A hydrogel-based in vitro assay for the fast prediction of antibiotic accumulation in Gram-negative bacteria

Materials Today Bio - Tập 8 - Trang 100084 - 2020
Robert Richter1,2, Mohamed.A.M. Kamal1, Mariel A. García-Rivera3, Jerome Kaspar4, Maximilian Junk4, Walid A.M. Elgaher1, Sanjay Kumar Srikakulam1, Alexander Gress1, Anja Beckmann5, Alexander Grißmer5, Carola Meier5, Michael Vielhaber4, Olga Kalinina1,6, Anna K.H. Hirsch1,2, Rolf W. Hartmann1, Mark Brönstrup3,7, Nicole Schneider-Daum1, Claus-Michael Lehr1,2
1Helmholtz Institute for Pharmaceutical Research Saarland (HIPS) – Helmholtz Centre for Infection Research (HZI), 66123 Saarbrücken, Germany
2Department of Pharmacy, Saarland University, 66123 Saarbrücken, Germany
3Department of Chemical Biology, Helmholtz Centre for Infection Research (HZI), 38124 Braunschweig, Germany
4Institute of Engineering Design, Saarland University, 66123 Saarbrücken, Germany
5Department of Anatomy and Cell Biology, Saarland University, 66421 Homburg, Germany
6Medical Faculty, Saarland University, 66421 Homburg, Germany
7German Centre for Infection Research (DZIF), 38124 Braunschweig, Germany

Tài liệu tham khảo

Nathan, 2014, Antibiotic resistance - problems, progress, and prospects, N. Engl. J. Med., 371, 1761, 10.1056/NEJMp1408040 Silver, 2011, Challenges of antibacterial discovery, Clin. Microbiol. Rev., 24, 71, 10.1128/CMR.00030-10 Aslam, 2018, Antibiotic resistance: a rundown of a global crisis, Infect. Drug Resist., 11, 1645, 10.2147/IDR.S173867 Theuretzbacher, 2017 Brown, 2016, Antibacterial drug discovery in the resistance era, Nature, 529, 336, 10.1038/nature17042 Nikaido, 2003, Molecular basis of bacterial outer membrane permeability revisited, Microbiol. Mol. Biol. Rev., 67, 593, 10.1128/MMBR.67.4.593-656.2003 Hancock, 1987, Role of porins in outer membrane permeability, J. Bacteriol., 169, 929, 10.1128/jb.169.3.929-933.1987 Santos, 2018, Nanomaterials and molecular transporters to overcome the bacterial envelope barrier: towards advanced delivery of antibiotics, Adv. Drug Deliv. Rev., 136–137, 28, 10.1016/j.addr.2017.12.010 Costerton, 1975, The role of the bacterial cell envelope in antibiotic resistance, J. Antimicrob. Chemother., 1, 363, 10.1093/jac/1.4.363 Graef, 2016, Anti-infectives in drug delivery—overcoming the gram-negative bacterial cell envelope, Curr. Top. Microbiol. Immunol., 398, 475 Hancock, 1988, Antibiotic uptake into gram-negative bacteria, Eur. J. Clin. Microbiol. Infect. Dis., 7, 713, 10.1007/BF01975036 Nakae, 1986, Outer-membrane permeability of bacteria, Crit. Rev. Microbiol., 13, 1, 10.3109/10408418609108734 Pagès, 2008, The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria, Nat. Rev. Microbiol., 6, 893, 10.1038/nrmicro1994 Masi, 2017, Mechanisms of envelope permeability and antibiotic influx and efflux in Gram-negative bacteria, Nat. Microbiol., 2, 10.1038/nmicrobiol.2017.1 Vergalli, 2020, The challenge of intracellular antibiotic accumulation, a function of fluoroquinolone influx versus bacterial efflux, Commun. Biol., 3, 1, 10.1038/s42003-020-0929-x Acosta-Gutiérrez, 2020 Richter, 2017, Predictive compound accumulation rules yield a broad-spectrum antibiotic, Nature, 545, 299, 10.1038/nature22308 Bafna, 2020, Kanamycin uptake into Escherichia coli is facilitated by OmpF and OmpC porin channels located in the outer membrane, ACS Infect. Dis., 6, 1855, 10.1021/acsinfecdis.0c00102 Yoshimura, 1985, Diffusion of β-lactam antibiotics through the porin channels of Escherichia coli K-12, Antimicrob, Agents Chemother, 27, 84, 10.1128/AAC.27.1.84 Galdiero, 2013, Microbe-host interactions: structure and role of gram-negative bacterial porins, Curr. Protein Pept. Sci., 13, 843, 10.2174/138920312804871120 Nikaido, 1983, Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins, J. Bacteriol., 153, 241, 10.1128/jb.153.1.241-252.1983 Ferreira, 2019, Antibiotic uptake across gram-negative outer membranes: better predictions towards better antibiotics, ACS Infect. Dis., 5, 2096, 10.1021/acsinfecdis.9b00201 Nakae, 1975, Outer membrane of Salmonella typhimurium: reconstitution of sucrose-permeable membrane vesicles, Biochem. Biophys. Res. Commun., 64, 1224, 10.1016/0006-291X(75)90823-2 Nestorovich, 2002, Designed to penetrate: time-resolved interaction of single antibiotic molecules with bacterial pores, Proc. Natl. Acad. Sci. U.S.A., 99, 9789, 10.1073/pnas.152206799 Bajaj, 2017, Bacterial outer membrane porins as electrostatic nanosieves: exploring transport rules of small polar molecules, ACS Nano, 11, 5465, 10.1021/acsnano.6b08613 Wang, 2020, Electrophysiological characterization of transport across outer membrane channels from Gram-negative bacteria in presence of lipopolysaccharides (LPS), Angew. Chem. Int. Ed., 1 Zimmermann, 1977, Function of the outer membrane of Escherichia coli as a permeability barrier to beta lactam antibiotics, Antimicrob. Agents Chemother., 12, 368, 10.1128/AAC.12.3.368 Decad, 1974, Permeability of Escherichia coli and Salmonella typhimurium cell wall to Oligosaccharides, Fed. Proc., 33, 1240 Prochnow, 2019, Subcellular quantification of uptake in gram-negative bacteria, Anal. Chem., 91, 1863, 10.1021/acs.analchem.8b03586 Iyer, 2017, Whole-cell-based assay to evaluate structure permeation relationships for carbapenem passage through the Pseudomonas aeruginosa porin OprD, ACS Infect. Dis., 3, 310, 10.1021/acsinfecdis.6b00197 Prajapati, 2017, Characterization of ciprofloxacin permeation pathways across the porin OmpC using metadynamics and a string method, J. Chem. Theor. Comput., 13, 4553, 10.1021/acs.jctc.7b00467 Acosta-Gutiérrez, 2018, Getting drugs into gram-negative bacteria: rational rules for permeation through general porins, ACS Infect. Dis., 4, 1487, 10.1021/acsinfecdis.8b00108 Pothula, 2016, Simulations of outer membrane channels and their permeability, Biochim. Biophys. Acta Biomembr., 1858, 1760, 10.1016/j.bbamem.2015.12.020 Sousa, 2017, The binding of free and copper-complexed fluoroquinolones to OmpF porins: an experimental and molecular docking study, RSC Adv., 7, 10009, 10.1039/C6RA26466B Decad, 1976, Outer membrane of gram negative bacteria. XII. Molecular sieving function of cell wall, J. Bacteriol., 128, 325, 10.1128/jb.128.1.325-336.1976 O'Shea, 2008, Physicochemical properties of antibacterial compounds: implications for drug discovery, J. Med. Chem., 51, 2871, 10.1021/jm700967e Brown, 2014, Trends and exceptions of physical properties on antibacterial activity for gram-positive and gram-negative pathogens, J. Med. Chem., 57, 10144, 10.1021/jm501552x Vergalli, 2019, Porins and small- molecule translocation across the outer membrane of Gram-negative bacteria, Nat. Rev. Microbiol., 18, 164, 10.1038/s41579-019-0294-2 Van Breemen, 2005, Caco-2 cell permeability assays to measure drug absorption, Expet Opin. Drug Metabol. Toxicol., 1, 175, 10.1517/17425255.1.2.175 Berben, 2018, Drug permeability profiling using cell-free permeation tools: overview and applications, Eur. J. Pharmaceut. Sci., 119, 219, 10.1016/j.ejps.2018.04.016 Tommasi, 2018, Antibacterial drug discovery: some assembly required, ACS Infect. Dis., 4, 686, 10.1021/acsinfecdis.8b00027 Graef, 2018, In vitro model of the gram-negative bacterial cell envelope for investigation of anti-infective permeation kinetics, ACS Infect. Dis., 4, 1188, 10.1021/acsinfecdis.7b00165 Lieleg, 2011, Biological hydrogels as selective diffusion barriers, Trends Cell Biol., 21, 543, 10.1016/j.tcb.2011.06.002 Wheeler, 2019, Mucin glycans attenuate the virulence of Pseudomonas aeruginosa in infection, Nat. Microbiol., 4, 2146, 10.1038/s41564-019-0581-8 Smithies, 1955, Zone electrophoresis in starch gels: group variations in the serum proteins of normal human adults, Biochem. J., 61, 629, 10.1042/bj0610629 Bachvaroff, 1964, Region of rapidly, Science (80-. ), 143, 1177, 10.1126/science.143.3611.1177 Lathe, 1956, Separation of substances and estimation of their relative molecular sizes by the use of columns of starch in water, Biochem. J., 62, 665, 10.1042/bj0620665 Elgaher, 2016, Discovery and structure-based optimization of 2-Ureidothiophene-3-carboxylic acids as dual bacterial RNA polymerase and viral reverse transcriptase inhibitors, J. Med. Chem., 59, 7212, 10.1021/acs.jmedchem.6b00730 Elgaher, 2014, Expanding the scaffold for bacterial RNA polymerase inhibitors: design, synthesis and structure-activity relationships of ureido-heterocyclic-carboxylic acids, RSC Adv., 4, 2177, 10.1039/C3RA45820B Liaw, 2002, Classification and regression by randomForest, R. News, 2, 18 Delcour, 2009, Outer membrane permeability and antibiotic resistance, Biochim. Biophys. Acta, 1794, 808, 10.1016/j.bbapap.2008.11.005 Williams, 1998, Accumulation of rifampicin by Escherichia coli and Staphylococcus aureus, J. Antimicrob. Chemother., 42, 597, 10.1093/jac/42.5.597 Vaara, 1993, Comparative activity of rifabutin and rifampicin against Gram-negative bacteria that have damaged or defective outer membranes, J. Antimicrob. Chemother., 31, 799, 10.1093/jac/31.5.799-a Amsden, 1998, Solute diffusion within hydrogels. Mechanisms and models, Macromolecules, 31, 8382, 10.1021/ma980765f Axpe, 2019, A multiscale model for solute diffusion in hydrogels, Macromolecules, 52, 6889, 10.1021/acs.macromol.9b00753 Wang, 2015, vol. 14 Siviello, 2016, Analysis of the aging effects on the viscoelasticity of alginate gels, Soft Matter, 12, 8726, 10.1039/C6SM01671E Alemán, 2007, Definitions of terms relating to the structure and processing of sols, gels, networks, and inorganic-organic hybrid materials (IUPAC recommendations 2007), Pure Appl. Chem., 79, 1801, 10.1351/pac200779101801 Phan, 2017, The fitness costs and trade-off shapes associated with the exclusion of nine antibiotics by OmpF porin channels, ISME J., 11, 1472, 10.1038/ismej.2016.202 Chopra, 2001, Tetracycline Antibiotics : mode of action , applications , molecular biology , and epidemiology of bacterial resistance, Microbiol. Mol. Biol. Rev., 65, 232, 10.1128/MMBR.65.2.232-260.2001 Someya, 1995, A novel glycylcycline, 9-(N,N-dimethylglycylamido)-6-demethyl-6- deoxytetracycline, is neither transported nor recognized by the transposon Tn10-encoded metal-tetracycline/H+ antiporter, Antimicrob. Agents Chemother., 39, 247, 10.1128/AAC.39.1.247 Richter, 2019, The challenge of converting gram-positive-only compounds into broad-spectrum antibiotics, Ann. N. Y. Acad. Sci., 1435, 18, 10.1111/nyas.13598 Ruggiu, 2019, Size matters and how you measure it: a gram-negative antibacterial example exceeding typical molecular weight limits, ACS Infect. Dis., 5, 1688, 10.1021/acsinfecdis.9b00256 Nikaido, 1994, Porins and specific diffusion channels in bacterial outer membranes, J. Biol. Chem., 269, 3905, 10.1016/S0021-9258(17)41716-9 Zgurskaya, 2015, Permeability barrier of gram-negative cell envelopes and approaches to bypass it, Physiol. Behav., 1, 512 Cooper, 2018, Molecular properties that define the activities of antibiotics in Escherichia coli and Pseudomonas aeruginosa, ACS Infect. Dis., 4, 1223, 10.1021/acsinfecdis.8b00036 Parker, 2019, Implementation of permeation rules leads to a FabI inhibitor with activity against Gram-negative pathogens, Nat. Microbiol., 1 Widya, 2019, Development and optimization of a higher-throughput bacterial compound accumulation assay, ACS Infect. Dis., 5, 394, 10.1021/acsinfecdis.8b00299 Tabary, 1987, Effect of DNA gyrase inhibitors pefloxacin, five other quinolones, novobiocin, and clorobiocin on Escherichia coli topoisomerase I, Antimicrob. Agents Chemother., 31, 1925, 10.1128/AAC.31.12.1925 2017 2020