Recent Breakthroughs in Various Antimicrobial Resistance Induced Quorum Sensing Biosynthetic Pathway Mediated Targets and Design of their Inhibitors

Author(s): Mohit Kumar, Mridula Saxena, Anil K. Saxena*, Sisir Nandi*

Journal Name: Combinatorial Chemistry & High Throughput Screening
Accelerated Technologies for Biotechnology, Bioassays, Medicinal Chemistry and Natural Products Research

Volume 23 , Issue 6 , 2020

Become EABM
Become Reviewer

Abstract:

Objective: The world is under the grasp of dangerous post-antibiotics and antimicrobials attack where common infections may become untreatable, leading to premature deaths due to antimicrobial resistance (AMR). While an estimated 7,00,000 people die annually due to AMR, which is a public health threat to all communities in different parts of the world regardless of their economic status; however, this threat is serious in low- and middle-income countries having lack of sanitation and health infrastructure. The 68th World Health Assembly endorsed the Global Action Plan on antimicrobial resistance. Consequently, many countries started drafting and committing to National Action Plans against AMR. As strong as National Action Plans are in terms of prescribing rational use of antimicrobials, infection control practices, and related public health measures, without strong healthcare systems, these measures will have a limited impact on AMR in developing countries.

Methods: The major reason for AMR is microbial quorum sensing (QS) that may strengthen the microbial community to generate inter-communication and virulence effects via quorum sensing mechanisms. Global stewardship to combat antimicrobial resistance aims to develop anti-quorum sensing compounds that can inhibit the biosynthetic pathway mediated different quorum sensing targets.

Results: It may pave an effective attempt to minimize microbial quorum sensing mediated antimicrobial resistance. The present review describes QS mediated various potential target enzymes, their connection to AMR, and finds out the corresponding QS biosynthetic target inhibitors.

Conclusion: These potential inhibitors can be derivatized to design and develop next-generation antimicrobial agents.

Keywords: Antimicrobial resistance (AMR), quorum sensing (QS), biosynthesis, target enzymes, design of next-generation, anti-QS inhibitors.

[1]
Hinchliffe, S.; Butcher, A.; Rahman, M.M. The AMR problem: demanding economies, biological margins and co-producing alternative strategies. Palgrave Commun., 2018, 4, 142.
[http://dx.doi.org/10.1057/s41599-018-0195-4]
[2]
As antibiotics fail, global consumption of antibiotics skyrockets, further driving drug resistance. https://www.eurekalert.org/pub_releases/2018-03/b-aaf032118.php (Accessed May 23, 2019).
[3]
Nandi, S.; Ahmed, S.; Saxena, A.K. Combinatorial design and virtual screening of potent anti-tubercular fluoroquinolone and isothiazoloquinolone compounds utilizing QSAR and pharmacophore modelling. SAR QSAR Environ. Res., 2018, 29(2), 151-170.
[http://dx.doi.org/10.1080/1062936X.2017.1419375] [PMID: 29347843]
[4]
O’Neill, J. Antimicrobial resistance: Tackling a crisis for the health and wealth of nations; Report, Wellcom Trust, December, 2014.
[5]
Crew, B. New report says antimicrobial resistance will kill 300 million by 2050; Report, 2014.
[6]
Walsh, C. Molecular mechanisms that confer antibacterial drug resistance. Nature, 2000, 406(6797), 775-781.
[http://dx.doi.org/10.1038/35021219] [PMID: 10963607]
[7]
Stewart, P.S.; Costerton, J.W. Antibiotic resistance of bacteria in biofilms. Lancet, 2001, 358(9276), 135-138.
[http://dx.doi.org/10.1016/S0140-6736(01)05321-1] [PMID: 11463434]
[8]
Nandi, S. Recent advances in ligand and structure-based screening of potent quorum sensing inhibitors against antibiotic resistance induced bacterial virulence. Recent Pat. Biotechnol., 2016, 10(2), 195-216.
[http://dx.doi.org/10.2174/1872208310666160728104450] [PMID: 27468815]
[9]
Winzer, K.; Hardie, K.R.; Burgess, N.; Doherty, N.; Kirke, D.; Holden, M.T.G.; Linforth, R.; Cornell, K.A.; Taylor, A.J.; Hill, P.J.; Williams, P. LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy-5-methyl-3(2H)-furanone. Microbiology, 2002, 148(Pt 4), 909-922.
[http://dx.doi.org/10.1099/00221287-148-4-909] [PMID: 11932438]
[10]
Chen, X.; Schauder, S.; Potier, N.; Van Dorsselaer, A.; Pelczer, I.; Bassler, B.L.; Hughson, F.M. Structural identification of a bacterial quorum-sensing signal containing boron. Nature, 2002, 415(6871), 545-549.
[http://dx.doi.org/10.1038/415545a] [PMID: 11823863]
[11]
Bao, Y.; Li, Y.; Jiang, Q.; Zhao, L.; Xue, T.; Hu, B.; Sun, B. Methylthioadenosine/S-adenosylhomocysteine nucleosidase (Pfs) of Staphylococcus aureus is essential for the virulence independent of LuxS/AI-2 system. Int. J. Med. Microbiol., 2013, 303(4), 190-200.
[http://dx.doi.org/10.1016/j.ijmm.2013.03.004] [PMID: 23611628]
[12]
Williams, P. Quorum sensing: an emerging target for antibacterial chemotherapy? Expert Opin. Ther. Targets, 2002, 6(3), 257-274.
[http://dx.doi.org/10.1517/14728222.6.3.257] [PMID: 12223068]
[13]
Jiang, T.; Li, M. Quorum sensing inhibitors: a patent review. Expert Opin. Ther. Pat., 2013, 23(7), 867-894.
[http://dx.doi.org/10.1517/13543776.2013.779674] [PMID: 23506025]
[14]
Otero, C.A.M.; Romero, B.M. Use of the cect 7426 strain for generating quorum quenching of the autoinducer-2 signal (AI-2) WO 2014057151 A1, 2014.
[15]
Dong, Y.H.; Wang, L.H.; Xu, J.L.; Zhang, H.B.; Zhang, X.F.; Zhang, L.H. Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 2001, 411(6839), 813-817.
[http://dx.doi.org/10.1038/35081101] [PMID: 11459062]
[16]
Moré, M.I.; Finger, L.D.; Stryker, J.L.; Fuqua, C.; Eberhard, A.; Winans, S.C. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates. Science, 1996, 272(5268), 1655-1658.
[http://dx.doi.org/10.1126/science.272.5268.1655] [PMID: 8658141]
[17]
Schaefer, A.L.; Val, D.L.; Hanzelka, B.L.; Cronan, J.E., Jr; Greenberg, E.P. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. Proc. Natl. Acad. Sci. USA, 1996, 93(18), 9505-9509.
[http://dx.doi.org/10.1073/pnas.93.18.9505] [PMID: 8790360]
[18]
Schramm, V.L. Methods and compositions for treating bacterial infections by inhibiting quorum sensing, US20110190265A1, 2011.
[19]
Zang, T.; Lee, B.W.; Cannon, L.M.; Ritter, K.A.; Dai, S.; Ren, D.; Wood, T.K.; Zhou, Z.S. A naturally occurring brominated furanone covalently modifies and inactivates LuxS. Bioorg. Med. Chem. Lett., 2009, 19(21), 6200-6204.
[http://dx.doi.org/10.1016/j.bmcl.2009.08.095] [PMID: 19775890]
[20]
Martin, J.L.; McMillan, F.M. SAM (dependent) I AM: the S-adenosylmethionine-dependent methyltransferase fold. Curr. Opin. Struct. Biol., 2002, 12(6), 783-793.
[http://dx.doi.org/10.1016/S0959-440X(02)00391-3] [PMID: 12504684]
[21]
Miller, D.J.; Ouellette, N.; Evdokimova, E.; Savchenko, A.; Edwards, A.; Anderson, W.F. Crystal complexes of a predicted S-adenosylmethionine-dependent methyltransferase reveal a typical AdoMet binding domain and a substrate recognition domain. Protein Sci., 2003, 12(7), 1432-1442.
[http://dx.doi.org/10.1110/ps.0302403] [PMID: 12824489]
[22]
Maravić, G. Macrolide resistance based on the Erm-mediated rRNA methylation. Curr. Drug Targets Infect. Disord., 2004, 4(3), 193-202.
[http://dx.doi.org/10.2174/1568005043340777] [PMID: 15379730]
[23]
Schmidberger, J.W.; James, A.B.; Edwards, R.; Naismith, J.H.; O’Hagan, D. Halomethane biosynthesis: structure of a SAM-dependent halide methyltransferase from Arabidopsis thaliana. Angew. Chem. Int. Ed. Engl., 2010, 49(21), 3646-3648.
[http://dx.doi.org/10.1002/anie.201000119] [PMID: 20376845]
[24]
Yu, F.; Li, M.J.; Xu, C.Y.; Sun, B.; Zhou, H.; Wang, Z.J.; Xu, Q.; Xie, M.Y.; Zuo, G.; Huang, P.; Guo, H.; Wang, Q.S.; He, J.H. Crystal structure of methyltransferase TleD complexed with SAH. Biochem. J., 2016, 473, 4385-4397.
[http://dx.doi.org/10.1042/BCJ20160695] [PMID: 27613858]
[25]
Pioszak, A.A.; Murayama, K.; Nakagawa, N.; Ebihara, A.; Kuramitsu, S.; Shirouzu, M.; Yokoyama, S. Crystal structure of Tt1595, a putative SAM-dependent methyltransferase from Thermus thermophillus HB8. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 2005, 61, 867-874.
[http://dx.doi.org/10.1107/S1744309105029842] [PMID: 16511182]
[26]
Zou, X.; Liu, Y.C.; Hsu, N.S.; Huang, C.J.; Lyu, S.Y.; Chan, H.C.; Chang, C.Y.; Yeh, H.W.; Lin, K.H.; Wu, C.J.; Tsai, M.D.; Li, T.L. Mutant structure of methyltransferase from Streptomyces hygroscopicus complexed with S-adenosyl-L-homocysteine and methylphenylpyruvic acid. Acta Crystallogr. D Biol. Crystallogr., 2014, 70, 1549-1560.
[http://dx.doi.org/10.1107/S1399004714005239] [PMID: 24914966]
[27]
Wang, Y.; Liu, B.; Grenier, D.; Yi, L. Regulatory mechanisms of LuxS/AI-2 System and bacterial resistance. Antimicrob. Agents Chemother., 2019, 63(10), e01186-e19.
[http://dx.doi.org/10.1128/AAC.01186-19] [PMID: 31383657]
[28]
Parveen, N.; Cornell, K.A. Methylthioadenosine/S-adenosyl-homocysteine nucleosidase, a critical enzyme for bacterial metabolism. Mol. Microbiol., 2011, 79(1), 7-20.
[http://dx.doi.org/10.1111/j.1365-2958.2010.07455.x] [PMID: 21166890]
[29]
Rao, R.M.; Pasha, S.N.; Sowdhamini, R. Genome-wide survey and phylogeny of S-Ribosylhomocysteinase (LuxS) enzyme in bacterial genomes. BMC Genomics, 2016, 17(1), 742.
[http://dx.doi.org/10.1186/s12864-016-3002-x] [PMID: 27650568]
[30]
Surette, M.G.; Miller, M.B.; Bassler, B.L. Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. Proc. Natl. Acad. Sci. USA, 1999, 96(4), 1639-1644.
[http://dx.doi.org/10.1073/pnas.96.4.1639] [PMID: 9990077]
[31]
Stroeher, U.H.; Paton, A.W.; Ogunniyi, A.D.; Paton, J.C. Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model. Infect. Immun., 2003, 71(6), 3206-3212.
[http://dx.doi.org/10.1128/IAI.71.6.3206-3212.2003] [PMID: 12761100]
[32]
Burgess, N.A.; Kirke, D.F.; Williams, P.; Winzer, K.; Hardie, K.R.; Meyers, N.L.; Aduse-Opoku, J.; Curtis, M.A.; Cámara, M. LuxS-dependent quorum sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence. Microbiology, 2002, 148(Pt 3), 763-772.
[http://dx.doi.org/10.1099/00221287-148-3-763] [PMID: 11882711]
[33]
Winzer, K.; Sun, Y.H.; Green, A.; Delory, M.; Blackley, D.; Hardie, K.R.; Baldwin, T.J.; Tang, C.M. Role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteremic infection. Infect. Immun., 2002, 70(4), 2245-2248.
[http://dx.doi.org/10.1128/IAI.70.4.2245-2248.2002] [PMID: 11895997]
[34]
Xavier, K.B.; Bassler, B.L. LuxS quorum sensing: more than just a numbers game. Curr. Opin. Microbiol., 2003, 6(2), 191-197.
[http://dx.doi.org/10.1016/S1369-5274(03)00028-6] [PMID: 12732311]
[35]
Xu, L.; Li, H.; Vuong, C.; Vadyvaloo, V.; Wang, J.; Yao, Y.; Otto, M.; Gao, Q. Role of the luxS quorum-sensing system in biofilm formation and virulence of Staphylococcus epidermidis. Infect. Immun., 2006, 74(1), 488-496.
[http://dx.doi.org/10.1128/IAI.74.1.488-496.2006] [PMID: 16369005]
[36]
Yadav, M.K.; Vidal, J.E.; Go, Y.Y.; Kim, S.H.; Chae, S.W.; Song, J.J. The LuxS/AI-2 quorum-sensing system of Streptococcus pneumoniae is required to cause disease, and to regulate virulence- and metabolism-related genes in a rat model of middle ear infection. Front. Cell. Infect. Microbiol., 2018, 8, 138.
[http://dx.doi.org/10.3389/fcimb.2018.00138] [PMID: 29780750]
[37]
Wang, Y.; Yi, L.; Wang, S.; Fan, H.; Ding, C.; Mao, X.; Lu, C. Crystal structure and identification of two key amino acids involved in ai-2 production and biofilm formation in Streptococcus suis LuxS. PLoS One, 2015, 10(10)e0138826
[http://dx.doi.org/10.1371/journal.pone.0138826] [PMID: 26484864]
[38]
Rajan, R.; Zhu, J.; Hu, X.; Pei, D.; Bell, C.E. Crystal structure of S-ribosylhomocysteinase (LuxS) in complex with a catalytic 2-ketone intermediate. Biochemistry, 2005, 44(10), 3745-3753.
[http://dx.doi.org/10.1021/bi0477384] [PMID: 15751951]
[39]
Ruzheinikov, S.N.; Das, S.K.; Sedelnikova, S.E.; Hartley, A.; Foster, S.J.; Horsburgh, M.J.; Cox, A.G.; McCleod, C.W.; Mekhalfia, A.; Blackburn, G.M.; Rice, D.W.; Baker, P.J. The 1.2 A structure of a novel quorum-sensing protein, Bacillus subtilis LuxS. J. Mol. Biol., 2001, 313(1), 111-122.
[http://dx.doi.org/10.1006/jmbi.2001.5027] [PMID: 11601850]
[40]
Lewis, H.A.; Furlong, E.B.; Laubert, B.; Eroshkina, G.A.; Batiyenko, Y.; Adams, J.M.; Bergseid, M.G.; Marsh, C.D.; Peat, T.S.; Sanderson, W.E.; Sauder, J.M.; Buchanan, S.G. A structural genomics approach to the study of quorum sensing: crystal structures of three LuxS orthologs. Structure, 2001, 9(6), 527-537.
[http://dx.doi.org/10.1016/S0969-2126(01)00613-X] [PMID: 11435117]
[41]
Shen, G.; Rajan, R.; Zhu, J.; Bell, C.E.; Pei, D. Design and synthesis of substrate analogue inhibitors of S-ribosyl-homocysteinase (LuxS). J. Med. Chem., 2001, 49(10), 3003-3011.
[http://dx.doi.org/10.1021/jm060047g] [PMID: 16686542]
[42]
Gould, T.A.; Schweizer, H.P.; Churchill, M.E. Structure of the Pseudomonas aeruginosa acyl-homoserinelactone synthase LasI. Mol. Microbiol., 2004, 53(4), 1135-1146.
[http://dx.doi.org/10.1111/j.1365-2958.2004.04211.x] [PMID: 15306017]
[43]
Swem, L.R.; Swem, D.L.; O’Loughlin, C.T.; Gatmaitan, R.; Zhao, B.; Ulrich, S.M.; Bassler, B.L. A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity. Mol. Cell, 2009, 35(2), 143-153.
[http://dx.doi.org/10.1016/j.molcel.2009.05.029] [PMID: 19647512]
[44]
Timmen, M.; Bassler, B.L.; Jung, K. AI-1 influences the kinase activity but not the phosphatase activity of LuxN of Vibrio harveyi. J. Biol. Chem., 2006, 281(34), 24398-24404.
[http://dx.doi.org/10.1074/jbc.M604108200] [PMID: 16807235]
[45]
Jung, K.; Odenbach, T.; Timmen, M. The quorum-sensing hybrid histidine kinase LuxN of Vibrio harveyi contains a periplasmically located N terminus. J. Bacteriol., 2007, 189(7), 2945-2948.
[http://dx.doi.org/10.1128/JB.01723-06] [PMID: 17259316]
[46]
Freeman, J.A.; Lilley, B.N.; Bassler, B.L. A genetic analysis of the functions of LuxN: a two-component hybrid sensor kinase that regulates quorum sensing in Vibrio harveyi. Mol. Microbiol., 2000, 35(1), 139-149.
[http://dx.doi.org/10.1046/j.1365-2958.2000.01684.x] [PMID: 10632884]
[47]
Swem, L.R.; Swem, D.L.; Wingreen, N.S.; Bassler, B.L. Deducing receptor signaling parameters from in vivo analysis: LuxN/AI-1 quorum sensing in Vibrio harveyi. Cell, 2008, 134(3), 461-473.
[http://dx.doi.org/10.1016/j.cell.2008.06.023] [PMID: 18692469]
[48]
Tu, K.C.; Bassler, B.L. Multiple small RNAs act additively to integrate sensory information and control quorum sensing in Vibrio harveyi. Genes Dev., 2007, 21(2), 221-233.
[http://dx.doi.org/10.1101/gad.1502407] [PMID: 17234887]
[49]
Pereira, C.S.; de Regt, A.K.; Brito, P.H.; Miller, S.T.; Xavier, K.B. Identification of functional LsrB-like autoinducer-2 receptors. J. Bacteriol., 2009, 191(22), 6975-6987.
[http://dx.doi.org/10.1128/JB.00976-09] [PMID: 19749048]
[50]
Miller, S.T.; Xavier, K.B.; Campagna, S.R.; Taga, M.E.; Semmelhack, M.F.; Bassler, B.L.; Hughson, F.M. Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2. Mol. Cell, 2004, 15(5), 677-687.
[http://dx.doi.org/10.1016/j.molcel.2004.07.020] [PMID: 15350213]
[51]
Kavanaugh, J.S.; Gakhar, L.; Horswill, A.R. The structure of LsrB from Yersinia pestis complexed with autoinducer-2. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun., 2011, 67(Pt 12), 1501-1505.
[http://dx.doi.org/10.1107/S1744309111042953] [PMID: 22139152]
[52]
Ayukekbong, J.A.; Ntemgwa, M.; Atabe, A.N. The threat of antimicrobial resistance in developing countries: causes and control strategies. Antimicrob. Resist. Infect. Control, 2017, 6, 47.
[http://dx.doi.org/10.1186/s13756-017-0208-x] [PMID: 28515903]
[53]
Zhang, J.; Zheng, Y.G. SAM/SAH Analogs as versatile tools for SAM-dependent methyltransferases. ACS Chem. Biol., 2016, 11(3), 583-597.
[http://dx.doi.org/10.1021/acschembio.5b00812] [PMID: 26540123]
[54]
Dung, T.T.; Yi, Y.S.; Heo, J.; Yang, W.S.; Kim, J.H.; Kim, H.G.; Park, J.G.; Yoo, B.C.; Cho, J.Y.; Hong, S. Critical role of protein L-isoaspartyl methyltransferase in basic fibroblast growth factor-mediated neuronal cell differentiation. BMB Rep., 2016, 49(8), 437-442.
[http://dx.doi.org/10.5483/BMBRep.2016.49.8.020] [PMID: 26973341]
[55]
Borchardt, R.T.; Patel, U.G.; Bartel, R.L. Adenosine dialdehyde: A potent inhibitor of S-adenosylhomocysteine hydrolase. In: Biochemistry of S-Adenosylmethionine and Related Compounds; Usdin, E.; Borchardt, R.T.; Creveling, C.R., Eds.; Palgrave Macmillan: London, 1982; pp. 645-652.
[http://dx.doi.org/10.1007/978-1-349-06343-7_88]
[56]
Miranda, T.B.; Cortez, C.C.; Yoo, C.B.; Liang, G.; Abe, M.; Kelly, T.K.; Marquez, V.E.; Jones, P.A. DZNep is a global histone methylation inhibitor that reactivates developmental genes not silenced by DNA methylation. Mol. Cancer Ther., 2009, 8(6), 1579-1588.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0013] [PMID: 19509260]
[57]
Zheng, W.; Ibáñez, G.; Wu, H.; Blum, G.; Zeng, H.; Dong, A.; Li, F.; Hajian, T.; Allali-Hassani, A.; Amaya, M.F.; Siarheyeva, A.; Yu, W.; Brown, P.J.; Schapira, M.; Vedadi, M.; Min, J.; Luo, M. Sinefungin derivatives as inhibitors and structure probes of protein lysine methyltransferase SETD2. J. Am. Chem. Soc., 2012, 134(43), 18004-18014.
[http://dx.doi.org/10.1021/ja307060p] [PMID: 23043551]
[58]
Devkota, K.; Lohse, B.; Liu, Q.; Wang, M.W.; Stærk, D.; Berthelsen, J.; Clausen, R.P. analogues of the natural product sinefungin as inhibitors of EHMT1 and EHMT2. ACS Med. Chem. Lett., 2014, 5(4), 293-297.
[http://dx.doi.org/10.1021/ml4002503] [PMID: 24900829]
[59]
Avila, M.A.; García-Trevijano, E.R.; Lu, S.C.; Corrales, F.J.; Mato, J.M. Methylthioadenosine. Int. J. Biochem. Cell Biol., 2004, 36(11), 2125-2130.
[http://dx.doi.org/10.1016/j.biocel.2003.11.016] [PMID: 15313459]
[60]
Williams-Ashman, H.G.; Seidenfeld, J.; Galletti, P. Trends in the biochemical pharmacology of 5′-deoxy-5′-methylthioadenosine. Biochem. Pharmacol., 1982, 31(3), 277-288.
[http://dx.doi.org/10.1016/0006-2952(82)90171-X] [PMID: 6803807]
[61]
Wang, S.; Haapalainen, A.M.; Yan, F.; Du, Q.; Tyler, P.C.; Evans, G.B.; Rinaldo-Matthis, A.; Brown, R.L.; Norris, G.E.; Almo, S.C.; Schramm, V.L. A picomolar transition state analogue inhibitor of MTAN as a specific antibiotic for Helicobacter pylori. Biochemistry, 2012, 51(35), 6892-6894.
[http://dx.doi.org/10.1021/bi3009664] [PMID: 22891633]
[62]
Wang, S.; Lim, J.; Thomas, K.; Yan, F.; Angeletti, R.H.; Schramm, V.L. A complex of methylthioadenosine/S-adenosylhomocysteine nucleosidase, transition state analogue, and nucleophilic water identified by mass spectrometry. J. Am. Chem. Soc., 2012, 134(3), 1468-1470.
[http://dx.doi.org/10.1021/ja211176q] [PMID: 22239413]
[63]
Schramm, V.L.; Clinch, K.; Gulab, S.A. Treatment of H. pylori infections using MTAN inhibitors, US20170166571A1, 2015.
[64]
Duan, K.; Dammel, C.; Stein, J.; Rabin, H.; Surette, M.G. Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol. Microbiol., 2003, 50(5), 1477-1491.
[http://dx.doi.org/10.1046/j.1365-2958.2003.03803.x] [PMID: 14651632]
[65]
Zhao, G.; Wan, W.; Mansouri, S.; Alfaro, J.F.; Bassler, B.L.; Cornell, K.A.; Zhou, Z.S. Chemical synthesis of S-ribosyl-L-homocysteine and activity assay as a LuxS substrate. Bioorg. Med. Chem. Lett., 2003, 13(22), 3897-3900.
[http://dx.doi.org/10.1016/j.bmcl.2003.09.015] [PMID: 14592470]
[66]
Alfaro, J.F.; Zhang, T.; Wynn, D.P.; Karschner, E.L.; Zhou, Z.S. Synthesis of LuxS inhibitors targeting bacterial cell-cell communication. Org. Lett., 2004, 6(18), 3043-3046.
[http://dx.doi.org/10.1021/ol049182i] [PMID: 15330583]
[67]
Shen, G.; Rajan, R.; Zhu, J.; Bell, C.E.; Pei, D. Design and synthesis of substrate and intermediate analogue inhibitors of S-ribosylhomocysteinase. J. Med. Chem., 2006, 49(10), 3003-3011.
[http://dx.doi.org/10.1021/jm060047g] [PMID: 16686542]
[68]
Wnuk, S.F.; Lalama, J.; Garmendia, C.A.; Robert, J.; Zhu, J.; Pei, D. S-Ribosylhomocysteine analogues with the carbon-5 and sulfur atoms replaced by a vinyl or (fluoro)vinyl unit. Bioorg. Med. Chem., 2008, 16(9), 5090-5102.
[http://dx.doi.org/10.1016/j.bmc.2008.03.028] [PMID: 18375129]
[69]
Wnuk, S.F.; Robert, J.; Sobczak, A.J.; Meyers, B.P.; Malladi, V.L.; Zhu, J.; Gopishetty, B.; Pei, D. Inhibition of S-ribosylhomocysteinase (LuxS) by substrate analogues modified at the ribosyl C-3 position. Bioorg. Med. Chem., 2009, 17(18), 6699-6706.
[http://dx.doi.org/10.1016/j.bmc.2009.07.057] [PMID: 19682914]
[70]
Malladi, V.L.; Sobczak, A.J.; Meyer, T.M.; Pei, D.; Wnuk, S.F. Inhibition of LuxS by S-ribosylhomocysteine analogues containing a [4-aza]ribose ring. Bioorg. Med. Chem., 2011, 19(18), 5507-5519.
[http://dx.doi.org/10.1016/j.bmc.2011.07.043] [PMID: 21855358]
[71]
Sobczak, A.J.; Chbib, C.; Wnuk, S.F. S-Ribosylhomocysteine analogs containing a [4-thio]ribose ring. Carbohydr. Res., 2015, 415, 39-47.
[http://dx.doi.org/10.1016/j.carres.2015.07.005] [PMID: 26279525]
[72]
Ni, N.; Li, M.; Wang, J.; Wang, B. Inhibitors and antagonists of bacterial quorum sensing. Med. Res. Rev., 2009, 29(1), 65-124.
[http://dx.doi.org/10.1002/med.20145] [PMID: 18956421]
[73]
Hoang, T.T.; Schweizer, H.P. Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis. J. Bacteriol., 1999, 181(17), 5489-5497.
[http://dx.doi.org/10.1128/JB.181.17.5489-5497.1999] [PMID: 10464225]
[74]
Wagner, S.; Sommer, R.; Hinsberger, S.; Lu, C.; Hartmann, R.W.; Empting, M.; Titz, A. novel strategies for the treatment of Pseudomonas aeruginosa infections. J. Med. Chem., 2016, 59(13), 5929-5969.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01698] [PMID: 26804741]
[75]
Parsek, M.R.; Val, D.L.; Hanzelka, B.L.; Cronan, J.E., Jr; Greenberg, E.P. Acyl homoserine-lactone quorum-sensing signal generation. Proc. Natl. Acad. Sci. USA, 1999, 96(8), 4360-4365.
[http://dx.doi.org/10.1073/pnas.96.8.4360] [PMID: 10200267]
[76]
Chang, C.Y.; Krishnan, T.; Wang, H.; Chen, Y.; Yin, W.F.; Chong, Y.M.; Tan, L.Y.; Chong, T.M.; Chan, K.G. Non-antibiotic quorum sensing inhibitors acting against N-acyl homoserine lactone synthase as druggable target. Sci. Rep., 2014, 4, 7245.
[http://dx.doi.org/10.1038/srep07245] [PMID: 25430794]
[77]
Raychaudhuri, A.; Tullock, A.; Tipton, P.A. Reactivity and reaction order in acylhomoserine lactone formation by Pseudomonas aeruginosa RhlI. Biochemistry, 2008, 47(9), 2893-2898.
[http://dx.doi.org/10.1021/bi702009n] [PMID: 18220361]
[78]
Kai, K.; Fujii, H.; Ikenaka, R.; Akagawa, M.; Hayashi, H. An acyl-SAM analog as an affinity ligand for identifying quorum sensing signal synthases. Chem. Commun. (Camb.), 2014, 50(62), 8586-8589.
[http://dx.doi.org/10.1039/C4CC03094J] [PMID: 24955553]
[79]
O’Loughlin, C.T.; Miller, L.C.; Siryaporn, A.; Drescher, K.; Semmelhack, M.F.; Bassler, B.L. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc. Natl. Acad. Sci. USA, 2013, 110(44), 17981-17986.
[http://dx.doi.org/10.1073/pnas.1316981110] [PMID: 24143808]
[80]
Castang, S.; Chantegrel, B.; Deshayes, C.; Dolmazon, R.; Gouet, P.; Haser, R. Reverchon, S.; Nasser, W.; Hugouvieux-Cotte-Pattat, N.; Doutheau, A. N-Sulfonylhomoserine lactones as antagonists of bacterial quorum sensing. Bioorg. Med. Chem. Lett., 2004, 14(20), 5145-5149.
[http://dx.doi.org/10.1016/j.bmcl.2004.07.088] [PMID: 15380216]
[81]
Frezza, M.; Castang, S.; Estephane, J.; Soulère, L.; Deshayes, C.; Chantegrel, B.; Nasser, W.; Queneau, Y.; Reverchon, S.; Doutheau, A. Synthesis and biological evaluation of homoserine lactone derived ureas as antagonists of bacterial quorum sensing. Bioorg. Med. Chem., 2006, 14(14), 4781-4791.
[http://dx.doi.org/10.1016/j.bmc.2006.03.017] [PMID: 16574415]
[82]
Persson, T.; Hansen, T.H.; Rasmussen, T.B.; Skindersø, M.E.; Givskov, M.; Nielsen, J. Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. Org. Biomol. Chem., 2005, 3(2), 253-262.
[http://dx.doi.org/10.1039/B415761C] [PMID: 15632967]
[83]
Blackwell, H.E.; Geske, G.D.; O'neill, J.C. Modulation of bacterial quorum sensing with synthetic ligands, WO2008116029, 2008.
[84]
Hjelmgaard, T.; Persson, T.; Rasmussen, T.B.; Givskov, M.; Nielsen, J. Synthesis of furanone-based natural product analogues with quorum sensing antagonist activity. Bioorg. Med. Chem., 2003, 11(15), 3261-3271.
[http://dx.doi.org/10.1016/S0968-0896(03)00295-5] [PMID: 12837536]
[85]
Wu, H.; Song, Z.; Hentzer, M.; Andersen, J.B.; Molin, S.; Givskov, M.; Høiby, N. Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J. Antimicrob. Chemother., 2004, 53(6), 1054-1061.
[http://dx.doi.org/10.1093/jac/dkh223] [PMID: 15117922]
[86]
Whiteley, M.; Lee, K.M.; Greenberg, P.E.; Muh, U. Quorum sensing signaling in bacteria, US6855513B1, 2005.
[87]
Pesci, E.C.; Iglewski, B.H.; Milbank, J.B.J.; Pearson, J.P.; Kende, A.S.; Greenberg, E.P. Autoinducer molecules and uses thereof US7442798, 2008.
[88]
Kimyon, Ö.; Ulutürk, Z.İ.; Nizalapur, S.; Lee, M.; Kutty, S.K.; Beckmann, S.; Kumar, N.; Manefield, M. N-acetylglucosamine inhibits LuxR, LasR and CviR based quorum sensing regulated gene expression levels. Front. Microbiol., 2016, 7, 1313.
[http://dx.doi.org/10.3389/fmicb.2016.01313] [PMID: 27602027]
[89]
Utsumi, R.; Igarashi, M. Two-component signal transduction as attractive drug targets in pathogenic bacteria. Yakugaku Zasshi, 2012, 132(1), 51-58.
[http://dx.doi.org/10.1248/yakushi.132.51] [PMID: 22214580]
[90]
Gilmour, R.; Foster, J.E.; Sheng, Q.; McClain, J.R.; Riley, A.; Sun, P.M.; Ng, W.L.; Yan, D.; Nicas, T.I.; Henry, K.; Winkler, M.E. New class of competitive inhibitor of bacterial histidine kinases. J. Bacteriol., 2005, 187(23), 8196-8200.
[http://dx.doi.org/10.1128/JB.187.23.8196-8200.2005] [PMID: 16291694]
[91]
Igarashi, M.; Watanabe, T.; Hashida, T.; Umekita, M.; Hatano, M.; Yanagida, Y.; Kino, H.; Kimura, T.; Kinoshita, N.; Inoue, K.; Sawa, R.; Nishimura, Y.; Utsumi, R.; Nomoto, A. Waldiomycin, a novel WalK-histidine kinase inhibitor from Streptomyces sp. MK844-mF10. J. Antibiot. (Tokyo), 2013, 66(8), 459-464.
[http://dx.doi.org/10.1038/ja.2013.33] [PMID: 23632918]
[92]
Boibessot, T.; Zschiedrich, C.P.; Lebeau, A.; Bénimèlis, D.; Dunyach-Rémy, C.; Lavigne, J.P.; Szurmant, H.; Benfodda, Z.; Meffre, P. The rational design, synthesis, and antimicrobial properties of thiophene derivatives that inhibit bacterial histidine kinases. J. Med. Chem., 2016, 59(19), 8830-8847.
[http://dx.doi.org/10.1021/acs.jmedchem.6b00580] [PMID: 27575438]
[93]
Velikova, N.; Fulle, S.; Manso, A.S.; Mechkarska, M.; Finn, P.; Conlon, J.M.; Oggioni, M.R.; Wells, J.M.; Marina, A. Putative histidine kinase inhibitors with antibacterial effect against multi-drug resistant clinical isolates identified by in vitro and in silico screens. Sci. Rep., 2016, 6, 26085.
[http://dx.doi.org/10.1038/srep26085] [PMID: 27173778]
[94]
Goswami, M.; Wilke, K.E.; Carlson, E.E. Rational design of selective adenine-based scaffolds for inactivation of bacterial histidine kinases. J. Med. Chem., 2017, 60(19), 8170-8182.
[http://dx.doi.org/10.1021/acs.jmedchem.7b01066] [PMID: 28933546]
[95]
Niu, C.; Afre, S.; Gilbert, E.S. Subinhibitory concentrations of cinnamaldehyde interfere with quorum sensing. Lett. Appl. Microbiol., 2006, 43(5), 489-494.
[http://dx.doi.org/10.1111/j.1472-765X.2006.02001.x] [PMID: 17032221]
[96]
Ren, D.; Sims, J.J.; Wood, T.K. Inhibition of biofilm formation and swarming of Escherichia coli by (5Z)-4-bromo-5-(bromome thylene)-3-butyl-2(5H)-furanone. Environ. Microbiol., 2001, 3(11), 731-736.
[http://dx.doi.org/10.1046/j.1462-2920.2001.00249.x] [PMID: 11846763]
[97]
Ren, D.; Zuo, R.; González Barrios, A.F.; Bedzyk, L.A.; Eldridge, G.R.; Pasmore, M.E.; Wood, T.K. Differential gene expression for investigation of Escherichia coli biofilm inhibition by plant extract ursolic acid. Appl. Environ. Microbiol., 2005, 71(7), 4022-4034.
[http://dx.doi.org/10.1128/AEM.71.7.4022-4034.2005] [PMID: 16000817]
[98]
Lee, J.; Bansal, T.; Jayaraman, A.; Bentley, W.E.; Wood, T.K. Enterohemorrhagic Escherichia coli biofilms are inhibited by 7-hydroxyindole and stimulated by isatin. Appl. Environ. Microbiol., 2007, 73(13), 4100-4109.
[http://dx.doi.org/10.1128/AEM.00360-07] [PMID: 17483266]
[99]
Widmer, K.W.; Soni, K.A.; Hume, M.E.; Beier, R.C.; Jesudhasan, P.; Pillai, S.D. Identification of poultry meat-derived fatty acids functioning as quorum sensing signal inhibitors to autoinducer-2 (AI-2). J. Food Sci., 2007, 72(9), M363-M368.
[http://dx.doi.org/10.1111/j.1750-3841.2007.00527.x] [PMID: 18034729]
[100]
Lu, L.; Hume, M.E.; Pillai, S.D. Autoinducer-2-like activity on vegetable produce and its potential involvement in bacterial biofilm formation on tomatoes. Foodborne Pathog. Dis., 2005, 2(3), 242-249.
[http://dx.doi.org/10.1089/fpd.2005.2.242] [PMID: 16156705]
[101]
Lu, L.; Hume, M.E.; Pillai, S.D. Autoinducer-2-like activity associated with foods and its interaction with food additives. J. Food Prot., 2004, 67(7), 1457-1462.
[http://dx.doi.org/10.4315/0362-028X-67.7.1457] [PMID: 15270501]
[102]
Soni, K.A.; Jesudhasan, P.; Cepeda, M.; Widmer, K.; Jayaprakasha, G.K.; Patil, B.S.; Hume, M.E.; Pillai, S.D. Identification of ground beef-derived fatty acid inhibitors of autoinducer-2-based cell signaling. J. Food Prot., 2008, 71(1), 134-138.
[http://dx.doi.org/10.4315/0362-028X-71.1.134] [PMID: 18236673]
[103]
Ni, N.; Chou, H.T.; Wang, J.; Li, M.; Lu, C.D.; Tai, P.C.; Wang, B. Identification of boronic acids as antagonists of bacterial quorum sensing in Vibrio harveyi. Biochem. Biophys. Res. Commun., 2008, 369(2), 590-594.
[http://dx.doi.org/10.1016/j.bbrc.2008.02.061] [PMID: 18295599]
[104]
Lowery, C.A.; Park, J.; Kaufmann, G.F.; Janda, K.D. An unexpected switch in the modulation of AI-2-based quorum sensing discovered through synthetic 4,5-dihydroxy-2,3-pentanedione analogues. J. Am. Chem. Soc., 2008, 130(29), 9200-9201.
[http://dx.doi.org/10.1021/ja802353j] [PMID: 18576653]
[105]
Roy, V.; Smith, J.A.; Wang, J.; Stewart, J.E.; Bentley, W.E.; Sintim, H.O. Synthetic analogs tailor native AI-2 signaling across bacterial species. J. Am. Chem. Soc., 2010, 132(32), 11141-11150.
[http://dx.doi.org/10.1021/ja102587w] [PMID: 20698680]
[106]
Roy, V.; Meyer, M.T.; Smith, J.A.; Gamby, S.; Sintim, H.O.; Ghodssi, R.; Bentley, W.E. AI-2 analogs and antibiotics: a synergistic approach to reduce bacterial biofilms. Appl. Microbiol. Biotechnol., 2013, 97(6), 2627-2638.
[http://dx.doi.org/10.1007/s00253-012-4404-6] [PMID: 23053069]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 23
ISSUE: 6
Year: 2020
Published on: 05 October, 2020
Page: [458 - 476]
Pages: 19
DOI: 10.2174/1386207323666200425205808
Price: $65

Article Metrics

PDF: 14
HTML: 2
EPUB: 1
PRC: 1