Biological evaluation of benzothiazole ethyl urea inhibitors of bacterial type II topoisomerases

Antimicrobial Agents and Chemotherapy

Volumn 57, Issue 12, 2013, Pages 5977-5986

  Stokes, Neil R ^a,c   Thomaides Brears, Helena B ^a   Barker, Stephanie ^a   Bennett, James M ^a   Berry, Joanne ^a   Collins, Ian ^a   Czaplewski, Lloyd G ^a,d   Gamble, Vicki ^a,e   Lancett, Paul ^a   Logan, Alastair ^a   Lunniss, Christopher J ^b   Peasley, Hilary ^a   Pommier, Stéphanie ^a,f   Price, Daniel ^a,g   Smee, Carol ^a,h   Haydon, David J ^a  

^a Biota Europe Ltd   (United Kingdom)

^b Biota Scientific Management Pty Ltd   (Australia)

^c REDX PHARMA   (United Kingdom)

^d Chemical Biology Ventures Limited   (United Kingdom)

^e Argenta Discovery Ltd   (United Kingdom)

^f INSERM   (France)

^g CARDIFF UNIVERSITY   (United Kingdom)

^h WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BENZOTHIAZOLE DERIVATIVE; BENZOTHIAZOLE ETHYL UREA DERIVATIVE; CIPROFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING) B; DNA TOPOISOMERASE IV; GYRASE INHIBITOR; LEVOFLOXACIN; LINEZOLID; NOVOBIOCIN; OXACILLIN; UNCLASSIFIED DRUG; VANCOMYCIN; ADENOSINE TRIPHOSPHATASE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE INHIBITOR; INTERLEUKIN DERIVATIVE; INTERLEUKIN-33, MOUSE; RECOMBINANT PROTEIN; UREA;

ANIMAL EXPERIMENT; ANTIBACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; AREA UNDER THE CURVE; ARTICLE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; CELL VIABILITY; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; DNA SUPERCOILING; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG HALF LIFE; DRUG PROTEIN BINDING; DRUG SCREENING; ENTEROCOCCUS; ENZYME ACTIVITY; ENZYME INHIBITION; GROWTH INHIBITION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PLASMA CONCENTRATION-TIME CURVE; PRIORITY JOURNAL; RAT; STAPHYLOCOCCUS; STREPTOCOCCUS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; GROWTH, DEVELOPMENT AND AGING; HEPG2 CELL LINE; METABOLISM; MICROBIAL SENSITIVITY TEST; SPRAGUE DAWLEY RAT;

ADENOSINE TRIPHOSPHATASES; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BENZOTHIAZOLES; CELL SURVIVAL; DNA TOPOISOMERASE IV; DNA TOPOISOMERASES, TYPE II; ESCHERICHIA COLI; GENE EXPRESSION; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HEP G2 CELLS; HUMANS; INTERLEUKINS; LEVOFLOXACIN; MALE; MICROBIAL SENSITIVITY TESTS; NOVOBIOCIN; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; TOPOISOMERASE INHIBITORS; UREA;

EID: 84887459275     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.00719-13     Document Type: Article

References (49)

1. Infectious Diseases Society of America. 2004. Bad bugs, no drugs: as antibiotic discovery stagnates, a public health crisis brews. Infectious Diseases Society of America, Alexandria, VA.
2. Spellberg B, Guidos R, Gilbert D, Bradley J, Bucher HW, Scheld WM, Bartlett JG, Edwards J, Jr. 2008. The epidemic of antibiotic-resistant infections: a call to arms for the medical community from the Infectious Diseases Society of America. Clin. Infect. Dis. 46:155-164.
3. Bush K, Courvalin P, Dantas G, Davies J, Eisenstein B, Huovinen P, Jacoby GA, Kishony R, Kreiswirth BN, Kutter E, Lerner SA, Levy S, Lewis K, Lomovskaya O, Miller JH, Mobashery S, Piddock LJV, Projan S, Thomas CM, Tomasz A, Tulkens PM, Walsh TR, Watson JD, Witkowski J, Witte W, Wright G, Yeh P, Zgurskaya HI. 2011. Tackling antibiotic resistance. Nat. Rev. Microbiol. 9:894-896.
4. Rice LB. 2008. Federal funding for the study of antimicrobial resistance in nosocomial pathogens: no ESKAPE. J. Infect. Dis. 197:1079-1081.
5. Fischbach MA, Walsh CT. 2009. Antibiotics for emerging pathogens. Science 325:1089-1093.
6. Payne DJ, Gwynn MN, Holmes DJ, Pompliano DL. 2007. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov. 6:29-40.
7. Jabes D. 2011. The antibiotic R&D pipeline: an update. Curr. Opin. Microbiol. 14:564-569.
8. Brötz-Oesterhelt H, Sass P. 2010. Postgenomic strategies in antibacterial drug discovery. Future Microbiol. 5:1553-1579.
9. Maxwell A. 1997. DNA gyrase as a drug target. Trends Microbiol. 5:102-109.
10. Pommier Y, Leo E, Zhang HL, Marchand C. 2010. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol. 17:421-433.
11. Collin F, Karkare S, Maxwell A. 2011. Exploiting bacterial DNA gyrase as a drug target: current state and perspectives. Appl. Microbiol. Biotechnol. 92:479-497.
12. Drlica K, Hiasa H, Kerns R, Malik M, Mustaev A, Zhao X. 2009. Quinolones: action and resistance updated. Curr. Top. Med. Chem. 9:981-998.
13. Lewis RJ, Singh OMP, Smith CV, Skarzynski T, Maxwell A, Wonacott AJ, Wigley DB. 1996. The nature of inhibition of DNA gyrase by the coumarins and the cyclothialidines revealed by X-ray crystallography. EMBO J. 15:1412-1420.
14. Stieger M, Angehrn Wohlgensinger B, Gmünder H. 1996. GyrB mutations in Staphylococcus aureus strains resistant to cyclothialidine, coumermycin, and novobiocin. Antimicrob. Agents Chemother. 40:1060-1062.
15. Silver LL. 2012. Polypharmacology as an emerging trend in antibacterial discovery, p 167-202. In Peters JU (ed), Polypharmacology in drug discovery. John Wiley & Sons, Inc, Hoboken, NJ.
16. East SP, Czaplewski LG, Haydon DJ. 2012. Case study 10: ethyl urea inhibitors of the bacterial type II topoisomerases DNA gyrase (GyrB) and topoisomerase IV (ParE), p 335-352. In Morphy RJ, Harris CJ (ed), Designing multi-target drugs. Royal Society of Chemistry, Cambridge, United Kingdom.
17. Silver LL. 2011. Challenges of antibacterial discovery. Clin. Microbiol. Rev. 24:74-109.
18. East SP, Silver LL. 2013. Multitarget ligands in antibacterial research: progress and opportunities. Expert Opin. Drug Discov. 8:143-156.
19. Brino L, Urzhumstev A, Mousli M, Bronner C, Mitschler A, Oudet P, Moras D. 2000. Dimerization of Escherichia coli DNA-gyrase B provides a structural mechanism for activating the ATPase catalytic center. J. Biol. Chem. 275:9468-9475.
20. Bellon S, Parsons JD, Wei Y, Hayakawa K, Swenson LL, Charifson PS, Lippke JA, Alsape R, Gross CH. 2004. Crystal structures of Escherichia coli topoisomerase IV ParE subunit (24 and 43 kilodaltons): a single residue dictates differences in novobiocin potency against topoisomerase IV and DNA gyrase. Antimicrob. Agents Chemother. 48:1856-1864.
21. Mani N, Gross CH, Parsons JD, Hanzelka B, Müh U, Mullin S, Liao Y, Grillot A-L, Stamos D, Charifson PS, Grossman TH. 2006. In vitro characterization of the antibacterial spectrum of novel bacterial type II topoisomerase inhibitors of the aminobenzimidazole class. Antimicrob. Agents Chemother. 50:1228-1237.
22. Grossman TH, Bartels DJ, Mullin S, Gross CH, Parsons JD, Liao Y, Grillot A-L, Stamos D, Olson ER, Charifson PS, Mani N. 2007. Dual targeting of GyrB and ParE by a novel aminobenzimidazole class of antibacterial compounds. Antimicrob. Agents Chemother. 51:657-666.
23. Charifson PS, Grillot A-L, Grossman TH, Parsons JD, Badia M, Bellon S, Deininger DD, Drumm JE, Gross CH, LeTiran A, Liao Y, Mani N, Nicolau DO, Perola E, Ronkin A, Shannon D, Swenson LL, Tang Q, Tessier PR, Tian S-K, Trudeau M, Wang T, Wei Y, Zhang H, Stamos D. 2008. Novel dual-targeting benzimidazole urea inhibitors of DNA gyrase and topoisomerase IV possessing potent antibacterial activity: intelligent design and evolution through the judicious use of structure-guided design and structure-activity relationships. J. Med. Chem. 51:5243-5263.
24. East SP, White CB, Barker O, Barker S, Bennett J, Brown D, Boyd EA, Brennan C, Chowdhury C, Collins I, Convers-Reignier E, Dymock BW, Fletcher R, Haydon DJ, Gardiner M, Hatcher S, Ingram P, Lancett P, Mortenson P, Papadopoulos K, Smee C, Thomaides-Brears HB, Tye H, Workman J, Czaplewski LG. 2009. DNA gyrase (GyrB)/topoisomerase IV (ParE) inhibitors: synthesis and antibacterial activity. Bioorg. Med. Chem. Lett. 19:894-899.
25. Starr JT, Sciotti RJ, Hanna DL, Huband MD, Mullins LM, Cai H, Gage JW, Lockard M, Rauckhorst MR, Owen RM, Lall MS, Tomilo M, Chen H, McCurdy SP, Barbachyn MR. 2009. 5-(2-Pyrimidinyl)-imidazo[1, 2-a]pyridines are antibacterial agents targeting the ATPase domains of DNA gyrase and topoisomerase IV. Bioorg. Med. Chem. Lett. 19:5302-5306.
26. Tanitame A, Oyamada Y, Ofuji K, Fukimoto M, Iwai N, Hiyama Y, Suzuki K, Ito H, Terauchi H, Kawasaki M, Nagai K, Wachi M, Yamagishi J-i. 2004. Synthesis and antibacterial activity of a novel series of potent DNA gyrase inhibitors. Pyrazole derivatives. J. Med. Chem. 47:3693-3696.
27. Manchester JI, Dussault DD, Rose JA, Boriack-Sjodin A, Uria-Nickelsen M, Ioannidis G, Bist S, Fleming P, Hull KG. 2012. Discovery of a novel azaindole class of antibacterial agents targeting the ATPase domains of DNA gyrase and topoisomerase IV. Bioorg. Med. Chem. Lett. 22:5150-5156.
28. Tari LW, Trzossa M, Bensen DC, Li X, Chen Z, Lam T, Zhang J, Creighton CJ, Cunningham ML, Kwan B, Stidham M, Shaw KJ, Lightstone FC, Wong SE, Nguyen TB, Nix J, Finn J. 2013. Pyrrolopyrimidine inhibitors of DNA gyrase B (GyrB) and topoisomerase IV (ParE), part I: structure guided discovery and optimization of dual targeting agents with potent, broad-spectrum enzymatic activity. Bioorg. Med. Chem. Lett. 23: 1529-1536.
29. Trzoss M, Bensen DC, Li X, Chen Z, Lam T, Zhang J, Creighton CJ, Cunningham ML, Kwan B, Stidham M, Nelson K, Brown-Driver V, Castellano A, Shaw KJ, Lightstone FC, Wong SE, Nguyen TB, Finn J, Tari LW. 2013. Pyrrolopyrimidine inhibitors ofDNAgyrase B (GyrB) and topoisomerase IV (ParE), part II: development of inhibitors with broad spectrum, Gram-negative antibacterial activity. Bioorg. Med. Chem. Lett. 23:1537-1543.
30. Palmer JT, Lunniss CJ, Offermann DA, Axford LC, Blair M, Mitchell D, Palmer N, Steele C, Atherall J, Watson D, Haydon D, Czaplewski L, Davies D, Collins I, Tyndall EM, Andrau L, Pitt GRW. April 2012. International patentWO2012/045124. Biota Europe Ltd, Begbroke, United Kingdom.
31. Clinical and Laboratory Standards Institute. 2006. Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically; approved standard, 7th ed. CLSI document M7-A7. Clinical and Laboratory Standards Institute, Wayne, PA.
32. Clinical and Laboratory Standards Institute. 2007. Methods for antimicrobial susceptibility testing of anaerobic bacteria; approved standard, 7th ed. CLSI document M11-A7. Clinical and Laboratory Standards Institute, Wayne, PA.
33. Pillai SK, Moellering RC, Jr, Eliopoulos GM. 2005. Antimicrobial combinations, p 365-440. In Lorian V (ed), Antibiotics in laboratory medicine. Lippincott Williams & Wilkins, Philadelphia, PA.
34. Odds FC. 2003. Synergy, antagonism, and what the chequerboard puts between them. J. Antimicrob. Chemother. 52:1.
35. Clinical and Laboratory Standards Institute. 1999. Methods for determining bactericidal activity of antimicrobial agents; approved guideline. CLSI document M26-A. Clinical and Laboratory Standards Institute, Wayne, PA.
36. Sugino A, Higgins NP, Brown PO, Peebles CL, Cozzarelli NR. 1978. Energy coupling in DNA gyrase and the mechanism of action of novobiocin. Proc. Natl. Acad. Sci. U. S. A. 75:4838-4842.
37. Arathoon EG, Hamilton JR, Hench CE, Stevens DA. 1990. Efficacy of short courses of oral novobiocin-rifampin in eradicating carrier state of methicillin-resistant Staphylococcus aureus and in in vitro killing studies of clinical isolates. Antimicrob. Agents Chemother. 34:1655-1659.
38. O'Neill AJ, Chopra I. 2004. Preclinical evaluation of novel antibacterial agents by microbiological and molecular techniques. Expert Opin. Investig. Drugs 13:1045-1063.
39. Vickers AA, O'Neill AJ, Chopra I. 2007. Emergence and maintenance of resistance to fluoroquinolones and coumarins in Staphylococcus aureus: predictions from in vitro studies. J. Antimicrob. Chemother. 60:269-273.
40. Neu HC, Chin N-X, Labthavikul P. 1984. Antibacterial activity of coumermycin alone and in combination with other antibiotics. Antimicrob. Agents Chemother. 25:687-689.
41. French P, Venuti E, Fraimow HS. 1993. In vitro activity of novobiocin against multiresistant strains of Enterococcus faecium. Antimicrob. Agents Chemother. 37:2736-2739.
42. Schick DG, Canawati HN, Montgomerie JZ. 1997. In vitro activity of the combination of trovafloxacin and other antibiotics against enterococci. Diagn. Microbiol. Infect. Dis. 29:233-239.
43. Chao L. 1978. An unusual interaction between the target of nalidixic acid and novobiocin. Nature 271:385-386.
44. Ma D, Cook DN, Albert M, Pon NG, Nikaido H, Hearst JE. 1993. Molecular cloning and characterization of acrA and acrE genes of Escherichia coli. J. Bacteriol. 175:6299-6313.
45. Symmons MF, Bokma E, Koranakis V, Hughes C, Koranakis V. 2009. The assembled structure of a complete tripartite bacterial multidrug efflux pump. Proc. Natl. Acad. Sci. U. S. A. 106:7173-7178.
46. Nikaido H. 2009. Multidrug resistance in bacteria. Annu. Rev. Biochem. 78:119-146.
47. Pankey GA, Sabath LD. 2004. Clinical relevance of bacteriostatic versus bactericidal mechanisms of action in the treatment of Gram-positive infections. Clin. Infect. Dis. 38:864-870.
48. Kreuzer KN, Cozzarelli NR. 1979. Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J. Bacteriol. 140:424-435.
49. Drlica K, Zhao X. 1997. DNA gyrase, topoisomerase IV, and the 4-quinolones. Microbiol. Mol. Biol. Rev. 61:377-392.