmonary infections. BMC Microbiol. 14:107–117. doi:10.1186/1471-2180-14-107
   PubMed Web of Science ®Google Scholar
• Amaya S, Pereira JA, Borkosky SA, Valdez JC, Bardon A, Arena ME. 2012. Inhibition of quorum sensing in Pseudomonas aeruginosa by sesquiterpene lactones. Phytomedicine. 19:1173–1177. doi:10.1016/j.phymed.2012.07.003
   PubMed Web of Science ®Google Scholar
• Aragón F, Carino S, Perdigón G, De Moreno de LeBlanc A. 2015. Inhibition of growth and metastasis of breast cancer in mice by milk fermented with Lactobacillus casei CRL 431. J Immunother. 38:185–196. doi:10.1097/CJI.0000000000000079
   PubMed Web of Science ®Google Scholar
• Bofinger MR, De Sousa LS, Fontes JEN, Marsaioli AJ. 2017. Diketopiperazines as cross-communication quorum-sensing signals between Cronobacter sakazakii and Bacillus cereus. ACS Omega. 2:1003–1008. doi:10.1021/acsomega.6b00513
   PubMed Web of Science ®Google Scholar
• Campbell J, Lin Q, Geske GD, Blackwell HE. 2009. New and unexpected insights into the modulation of LuxR-type quorum sensing by cyclic dipeptides. ACS Chem Biol. 4:1051–1059. doi:10.1021/cb900165y
   PubMed Web of Science ®Google Scholar
• Castillo-Juarez I, Garcia-Contreras R, Velázquez-Guadarrama N, Soto-Hernandez M, Martinez-Vazquez M. 2013. Amphypterygium adstringens anacardic acid mixture inhibits quorum sensing-controlled virulence factors of Chromobacterium violaceum and Pseudomonas aeruginosa. Arch Med Res. 44:488–494. doi:10.1016/j.arcmed.2013.10.004
   PubMed Web of Science ®Google Scholar
• Ceresa C, Tessarolo F, Caola I, Nollo G, Cavallo M, Rinaldi M, Fracchia L. 2015. Inhibition of Candida albicans adhesion on medical-grade silicone by a Lactobacillus-derived biosurfactant. J Appl Microbiol. 118:1116–1125. doi:10.1111/jam.12760
   PubMed Web of Science ®Google Scholar
• Cheng G, Hao H, Xie S, Wang X, Dai M, Huang L, Yuan Z. 2014. Antibiotic alternatives: the substitution of antibiotics in animal husbandry? Front Microbiol. 5:217. doi:10.3389/fmicb.2014.00217
   PubMed Web of Science ®Google Scholar
• Degrassi G, Aguilar C, Bosco M, Zahariev S, Pongor S, Venturi V. 2002. Plant growth-promoting Pseudomonas putida WCS358 produces and secretes four cyclic dipeptides: cross-talk with quorum sensing bacterial sensors. Curr Microbiol. 45:250–254. doi:10.1007/s00284-002-3704-y
   PubMed Web of Science ®Google Scholar
• Eickhoff MJ, Bassler BL. 2018. SnapShot: bacterial quorum sensing. Cell. 174:1328–1328e1. doi:10.1016/j.cell.2018.08.003
   PubMed Web of Science ®Google Scholar
• El-Gendy BEM, Rateb ME. 2015. Antibacterial activity of diketopiperazines isolated from a marine fungus using t-butoxycarbonyl group as a simple tool for purification. Bioorg Med Chem Lett. 25:3125–3128. doi:10.1016/j.bmcl.2015.06.010
   PubMed Web of Science ®Google Scholar
• González SN, Cardozo R, Apella MC, Oliver G. 1994. Biotherapeutic role of fermented milk. Biotherapy. 8:129–134. doi:10.1007/BF01878496
   PubMedGoogle Scholar
• Hansen MR, Jakobsen TH, Bang CG, Cohrt AE, Hansen CL, Clausen JW, Le Quement ST, Tolker-Nielsen T, Givskov M, Nielsen TE. 2015. Triazole-containing N-acyl homoserine lactones targeting the quorum sensing system in Pseudomonas aeruginosa. Bioorg Med Chem. 23:1638–1650. doi:10.1016/j.bmc.2015.01.038
   PubMed Web of Science ®Google Scholar
• Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, et al. 2014. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 11:506–514. doi:10.1038/nrgastro.2014.66
   PubMed Web of Science ®Google Scholar
• Jadhav S, Shah R, Bhave M, Palombo EA. 2013. Inhibitory activity of yarrow essential oil on Listeria planktonic cells and biofilms. Food Control. 29:125–130. doi:10.1016/j.foodcont.2012.05.071
   Web of Science ®Google Scholar
• Kanjan P, Hongpattarakere T. 2016. Antibacterial metabolites secreted under glucose-limited environment of the mimicked proximal colon model by lactobacilli abundant in infant feces. Appl Microbiol Biotechnol. 100:7651–7664. doi:10.1007/s00253-016-7606-5
   PubMed Web of Science ®Google Scholar
• Kariminik A, Baseri-Salehi M, Kheirkhah B. 2017. Pseudomonas aeruginosa quorum sensing modulates immune responses: an updated review article. Immunol Lett. 190:1–6. doi:10.1016/j.imlet.2017.07.002
   PubMed Web of Science ®Google Scholar
• Kumar L, Chhibber S, Kumar R, Kumar M, Harjai K. 2015. Zingerone silences quorum sensing and attenuates virulence of Pseudomonas aeruginosa. Fitoterapia. 102:84–95. doi:10.1016/j.fitote.2015.02.002
   PubMed Web of Science ®Google Scholar
• Kumar SN, Mohandas C, Siji JV, Rajasekharan KN, Nambisan B. 2012. Identification of antimicrobial compound, diketopiperazines, from a Bacillus sp. N strain associated with a rhabditid entomopathogenic nematode against major plant pathogenic fungi. J Appl Microbiol. 113:914–924. doi:10.1111/j.1365-2672.2012.05385.x
   PubMed Web of Science ®Google Scholar
• Li X, Dobretsov S, Xu Y, Xiao X, Hung OS, Qian P. 2006. Antifouling diketopiperazines produced by a deepsea bacterium, Streptomyces fungicidicus. Biofouling. 22:187–194. doi:10.1080/08927010600780771
   PubMed Web of Science ®Google Scholar
• Li J, Wang W, Xu SX, Magarvey NA, McCormick JK. 2011. Lactobacillus reuteri-produced cyclic dipeptides quench agr-mediated expression of toxic shock syndrome toxin-1 in staphylococci. Proc Natl Acad Sci Usa. 108:3360–3365. doi:10.1073/pnas.1017431108
   PubMed Web of Science ®Google Scholar
• Livermore D. 2004. Can better prescribing turn the tide of resistance? Nat Rev Microbiol. 2:73–78. doi:10.1038/nrmicro798
   PubMed Web of Science ®Google Scholar
• Lu C, Maurer CK, Kirsch B, Steinbach A, Hartmann RW. 2014. Overcoming the unexpected functional inversion of a PqsR antagonist in Pseudomonas aeruginosa: an in vivo potent antivirulence agent targeting pqs quorum sensing. Angew Chem Int Ed Engl. 53:1109–1112. doi:10.1002/anie.201307547
   PubMed Web of Science ®Google Scholar
• Luciardi MC, Blázquez MA, Alberto MR, Cartagena E, Arena ME. 2020. Grapefruit essential oils inhibit quorum sensing of Pseudomonas aeruginosa. Food Sci Technol Int. 26:231–241. doi:10.1177/1082013219883465
   PubMed Web of Science ®Google Scholar
• Luciardi MC, Blázquez MA, Cartagena E, Bardón A, Arena ME. 2016. Mandarin essential oils inhibit quorum sensing and virulence factors of Pseudomonas aeruginosa. LWT - Food Sci Technol. 68:373–380. doi:10.1016/j.lwt.2015.12.056
   Web of Science ®Google Scholar
• Marcinkevicius K, Salvatore SA, Bardón A, Cartagena E, Arena ME, Vera NR. 2017. Insecticidal activities of diketopiperazines of Nomuraea rileyi entomopathogenic fungus. IJEAB. 2:1586–1596. doi:10.22161/ijeab/2.4.18
   Google Scholar
• Marrez DA, Abdel-Rahman GN, Salem SH. 2019. Evaluation of Pseudomonas fluorescens extracts as biocontrol agents against some foodborne microorganisms. Jordan J Biol Sci. 12:535–541.
   Google Scholar
• McClean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, Lamb JH, Swift S, Bycroft BW, et al. 1997. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology. 143:3703–3711. doi:10.1099/00221287-143-12-3703
   PubMed Web of Science ®Google Scholar
• McLean RJC, Pierson LS, Fuqua C. 2004. A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods. 58:351–360. doi:10.1016/j.mimet.2004.04.016
   PubMed Web of Science ®Google Scholar
• Medellin-Pena MJ, Wang H, Johnson R, Anand S, Griffiths MW. 2007. Probiotics affect virulence-related gene expression in Escherichia coli O157:H7. Appl Environ Microbiol. 73:4259–4267. doi:10.1128/AEM.00159-07
   PubMed Web of Science ®Google Scholar
• Molina RDI, Campos-Silva R, Macedo AJ, Blázquez MA, Alberto MR, Arena ME. 2020. Antibiofilm activity of coriander (Coriander sativum L.) grown in Argentina against food contaminants and human pathogenic bacteria. Ind Crops Prod. 151:112380. doi:10.1016/j.indcrop.2020.112380
   Web of Science ®Google Scholar
• Musthafa KS, Sivamaruthi BS, Pandian SK, Ravi AV. 2012. Quorum sensing inhibition in Pseudomonas aeruginosa PAO1 by antagonistic compound phenylacetic acid. Curr Microbiol. 65:475–480. doi:10.1007/s00284-012-0181-9
   PubMed Web of Science ®Google Scholar
• O'Malley YQ, Reszka KJ, Rasmussen GT, Abdalla MY, Denning GM, Britigan BE. 2003. The Pseudomonas secretory product pyocyanin inhibits catalase activity in human lung epithelial cells. Am J Physiol Lung Cell Mol Physiol. 285:L1077–1086. doi:10.1152/ajplung.00198.2003
   PubMed Web of Science ®Google Scholar
• O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol. 28:449–461. doi:10.1046/j.1365-2958.1998.00797.x
   PubMed Web of Science ®Google Scholar
• Pachori P, Gothalwal R, Gandhi P. 2019. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis. 6:109–119. doi:10.1016/j.gendis.2019.04.001
   PubMed Web of Science ®Google Scholar
• Pang Z, Raudonis R, Glick BR, Lin TJ, Cheng Z. 2019. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and alternative therapeutic strategies. Biotechnol Adv. 37:177–192. doi:10.1016/j.biotechadv.2018.11.013
   PubMed Web of Science ®Google Scholar
• Parasuraman P, Devadatha B, Sarma VV, Ranganathan S, Ampasala DR, Siddhardha B. 2020. Anti-quorum sensing and antibiofilm activities of Blastobotrys parvus PPR3 against Pseudomonas aeruginosa PAO1. Microb Pathog. 138:103811. doi:10.1016/j.micpath.2019.103811  
   PubMed Web of Science ®Google Scholar
• Park DK, Lee KE, Baek CH, Kim IH, Kwon JH, Lee WK, Lee KH, Kim BS, Choi SH, Kim KS. 2006. Cyclo(Phe-Pro) modulates the expression of ompU in Vibrio spp. J Bacteriol. 188:2214–2221. doi:10.1128/JB.188.6.2214-2221.2006
   PubMed Web of Science ®Google Scholar
• Pattnaik S, Ahmed T, Ranganathan SK, Ampasala DR, Sarma VV, Busi S. 2018. Aspergillus ochraceopetaliformis SSP13 modulates quorum sensing regulated virulence and biofilm formation in Pseudomonas aeruginosa PAO1. Biofouling. 34:410–425. doi:10.1080/08927014.2018.1460748
   PubMed Web of Science ®Google Scholar
• Perdigón G, Maldonado GC, Valdez JC, Medici M. 2002. Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr. 56:S21–S26. doi:10.1038/sj.ejcn.1601658
   PubMed Web of Science ®Google Scholar
• Ramos AN, Sesto Cabral ME, Arena ME, Arrighi CF, Arroyo Aguilar AA, Valdez JC. 2015. Compounds from Lactobacillus plantarum culture supernatants with potential pro-healing and anti-pathogenic properties in skin chronic wounds. Pharm Biol. 53:350–358. doi:10.3109/13880209.2014.920037
   PubMed Web of Science ®Google Scholar
• Rudrappa T, Bais HP. 2008. Curcumin, a known phenolic from Curcuma longa, attenuates the virulence of Pseudomonas aeruginosa PAO1 in whole plant and animal pathogenicity models. J Agric Food Chem. 56:1955–1962. doi:10.1021/jf072591j
   PubMed Web of Science ®Google Scholar
• Schuster M, Greenberg EP. 2006. A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol. 296:73–81. doi:10.1016/j.ijmm.2006.01.036
   PubMed Web of Science ®Google Scholar
• Silva LN, Zimmer KR, Macedo AJ, Trentin DS. 2016. Plant natural products targeting bacterial virulence factors. Chem Rev. 116:9162–9236. doi:10.1021/acs.chemrev.6b00184
   PubMed Web of Science ®Google Scholar
• Srivastava S, Srivastava A, Chandra N, Kumar S. 2017. Antimicrobial metabolites of probiotic bacteria: its properties and diversity. Res Rev Biotechnol Biosci. 4:49–56.
   Google Scholar
• Ström K, Sjögren J, Broberg A, Schnürer J. 2002. Lactobacillus plantarum MiLAB 393 produces the antifungal cyclic dipeptides cyclo(L-Phe-L-Pro) and cyclo(L-Phe-trans-4-OH-L-Pro) and 3-phenyllactic acid . Appl Environ Microbiol. 68:4322–4327. doi:10.1128/aem.68.9.4322-4327.2002
   PubMed Web of Science ®Google Scholar
• Sun S, Dai X, Sun J, Bu X, Weng C, Li H, Zhu HA. 2016. Diketopiperazine factor from Rheinheimera aquimaris QSI02 exhibits anti-quorum sensing activity. Sci Rep. 6:39637. doi:10.1038/srep39637
   PubMed Web of Science ®Google Scholar
• Taylor PK, Yeung AT, Hancock RE. 2014. Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol. 191:121–130. doi:10.1016/j.jbiotec.2014.09.003
   PubMed Web of Science ®Google Scholar
• Viola CM, Torres-Carro R, Cartagena E, Isla MI, Alberto MR, Arena ME. 2018. Effect of wine wastes extracts on the viability and biofilm formation of Pseudomonas aeruginosa and Staphylococcus aureus strains. Evid Based Complement Altern Med. 2018:1–9. doi:10.1155/2018/9526878
   Google Scholar
• Williams P. 2002. Quorum sensing: an emerging target for antibacterial chemotherapy? Expert Opin Ther Targets. 6:257–274. doi:10.1517/14728222.6.3.257
   PubMedGoogle Scholar
• Yadav MK, Chae SW, Go YY, Im GJ, Song JJ. 2017. In vitro multi-species biofilms of methicillin-resistant Staphylococcus aureus and Pseudomonas aeruginosa and their host interaction during in vivo colonization of an otitis media rat model. Front Cell Infect Microbiol. 7:125. doi:10.3389/fcimb.2017.00125
   PubMed Web of Science ®Google Scholar
• Yang EJ, Chang HC. 2010. Purification of a new antifungal compound produced by Lactobacillus plantarum AF1 isolated from kimchi. Int J Food Microbiol. 139:56–63. doi:10.1016/j.ijfoodmicro.2010.02.012
   PubMed Web of Science ®Google Scholar
• Zhang LH. 2003. Quorum quenching and proactive host defense. Trends Plant Sci. 8:238–244. doi:10.1016/S1360-1385(03)00063-3
   PubMed Web of Science ®Google Scholar