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Current Medicinal Chemistry

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ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

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Review Article

Transition Towards Antibiotic Hybrid Vehicles: The Next Generation Antibacterials

Author(s): Rajesh Kuppusamy, Katrina Browne, Dittu Suresh, Romano Maximo Do Rosario, Sudip Chakraborty, Sandy Yang, Mark Willcox, David Black, Renxun Chen* and Naresh Kumar*

Volume 30, Issue 1, 2023

Published on: 09 September, 2022

Page: [104 - 125] Pages: 22

DOI: 10.2174/0929867329666220613105424

Price: $65

Abstract

Antibiotic resistance is a growing global health problem when the discovery and development of novel antibiotics are diminishing. Various strategies have been proposed to address the problem of growing antibacterial resistance. One such strategy is the development of hybrid antibiotics. These therapeutic systems have been designed for two or more pharmacophores of known antimicrobial agents. This review highlights the latest development of antibiotic hybrids comprising two antibiotics (cleavable and non-cleavable) and combinations of biocidal and novel compounds to treat bacterial infections. The approach of dual-acting hybrid compounds has a promising future in overcoming drug resistance in bacterial pathogens.

Keywords: Antibiotic hybrids, nitric oxide donor hybrids, adjuvant therapies, antibiotic potentiators, efflux pump inhibitor hybrids, antibacterials, quorum sensing inhibitors hybrids.

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[1]
Angst, D.C.; Tepekule, B.; Sun, L.; Bogos, B.; Bonhoeffer, S. Comparing treatment strategies to reduce antibiotic resistance in an in vitro epidemiological setting. Proc. Natl. Acad. Sci. USA, 2021, 118(13), e2023467118.
[http://dx.doi.org/10.1073/pnas.2023467118] [PMID: 33766914]
[2]
Schmid, A.; Wolfensberger, A.; Nemeth, J.; Schreiber, P.W.; Sax, H.; Kuster, S.P. Monotherapy versus combination therapy for multidrug-resistant Gram-negative infections: Systematic review and meta-analysis. Sci. Rep., 2019, 9(1), 15290.
[http://dx.doi.org/10.1038/s41598-019-51711-x] [PMID: 31664064]
[3]
Tamma, P.D.; Cosgrove, S.E.; Maragakis, L.L. Combination therapy for treatment of infections with gram-negative bacteria. Clin. Microbiol. Rev., 2012, 25(3), 450-470.
[4]
Domalaon, R.; Idowu, T.; Zhanel, G.G.; Schweizer, F. Antibiotic hybrids: The next generation of agents and adjuvants against gram-negative pathogens? 2018, 31(2), e00077-00017.
[http://dx.doi.org/10.1128/CMR.00077-17]
[5]
Grapsas, I.; Lerner, S.A.; Mobashery, S. Conjoint molecules of cephalosporins and aminoglycosides. Arch. Pharm. (Weinheim), 2001, 334(8-9), 295-301.
[http://dx.doi.org/10.1002/1521-4184(200109)334:8/9<295::AID-ARDP295>3.0.CO;2-3] [PMID: 11688141]
[6]
Klahn, P.; Brönstrup, M. Bifunctional antimicrobial conjugates and hybrid antimicrobials. Nat. Prod. Rep., 2017, 34(7), 832-885.
[http://dx.doi.org/10.1039/C7NP00006E] [PMID: 28530279]
[7]
Jia, Y.; Zhao, L. The antibacterial activity of fluoroquinolone derivatives: An update (2018-2021). Eur. J. Med. Chem., 2021, 224, 113741.
[http://dx.doi.org/10.1016/j.ejmech.2021.113741] [PMID: 34365130]
[8]
Surur, A.S.; Sun, D. Macrocycle-antibiotic hybrids: A path to clinical Candidates. Front. Chem., 2021, 9, 659845.
[http://dx.doi.org/10.3389/fchem.2021.659845] [PMID: 33996753]
[9]
Tyers, M.; Wright, G.D. Drug combinations: A strategy to extend the life of antibiotics in the 21st century. Nat. Rev. Microbiol., 2019, 17(3), 141-155.
[http://dx.doi.org/10.1038/s41579-018-0141-x] [PMID: 30683887]
[10]
Arzanlou, M.; Chai, W.C.; Venter, H.J.E.i.b. Intrinsic, adaptive and acquired antimicrobial resistance in Gram-negative bacteria. Essays Biochem., 2017, 61(1), 49-59.
[11]
Liu, Y.; Li, R.; Xiao, X.; Wang, Z.J.C.r.i.m. Antibiotic adjuvants: An alternative approach to overcome multi-drug resistant Gram-negative bacteria. Crit. Rev. Microbiol., 2019, 45(3), 301-314.
[http://dx.doi.org/10.1080/1040841X.2019.1599813]
[12]
Nguyen, L.T.; Haney, E.F.; Vogel, H.J. The expanding scope of antimicrobial peptide structures and their modes of action. Trends Biotechnol., 2011, 29(9), 464-472.
[http://dx.doi.org/10.1016/j.tibtech.2011.05.001] [PMID: 21680034]
[13]
Peschel, A.; Sahl, H-G. The co-evolution of host cationic antimicrobial peptides and microbial resistance. Nat. Rev. Microbiol., 2006, 4(7), 529-536.
[http://dx.doi.org/10.1038/nrmicro1441] [PMID: 16778838]
[14]
Nicolas, P. Multifunctional host defense peptides: Intracellular-targeting antimicrobial peptides. 2009, 276(22), 6483-6496.
[http://dx.doi.org/10.1111/j.1742-4658.2009.07359.x]
[15]
Maria-Neto, S.; de Almeida, K.C.; Macedo, M.L.R.; Franco, O.L. Understanding bacterial resistance to antimicrobial peptides: From the surface to deep inside. Biochim. Biophys. Acta, 2015, 1848(11 Pt B), 3078-3088.
[http://dx.doi.org/10.1016/j.bbamem.2015.02.017] [PMID: 25724815]
[16]
Reinhardt, A.; Neundorf, I. Design and application of antimicrobial peptide conjugates. Int. J. Mol. Sci., 2016, 17(5), 701.
[http://dx.doi.org/10.3390/ijms17050701] [PMID: 27187357]
[17]
Kumar, M.; Sarma, D.K.; Shubham, S.; Kumawat, M.; Verma, V.; Nina, P.B.; Jp, D.; Kumar, S.; Singh, B.; Tiwari, R.R. Futuristic non-antibiotic therapies to combat antibiotic resistance: A review. Front. Microbiol., 2021, 12, 609459.
[http://dx.doi.org/10.3389/fmicb.2021.609459] [PMID: 33574807]
[18]
Hubschwerlen, C.; Specklin, J-L.; Sigwalt, C.; Schroeder, S.; Locher, H.H. Design, synthesis and biological evaluation of oxazolidinone-quinolone hybrids. Bioorg. Med. Chem., 2003, 11(10), 2313-2319.
[http://dx.doi.org/10.1016/S0968-0896(03)00083-X] [PMID: 12713843]
[19]
Shavit, M.; Pokrovskaya, V.; Belakhov, V.; Baasov, T. Covalently linked kanamycin - Ciprofloxacin hybrid antibiotics as a tool to fight bacterial resistance. Bioorg. Med. Chem., 2017, 25(11), 2917-2925.
[http://dx.doi.org/10.1016/j.bmc.2017.02.068] [PMID: 28343755]
[20]
Mölstad, S.; Lundborg, C.S.; Karlsson, A.K.; Cars, O. Antibiotic prescription rates vary markedly between 13 European countries. Scand. J. Infect. Dis., 2002, 34(5), 366-371.
[http://dx.doi.org/10.1080/00365540110080034] [PMID: 12069022]
[21]
Durkin, M.J.; Jafarzadeh, S.R.; Hsueh, K.; Sallah, Y.H.; Munshi, K.D.; Henderson, R.R.; Fraser, V.J. Outpatient antibiotic prescription trends in the United States: A National Cohort Study. Infect. Control Hosp. Epidemiol., 2018, 39(5), 584-589.
[http://dx.doi.org/10.1017/ice.2018.26] [PMID: 29485018]
[22]
Fleming, A. On the antibacterial action of cultures of a Penicillium, with special reference to their Use in the Isolation of B. influenzæ. Br. J. Exp. Pathol., 1929, 10(3), 226-236.
[23]
González-Bello, C. Antibiotic adjuvants - A strategy to unlock bacterial resistance to antibiotics. Bioorg. Med. Chem. Lett., 2017, 27(18), 4221-4228.
[http://dx.doi.org/10.1016/j.bmcl.2017.08.027] [PMID: 28827113]
[24]
Bonomo, R.A. β-Lactamases: A focus on current challenges. Cold Spring Harb. Perspect. Med., 2017, 7(1), a025239.
[http://dx.doi.org/10.1101/cshperspect.a025239] [PMID: 27742735]
[25]
Drawz, S.M.; Bonomo, R.A. Three decades of beta-lactamase inhibitors. Clin. Microbiol. Rev., 2010, 23(1), 160-201.
[http://dx.doi.org/10.1128/CMR.00037-09] [PMID: 20065329]
[26]
Tooke, C.L.; Hinchliffe, P.; Bragginton, E.C.; Colenso, C.K.; Hirvonen, V.H.A.; Takebayashi, Y.; Spencer, J. β-Lactamases and β-Lactamase Inhibitors in the 21st Century. J. Mol. Biol., 2019, 431(18), 3472-3500.
[http://dx.doi.org/10.1016/j.jmb.2019.04.002] [PMID: 30959050]
[27]
Barnes, M.D.; Kumar, V.; Bethel, C.R.; Moussa, S.H.; O’Donnell, J.; Rutter, J.D.; Good, C.E.; Hujer, K.M.; Hujer, A.M.; Marshall, S.H.; Kreiswirth, B.N.; Richter, S.S.; Rather, P.N.; Jacobs, M.R.; Papp-Wallace, K.M.; van den Akker, F.; Bonomo, R.A. Targeting multidrug-resistant Acinetobacter spp.: Sulbactam and the Diazabicyclooctenone β-Lactamase inhibitor ETX2514 as a novel therapeutic agent. MBio, 2019, 10(2), e00159-19.
[http://dx.doi.org/10.1128/mBio.00159-19] [PMID: 30862744]
[28]
Domalaon, R.; Yang, X.; Lyu, Y.; Zhanel, G.G.; Schweizer, F. Polymyxin B3–tobramycin hybrids with Pseudomonas aeruginosa-selective antibacterial activity and strong potentiation of rifampicin, minocycline, and vancomycin. ACS Infect. Dis., 2017, 3(12), 941-954.
[http://dx.doi.org/10.1021/acsinfecdis.7b00145] [PMID: 29045123]
[29]
Yang, X.; Goswami, S.; Gorityala, B.K.; Domalaon, R.; Lyu, Y.; Kumar, A.; Zhanel, G.G.; Schweizer, F.J.J. A tobramycin vector enhances synergy and efficacy of efflux pump inhibitors against multidrug-resistant Gram-negative bacteria. J. Med. Chem., 2017, 60(9), 3913-3932.
[http://dx.doi.org/10.1021/acs.jmedchem.7b00156]
[30]
Lyu, Y.; Yang, X.; Goswami, S.; Gorityala, B.K.; Idowu, T.; Domalaon, R.; Zhanel, G.G.; Shan, A.; Schweizer, F. Amphiphilic tobramycin–lysine conjugates sensitize multidrug resistant gram-negative bacteria to rifampicin and minocycline. J. Med. Chem., 2017, 60(9), 3684-3702.
[http://dx.doi.org/10.1021/acs.jmedchem.6b01742] [PMID: 28409644]
[31]
Negash, K.H.; Norris, J.K.S.; Hodgkinson, J.T. Siderophore–antibiotic conjugate design: New drugs for bad bugs? Molecules, 2019, 24(18), 3314.
[http://dx.doi.org/10.3390/molecules24183314] [PMID: 31514464]
[32]
Yusuf, E.; Bax, H.I.; Verkaik, N.J.; van Westreenen, M. An update on eight “new” antibiotics against multidrug-resistant gram-negative bacteria. J. Clin. Med., 2021, 10(5), 1068.
[http://dx.doi.org/10.3390/jcm10051068] [PMID: 33806604]
[33]
Liu, R.; Miller, P.A.; Vakulenko, S.B.; Stewart, N.K.; Boggess, W.C.; Miller, M.J. A synthetic dual drug Sideromycin Induces Gram-Negative bacteria To Commit Suicide with a Gram-Positive antibiotic. J. Med. Chem., 2018, 61(9), 3845-3854.
[http://dx.doi.org/10.1021/acs.jmedchem.8b00218] [PMID: 29554424]
[34]
Antonoplis, A.; Zang, X.; Huttner, M.A.; Chong, K.K.L.; Lee, Y.B.; Co, J.Y.; Amieva, M.R.; Kline, K.A.; Wender, P.A.; Cegelski, L. A dual-function antibiotic-transporter conjugate exhibits superior activity in sterilizing MRSA biofilms and killing persister cells. J. Am. Chem. Soc., 2018, 140(47), 16140-16151.
[http://dx.doi.org/10.1021/jacs.8b08711] [PMID: 30388366]
[35]
Koopmans, T.; Wood, T.M.; ’t Hart, P.; Kleijn, L.H.; Hendrickx, A.P.; Willems, R.J.; Breukink, E.; Martin, N.I. Semisynthetic lipopeptides derived from nisin display antibacterial activity and lipid II binding on par with that of the parent compound. J. Am. Chem. Soc., 2015, 137(29), 9382-9389.
[http://dx.doi.org/10.1021/jacs.5b04501] [PMID: 26122963]
[36]
Bolt, H.L.; Kleijn, L.H.J.; Martin, N.I.; Cobb, S.L. Synthesis of antibacterial Nisin-Peptoid Hybrids using click methodology. Molecules, 2018, 23(7), 1566.
[http://dx.doi.org/10.3390/molecules23071566] [PMID: 29958423]
[37]
Wu, L.; Estrada, O.; Zaborina, O.; Bains, M.; Shen, L.; Kohler, J.E.; Patel, N.; Musch, M.W.; Chang, E.B.; Fu, Y-X.; Jacobs, M.A.; Nishimura, M.I.; Hancock, R.E.W.; Turner, J.R.; Alverdy, J.C. Recognition of host immune activation by Pseudomonas aeruginosa. Science, 2005, 309(5735), 774-777.
[http://dx.doi.org/10.1126/science.1112422] [PMID: 16051797]
[38]
Luther, A.; Urfer, M.; Zahn, M.; Müller, M.; Wang, S-Y.; Mondal, M.; Vitale, A.; Hartmann, J-B.; Sharpe, T.; Monte, F.L.; Kocherla, H.; Cline, E.; Pessi, G.; Rath, P.; Modaresi, S.M.; Chiquet, P.; Stiegeler, S.; Verbree, C.; Remus, T.; Schmitt, M.; Kolopp, C.; Westwood, M-A.; Desjonquères, N.; Brabet, E.; Hell, S.; LePoupon, K.; Vermeulen, A.; Jaisson, R.; Rithié, V.; Upert, G.; Lederer, A.; Zbinden, P.; Wach, A.; Moehle, K.; Zerbe, K.; Locher, H.H.; Bernardini, F.; Dale, G.E.; Eberl, L.; Wollscheid, B.; Hiller, S.; Robinson, J.A.; Obrecht, D. Chimeric peptidomimetic antibiotics against Gram-negative bacteria. Nature, 2019, 576(7787), 452-458.
[http://dx.doi.org/10.1038/s41586-019-1665-6] [PMID: 31645764]
[39]
Barker, W.T.; Martin, S.E.; Chandler, C.E.; Nguyen, T.V.; Harris, T.L.; Goodell, C.; Melander, R.J.; Doi, Y.; Ernst, R.K.; Melander, C. Small molecule adjuvants that suppress both chromosomal and mcr-1 encoded colistin-resistance and amplify colistin efficacy in polymyxin-susceptible bacteria. Bioorg. Med. Chem., 2017, 25(20), 5749-5753.
[http://dx.doi.org/10.1016/j.bmc.2017.08.055] [PMID: 28958847]
[40]
Douafer, H.; Andrieu, V.; Phanstiel, O., IV; Brunel, J.M. Antibiotic adjuvants: Make antibiotics great again! J. Med. Chem., 2019, 62(19), 8665-8681.
[http://dx.doi.org/10.1021/acs.jmedchem.8b01781] [PMID: 31063379]
[41]
Yang, X.; Ammeter, D.; Idowu, T.; Domalaon, R.; Brizuela, M.; Okunnu, O.; Bi, L.; Guerrero, Y.A.; Zhanel, G.G.; Kumar, A.; Schweizer, F. Amphiphilic nebramine-based hybrids Rescue legacy antibiotics from intrinsic resistance in multidrug-resistant Gram-negative bacilli. Eur. J. Med. Chem., 2019, 175, 187-200.
[http://dx.doi.org/10.1016/j.ejmech.2019.05.003] [PMID: 31078866]
[42]
Tevyashova, A.N.; Bychkova, E.N.; Korolev, A.M.; Isakova, E.B.; Mirchink, E.P.; Osterman, I.A.; Erdei, R.; Szücs, Z.; Batta, G. Synthesis and evaluation of biological activity for dual-acting antibiotics on the basis of azithromycin and glycopeptides. Bioorg. Med. Chem. Lett., 2019, 29(2), 276-280.
[http://dx.doi.org/10.1016/j.bmcl.2018.11.038] [PMID: 30473176]
[43]
Idowu, T.; Arthur, G.; Zhanel, G.G.; Schweizer, F. Heterodimeric Rifampicin-Tobramycin conjugates break intrinsic resistance of Pseudomonas aeruginosa to doxycycline and chloramphenicol in vitro and in a Galleria mellonella in vivo model. Eur. J. Med. Chem., 2019, 174, 16-32.
[http://dx.doi.org/10.1016/j.ejmech.2019.04.034] [PMID: 31022550]
[44]
Corbett, D.; Wise, A.; Langley, T.; Skinner, K.; Trimby, E.; Birchall, S.; Dorali, A.; Sandiford, S.; Williams, J.; Warn, P.J. Potentiation of antibiotic activity by a novel cationic peptide: Potency and spectrum of activity of SPR741. Antimicrob. Agents Chemother., 2017, 61(8), e00200-e00217.
[45]
Johnson, R.A.; Chan, A.N.; Ward, R.D.; McGlade, C.A.; Hatfield, B.M.; Peters, J.M.; Li, B. Inhibition of Isoleucyl-tRNA synthetase by the hybrid antibiotic thiomarinol. J. Am. Chem. Soc., 2021, 143(31), 12003-12013.
[http://dx.doi.org/10.1021/jacs.1c02622] [PMID: 34342433]
[46]
Delcour, A.H. Outer membrane permeability and antibiotic resistance. Biochim. Biophys. Acta, 2009, 1794(5), 808-816.
[http://dx.doi.org/10.1016/j.bbapap.2008.11.005] [PMID: 19100346]
[47]
Ayoub Moubareck, C. Polymyxins and bacterial membranes: A review of antibacterial activity and mechanisms of resistance. Membranes (Basel), 2020, 10(8), 181.
[http://dx.doi.org/10.3390/membranes10080181] [PMID: 32784516]
[48]
Azad, M.A.K.; Nation, R.L.; Velkov, T.; Li, J. Mechanisms of Polymyxin-induced nephrotoxicity. Adv. Exp. Med. Biol., 2019, 1145, 305-319.
[http://dx.doi.org/10.1007/978-3-030-16373-0_18] [PMID: 31364084]
[49]
Zurawski, D.V.; Reinhart, A.A.; Alamneh, Y.A.; Pucci, M.J.; Si, Y.; Abu-Taleb, R.; Shearer, J.P.; Demons, S.T.; Tyner, S.D.; Lister, T. SPR741, an antibiotic adjuvant, potentiates the in vitro and in vivo activity of Rifampin against clinically relevant extensively drug-resistant Acinetobacter baumannii. Antimicrob. Agents Chemother., 2017, 61(12), e01239-17.
[http://dx.doi.org/10.1128/AAC.01239-17] [PMID: 28947471]
[50]
Ferrer-Espada, R.; Shahrour, H.; Pitts, B.; Stewart, P.S.; Sánchez-Gómez, S.; Martínez-de-Tejada, G. A permeability-increasing drug synergizes with bacterial efflux pump inhibitors and restores susceptibility to antibiotics in multi-drug resistant Pseudomonas aeruginosa strains. Sci. Rep., 2019, 9(1), 3452.
[http://dx.doi.org/10.1038/s41598-019-39659-4] [PMID: 30837499]
[51]
van Groesen, E.; Slingerland, C.J.; Innocenti, P.; Mihajlovic, M.; Masereeuw, R.; Martin, N.I. Vancomyxins: Vancomycin-Polymyxin nonapeptide conjugates that retain Anti-Gram-Positive activity with enhanced potency against Gram-Negative Strains. ACS Infect. Dis., 2021, 7(9), 2746-2754.
[http://dx.doi.org/10.1021/acsinfecdis.1c00318] [PMID: 34387988]
[52]
Cassone, M.; Otvos, L.J.E., Jr. Synergy among antibacterial peptides and between peptides and small-molecule antibiotics. Expert. Rev. Anti. Infect. Ther., 2010, 8(6), 703-716.
[http://dx.doi.org/10.1586/eri.10.38]
[53]
Li, W.; O'Brien-Simpson, N.M.; Holden, J.A.; Otvos, L.; Reynolds, E.C.; Separovic, F.; Hossain, M.A.; Wade, J.D.J.P.S. Covalent conjugation of cationic antimicrobial peptides with a β-lactam antibiotic core. Peptide Sci., 2018, 110(3), e24059.
[http://dx.doi.org/10.1002/pep2.24059]
[54]
Brezden, A.; Mohamed, M.F.; Nepal, M.; Harwood, J.S.; Kuriakose, J.; Seleem, M.N.; Chmielewski, J. Dual targeting of intracellular pathogenic bacteria with a cleavable conjugate of kanamycin and an antibacterial cell-penetrating peptide. J. Am. Chem. Soc., 2016, 138(34), 10945-10949.
[http://dx.doi.org/10.1021/jacs.6b04831] [PMID: 27494027]
[55]
Kuriakose, J.; Hernandez-Gordillo, V.; Nepal, M.; Brezden, A.; Pozzi, V.; Seleem, M.N.; Chmielewski, J. Targeting intracellular pathogenic bacteria with unnatural proline-rich peptides: Coupling antibacterial activity with macrophage penetration. Angew. Chem. Int. Ed. Engl., 2013, 52(37), 9664-9667.
[http://dx.doi.org/10.1002/anie.201302693] [PMID: 23960012]
[56]
Arnusch, C.J.; Pieters, R.J.; Breukink, E. Enhanced membrane pore formation through high-affinity targeted antimicrobial peptides. PLoS One, 2012, 7(6), e39768-e39768.
[http://dx.doi.org/10.1371/journal.pone.0039768] [PMID: 22768121]
[57]
Ludtke, S.J.; He, K.; Heller, W.T.; Harroun, T.A.; Yang, L.; Huang, H.W. Membrane pores induced by magainin. Biochemistry, 1996, 35(43), 13723-13728.
[http://dx.doi.org/10.1021/bi9620621] [PMID: 8901513]
[58]
Ahmad, I.; Perkins, W.R.; Lupan, D.M.; Selsted, M.E.; Janoff, A.S. Liposomal entrapment of the neutrophil-derived peptide indolicidin endows it with in vivo antifungal activity. Biochim. Biophys. Acta, 1995, 1237(2), 109-114.
[http://dx.doi.org/10.1016/0005-2736(95)00087-J] [PMID: 7632702]
[59]
Selsted, M.E.; Novotny, M.J.; Morris, W.L.; Tang, Y-Q.; Smith, W.; Cullor, J.S. Indolicidin, a novel bactericidal tridecapeptide amide from neutrophils. J. Biol. Chem., 1992, 267(7), 4292-4295.
[http://dx.doi.org/10.1016/S0021-9258(18)42830-X] [PMID: 1537821]
[60]
Aley, S.B.; Zimmerman, M.; Hetsko, M.; Selsted, M.E.; Gillin, F.D. Killing of Giardia lamblia by cryptdins and cationic neutrophil peptides. Infect. Immun., 1994, 62(12), 5397-5403.
[http://dx.doi.org/10.1128/iai.62.12.5397-5403.1994] [PMID: 7960119]
[61]
Schluesener, H.J.; Radermacher, S.; Melms, A.; Jung, S. Leukocytic antimicrobial peptides kill autoimmune T cells. J. Neuroimmunol., 1993, 47(2), 199-202.
[http://dx.doi.org/10.1016/0165-5728(93)90030-3] [PMID: 8370771]
[62]
Ghaffar, K.A.; Hussein, W.M.; Khalil, Z.G.; Capon, R.J.; Skwarczynski, M.; Toth, I. Levofloxacin and indolicidin for combination antimicrobial therapy. Curr. Drug Deliv., 2015, 12(1), 108-114.
[http://dx.doi.org/10.2174/1567201811666140910094050] [PMID: 25213074]
[63]
Pini, A.; Falciani, C.; Mantengoli, E.; Bindi, S.; Brunetti, J.; Iozzi, S.; Rossolini, G.M.; Bracci, L. A novel tetrabranched antimicrobial peptide that neutralizes bacterial lipopolysaccharide and prevents septic shock in vivo. FASEB J., 2010, 24(4), 1015-1022.
[http://dx.doi.org/10.1096/fj.09-145474] [PMID: 19917670]
[64]
Ceccherini, F.; Falciani, C.; Onori, M.; Scali, S.; Pollini, S.; Rossolini, G.M.; Bracci, L.; Pini, A. Antimicrobial activity of levofloxacin - M33 peptide conjugation or combination. MedChemComm, 2016, 7(2), 258-262.
[http://dx.doi.org/10.1039/C5MD00392J]
[65]
De Groote, M.A.; Fang, F.C.; Inhibitions, N.O. NO inhibitions: Antimicrobial properties of nitric oxide. Clin. Infect. Dis., 1995, 21(Suppl. 2), S162-S165.
[http://dx.doi.org/10.1093/clinids/21.Supplement_2.S162] [PMID: 8845445]
[66]
Chi, D.S.; Qui, M.; Krishnaswamy, G.; Li, C.; Stone, W. Regulation of nitric oxide production from macrophages by lipopolysaccharide and catecholamines. Nitric Oxide, 2003, 8(2), 127-132.
[http://dx.doi.org/10.1016/S1089-8603(02)00148-9] [PMID: 12620376]
[67]
Wink, D.A.; Kasprzak, K.S.; Maragos, C.M.; Elespuru, R.K.; Misra, M.; Dunams, T.M.; Cebula, T.A.; Koch, W.H.; Andrews, A.W.; Allen, J.S.; Keefer, L.K. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science, 1991, 254(5034), 1001-1003.
[http://dx.doi.org/10.1126/science.1948068] [PMID: 1948068]
[68]
Shiloh, M.U.; MacMicking, J.D.; Nicholson, S.; Brause, J.E.; Potter, S.; Marino, M.; Fang, F.; Dinauer, M.; Nathan, C. Phenotype of mice and macrophages deficient in both phagocyte oxidase and inducible nitric oxide synthase. Immunity, 1999, 10(1), 29-38.
[http://dx.doi.org/10.1016/S1074-7613(00)80004-7] [PMID: 10023768]
[69]
Barraud, N.; Hassett, D.J.; Hwang, S.H.; Rice, S.A.; Kjelleberg, S.; Webb, J.S. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol., 2006, 188(21), 7344-7353.
[http://dx.doi.org/10.1128/JB.00779-06] [PMID: 17050922]
[70]
Kostakioti, M.; Hadjifrangiskou, M.; Hultgren, S.J. Bacterial biofilms: Development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb. Perspect. Med., 2013, 3(4), a010306.
[http://dx.doi.org/10.1101/cshperspect.a010306] [PMID: 23545571]
[71]
Brooun, A.; Liu, S.; Lewis, K. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. Antimicrob. Agents Chemother., 2000, 44(3), 640-646.
[http://dx.doi.org/10.1128/AAC.44.3.640-646.2000] [PMID: 10681331]
[72]
Wang, P.G.; Xian, M.; Tang, X.; Wu, X.; Wen, Z.; Cai, T.; Janczuk, A.J. Nitric oxide donors: Chemical activities and biological applications. Chem. Rev., 2002, 102(4), 1091-1134.
[http://dx.doi.org/10.1021/cr000040l] [PMID: 11942788]
[73]
Kutty, S.K.; Ka Kit Ho, K.; Kumar, N. Nitric Oxide Donors; Seabra, A.B., Ed.; Academic Press: FL, USA, 2017, pp. 169-189.
[http://dx.doi.org/10.1016/B978-0-12-809275-0.00007-7]
[74]
Rouillard, K.R.; Novak, O.P.; Pistiolis, A.M.; Yang, L.; Ahonen, M.J.R.; McDonald, R.A.; Schoenfisch, M.H. Exogenous Nitric Oxide improves antibiotic susceptibility in resistant bacteria. ACS Infect. Dis., 2021, 7(1), 23-33.
[http://dx.doi.org/10.1021/acsinfecdis.0c00337] [PMID: 33291868]
[75]
Barraud, N.; Kardak, B.G.; Yepuri, N.R.; Howlin, R.P.; Webb, J.S.; Faust, S.N.; Kjelleberg, S.; Rice, S.A.; Kelso, M.J. Cephalosporin-3′-diazeniumdiolates: Targeted NO-donor prodrugs for dispersing bacterial biofilms. Angew. Chem. Int. Ed. Engl., 2012, 51(36), 9057-9060.
[http://dx.doi.org/10.1002/anie.201202414] [PMID: 22890975]
[76]
Yepuri, N.R.; Barraud, N.; Mohammadi, N.S.; Kardak, B.G.; Kjelleberg, S.; Rice, S.A.; Kelso, M.J. Synthesis of cephalosporin-3′-diazeniumdiolates: Biofilm dispersing NO-donor prodrugs activated by β-lactamase. Chem. Commun. (Camb.), 2013, 49(42), 4791-4793.
[http://dx.doi.org/10.1039/c3cc40869h] [PMID: 23603842]
[77]
Collins, S.A.; Kelso, M.J.; Rineh, A.; Yepuri, N.R.; Coles, J.; Jackson, C.L.; Halladay, G.D.; Walker, W.T.; Webb, J.S.; Hall-Stoodley, L.; Connett, G.J.; Feelisch, M.; Faust, S.N.; Lucas, J.S.A.; Allan, R.N. Cephalosporin-3′-Diazeniumdiolate NO Donor Prodrug PYRRO-C3D enhances azithromycin susceptibility of nontypeable haemophilus influenzae biofilms. Antimicrob. Agents Chemother., 2017, 61(2), e02086-e02016.
[http://dx.doi.org/10.1128/AAC.02086-16] [PMID: 27919896]
[78]
Allan, R.N.; Kelso, M.J.; Rineh, A.; Yepuri, N.R.; Feelisch, M.; Soren, O.; Brito-Mutunayagam, S.; Salib, R.J.; Stoodley, P.; Clarke, S.C.; Webb, J.S.; Hall-Stoodley, L.; Faust, S.N. Cephalosporin-NO-donor prodrug PYRRO-C3D shows β-lactam-mediated activity against Streptococcus pneumoniae biofilms. Nitric Oxide, 2017, 65, 43-49.
[http://dx.doi.org/10.1016/j.niox.2017.02.006] [PMID: 28235635]
[79]
Bertinaria, M.; Galli, U.; Sorba, G.; Fruttero, R.; Gasco, A.; Brenciaglia, M.I.; Scaltrito, M.M.; Dubini, F. Synthesis and anti-Helicobacter pylori properties of NO-donor/metronidazole hybrids and related compounds. Drug Dev. Res., 2003, 60(3), 225-239.
[http://dx.doi.org/10.1002/ddr.10284]
[80]
Gasco, A.; Fruttero, R.; Sorba, G.; Stilo, A.D.; Calvino, R. NO donors: Focus on furoxan derivatives. Pure Appl. Chem., 2004, 76(5), 973-981.
[http://dx.doi.org/10.1351/pac200476050973]
[81]
Aziz, H.A.; Moustafa, G.A.I.; Abbas, S.H.; Hauk, G.; Siva Krishna, V.; Sriram, D.; Berger, J.M.; Abuo-Rahma, G.E-D.A. New fluoroquinolones/nitric oxide donor hybrids: Design, synthesis and antitubercular activity. Med. Chem. Res., 2019, 28(8), 1272-1283.
[http://dx.doi.org/10.1007/s00044-019-02372-y]
[82]
Tang, X.; Cai, T.; Wang, P.G. Synthesis of beta-lactamase activated nitric oxide donors. Bioorg. Med. Chem. Lett., 2003, 13(10), 1687-1690.
[http://dx.doi.org/10.1016/S0960-894X(03)00242-7] [PMID: 12729642]
[83]
Hrabie, J.A.; Keefer, L.K. Chemistry of the nitric oxide-releasing diazeniumdiolate (“nitrosohydroxylamine”) functional group and its oxygen-substituted derivatives. Chem. Rev., 2002, 102(4), 1135-1154.
[http://dx.doi.org/10.1021/cr000028t] [PMID: 11942789]
[84]
Rineh, A.; Soren, O.; McEwan, T.; Ravikumar, V.; Poh, W.H.; Azamifar, F.; Naimi-Jamal, M.R.; Cheung, C.Y.; Elliott, A.G.; Zuegg, J.; Blaskovich, M.A.T.; Cooper, M.A.; Dolange, V.; Christodoulides, M.; Cook, G.M.; Rice, S.A.; Faust, S.N.; Webb, J.S.; Kelso, M.J. Discovery of Cephalosporin-3′-Diazeniumdiolates that show dual antibacterial and antibiofilm effects against Pseudomonas aeruginosa clinical cystic fibrosis isolates and efficacy in a murine respiratory infection model. ACS Infect. Dis., 2020, 6(6), 1460-1479.
[http://dx.doi.org/10.1021/acsinfecdis.0c00070] [PMID: 32329596]
[85]
Kutty, S.K.; Barraud, N.; Pham, A.; Iskander, G.; Rice, S.A.; Black, D.S.; Kumar, N. Design, synthesis, and evaluation of fimbrolide-nitric oxide donor hybrids as antimicrobial agents. J. Med. Chem., 2013, 56(23), 9517-9529.
[http://dx.doi.org/10.1021/jm400951f] [PMID: 24191659]
[86]
Kutty, S.K.; Barraud, N.; Ho, K.K.K.; Iskander, G.M.; Griffith, R.; Rice, S.A.; Bhadbhade, M.; Willcox, M.D.P.; Black, D.S.; Kumar, N. Hybrids of acylated homoserine lactone and nitric oxide donors as inhibitors of quorum sensing and virulence factors in Pseudomonas aeruginosa. Org. Biomol. Chem., 2015, 13(38), 9850-9861.
[http://dx.doi.org/10.1039/C5OB01373A] [PMID: 26282835]
[87]
Nguyen, T-K.; Selvanayagam, R.; Ho, K.K.K.; Chen, R.; Kutty, S.K.; Rice, S.A.; Kumar, N.; Barraud, N.; Duong, H.T.T.; Boyer, C. Co-delivery of nitric oxide and antibiotic using polymeric nanoparticles. Chem. Sci. (Camb.), 2016, 7(2), 1016-1027.
[http://dx.doi.org/10.1039/C5SC02769A] [PMID: 28808526]
[88]
Sundaramoorthy, N.S.; Suresh, P.; Selva Ganesan, S.; GaneshPrasad, A.; Nagarajan, S. Restoring colistin sensitivity in colistin-resistant E. coli: Combinatorial use of MarR inhibitor with efflux pump inhibitor. Sci. Rep., 2019, 9(1), 19845.
[http://dx.doi.org/10.1038/s41598-019-56325-x] [PMID: 31882661]
[89]
Asaithampi, G. Identification of benzochromene derivatives as a highly specific NorA efflux pump inhibitor to mitigate the drug resistant strains of S. aureus. In: RSC Advances; , 2016; 6, pp. (36)30258-30267.
[90]
Yang, X.; Domalaon, R.; Lyu, Y.; Zhanel, G.G.; Schweizer, F. Tobramycin-linked efflux pump inhibitor conjugates synergize Fluoroquinolones, Rifampicin and Fosfomycin against multidrug-resistant Pseudomonas aeruginosa. J. Clin. Med., 2018, 7(7), 158.
[http://dx.doi.org/10.3390/jcm7070158] [PMID: 29932132]
[91]
Yamaguchi, A.; Ohmori, H.; Kaneko-Ohdera, M.; Nomura, T.; Sawai, T. Delta pH-dependent accumulation of tetracycline in Escherichia coli. Antimicrob. Agents Chemother., 1991, 35(1), 53-56.
[http://dx.doi.org/10.1128/AAC.35.1.53] [PMID: 2014981]
[92]
Zhang, L-H.; Dong, Y-H. Quorum sensing and signal interference: Diverse implications. Mol. Microbiol., 2004, 53(6), 1563-1571.
[http://dx.doi.org/10.1111/j.1365-2958.2004.04234.x] [PMID: 15341639]
[93]
Rajput, A.; Kaur, K.; Kumar, M. SigMol: Repertoire of quorum sensing signaling molecules in prokaryotes. Nucleic Acids Res., 2016, 44(D1), D634-D639.
[http://dx.doi.org/10.1093/nar/gkv1076] [PMID: 26490957]
[94]
Waters, C.M.; Bassler, B.L. Quorum sensing: Cell-to-cell communication in bacteria. Annu. Rev. Cell Dev. Biol., 2005, 21(1), 319-346.
[http://dx.doi.org/10.1146/annurev.cellbio.21.012704.131001] [PMID: 16212498]
[95]
Lansdown, A.B.G. Silver in health care: Antimicrobial effects and safety in use. Curr. Probl. Dermatol., 2006, 33, 17-34.
[http://dx.doi.org/10.1159/000093928] [PMID: 16766878]
[96]
Yu, H.; Sun, H.; Yin, C.; Lin, Z. Combination of sulfonamides, silver antimicrobial agents and quorum sensing inhibitors as a preferred approach for improving antimicrobial efficacy against Bacillus subtilis. Ecotoxicol. Environ. Saf., 2019, 181, 43-48.
[http://dx.doi.org/10.1016/j.ecoenv.2019.05.064] [PMID: 31158722]
[97]
Zarfl, C.; Matthies, M.; Klasmeier, J. A mechanistical model for the uptake of sulfonamides by bacteria. Chemosphere, 2008, 70(5), 753-760.
[http://dx.doi.org/10.1016/j.chemosphere.2007.07.045] [PMID: 17765286]
[98]
Wang, D.; Lin, Z.; Ding, X.; Hu, J.; Liu, Y. The Comparison of the Combined Toxicity between Gram-negative and Gram-positive bacteria: A case study of antibiotics and Quorum-sensing inhibitors. Mol. Inform., 2016, 35(2), 54-61.
[http://dx.doi.org/10.1002/minf.201500061] [PMID: 27491790]
[99]
Allegra, C.J.; Boarman, D.; Kovacs, J.A.; Morrison, P.; Beaver, J.; Chabner, B.A.; Masur, H. Interaction of sulfonamide and sulfone compounds with Toxoplasma gondii dihydropteroate synthase. J. Clin. Invest., 1990, 85(2), 371-379.
[http://dx.doi.org/10.1172/JCI114448] [PMID: 2298911]
[100]
Ejim, L.; Farha, M.A.; Falconer, S.B.; Wildenhain, J.; Coombes, B.K.; Tyers, M.; Brown, E.D.; Wright, G.D. Combinations of antibiotics and nonantibiotic drugs enhance antimicrobial efficacy. Nat. Chem. Biol., 2011, 7(6), 348-350.
[http://dx.doi.org/10.1038/nchembio.559] [PMID: 21516114]
[101]
Bernal, P.; Molina-Santiago, C.; Daddaoua, A.; Llamas, M.A. Antibiotic adjuvants: Identification and clinical use. Microb. Biotechnol., 2013, 6(5), 445-449.
[http://dx.doi.org/10.1111/1751-7915.12044] [PMID: 23445397]
[102]
Sharma, A.; Gupta, V.K.; Pathania, R. Efflux pump inhibitors for bacterial pathogens: From bench to bedside. Indian J. Med. Res., 2019, 149(2), 129-145.
[http://dx.doi.org/10.4103/ijmr.IJMR_2079_17] [PMID: 31219077]
[103]
Martin, J.K., II; Sheehan, J.P.; Bratton, B.P.; Moore, G.M.; Mateus, A.; Li, S.H.-J.; Kim, H.; Rabinowitz, J.D.; Typas, A.; Savitski, M.M.J.C. A dual-mechanism antibiotic kills gram-negative bacteria and avoids drug resistance. Cell, 2020, 181(7), 1518-1532.
[http://dx.doi.org/10.1016/j.cell.2020.05.005]

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