Potent, specific MEPicides for treatment of zoonotic staphylococci
Autoři:
Rachel L. Edwards aff001; Isabel Heueck aff001; Soon Goo Lee aff002; Ishaan T. Shah aff001; Justin J. Miller aff001; Andrew J. Jezewski aff003; Marwa O. Mikati aff001; Xu Wang aff004; Robert C. Brothers aff004; Kenneth M. Heidel aff004; Damon M. Osbourn aff005; Carey-Ann D. Burnham aff001; Sophie Alvarez aff007; Stephanie A. Fritz aff001; Cynthia S. Dowd aff004; Joseph M. Jez aff008; Audrey R. Odom John aff001
Působiště autorů:
Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri, United States of America
aff001; University of North Carolina-Wilmington, Wilmington, North Carolina, United States of America
aff002; Department of Molecular Microbiology, Washington University School of Medicine, St. Louis, Missouri, United States of America
aff003; Department of Chemistry, George Washington University, Washington, DC, United States of America
aff004; Department of Chemistry, Saint Louis University, St. Louis, Missouri, United States of America
aff005; Department of Pathology and Immunology, Washington University School of Medicine, St. Louis, Missouri, United States of America
aff006; Department of Agronomy and Horticulture, University of Nebraska-Lincoln, Lincoln, Nebraska, United States of America
aff007; Department of Biology, Washington University, St. Louis, Missouri, United States of America
aff008
Vyšlo v časopise:
Potent, specific MEPicides for treatment of zoonotic staphylococci. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1007806
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.ppat.1007806
Souhrn
Coagulase-positive staphylococci, which frequently colonize the mucosal surfaces of animals, also cause a spectrum of opportunistic infections including skin and soft tissue infections, urinary tract infections, pneumonia, and bacteremia. However, recent advances in bacterial identification have revealed that these common veterinary pathogens are in fact zoonoses that cause serious infections in human patients. The global spread of multidrug-resistant zoonotic staphylococci, in particular the emergence of methicillin-resistant organisms, is now a serious threat to both animal and human welfare. Accordingly, new therapeutic targets that can be exploited to combat staphylococcal infections are urgently needed. Enzymes of the methylerythritol phosphate pathway (MEP) of isoprenoid biosynthesis represent potential targets for treating zoonotic staphylococci. Here we demonstrate that fosmidomycin (FSM) inhibits the first step of the isoprenoid biosynthetic pathway catalyzed by deoxyxylulose phosphate reductoisomerase (DXR) in staphylococci. In addition, we have both enzymatically and structurally determined the mechanism by which FSM elicits its effect. Using a forward genetic screen, the glycerol-3-phosphate transporter GlpT that facilitates FSM uptake was identified in two zoonotic staphylococci, Staphylococcus schleiferi and Staphylococcus pseudintermedius. A series of lipophilic ester prodrugs (termed MEPicides) structurally related to FSM were synthesized, and data indicate that the presence of the prodrug moiety not only substantially increased potency of the inhibitors against staphylococci but also bypassed the need for GlpT-mediated cellular transport. Collectively, our data indicate that the prodrug MEPicides selectively and robustly inhibit DXR in zoonotic staphylococci, and further, that DXR represents a promising, druggable target for future development.
Klíčová slova:
Antimicrobial resistance – Esters – Isoprenoids – Staphylococcal infection – Staphylococcus – Zoonoses – Pro-drugs – Phosphonic acids
Zdroje
1. Jindal A, Shivpuri D, Sood S. Staphylococcus schleiferi meningitis in a child. Pediatr Infect J. 2015;34(3):329.
2. Somayaji R, Rubin JE, Priyantha MA, Church D. Exploring Staphylococcus pseudintermedius: an emerging zoonotic pathogen? Future Microbiol. 2016 Oct 18;11(11):1371–4.
3. Börjesson S, Gómez-Sanz E, Ekström K, Torres C, Grönlund U. Staphylococcus pseudintermedius can be misdiagnosed as Staphylococcus aureus in humans with dog bite wounds. Eur J Clin Microbiol Infect Dis. 2015 Apr 23;34(4):839–44. doi: 10.1007/s10096-014-2300-y 25532507
4. Lainhart W, Yarbrough ML, Burnham CA. The brief case: Staphylococcus intermedius group-look what the dog dragged in. J Clin Microbiol. 2018 Feb;56(2).
5. Rojas-Marte G, Victor J, Shenoy A, Yakubov S, Chapnick E, Lin YS. Pacemaker-associated infective endocarditis caused by Staphylococcus schleiferi. Infect Dis Clin Pract. 2014;22(5):302–4.
6. Pottumarthy S, Schapiro JM, Prentice JL, Houze YB, Swanzy SR, Fang FC, et al. Clinical isolates of Staphylococcus intermedius masquerading as methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2004 Dec 1;42(12):5881–4. doi: 10.1128/JCM.42.12.5881-5884.2004 15583331
7. Yarbrough ML, Lainhart W, Burnham CA. Epidemiology, clinical characteristics, and antimicrobial susceptibility profiles of human clinical isolates of Staphylococcus intermedius group. J Clin Microbiol. 2018 Mar 1;56(3):e01788–17. doi: 10.1128/JCM.01788-17 29305548
8. Ross Fitzgerald J. The Staphylococcus intermedius group of bacterial pathogens: species re-classification, pathogenesis and the emergence of meticillin resistance. Vet Dermatol. 2009 Oct;20(5–6):490–5. doi: 10.1111/j.1365-3164.2009.00828.x 20178486
9. Humphries RM, Wu MT, Westblade LF, Robertson AE, Burnham C-AD, Wallace MA, et al. In vitro antimicrobial susceptibility of Staphylococcus pseudintermedius isolates of human and animal origin. J Clin Microbiol. 2016;54(5):1391–4. doi: 10.1128/JCM.00270-16 26962087
10. Beever L, Bond R, Graham PA, Jackson B, Lloyd DH, Loeffler A. Increasing antimicrobial resistance in clinical isolates of Staphylococcus intermedius group bacteria and emergence of MRSP in the UK. Vet Rec. 2015 Feb 14;176(7):172. doi: 10.1136/vr.102651 25376505
11. Lange BM, Rujan T, Martin W, Croteau R. Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes. Proc Natl Acad Sci. 2000;97(24):13172–7. doi: 10.1073/pnas.240454797 11078528
12. Wilding EI, Kim DY, Bryant AP, Gwynn MN, Lunsford RD, McDevitt D, et al. Essentiality, expression, and characterization of the class II 3-hydroxy-3-methylglutaryl coenzyme A reductase of Staphylococcus aureus. J Bacteriol. 2000 Sep;182(18):5147–52. doi: 10.1128/jb.182.18.5147-5152.2000 10960099
13. Matsumoto Y, Yasukawa J, Ishii M, Hayashi Y, Miyazaki S, Sekimizu K. A critical role of mevalonate for peptidoglycan synthesis in Staphylococcus aureus. Sci Rep. 2016 Mar 10;6:22894. doi: 10.1038/srep22894 26961421
14. Liu C-I, Liu GY, Song Y, Yin F, Hensler ME, Jeng W-Y, et al. A cholesterol biosynthesis inhibitor blocks Staphylococcus aureus virulence. Science. 2008 Mar 7;319(5868):1391–4. doi: 10.1126/science.1153018 18276850
15. Misic AM, Cain CL, Morris DO, Rankin SC, Beiting DP. Divergent isoprenoid biosynthesis pathways in Staphylococcus species constitute a drug target for treating infections in companion animals. mSphere. 2014;1(5):1–11.
16. Nair SC, Brooks CF, Goodman CD, Sturm A, Strurm A, McFadden GI, et al. Apicoplast isoprenoid precursor synthesis and the molecular basis of fosmidomycin resistance in Toxoplasma gondii. J Exp Med. 2011 Jul 4;208(7):1547–59. doi: 10.1084/jem.20110039 21690250
17. Odom AR, Van Voorhis WC. Functional genetic analysis of the Plasmodium falciparum deoxyxylulose 5-phosphate reductoisomerase gene. Mol Biochem Parasitol. 2010 Apr;170(2):108–11. doi: 10.1016/j.molbiopara.2009.12.001 20018214
18. Brown AC, Parish T. Dxr is essential in Mycobacterium tuberculosis and fosmidomycin resistance is due to a lack of uptake. BMC Microbiol. 2008 May 20;8:78. doi: 10.1186/1471-2180-8-78 18489786
19. McAteer S, Coulson A, McLennan N, Masters M. The lytB gene of Escherichia coli is essential and specifies a product needed for isoprenoid biosynthesis. J Bacteriol. 2001 Dec;183(24):7403–7. doi: 10.1128/JB.183.24.7403-7407.2001 11717301
20. Wagner WP, Helmig D, Fall R. Isoprene biosynthesis in Bacillus subtilis via the methylerythritol phosphate pathway. J Nat Prod. 2000 Jan 63(1):37–40. doi: 10.1021/np990286p 10650075
21. McKenney ES, Sargent M, Khan H, Uh E, Jackson ER, San Jose G, et al. Lipophilic prodrugs of FR900098 are antimicrobial against Francisella novicida in vivo and in vitro and show GlpT independent efficacy. PLoS One. 2012;7(10):e38167. doi: 10.1371/journal.pone.0038167 23077474
22. Koppisch AT, Fox DT, Blagg BSJ, Poulter CD. E. coli MEP synthase: Steady-state kinetic analysis and substrate binding. Biochemistry. 2002;41(1):236–43. doi: 10.1021/bi0118207 11772021
23. Kuemmerle HP, Murakawa T, Sakamoto H, Sato N, Konishi T, De Santis F. Fosmidomycin, a new phosphonic acid antibiotic. Part II: 1. Human pharmacokinetics. 2. Preliminary early phase IIa clinical studies. Int J Clin Pharmacol Ther Toxicol. 1985 Oct;23(10):521–8. 4066076
24. Borrmann S, Lundgren I, Oyakhirome S, Impouma B, Matsiegui P-B, Adegnika AA, et al. Fosmidomycin plus clindamycin for treatment of pediatric patients aged 1 to 14 years with Plasmodium falciparum malaria. Antimicrob Agents Chemother. 2006 Aug 1;50(8):2713–8. doi: 10.1128/AAC.00392-06 16870763
25. Tsuchiya T, Ishibashi K, Terakawa M, Nishiyama M, Itoh N, Noguchi H. Pharmacokinetics and metabolism of fosmidomycin, a new phosphonic acid, in rats and dogs. Eur J Drug Metab Pharmacokinet.1982;7(1):59–64. doi: 10.1007/BF03189544 7067725
26. Dhiman RK, Schaeffer ML, Bailey AM, Testa CA, Scherman H, Crick DC. 1-deoxy-D-xylulose 5-phosphate reductoisomerase (IspC) from Mycobacterium tuberculosis: towards understanding mycobacterial resistance to fosmidomycin. J Bacteriol. 2005 Dec;187(24):8395–402. doi: 10.1128/JB.187.24.8395-8402.2005 16321944
27. Mackie RS, McKenney ES, van Hoek ML. Resistance of Francisella novicida to fosmidomycin associated with mutations in the glycerol-3-phosphate transporter. Front Microbiol. 2012;3:226. doi: 10.3389/fmicb.2012.00226 22905031
28. Sakamoto Y, Furukawa S, Ogihara H, Yamasaki M. Fosmidomycin resistance in adenylate cyclase deficient (cya) mutants of Escherichia coli. Biosci Biotechnol Biochem. 2003 Jan 22;67(9):2030–3. doi: 10.1271/bbb.67.2030 14519998
29. Argyrou A, Blanchard JS. Kinetic and chemical mechanism of Mycobacterium tuberculosis 1-deoxy-D-xylulose-5-phosphate isomeroreductase. Biochemistry. 2004;43(14):4375–84. doi: 10.1021/bi049974k 15065882
30. Kuzuyama T, Takahashi S, Takagi M, Seto H. Characterization of 1-deoxy-D-xylulose 5-phosphate reductoisomerase, an enzyme involved in isopentenyl diphosphate biosynthesis, and identification of its catalytic amino acid residues. J Biol Chem. 2000;275(26):19928–32. doi: 10.1074/jbc.M001820200 10787409
31. Yajima Shunsuke, Hara Kodai, Sanders John M., Yin Fenglin, Ohsawa Kanju, Wiesner Jochen, et al. Crystallographic structures of two bisphosphonate:1-deoxyxylulose-5-phosphate reductoisomerase complexes. 2004; 126(35):10824–10825. doi: 10.1021/ja040126m 15339150
32. Yajima S, Nonaka T, Kuzuyama T, Seto H, Ohsawa K. Crystal structure of 1-deoxy-D-xylulose 5-phosphate reductoisomerase complexed with cofactors: implications of a flexible loop movement upon substrate binding. J Biochem. 2002;131(3):313–7. doi: 10.1093/oxfordjournals.jbchem.a003105 11872159
33. Yajima S, Hara K, Iino D, Sasaki Y, Kuzuyama T, Ohsawa K, et al. Structure of 1-deoxy-D-xylulose 5-phosphate reductoisomerase in a quaternary complex with a magnesium ion, NADPH and the antimalarial drug fosmidomycin. Acta Crystallogr Sect F Struct Biol Cryst Commun. 2007 Jun 1;63(Pt 6):466–70. doi: 10.1107/S1744309107024475 17554164
34. Behrendt CT, Kunfermann A, Illarionova V, Matheeussen A, Pein MK, Gräwert T, et al. Reverse fosmidomycin derivatives against the antimalarial drug target IspC (Dxr). J Med Chem. 2011 Oct 13;54(19):6796–802. doi: 10.1021/jm200694q 21866890
35. Deng L, Endo K, Kato M, Cheng G, Yajima S, Song Y. Structures of 1-deoxy-D-xylulose-5-phosphate reductoisomerase/lipophilic phosphonate complexes. ACS Med Chem Lett. 2011 Feb 10;2(2):165–70. doi: 10.1021/ml100243r 21379374
36. Sooriyaarachchi S, Chofor R, Risseeuw MDP, Bergfors T, Pouyez J, Dowd CS, et al. Targeting an aromatic hotspot in Plasmodium falciparum 1-deoxy-D-xylulose-5-phosphate reductoisomerase with β-arylpropyl analogues of fosmidomycin. ChemMedChem. 2016 Sep 20;11(18):2024–36. doi: 10.1002/cmdc.201600249 27487410
37. Mac Sweeney A, Lange R, Fernandes RPM, Schulz H, Dale GE, Douangamath A, et al. The crystal structure of E. coli 1-deoxy-D-xylulose-5-phosphate reductoisomerase in a ternary complex with the antimalarial compound fosmidomycin and NADPH reveals a tight-binding closed enzyme conformation. J Mol Biol. 2005 Jan 7;345(1):115–27. doi: 10.1016/j.jmb.2004.10.030 15567415
38. Kholodar SA, Tombline G, Liu J, Tan Z, Allen CL, Gulick AM, et al. Alteration of the flexible loop in 1-deoxy-D-xylulose-5-phosphate reductoisomerase boosts enthalpy-driven inhibition by fosmidomycin. Biochemistry. 2014 Jun 3;53(21):3423–31. doi: 10.1021/bi5004074 24825256
39. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, Bork P, et al. A method and server for predicting damaging missense mutations. Nat Methods. 2010 Apr;7(4):248–9. doi: 10.1038/nmeth0410-248 20354512
40. Murakawa T, Sakamoto H, Fukada S, Konishi T, Nishida M. Pharmacokinetics of fosmidomycin, a new phosphonic acid antibiotic. Antimicrob Agents Chemother. 1982 Feb;21(2):224–30. doi: 10.1128/aac.21.2.224 7073262
41. Jackson ER, San Jose G, Brothers RC, Edelstein EK, Sheldon Z, Haymond A, et al. The effect of chain length and unsaturation on Mtb Dxr inhibition and antitubercular killing activity of FR900098 analogs. Bioorg Med Chem Lett. 2014 Jan 15;24(2):649–53. doi: 10.1016/j.bmcl.2013.11.067 24360562
42. Edwards RL, Brothers RC, Wang X, Maron MI, Ziniel PD, Tsang PS, et al. MEPicides: potent antimalarial prodrugs targeting isoprenoid biosynthesis. Sci Rep. 2017;7(1):8400. doi: 10.1038/s41598-017-07159-y 28827774
43. Uh E, Jackson ER, San Jose G, Maddox M, Lee RE, Lee RE, et al. Antibacterial and antitubercular activity of fosmidomycin, FR900098, and their lipophilic analogs. Bioorg Med Chem Lett. 2011 Dec 1;21(23):6973–6. doi: 10.1016/j.bmcl.2011.09.123 22024034
44. San Jose G, Jackson ER, Haymond A, Johny C, Edwards RL, Wang X, et al. Structure–Activity Relationships of the MEPicides: N -Acyl and O -Linked Analogs of FR900098 as Inhibitors of Dxr from Mycobacterium tuberculosis and Yersinia pestis. ACS Infect Dis. 2016;2(12):923–35. doi: 10.1021/acsinfecdis.6b00125 27676224
45. Brücher K, Gräwert T, Konzuch S, Held J, Lienau C, Behrendt C, et al. Prodrugs of reverse fosmidomycin analogues. J Med Chem. 2015 Feb 26;58(4):2025–35. doi: 10.1021/jm5019719 25633870
46. Faísca Phillips AM, Nogueira F, Murtinheira F, Barros MT. Synthesis and antimalarial evaluation of prodrugs of novel fosmidomycin analogues. Bioorg Med Chem Lett. 2015 Jan;25(10):2112–6. doi: 10.1016/j.bmcl.2015.03.077 25881827
47. Brücher K, Illarionov B, Held J, Tschan S, Kunfermann A, Pein MK, et al. α-Substituted β-oxa isosteres of fosmidomycin: synthesis and biological evaluation. J Med Chem. 2012 Jul 26;55(14):6566–75. doi: 10.1021/jm300652f 22731758
48. Haemers T, Wiesner J, Giessmann D, Verbrugghen T, Hillaert U, Ortmann R, et al. Synthesis of β- and γ-oxa isosteres of fosmidomycin and FR900098 as antimalarial candidates. Bioorg Med Chem. 2008 Mar 15;16(6):3361–71. doi: 10.1016/j.bmc.2007.12.001 18158249
49. Wiesner J, Ortmann R, Jomaa H, Schlitzer M. Double ester prodrugs of FR900098 display enhanced in-vitro antimalarial activity. Arch Pharm (Weinheim). 2007 Dec;340(12):667–9. doi: 10.1002/ardp.200700069 17994601
50. Kurz T, Schlüter K, Pein M, Behrendt C, Bergmann B, Walter RD. Conformationally restrained aromatic analogues of fosmidomycin and FR900098. Arch Pharm (Weinheim). 2007 Jul 1;340(7):339–44. doi: 10.1002/ardp.200700013 17611943
51. Kurz T, Schlüter K, Kaula U, Bergmann B, Walter RD, Geffken D. Synthesis and antimalarial activity of chain substituted pivaloyloxymethyl ester analogues of fosmidomycin and FR900098. Bioorg Med Chem. 2006;14(15):5121–35. doi: 10.1016/j.bmc.2006.04.018 16679022
52. Schlüter K, Walter RD, Bergmann B, Kurz T. Arylmethyl substituted derivatives of fosmidomycin: synthesis and antimalarial activity. Eur J Med Chem. 2006 Dec 1;41(12):1385–97. doi: 10.1016/j.ejmech.2006.06.015 17055117
53. Wang X, Edwards R, Ball H, Johnson C, Haymond A, Girma M, et al. MEPicides: α,β-unsaturated fosmidomycin analogs as DXR inhibitors against malaria. J Med Chem. 2018;61(19):8847–58. doi: 10.1021/acs.jmedchem.8b01026 30192536
54. Weese JS, van Duijkeren E. Methicillin-resistant Staphylococcus aureus and Staphylococcus pseudintermedius in veterinary medicine. Vet Microbiol. 2010 Jan 27;140(3–4):418–29. doi: 10.1016/j.vetmic.2009.01.039 19246166
55. Kuemmerle HP, Murakawa T, Soneoka K, Konishi T. Fosmidomycin: a new phosphonic acid antibiotic. Part I: Phase I tolerance studies. Int J Clin Pharmacol Ther Toxicol. 1985 Oct;23(10):515–20. 4066075
56. Borrmann S, Adegnika AA, Moussavou F, Oyakhirome S, Esser G, Matsiegui P-B, et al. Short-course regimens of artesunate-fosmidomycin in treatment of uncomplicated Plasmodium falciparum malaria. Antimicrob Agents Chemother. 2005 Sep; 49(9):3749–54. doi: 10.1128/AAC.49.9.3749-3754.2005 16127049
57. Silbergeld EK, Graham J, Price LB. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health. 2008 Apr 18;29(1):151–69.
58. Holmes A, Moore L, Sundsfjord A, Steinbakk M, Regmi S, Karkey A, et al. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet. 2016 Nov 18;387(10014):176–87. doi: 10.1016/S0140-6736(15)00473-0 26603922
59. Robinson TP, Bu DP, Carrique-Mas J, Fèvre EM, Gilbert M, Grace D, et al. Antibiotic resistance is the quintessential One Health issue. Trans R Soc Trop Med Hyg. 2016;110(7):377–80. doi: 10.1093/trstmh/trw048 27475987
60. Robinson TP, Wertheim HFL, Kakkar M, Kariuki S, Bu D, Price LB. Animal production and antimicrobial resistance in the clinic. Lancet. 2016 Jan 9;387(10014):e1–3. doi: 10.1016/S0140-6736(15)00730-8 26603925
61. Guardabassi L, Schwarz S, Lloyd DH. Pet animals as reservoirs of antimicrobial-resistant bacteria. Vol. 54, J Antimicrob Chemother. 2004. p. 321–32. doi: 10.1093/jac/dkh332 15254022
62. Martins LRL, Pina SMR, Simões RLR, de Matos AJF, Rodrigues P, da Costa PMR. Common phenotypic and genotypic antimicrobial resistance patterns found in a case study of multiresistant E. coli from cohabitant pets, humans, and household surfaces. J Environ Health. 2013;75(6):74–81. 23397653
63. Lloyd DH. Reservoirs of antimicrobial resistance in pet animals. Clin Infect Dis. 2007 Sep 1;45(Supplement_2):S148–52.
64. Takahata S, Ida T, Hiraishi T, Sakakibara S, Maebashi K, Terada S, et al. Molecular mechanisms of fosfomycin resistance in clinical isolates of Escherichia coli. Int J Antimicrob Agents. 2010 Apr 1;35(4):333–7. doi: 10.1016/j.ijantimicag.2009.11.011 20071153
65. Chekan JR, Cogan DP, Nair SK. Molecular basis for resistance against phosphonate antibiotics and herbicides. Medchemcomm. 2016 Jan 1;7(1):28–36. doi: 10.1039/C5MD00351B 26811741
66. Castañeda-García A, Blázquez J, Rodríguez-Rojas A. Molecular mechanisms and clinical impact of acquired and intrinsic fosfomycin resistance. Antibiot (Basel, Switzerland). 2013 Apr 16;2(2):217–36.
67. Biavasco F, Giovanetti E, Montanari MP, Lupidi R, Varaldo PE. Development of in-vitro resistance to glycopeptide antibiotics: assessment in staphylococci of different species. J Antimicrob Chemother. 1991 Jan 1;27(1):71–9. doi: 10.1093/jac/27.1.71 1828799
68. Watanakunakorn C. In-vitro selection of resistance of Staphylococcus aureus to teicoplanin and vancomycin. J Antimicrob Chemother. 1990 Jan 1;25(1):69–72. doi: 10.1093/jac/25.1.69 2138602
69. Blumberg HM, Rimland D, Carroll DJ, Terry Pamela, Wachsmuth IK. Rapid development of ciprofloxacin resistance in methicillin-susceptible and -resistant Staphylococcus aureus. J Infect Dis. 1991 Jun 1;163(6):1279–85. doi: 10.1093/infdis/163.6.1279 2037793
70. Gilbert DN, Kohlhepp SJ, Slama KA, Grunkemeier G, Lewis G, Dworkin RJ, et al. Phenotypic resistance of Staphylococcus aureus, selected Enterobacteriaceae and Pseudomonas aeruginosa after single and multiple in vitro exposures to ciprofloxacin, levofloxacin, and trovafloxacin. Antimicrob Agents Chemother.2001; 45(3):883–892. doi: 10.1128/AAC.45.3.883-892.2001 11181375
71. Guay DRP. Review of cefditoren, an advanced-generation, broad-spectrum oral cephalosporin. Clin Ther. 2001 Dec 1;23(12):1924–37. doi: 10.1016/s0149-2918(01)80147-8 11813929
72. Alexandrov A, Vignali M, LaCount DJ, Quartley E, de Vries C, De Rosa D, et al. A facile method for high-throughput co-expression of protein pairs. Mol Cell Proteomics. 2004 Sep 1;3(9):934–8. doi: 10.1074/mcp.T400008-MCP200 15240823
73. Armstrong CM, Meyers DJ, Imlay LS, Freel Meyers C, Odom AR. Resistance to the antimicrobial agent fosmidomycin and an FR900098 prodrug through mutations in the deoxyxylulose phosphate reductoisomerase gene (dxr). Antimicrob Agents Chemother. 2015;59(9):5511–9. doi: 10.1128/AAC.00602-15 26124156
74. Minor W, Cymborowski M, Otwinowski Z, Chruszcz M, IUCr. HKL -3000: the integration of data reduction and structure solution–from diffraction images to an initial model in minutes. Acta Crystallogr Sect D Biol Crystallogr. 2006 Aug 1;62(8):859–66.
75. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr. 2007;40(Pt 4):658–74. doi: 10.1107/S0021889807021206 19461840
76. Emsley P, Cowtan K, IUCr. Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Biol Crystallogr. 2004 Dec 1;60(12):2126–32.
77. Adams PD, Afonine P V., Bunkóczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Biol Crystallogr. 2010 Feb 1;66(2):213–21.
78. Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect. 2003 Aug 1;9(8):ix–xv.
79. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The sequence alignment/map format and SAMtools. Bioinformatics. 2009 Aug 15;25(16):2078–9. doi: 10.1093/bioinformatics/btp352 19505943
80. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011 Aug 1;27(15):2156–8. doi: 10.1093/bioinformatics/btr330 21653522
81. Cingolani P, Platts A, Wang LL, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 2012;6(2):80–92. doi: 10.4161/fly.19695 22728672
82. Omasits U, Ahrens CH, Müller S, Wollscheid B. Protter: interactive protein feature visualization and integration with experimental proteomic data. Bioinformatics. 2014 Mar 15;30(6):884–6. doi: 10.1093/bioinformatics/btt607 24162465
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