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Published in: European Journal of Clinical Microbiology & Infectious Diseases 2/2021

01-02-2021 | Antibiotic | Brief Report

Inhibitory effects of novel 1,4-disubstituted 1,2,3-triazole compounds on quorum-sensing of P. aeruginosa PAO1

Authors: Shuang Li, Yumin Zhang, Kai Jiang, Huiying Wang, Feng Lin

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 2/2021

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Abstract

Quorum sensing (QS) inhibition is an essential strategy to combat bacterial infection. Previously, we have synthesized a series of thymidine derivatives bearing isoxazole and 1,2,3-triazole rings (TITL). Herein, the inhibitory effects of TITL on QS of Pseudomonas aeruginosa PAO1 were evaluated. In vitro results demonstrated that TITL effectively inhibited biofilm formation and reduced the virulence factors of P. aeruginosa PAO1. In combination with antibiotics, our TITL compounds significantly prolonged the lifespans of Caenorhabditis elegans N2 nematodes that were infected with P. aeruginosa PAO1 in vivo. In conclusion, TITL compounds are promising candidates for the treatment of antibiotic-resistant P. aeruginosa PAO1.
Literature
1.
go back to reference Struss AK, Nunes A, Waalen J, Lowery CA, Pullanikat P, Denery JR, Conrad DJ, Kaufmann GF, Janda KD (2013) Toward implementation of quorum sensing autoinducers as biomarkers for infectious disease states. Anal Chem 85(6):3355–3362CrossRef Struss AK, Nunes A, Waalen J, Lowery CA, Pullanikat P, Denery JR, Conrad DJ, Kaufmann GF, Janda KD (2013) Toward implementation of quorum sensing autoinducers as biomarkers for infectious disease states. Anal Chem 85(6):3355–3362CrossRef
2.
go back to reference Chua SL, Yam JK, Hao P, Adav SS, Salido MM, Liu Y, Givskov M, Sze SK, Tolker NT, Yang L (2016) Selective labelling and eradication of antibiotic-tolerant bacterial populations in Pseudomonas aeruginosa biofilms. Nat Commun 7:10750CrossRef Chua SL, Yam JK, Hao P, Adav SS, Salido MM, Liu Y, Givskov M, Sze SK, Tolker NT, Yang L (2016) Selective labelling and eradication of antibiotic-tolerant bacterial populations in Pseudomonas aeruginosa biofilms. Nat Commun 7:10750CrossRef
3.
go back to reference Gholamrezazadeh M, Shakibaie MR, Monirzadeh F, Masoumi S, Hashemizadeh Z (2018) Effect of nano-silver, nano-copper, deconex and benzalkonium chloride on biofilm formation and expression of transcription regulatory quorum sensing gene (rh1R) in drug-resistance Pseudomonas aeruginosa burn isolates. Burns 44(3):700–708CrossRef Gholamrezazadeh M, Shakibaie MR, Monirzadeh F, Masoumi S, Hashemizadeh Z (2018) Effect of nano-silver, nano-copper, deconex and benzalkonium chloride on biofilm formation and expression of transcription regulatory quorum sensing gene (rh1R) in drug-resistance Pseudomonas aeruginosa burn isolates. Burns 44(3):700–708CrossRef
4.
go back to reference Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112(9):1300–1307CrossRef Hentzer M, Givskov M (2003) Pharmacological inhibition of quorum sensing for the treatment of chronic bacterial infections. J Clin Invest 112(9):1300–1307CrossRef
5.
go back to reference Schuster M, Greenberg EP (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296(2–3):73–81CrossRef Schuster M, Greenberg EP (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296(2–3):73–81CrossRef
6.
go back to reference Li H, Li X, Song C, Zhang Y, Wang Z, Liu Z, Wei H, Yu J (2017) Autoinducer-2 facilitates Pseudomonas aeruginosa PAO1 pathogenicity in vitro and in vivo. Front Microbiol 8:1944CrossRef Li H, Li X, Song C, Zhang Y, Wang Z, Liu Z, Wei H, Yu J (2017) Autoinducer-2 facilitates Pseudomonas aeruginosa PAO1 pathogenicity in vitro and in vivo. Front Microbiol 8:1944CrossRef
7.
go back to reference Yin SL, Cang YJ, Deng SP, Wang QC, Yu WG, Gong QH (2011) Research progress of new antibacterial drugs that target bacterial quorum sensing systems. Acta Pharm Sin 46(6):613–621 Yin SL, Cang YJ, Deng SP, Wang QC, Yu WG, Gong QH (2011) Research progress of new antibacterial drugs that target bacterial quorum sensing systems. Acta Pharm Sin 46(6):613–621
8.
go back to reference Zhao M, Yu Y, Hua Y, Feng F, Tong Y, Yang X, Xiao J, Song H (2013) Design, synthesis and biological evaluation of N-sulfonyl homoserine lactone derivatives as inhibitors of quorum sensing in Chromobacterium violaceum. Molecules 18(3):3266–3278CrossRef Zhao M, Yu Y, Hua Y, Feng F, Tong Y, Yang X, Xiao J, Song H (2013) Design, synthesis and biological evaluation of N-sulfonyl homoserine lactone derivatives as inhibitors of quorum sensing in Chromobacterium violaceum. Molecules 18(3):3266–3278CrossRef
9.
go back to reference Barbachyn MR, Cleek GJ, Dolak LA, Garmon SA, Morris J, Seest EP, Thomas RC, Toops DS, Watt W, Wishka DG, Ford CW, Zurenko GE, Hamel JC, Schaadt RD, Stapert D, Yagi BH, Adams WJ, Friis JM, Slatter JG, Sams JP, Oien NL, Zaya MJ, Wienkers LC, Wynalda MA (2003) Identification of phenylisoxazolines as novel and viable antibacterial agents active against gram-positive pathogens. J Med Chem 46(2):284–302CrossRef Barbachyn MR, Cleek GJ, Dolak LA, Garmon SA, Morris J, Seest EP, Thomas RC, Toops DS, Watt W, Wishka DG, Ford CW, Zurenko GE, Hamel JC, Schaadt RD, Stapert D, Yagi BH, Adams WJ, Friis JM, Slatter JG, Sams JP, Oien NL, Zaya MJ, Wienkers LC, Wynalda MA (2003) Identification of phenylisoxazolines as novel and viable antibacterial agents active against gram-positive pathogens. J Med Chem 46(2):284–302CrossRef
10.
go back to reference Ali OM, Amr AEE, Mostafa EE (2014) Synthesis and antimicrobial of some new substituted tetrazolomethylbenzo[d]-[1–3]triazole derivatives using 1Hbenzo[d][1–3]triazole as starting material. Res Chem Intermed 40:1545–1556CrossRef Ali OM, Amr AEE, Mostafa EE (2014) Synthesis and antimicrobial of some new substituted tetrazolomethylbenzo[d]-[1–3]triazole derivatives using 1Hbenzo[d][1–3]triazole as starting material. Res Chem Intermed 40:1545–1556CrossRef
11.
go back to reference Miyakoshi H, Miyahara S, Yokogawa T, Endoh K, Muto T, Yano W, Wakasa T, Ueno H, Chong KT, Taguchi J, Nomura M, Takao Y, Fujioka A, Hashimoto A, Itou K, Yamamura K, Shuto S, Nagasawa H, Fukuoka M (2012) 1,2,3-Triazole-containing uracil derivatives with excellent pharmacokinetics as a novel class of potent human deoxyuridine triphosphatase inhibitors. J Med Chem 55(14):6427–6437CrossRef Miyakoshi H, Miyahara S, Yokogawa T, Endoh K, Muto T, Yano W, Wakasa T, Ueno H, Chong KT, Taguchi J, Nomura M, Takao Y, Fujioka A, Hashimoto A, Itou K, Yamamura K, Shuto S, Nagasawa H, Fukuoka M (2012) 1,2,3-Triazole-containing uracil derivatives with excellent pharmacokinetics as a novel class of potent human deoxyuridine triphosphatase inhibitors. J Med Chem 55(14):6427–6437CrossRef
12.
go back to reference Gupta RA, Kaskhedikar SG (2013) Synthesis, antitubercular activity, and QSAR analysis of substituted nitroaryl analogs: chalcone, pyrazole, isoxazole, and pyrimidines. Med Chem Res 22(8):3863–3880CrossRef Gupta RA, Kaskhedikar SG (2013) Synthesis, antitubercular activity, and QSAR analysis of substituted nitroaryl analogs: chalcone, pyrazole, isoxazole, and pyrimidines. Med Chem Res 22(8):3863–3880CrossRef
13.
go back to reference O’Brien KT, Noto JG, O’Neill LN, Perez LJ (2015) Potent irreversible inhibitors of lasr quorum sensing in Pseudomonas aeruginosa. ACS Med Chem Lett 6(2):162–167CrossRef O’Brien KT, Noto JG, O’Neill LN, Perez LJ (2015) Potent irreversible inhibitors of lasr quorum sensing in Pseudomonas aeruginosa. ACS Med Chem Lett 6(2):162–167CrossRef
14.
go back to reference Igarashi Y, Yamamoto K, Fukuda T, Shojima A, Nakayama J, Carro L, Trujillo ME (2015) Arthroamide, a cyclic depsipeptide with quorum sensing inhibitory activity from arthrobacter sp. J Nat Prod 78(11):2827–2831CrossRef Igarashi Y, Yamamoto K, Fukuda T, Shojima A, Nakayama J, Carro L, Trujillo ME (2015) Arthroamide, a cyclic depsipeptide with quorum sensing inhibitory activity from arthrobacter sp. J Nat Prod 78(11):2827–2831CrossRef
15.
go back to reference Zhang DW, Zhang YM, Li J, Zhao TQ, Gu Q, Lin F (2017) Ultrasonic-assisted synthesis of 1,4-disubstituted 1,2,3 triazoles via various terminal acetylenes and azide and their quorum sensing inhibition. Ultrason Sonochem 36:343–353CrossRef Zhang DW, Zhang YM, Li J, Zhao TQ, Gu Q, Lin F (2017) Ultrasonic-assisted synthesis of 1,4-disubstituted 1,2,3 triazoles via various terminal acetylenes and azide and their quorum sensing inhibition. Ultrason Sonochem 36:343–353CrossRef
16.
go back to reference Peeters E, Nelis HJ, Coenye T (2009) In vitro activity of ceftazidime, ciprofloxacin, meropenem, minocycline, tobramycin and trimethoprim-sulfamethoxazole against planktonic and sessile Burkholderia cepacia complex bacteria. J Antimicrob Chemoth 64(4):801–809CrossRef Peeters E, Nelis HJ, Coenye T (2009) In vitro activity of ceftazidime, ciprofloxacin, meropenem, minocycline, tobramycin and trimethoprim-sulfamethoxazole against planktonic and sessile Burkholderia cepacia complex bacteria. J Antimicrob Chemoth 64(4):801–809CrossRef
17.
go back to reference Guo Q, Wei Y, Xia B, Jin Y, Liu C, Pan X, Shi J, Zhu F, Li J, Qian L, Liu X, Cheng Z, Jin S, Lin J, Wu W (2016) Identification of a small molecule that simultaneously suppresses virulence and antibiotic resistance of Pseudomonas aeruginosa. Sci Rep 6:19141CrossRef Guo Q, Wei Y, Xia B, Jin Y, Liu C, Pan X, Shi J, Zhu F, Li J, Qian L, Liu X, Cheng Z, Jin S, Lin J, Wu W (2016) Identification of a small molecule that simultaneously suppresses virulence and antibiotic resistance of Pseudomonas aeruginosa. Sci Rep 6:19141CrossRef
18.
go back to reference O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30(2):295–304CrossRef O’Toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30(2):295–304CrossRef
19.
go back to reference Essar DW, Eberly L, Hadero A, Crawford IP (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(2):884–900CrossRef Essar DW, Eberly L, Hadero A, Crawford IP (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(2):884–900CrossRef
20.
go back to reference Pearson JP, Pesci EC, Iglewski BH (1997) Roles of Pseudomonas aeruginosa Las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179(18):5756–5767CrossRef Pearson JP, Pesci EC, Iglewski BH (1997) Roles of Pseudomonas aeruginosa Las and rhl quorum-sensing systems in control of elastase and rhamnolipid biosynthesis genes. J Bacteriol 179(18):5756–5767CrossRef
21.
go back to reference Grosso-Becerra MV (2016) Pseudomonas aeruginosa ATCC 9027 is a non-virulent strain suitable for mono-rhamnolipids production. Appl Microbiol Biotechnol 100(23):9995–10004CrossRef Grosso-Becerra MV (2016) Pseudomonas aeruginosa ATCC 9027 is a non-virulent strain suitable for mono-rhamnolipids production. Appl Microbiol Biotechnol 100(23):9995–10004CrossRef
22.
go back to reference Prithiviraj B, Bais HP, Weir T, Suresh B, Najarro EH, Dayakar BV, Schweizer HP, Vivanco JM (2005) Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect Immun 73(9):5319–5328CrossRef Prithiviraj B, Bais HP, Weir T, Suresh B, Najarro EH, Dayakar BV, Schweizer HP, Vivanco JM (2005) Down regulation of virulence factors of Pseudomonas aeruginosa by salicylic acid attenuates its virulence on Arabidopsis thaliana and Caenorhabditis elegans. Infect Immun 73(9):5319–5328CrossRef
23.
go back to reference Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, Kjelleberg S, Givskov M (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148(Pt 1):87–102CrossRef Hentzer M, Riedel K, Rasmussen TB, Heydorn A, Andersen JB, Parsek MR, Rice SA, Eberl L, Molin S, Høiby N, Kjelleberg S, Givskov M (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148(Pt 1):87–102CrossRef
24.
go back to reference Udrappa T, Bais HP (2008) Curcumin, a known phenolic from Curcuma Longa, attenua-tes the virulence of Pseudomonas aeruginosa PAO1 in whole plant and animal pathogenicity models. J Agric Food Chem 56(6):1955–1962CrossRef Udrappa T, Bais HP (2008) Curcumin, a known phenolic from Curcuma Longa, attenua-tes the virulence of Pseudomonas aeruginosa PAO1 in whole plant and animal pathogenicity models. J Agric Food Chem 56(6):1955–1962CrossRef
25.
go back to reference Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 97(9):4885–4890CrossRef Rashid MH, Kornberg A (2000) Inorganic polyphosphate is needed for swimming, swarming, and twitching motilities of Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 97(9):4885–4890CrossRef
26.
go back to reference Tan MW, Mahajan-Miklos S, Ausubel FM (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96(2):715–720CrossRef Tan MW, Mahajan-Miklos S, Ausubel FM (1999) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96(2):715–720CrossRef
27.
go back to reference Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilm. Int J Antimicrob 35(4):322–332CrossRef Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilm. Int J Antimicrob 35(4):322–332CrossRef
28.
go back to reference Gupta RK, Setia S, Harjai K (2011) Expression of quorum sensing and virulence factors are interlinked in Pseudomonas aeruginosa: an in vitro approach. Am J Biomed Sci 3:116–125CrossRef Gupta RK, Setia S, Harjai K (2011) Expression of quorum sensing and virulence factors are interlinked in Pseudomonas aeruginosa: an in vitro approach. Am J Biomed Sci 3:116–125CrossRef
29.
go back to reference Ben Hai Khalifa A, Moissenet D, Vu Thien H, Khedher M (2011) Virulence factors in Pseudomonas aeruginosa: mechanisms and modes of regulation. Ann Biol Clin (Paris) 69(4):393–403 Ben Hai Khalifa A, Moissenet D, Vu Thien H, Khedher M (2011) Virulence factors in Pseudomonas aeruginosa: mechanisms and modes of regulation. Ann Biol Clin (Paris) 69(4):393–403
30.
go back to reference Lee KM, Yoon MY, Park Y, Lee JH, Yoon SS (2011) Anaerobiosis-induced loss of cytotoxicity is due to inactivation of quorum sensing in Pseudomonas aeruginosa. Infect Immun 79(7):2792–2800CrossRef Lee KM, Yoon MY, Park Y, Lee JH, Yoon SS (2011) Anaerobiosis-induced loss of cytotoxicity is due to inactivation of quorum sensing in Pseudomonas aeruginosa. Infect Immun 79(7):2792–2800CrossRef
31.
go back to reference Welsh MA, Eibergen NR, Moore JD, Blackwell HE (2015) Small molecule disruption of quorum sensing cross-regulation in Pseudomonas aeruginosa causes major and unexpected alterations to virulence phenotypes. J Am Chem Soc 137(4):1510–1519CrossRef Welsh MA, Eibergen NR, Moore JD, Blackwell HE (2015) Small molecule disruption of quorum sensing cross-regulation in Pseudomonas aeruginosa causes major and unexpected alterations to virulence phenotypes. J Am Chem Soc 137(4):1510–1519CrossRef
32.
go back to reference Ochsner UA, Reiser J (1995) Autoinducer mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92(14):6424–6428CrossRef Ochsner UA, Reiser J (1995) Autoinducer mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 92(14):6424–6428CrossRef
33.
go back to reference Radji M, Agustama RA, Elya B, Tjampakasari CR (2013) Antimicrobial activity of green tea extract against isolates of methicillin-resistant Staphylococcus aureus and multi-drug resistant Pseudomonas aeruginosa. Asian Pac J Trop Biomed 3(8):663–667CrossRef Radji M, Agustama RA, Elya B, Tjampakasari CR (2013) Antimicrobial activity of green tea extract against isolates of methicillin-resistant Staphylococcus aureus and multi-drug resistant Pseudomonas aeruginosa. Asian Pac J Trop Biomed 3(8):663–667CrossRef
34.
go back to reference Romero R, Schaudinn C, Kusanovic JP, Gorur A, Gotsch F, Webster P, Nhan-Chang CL, Erez O, Kim CJ, Espinoza J, Goncalves LF, Vaisbuch E, Mazaki-Tovi S, Hassan SS, Costerton JW (2008) Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol 198(1):1351–1355CrossRef Romero R, Schaudinn C, Kusanovic JP, Gorur A, Gotsch F, Webster P, Nhan-Chang CL, Erez O, Kim CJ, Espinoza J, Goncalves LF, Vaisbuch E, Mazaki-Tovi S, Hassan SS, Costerton JW (2008) Detection of a microbial biofilm in intraamniotic infection. Am J Obstet Gynecol 198(1):1351–1355CrossRef
35.
go back to reference Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138CrossRef Stewart PS, Costerton JW (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358(9276):135–138CrossRef
36.
go back to reference 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. Antimicrob Agents Ch 55(6):2655–2661CrossRef 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. Antimicrob Agents Ch 55(6):2655–2661CrossRef
Metadata
Title
Inhibitory effects of novel 1,4-disubstituted 1,2,3-triazole compounds on quorum-sensing of P. aeruginosa PAO1
Authors
Shuang Li
Yumin Zhang
Kai Jiang
Huiying Wang
Feng Lin
Publication date
01-02-2021
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 2/2021
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-020-03998-2

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