Prospects for developing new antibacterials targeting bacterial type IIA topoisomerases

Current Topics in Medicinal Chemistry

Volumn 14, Issue 1, 2014, Pages 130-151

  Tomašić, Tihomir ^a   Mašič, Lucija Peterlin ^a  

^a UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Antibacterial; ATP; DNA gyrase; Dual inhibitors; Structure based design; Topoisomerase

Indexed keywords

4 AMINOPIPERIDINE; 9 CYCLOPROPYL 6 FLUORO 3,4 DIOXO 7 (1 PIPERAZINYL)ISOTHIAZOLO[5,4 B]QUINOLINE; ACH 702; AMINOCOUMARIN DERIVATIVE; ANTOFLOXACIN; CIPROFLOXACIN; CYCLOHEXYLAMINE; DELAFLOXACIN; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE IV; FINAFLOXACIN; GCK 299423; GYRAMIDE A; GYRAMIDES B; GYRAMIDES C; GYRASE INHIBITOR; MBX 500; MOXIFLOXACIN; NEMONOXACIN; NLX 101; PD 0305970; PIPERIDINE; PNU 286607; PROTEIN PARE; PYRUVATE DEHYDROGENASE KINASE; QUINOLINE DERIVATIVE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SELENOPHENE DERIVATIVE; SIMOCYCLINONE D8; TETRAHYDROINDAZOLE; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ACINETOBACTER BAUMANNII; ANTIBACTERIAL ACTIVITY; ARTICLE; BACILLUS ANTHRACIS; BACTERIAL INFECTION; CRYSTALLOGRAPHY; DNA REPAIR; DNA REPLICATION; DRUG DESIGN; ENZYME ACTIVE SITE; GENE MUTATION; HIGH THROUGHPUT SCREENING; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); PHASE 3 CLINICAL TRIAL (TOPIC); PROTEIN BINDING; RESPIRATORY TRACT INFECTION; SEQUENCE ALIGNMENT; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; STAPHYLOCOCCUS INFECTION; STRUCTURE ACTIVITY RELATION; THERMUS THERMOPHILUS; URINARY TRACT INFECTION;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BINDING SITES; DNA GYRASE; DRUG DESIGN; HIGH-THROUGHPUT SCREENING ASSAYS; PROTEIN CONFORMATION; QUINOLONES; STRUCTURE-ACTIVITY RELATIONSHIP; TOPOISOMERASE II INHIBITORS;

EID: 84891801093     PISSN: 15680266     EISSN: 18734294     Source Type: Journal    
DOI: 10.2174/1568026613666131113153251     Document Type: Article

References (140)

1. Levy, S.B.; Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med., 2004, 10, S122-129.
2. Boucher, H.W.; Talbot, G.H.; Bradley, J.S.; Edwards, J.E.; Gilbert, D.; Rice, L.B.; Scheld, M.; Spellberg, B.; Bartlett, J. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin. Infect. Dis., 2009, 48, 1-12.
3. Boucher, H.W.; Talbot, G.H.; Benjamin, D.K., Jr.; Bradley, J.; Guidos, R.J.; Jones, R.N.; Murray, B.E.; Bonomo, R.A.; Gilbert, D. 10 x '20 Progress-development of new drugs active against gram-negative bacilli: an update from the Infectious Diseases Society of America. Clin. Infect. Dis., 2013, 56, 1685-1694.
4. Silver, L.L. Challenges of antibacterial discovery. Clin. Microbiol. Rev., 2011, 24, 71-109.
5. Gwynn, M.N.; Portnoy, A.; Rittenhouse, S.F.; Payne, D.J. Challenges of antibacterial discovery revisited. Ann. N.Y. Acad. Sci., 2010, 1213, 5-19.
6. Payne, D.J.; Gwynn, M.N.; Holmes, D.J.; Pompliano, D.L. Drugs for bad bugs: confronting the challenges of antibacterial discovery. Nat. Rev. Drug Discov., 2007, 6, 29-40.
7. Collin, F.; Karkare, S.; Maxwell, A. Exploiting bacterial DNA gyrase as a drug target: current state and perspectives. Appl. Microbiol. Biotechnol., 2011, 92, 479-497.
8. Sissi, C.; Palumbo, M., In front of and behind the replication fork: bacterial type IIA topoisomerases. Cell Mol Life Sci, 2010, 67, 2001-2024.
9. Sanyal, G.; Doig, P. Bacterial DNA replication enzymes as targets for antibacterial drug discovery. Expert Opin. Drug Discov., 2012, 7, 327-339.
10. Champoux, J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 2001, 70, 369-413.
11. Emmerson, A.M.; Jones, A.M. The quinolones: decades of development and use. J. Antimicrob. Chemother., 2003, 51 Suppl 1, 13-20.
12. Oblak, M.; Kotnik, M.; Šolmajer, T. Discovery and development of ATPase inhibitors of DNA gyrase as antibacterial agents. Curr. Med. Chem., 2007, 14, 2033-2047.
13. Drlica, K.; Malik, M., Fluoroquinolones: action and resistance. Curr. Top. Med. Chem., 2003, 3, 249-282.
14. Contreras, A.; Maxwell, A. gyrB mutations which confer coumarin resistance also affect DNA supercoiling and ATP hydrolysis by Escherichia coli DNA gyrase. Mol. Microbiol., 1992, 6, 1617-1624.
15. Butler, M.S.; Cooper, M.A. Antibiotics in the clinical pipeline in, 2011. J. Antibiot. (Tokyo), 2011, 64, 413-425.
16. Konc, J.; Janežič, D. ProBiS-2012: web server and web services for detection of structurally similar binding sites in proteins. Nucleic Acids Res., 2012, 40, W214-221.
17. East, S.P.; Silver, L.L. Multitarget ligands in antibacterial research: progress and opportunities. Expert Opin. Drug Discov., 2013, 8, 143-156.
18. Wigley, D.B.; Davies, G.J.; Dodson, E.J.; Maxwell, A.; Dodson, G. Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature, 1991, 351, 624-629.
19. Morais Cabral, J.H.; Jackson, A.P.; Smith, C.V.; Shikotra, N.; Maxwell, A.; Liddington, R.C. Crystal structure of the breakagereunion domain of DNA gyrase. Nature, 1997, 388, 903-906.
20. Corbett, K.D.; Shultzaberger, R.K.; Berger, J.M. The C-terminal domain of DNA gyrase A adopts a DNA-bending beta-pinwheel fold. Proc. Natl. Acad. Sci. U.S.A., 2004, 101, 7293-7298.
21. Schoeffler, A.J.; May, A.P.; Berger, J.M. A domain insertion in Escherichia coli GyrB adopts a novel fold that plays a critical role in gyrase function. Nucleic Acids Res., 2010, 38, 7830-7844.
22. Wohlkonig, A.; Chan, P.F.; Fosberry, A.P.; Homes, P.; Huang, J.; Kranz, M.; Leydon, V.R.; Miles, T.J.; Pearson, N.D.; Perera, R.L.; Shillings, A.J.; Gwynn, M.N.; Bax, B.D. Structural basis of quinolone inhibition of type IIA topoisomerases and targetmediated resistance. Nat. Struct. Mol. Biol., 2010, 17, 1152-1153.
23. Laponogov, I.; Pan, X.S.; Veselkov, D.A.; McAuley, K.E.; Fisher, L.M.; Sanderson, M.R. Structural basis of gate-DNA breakage and resealing by type II topoisomerases. PLoS One, 2010, 5, e11338.
24. Laponogov, I.; Sohi, M.K.; Veselkov, D.A.; Pan, X.S.; Sawhney, R.; Thompson, A.W.; McAuley, K.E.; Fisher, L.M.; Sanderson, M.R. Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases. Nat. Struct. Mol. Biol., 2009, 16, 667-669.
25. Rudolph, M.G.; Klostermeier, D. Mapping the spectrum of conformational states of the DNA-and C-gates in Bacillus subtilis gyrase. J. Mol. Biol., 2013, 425, 2632-2640.
26. Wendorff, T.J.; Schmidt, B.H.; Heslop, P.; Austin, C.A.; Berger, J.M. The structure of DNA-bound human topoisomerase II alpha: conformational mechanisms for coordinating inter-subunit interactions with DNA cleavage. J. Mol. Biol., 2012, 424, 109-124.
27. Brino, L.; Urzhumtsev, A.; Mousli, M.; Bronner, C.; Mitschler, A.; Oudet, P.; Moras, D. Dimerization of Escherichia coli DNA-gyrase B provides a structural mechanism for activating the ATPase catalytic center. J. Biol. Chem., 2000, 275, 9468-9475.
28. Lamour, V.; Hoermann, L.; Jeltsch, J.M.; Oudet, P.; Moras, D. An open conformation of the Thermus thermophilus gyrase B ATPbinding domain. J. Biol. Chem., 2002, 277, 18947-18953.
29. Lafitte, D.; Lamour, V.; Tsvetkov, P.O.; Makarov, A.A.; Klich, M.; Deprez, P.; Moras, D.; Briand, C.; Gilli, R. DNA gyrase interaction with coumarin-based inhibitors: the role of the hydroxybenzoate isopentenyl moiety and the 5'-methyl group of the noviose. Biochemistry, 2002, 41, 7217-7223.
30. Ronkin, S.M.; Badia, M.; Bellon, S.; Grillot, A.L.; Gross, C.H.; Grossman, T.H.; Mani, N.; Parsons, J.D.; Stamos, D.; Trudeau, M.; Wei, Y.; Charifson, P.S. Discovery of pyrazolthiazoles as novel and potent inhibitors of bacterial gyrase. Bioorg. Med. Chem. Lett., 2010, 20, 2828-2831.
31. Sherer, B.A.; Hull, K.; Green, O.; Basarab, G.; Hauck, S.; Hill, P.; Loch, J.T., 3rd; Mullen, G.; Bist, S.; Bryant, J.; Boriack-Sjodin, A.; Read, J.; DeGrace, N.; Uria-Nickelsen, M.; Illingworth, R.N.; Eakin, A.E. Pyrrolamide DNA gyrase inhibitors: optimization of antibacterial activity and efficacy. Bioorg. Med. Chem. Lett., 2011, 21, 7416-7420.
32. Eakin, A.E.; Green, O.; Hales, N.; Walkup, G.K.; Bist, S.; Singh, A.; Mullen, G.; Bryant, J.; Embrey, K.; Gao, N.; Breeze, A.; Timms, D.; Andrews, B.; Uria-Nickelsen, M.; Demeritt, J.; Loch, J.T., 3rd; Hull, K.; Blodgett, A.; Illingworth, R.N.; Prince, B.; Boriack-Sjodin, P.A.; Hauck, S.; MacPherson, L.J.; Ni, H.; Sherer, B. Pyrrolamide DNA gyrase inhibitors: fragment-based nuclear magnetic resonance screening to identify antibacterial agents. Antimicrob. Agents Chemother., 2012, 56, 1240-1246.
33. Brvar, M.; Perdih, A.; Renko, M.; Anderluh, G.; Turk, D.; Šolmajer, T. Structure-based discovery of substituted 4, 5'-bithiazoles as novel DNA gyrase inhibitors. J. Med. Chem, 2012, 55, 6413-6426.
34. Shirude, P.S.; Madhavapeddi, P.; Tucker, J.A.; Murugan, K.; Patil, V.; Basavarajappa, H.; Raichurkar, A.V.; Humnabadkar, V.; Hussein, S.; Sharma, S.; Ramya, V.K.; Narayan, C.B.; Balganesh, T.S.; Sambandamurthy, V.K. Aminopyrazinamides: novel and specific GyrB inhibitors that kill replicating and nonreplicating Mycobacterium tuberculosis. ACS Chem. Biol., 2013, 8, 519-523.
35. Tari, L.W.; Trzoss, M.; Bensen, D.C.; Li, X.; Chen, Z.; Lam, T.; Zhang, J.; Creighton, C.J.; Cunningham, M.L.; Kwan, B.; Stidham, M.; Shaw, K.J.; Lightstone, F.C.; Wong, S.E.; Nguyen, T.B.; Nix, J.; Finn, J. 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., 2013, 23, 1529-1536.
36. Trzoss, M.; Bensen, D.C.; Li, X.; Chen, Z.; Lam, T.; Zhang, J.; Creighton, C.J.; Cunningham, M.L.; Kwan, B.; Stidham, M.; Nelson, K.; Brown-Driver, V.; Castellano, A.; Shaw, K.J.; Lightstone, F.C.; Wong, S.E.; Nguyen, T.B.; Finn, J.; Tari, L.W. Pyrrolopyrimidine inhibitors of DNA gyrase B (GyrB) and topoisomerase IV (ParE), Part II: development of inhibitors with broad spectrum, Gram-negative antibacterial activity. Bioorg. Med. Chem. Lett., 2013, 23, 1537-1543.
37. Bax, B.D.; Chan, P.F.; Eggleston, D.S.; Fosberry, A.; Gentry, D.R.; Gorrec, F.; Giordano, I.; Hann, M.M.; Hennessy, A.; Hibbs, M.; Huang, J.; Jones, E.; Jones, J.; Brown, K.K.; Lewis, C.J.; May, E.W.; Saunders, M.R.; Singh, O.; Spitzfaden, C.E.; Shen, C.; Shillings, A.; Theobald, A.J.; Wohlkonig, A.; Pearson, N.D.; Gwynn, M.N. Type IIA topoisomerase inhibition by a new class of antibacterial agents. Nature, 2010, 466, 935-940.
38. Edwards, M.J.; Flatman, R.H.; Mitchenall, L.A.; Stevenson, C.E.; Le, T.B.; Clarke, T.A.; McKay, A.R.; Fiedler, H.P.; Buttner, M.J.; Lawson, D.M.; Maxwell, A. A crystal structure of the bifunctional antibiotic simocyclinone D8, bound to DNA gyrase. Science, 2009, 326, 1415-1418.
39. Chu, D.T.; Hallas, R.; Clement, J.J.; Alder, J.; McDonald, E.; Plattner, J.J. Synthesis and antitumour activities of quinolone antineoplastic agents. Drugs Exp. Clin. Res., 1992, 18, 275-282.
40. Škedelj, V.; Tomašić, T.; Mašić, L.P.; Zega, A. ATP-binding site of bacterial enzymes as a target for antibacterial drug design. J. Med. Chem., 2011, 54, 915-929.
41. Corbett, K.D.; Berger, J.M. Structural dissection of ATP turnover in the prototypical GHL ATPase TopoVI. Structure, 2005, 13, 873-882.
42. Wei, H.; Ruthenburg, A.J.; Bechis, S.K.; Verdine, G.L. Nucleotide-dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase. J. Biol. Chem., 2005, 280, 37041-37047.
43. Dutta, R.; Inouye, M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci., 2000, 25, 24-28.
44. Kukimoto-Niino, M.; Tokmakov, A.; Terada, T.; Ohbayashi, N.; Fujimoto, T.; Gomi, S.; Shiromizu, I.; Kawamoto, M.; Matsusue, T.; Shirouzu, M.; Yokoyama, S. Inhibitor-bound structures of human pyruvate dehydrogenase kinase 4. Acta Crystallogr. D, Biol. Crystallogr., 2011, 67, 763-773.
45. Machius, M.; Chuang, J.L.; Wynn, R.M.; Tomchick, D.R.; Chuang, D.T. Structure of rat BCKD kinase: nucleotide-induced domain communication in a mitochondrial protein kinase. Proc. Natl. Acad. Sci. U.S.A., 2001, 98, 11218-11223.
46. Takei, M.; Fukuda, H.; Kishii, R.; Hosaka, M. Target preference of 15 quinolones against Staphylococcus aureus, based on antibacterial activities and target inhibition. Antimicrob. Agents Chemother., 2001, 45, 3544-3547.
47. Mitscher, L.A. Bacterial topoisomerase inhibitors: quinolone and pyridone antibacterial agents. Chem. Rev., 2005, 105, 559-592.
48. Andresson, M.I.; MacGowan, A.P. Development of the quinolones. J. Antimicrob. Chemother., 2003, 51 (Suppl. 1), 1-11.
49. Drlica, K.; Hiasa, H.; Kerns, R.; Malik, M.; Mustaev, A.; Zhao, X. Quinolones: action and resistance updated. Curr. Top. Med. Chem., 2009, 9, 981-998.
50. Aldred, K.J.; McPherson, S.A.; Wang, P.; Kerns, R.J.; Graves, D.E.; Turnbough, C.L., Jr.; Osheroff, N. Drug interactions with Bacillus anthracis topoisomerase IV: biochemical basis for quinolone action and resistance. Biochemistry, 2012, 51, 370-381.
51. Aldred, K.J.; McPherson, S.A.; Turnbough, C.L., Jr.; Kerns, R.J.; Osheroff, N. Topoisomerase IV-quinolone interactions are mediated through a water-metal ion bridge: mechanistic basis of quinolone resistance. Nucleic Acids Res., 2013, 41, 4628-4639.
52. Cattoir, V.; Nordmann, P. Plasmid-mediated quinolone resistance in gram-negative bacterial species: an update. Curr. Med. Chem., 2009, 16, 1028-1046.
53. Zhi, C.; Long, Z.Y.; Manikowski, A.; Comstock, J.; Xu, W.C.; Brown, N.C.; Tarantino, P.M., Jr.; Holm, K.A.; Dix, E.J.; Wright, G.E.; Barnes, M.H.; Butler, M.M.; Foster, K.A.; LaMarr, W.A.; Bachand, B.; Bethell, R.; Cadilhac, C.; Charron, S.; Lamothe, S.; Motorina, I.; Storer, R. Hybrid antibacterials. DNA polymerase-topoisomerase inhibitors. J. Med. Chem., 2006, 49, 1455-1465.
54. Butler, M.M.; Lamarr, W.A.; Foster, K.A.; Barnes, M.H.; Skow, D.J.; Lyden, P.T.; Kustigian, L.M.; Zhi, C.; Brown, N.C.; Wright, G.E.; Bowlin, T.L. Antibacterial activity and mechanism of action of a novel anilinouracil-fluoroquinolone hybrid compound. Antimicrob. Agents Chemother., 2007, 51, 119-127.
55. Butler, M.M.; Shinabarger, D.L.; Citron, D.M.; Kelly, C.P.; Dvoskin, S.; Wright, G.E.; Feng, H.; Tzipori, S.; Bowlin, T.L. MBX-500, a hybrid antibiotic with in vitro and in vivo efficacy against toxigenic Clostridium difficile. Antimicrob. Agents Chemother., 2012, 56, 4786-4792.
56. Robertson, G.T.; Bonventre, E.J.; Doyle, T.B.; Du, Q.; Duncan, L.; Morris, T.W.; Roche, E.D.; Yan, D.; Lynch, A.S. In vitro evaluation of CBR-2092, a novel rifamycin-quinolone hybrid antibiotic: studies of the mode of action in Staphylococcus aureus. Antimicrob. Agents Chemother., 2008, 52, 2313-2323.
57. Robertson, G.T.; Bonventre, E.J.; Doyle, T.B.; Du, Q.; Duncan, L.; Morris, T.W.; Roche, E.D.; Yan, D.; Lynch, A.S. In vitro evaluation of CBR-2092, a novel rifamycin-quinolone hybrid antibiotic: microbiology profiling studies with staphylococci and streptococci. Antimicrob. Agents Chemother., 2008, 52, 2324-2334.
58. Chu, D.T.; Fernandes, P.B.; Claiborne, A.K.; Shen, L.; Pernet, A.G. Structure-activity relationships in quinolone antibacterials: design, synthesis and biological activities of novel isothiazoloquinolones. Drugs Exp. Clin. Res., 1988, 14, 379-383.
59. Kohlbrenner, W.E.; Wideburg, N.; Weigl, D.; Saldivar, A.; Chu, D.T. Induction of calf thymus topoisomerase II-mediated DNA breakage by the antibacterial isothiazoloquinolones A-65281 and A-65282. Antimicrob. Agents Chemother., 1992, 36, 81-86.
60. Wiles, J.A.; Wang, Q.; Lucien, E.; Hashimoto, A.; Song, Y.; Cheng, J.; Marlor, C.W.; Ou, Y.; Podos, S.D.; Thanassi, J.A.; Thoma, C.L.; Deshpande, M.; Pucci, M.J.; Bradbury, B.J. Isothiazoloquinolones containing functionalized aromatic hydrocarbons at the 7-position: synthesis and in vitro activity of a series of potent antibacterial agents with diminished cytotoxicity in human cells. Bioorg. Med. Chem. Lett., 2006, 16, 1272-1276.
61. Wiles, J.A.; Song, Y.; Wang, Q.; Lucien, E.; Hashimoto, A.; Cheng, J.; Marlor, C.W.; Ou, Y.; Podos, S.D.; Thanassi, J.A.; Thoma, C.L.; Deshpande, M.; Pucci, M.J.; Bradbury, B.J. Biological evaluation of isothiazoloquinolones containing aromatic heterocycles at the 7-position: In vitro activity of a series of potent antibacterial agents that are effective against methicillin-resistant Staphylococcus aureus. Bioorg. Med. Chem. Lett., 2006, 16, 1277-1281.
62. Wang, Q.; Lucien, E.; Hashimoto, A.; Pais, G.C.; Nelson, D.M.; Song, Y.; Thanassi, J.A.; Marlor, C.W.; Thoma, C.L.; Cheng, J.; Podos, S.D.; Ou, Y.; Deshpande, M.; Pucci, M.J.; Buechter, D.D.; Bradbury, B.J.; Wiles, J.A. Isothiazoloquinolones with enhanced antistaphylococcal activities against multidrug-resistant strains: effects of structural modifications at the 6-, 7-, and 8-positions. J. Med. Chem., 2007, 50, 199-210.
63. Kim, H.Y.; Wiles, J.A.; Wang, Q.; Pais, G.C.; Lucien, E.; Hashimoto, A.; Nelson, D.M.; Thanassi, J.A.; Podos, S.D.; Deshpande, M.; Pucci, M.J.; Bradbury, B.J. Exploration of the activity of 7-pyrrolidino-8-methoxyisothiazoloquinolones against methicillin-resistant Staphylococcus aureus (MRSA). J. Med. Chem., 2011, 54, 3268-3282.
64. Pucci, M.J.; Cheng, J.; Podos, S.D.; Thoma, C.L.; Thanassi, J.A.; Buechter, D.D.; Mushtaq, G.; Vigliotti, G.A., Jr.; Bradbury, B.J.; Deshpande, M. In vitro and in vivo antibacterial activities of heteroaryl isothiazolones against resistant gram-positive pathogens. Antimicrob. Agents Chemother., 2007, 51, 1259-1267.
65. Cheng, J.; Thanassi, J.A.; Thoma, C.L.; Bradbury, B.J.; Deshpande, M.; Pucci, M.J. Dual targeting of DNA gyrase and topoisomerase IV: target interactions of heteroaryl isothiazolones in Staphylococcus aureus. Antimicrob. Agents Chemother., 2007, 51, 2445-2453.
66. Aravind, L.; Leipe, D.D.; Koonin, E.V. Toprim-a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucleic Acids Res., 1998, 26, 4205-4213.
67. Podos, S.D.; Thanassi, J.A.; Leggio, M.; Pucci, M.J. Bactericidal activity of ACH-702 against nondividing and biofilm Staphylococci. Antimicrob. Agents Chemother., 2012, 56, 3812-3818.
68. Pucci, M.J.; Podos, S.D.; Thanassi, J.A.; Leggio, M.J.; Bradbury, B.J.; Deshpande, M. In vitro and in vivo profiles of ACH-702, an isothiazoloquinolone, against bacterial pathogens. Antimicrob. Agents Chemother., 2011, 55, 2860-2871.
69. Ellsworth, E.L.; Tran, T.P.; Showalter, H.D.; Sanchez, J.P.; Watson, B.M.; Stier, M.A.; Domagala, J.M.; Gracheck, S.J.; Joannides, E.T.; Shapiro, M.A.; Dunham, S.A.; Hanna, D.L.; Huband, M.D.; Gage, J.W.; Bronstein, J.C.; Liu, J.Y.; Nguyen, D.Q.; Singh, R. 3-aminoquinazolinediones as a new class of antibacterial agents demonstrating excellent antibacterial activity against wild-type and multidrug resistant organisms. J. Med. Chem., 2006, 49, 6435-6438.
70. Tran, T.P.; Ellsworth, E.L.; Sanchez, J.P.; Watson, B.M.; Stier, M.A.; Showalter, H.D.; Domagala, J.M.; Shapiro, M.A.; Joannides, E.T.; Gracheck, S.J.; Nguyen, D.Q.; Bird, P.; Yip, J.; Sharadendu, A.; Ha, C.; Ramezani, S.; Wu, X.; Singh, R. Structureactivity relationships of 3-aminoquinazolinediones, a new class of bacterial type-2 topoisomerase (DNA gyrase and topo IV) inhibitors. Bioorg. Med. Chem. Lett., 2007, 17, 1312-1320.
71. Huband, M.D.; Cohen, M.A.; Zurack, M.; Hanna, D.L.; Skerlos, L.A.; Sulavik, M.C.; Gibson, G.W.; Gage, J.W.; Ellsworth, E.; Stier, M.A.; Gracheck, S.J. In vitro and in vivo activities of PD 0305970 and PD 0326448, new bacterial gyrase/topoisomerase inhibitors with potent antibacterial activities versus multidrugresistant gram-positive and fastidious organism groups. Antimicrob. Agents Chemother., 2007, 51, 1191-1201.
72. Hutchings, K.M.; Tran, T.P.; Ellsworth, E.L.; Watson, B.M.; Sanchez, J.P.; Hollis Showalter, H.D.; Stier, M.A.; Shapiro, M.; Themis Joannides, E.; Huband, M.; Nguyen, D.Q.; Maiti, S.; Li, T.; Tailor, J.; Thomas, G.; Ha, C.; Singh, R. Synthesis and antibacterial activity of the C-7 side chain of 3-aminoquinazolinediones. Bioorg. Med. Chem. Lett., 2008, 18, 5087-5090.
73. Pan, X.S.; Gould, K.A.; Fisher, L.M. Probing the differential interactions of quinazolinedione PD 0305970 and quinolones with gyrase and topoisomerase IV. Antimicrob. Agents Chemother., 2009, 53, 3822-3831.
74. Black, M.T.; Stachyra, T.; Platel, D.; Girard, A.M.; Claudon, M.; Bruneau, J.M.; Miossec, C. Mechanism of action of the antibiotic NXL101, a novel nonfluoroquinolone inhibitor of bacterial type II topoisomerases. Antimicrob. Agents Chemother., 2008, 52, 3339-3349.
75. Black, M.T.; Coleman, K. New inhibitors of bacterial topoisomerase GyrA/ParC subunits. Curr. Opin. Investig. Drugs, 2009, 10, 804-810.
76. Widdowson, K.; Hennessy, A. Advances in structure-based drug design of novel bacterial topoisomerase inhibitors. Future Med. Chem., 2010, 2, 1619-1622.
77. Miles, T.J.; Barfoot, C.; Brooks, G.; Brown, P.; Chen, D.; Dabbs, S.; Davies, D.T.; Downie, D.L.; Eyrisch, S.; Giordano, I.; Gwynn, M.N.; Hennessy, A.; Hoover, J.; Huang, J.; Jones, G.; Markwell, R.; Rittenhouse, S.; Xiang, H.; Pearson, N. Novel cyclohexylamides as potent antibacterials targeting bacterial type IIA topoisomerases. Bioorg. Med. Chem. Lett., 2011, 21, 7483-7488.
78. Miles, T.J.; Axten, J.M.; Barfoot, C.; Brooks, G.; Brown, P.; Chen, D.; Dabbs, S.; Davies, D.T.; Downie, D.L.; Eyrisch, S.; Gallagher, T.; Giordano, I.; Gwynn, M.N.; Hennessy, A.; Hoover, J.; Huang, J.; Jones, G.; Markwell, R.; Miller, W.H.; Minthorn, E.A.; Rittenhouse, S.; Seefeld, M.; Pearson, N. Novel aminopiperidines as potent antibacterials targeting bacterial type IIA topoisomerases. Bioorg. Med. Chem. Lett., 2011, 21, 7489-7495.
79. Geng, B.; Comita-Prevoir, J.; Eyermann, C.J.; Reck, F.; Fisher, S. Exploring left-hand-side substitutions in the benzoxazinone series of 4-amino-piperidine bacterial type IIA topoisomerase inhibitors. Bioorg. Med. Chem. Lett., 2011, 21, 5432-5435.
80. Reck, F.; Alm, R.; Brassil, P.; Newman, J.; Dejonge, B.; Eyermann, C.J.; Breault, G.; Breen, J.; Comita-Prevoir, J.; Cronin, M.; Davis, H.; Ehmann, D.; Galullo, V.; Geng, B.; Grebe, T.; Morningstar, M.; Walker, P.; Hayter, B.; Fisher, S. Novel N-linked aminopiperidine inhibitors of bacterial topoisomerase type II: broad-spectrum antibacterial agents with reduced hERG activity. J. Med. Chem., 2011, 54, 7834-7847.
81. Reck, F.; Alm, R.A.; Brassil, P.; Newman, J.V.; Ciaccio, P.; McNulty, J.; Barthlow, H.; Goteti, K.; Breen, J.; Comita-Prevoir, J.; Cronin, M.; Ehmann, D.E.; Geng, B.; Godfrey, A.A.; Fisher, S.L. Novel N-linked aminopiperidine inhibitors of bacterial topoisomerase type II with reduced pKa: antibacterial agents with an improved safety profile. J. Med. Chem., 2012, 55, 6916-6933.
82. Shapiro, A.B.; Andrews, B. Allosteric inhibition of the DNAdependent ATPase activity of Escherichia coli DNA gyrase by a representative of a novel class of inhibitors. Biochem. Pharmacol., 2012, 84, 900-904.
83. Mitton-Fry, M.J.; Brickner, S.J.; Hamel, J.C.; Brennan, L.; Casavant, J.M.; Chen, M.; Chen, T.; Ding, X.; Driscoll, J.; Hardink, J.; Hoang, T.; Hua, E.; Huband, M.D.; Maloney, M.; Marfat, A.; McCurdy, S.P.; McLeod, D.; Plotkin, M.; Reilly, U.; Robinson, S.; Schafer, J.; Shepard, R.M.; Smith, J.F.; Stone, G.G.; Subramanyam, C.; Yoon, K.; Yuan, W.; Zaniewski, R.P.; Zook, C. Novel quinoline derivatives as inhibitors of bacterial DNA gyrase and topoisomerase IV. Bioorg. Med. Chem. Lett., 2013, 23, 2955-2961.
84. Gomez, L.; Hack, M.D.; Wu, J.; Wiener, J.J.; Venkatesan, H.; Santillan, A., Jr.; Pippel, D.J.; Mani, N.; Morrow, B.J.; Motley, S.T.; Shaw, K.J.; Wolin, R.; Grice, C.A.; Jones, T.K. Novel pyrazole derivatives as potent inhibitors of type II topoisomerases. Part 1: synthesis and preliminary SAR analysis. Bioorg. Med. Chem. Lett., 2007, 17, 2723-2727.
85. Wiener, J.J.; Gomez, L.; Venkatesan, H.; Santillan, A., Jr.; Allison, B.D.; Schwarz, K.L.; Shinde, S.; Tang, L.; Hack, M.D.; Morrow, B.J.; Motley, S.T.; Goldschmidt, R.M.; Shaw, K.J.; Jones, T.K.; Grice, C.A. Tetrahydroindazole inhibitors of bacterial type II topoisomerases. Part 2: SAR development and potency against multidrug-resistant strains. Bioorg. Med. Chem. Lett., 2007, 17, 2718-2722.
86. Wiles, J.A.; Phadke, A.S.; Bradbury, B.J.; Pucci, M.J.; Thanassi, J.A.; Deshpande, M. Selenophene-containing inhibitors of type IIA bacterial topoisomerases. J. Med. Chem., 2011, 54, 3418-3425.
87. Ruble, J.C.; Hurd, A.R.; Johnson, T.A.; Sherry, D.A.; Barbachyn, M.R.; Toogood, P.L.; Bundy, G.L.; Graber, D.R.; Kamilar, G.M. Synthesis of (-)-PNU-286607 by asymmetric cyclization of alkylidene barbiturates. J. Am. Chem. Soc., 2009, 131, 3991-3997.
88. Miller, A.A.; Bundy, G.L.; Mott, J.E.; Skepner, J.E.; Boyle, T.P.; Harris, D.W.; Hromockyj, A.E.; Marotti, K.R.; Zurenko, G.E.; Munzner, J.B.; Sweeney, M.T.; Bammert, G.F.; Hamel, J.C.; Ford, C.W.; Zhong, W.Z.; Graber, D.R.; Martin, G.E.; Han, F.; Dolak, L.A.; Seest, E.P.; Ruble, J.C.; Kamilar, G.M.; Palmer, J.R.; Banitt, L.S.; Hurd, A.R.; Barbachyn, M.R. Discovery and characterization of QPT-1, the progenitor of a new class of bacterial topoisomerase inhibitors. Antimicrob. Agents Chemother., 2008, 52, 2806-2812.
89. Mukherjee, S.; Robinson, C.A.; Howe, A.G.; Mazor, T.; Wood, P.A.; Urgaonkar, S.; Hebert, A.M.; Raychaudhuri, D.; Shaw, J.T. NBenzyl-3-sulfonamidopyrrolidines as novel inhibitors of cell division in E. coli. Bioorg. Med. Chem. Lett., 2007, 17, 6651-6655.
90. Foss, M.H.; Hurley, K.A.; Sorto, N.; Lackner, L.L.; Thornton, K.M.; Shaw, J.T.; Weibel, D.B. N-Benzyl-3-sulfonamidopyrrolidines are a new class of bacterial DNA gyrase inhibitors. ACS Med. Chem. Lett., 2011, 2, 289-292.
91. Ostrov, D.A.; Hernandez Prada, J.A.; Corsino, P.E.; Finton, K.A.; Le, N.; Rowe, T.C. Discovery of novel DNA gyrase inhibitors by high-throughput virtual screening. Antimicrob. Agents Chemother., 2007, 51, 3688-3698.
92. Flatman, R.H.; Howells, A.J.; Heide, L.; Fiedler, H.P.; Maxwell, A. Simocyclinone D8, an inhibitor of DNA gyrase with a novel mode of action. Antimicrob. Agents Chemother., 2005, 49, 1093-1100.
93. Sadiq, A.A.; Patel, M.R.; Jacobson, B.A.; Escobedo, M.; Ellis, K.; Oppegard, L.M.; Hiasa, H.; Kratzke, R.A. Anti-proliferative effects of simocyclinone D8 (SD8), a novel catalytic inhibitor of topoisomerase II. Invest. New Drugs, 2010, 28, 20-25.
94. Bellon, S.; Parsons, J.D.; Wei, Y.; Hayakawa, K.; Swenson, L.L.; Charifson, P.S.; Lippke, J.A.; Aldape, R.; Gross, C.H. 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., 2004, 48, 1856-1864.
95. Lewis, R.J.; Singh, O.M.; Smith, C.V.; Skarzynski, T.; Maxwell, A.; Wonacott, A.J.; Wigley, D.B. The nature of inhibition of DNA gyrase by the coumarins and the cyclothialidines revealed by X-ray crystallography. EMBO J., 1996, 15, 1412-1420.
96. Holdgate, G.A.; Tunnicliffe, A.; Ward, W.H.; Weston, S.A.; Rosenbrock, G.; Barth, P.T.; Taylor, I.W.; Pauptit, R.A.; Timms, D. The entropic penalty of ordered water accounts for weaker binding of the antibiotic novobiocin to a resistant mutant of DNA gyrase: a thermodynamic and crystallographic study. Biochemistry, 1997, 36, 9663-9673.
97. Tsai, F.T.; Singh, O.M.; Skarzynski, T.; Wonacott, A.J.; Weston, S.; Tucker, A.; Pauptit, R.A.; Breeze, A.L.; Poyser, J.P.; O'Brien, R.; Ladbury, J.E.; Wigley, D.B. The high-resolution crystal structure of a 24-kDa gyrase B fragment from E. coli complexed with one of the most potent coumarin inhibitors, clorobiocin. Proteins, 1997, 28, 41-52.
98. del Castillo, I.; Vizán, J.L.; Rodríguez-Sáinz, M.C.; Moreno, F. An unusual mechanism for resistance to the antibiotic coumermycin A1. Proc. Natl. Acad. Sci. U.S.A., 1991, 88, 8860-8864.
99. Anderle, C.; Stieger, M.; Burrell, M.; Reinelt, S.; Maxwell, A.; Page, M.; Heide, L. Biological activities of novel gyrase inhibitors of the aminocoumarin class. Antimicrob. Agents Chemother., 2008, 52, 1982-1990.
100. Alt, S.; Mitchenall, L.A.; Maxwell, A.; Heide, L. Inhibition of DNA gyrase and DNA topoisomerase IV of Staphylococcus aureus and Escherichia coli by aminocoumarin antibiotics. J. Antimicrob. Chemother., 2011, 66, 2061-2069.
101. Nakada, N.; Gmunder, H.; Hirata, T.; Arisawa, M. Mechanism of inhibition of DNA gyrase by cyclothialidine, a novel DNA gyrase inhibitor. Antimicrob. Agents Chemother., 1994, 38, 1966-1973.
102. Angehrn, P.; Buchmann, S.; Funk, C.; Goetschi, E.; Gmuender, H.; Hebeisen, P.; Kostrewa, D.; Link, H.; Luebbers, T.; Masciadri, R.; Nielsen, J.; Reindl, P.; Ricklin, F.; Schmitt-Hoffmann, A.; Theil, F.P. New antibacterial agents derived from the DNA gyrase inhibitor cyclothialidine. J. Med. Chem., 2004, 47, 1487-1513.
103. Angehrn, P.; Goetschi, E.; Gmuender, H.; Hebeisen, P.; Hennig, M.; Kuhn, B.; Luebbers, T.; Reindl, P.; Ricklin, F.; Schmitt-Hoffmann, A. A new DNA gyrase inhibitor subclass of the cyclothialidine family based on a bicyclic dilactam-lactone scaffold. Synthesis and antibacterial properties. J. Med. Chem., 2011, 54, 2207-2224.
104. Saiz-Urra, L.; Cabrera Perez, M.A.; Helguera, A.M.; Froeyen, M. Combining molecular docking and QSAR studies for modelling the antigyrase activity of cyclothialidine derivatives. Eur. J. Med. Chem., 2011, 46, 2736-2747.
105. Phillips, J.W.; Goetz, M.A.; Smith, S.K.; Zink, D.L.; Polishook, J.; Onishi, R.; Salowe, S.; Wiltsie, J.; Allocco, J.; Sigmund, J.; Dorso, K.; Lee, S.; Skwish, S.; de la Cruz, M.; Martin, J.; Vicente, F.; Genilloud, O.; Lu, J.; Painter, R.E.; Young, K.; Overbye, K.; Donald, R.G.; Singh, S.B. Discovery of kibdelomycin, a potent new class of bacterial type II topoisomerase inhibitor by chemicalgenetic profiling in Staphylococcus aureus. Chem. Biol., 2011, 18, 955-965.
106. Singh, S.B.; Goetz, M.A.; Smith, S.K.; Zink, D.L.; Polishook, J.; Onishi, R.; Salowe, S.; Wiltsie, J.; Allocco, J.; Sigmund, J.; Dorso, K.; de la Cruz, M.; Martin, J.; Vicente, F.; Genilloud, O.; Donald, R.G.; Phillips, J.W. Kibdelomycin A, a congener of kibdelomycin, derivatives and their antibacterial activities. Bioorg. Med. Chem. Lett., 2012, 22, 7127-7130.
107. Sawa, R.; Takahashi, Y.; Hashizume, H.; Sasaki, K.; Ishizaki, Y.; Umekita, M.; Hatano, M.; Abe, H.; Watanabe, T.; Kinoshita, N.; Homma, Y.; Hayashi, C.; Inoue, K.; Ohba, S.; Masuda, T.; Arakawa, M.; Kobayashi, Y.; Hamada, M.; Igarashi, M.; Adachi, H.; Nishimura, Y.; Akamatsu, Y. Amycolamicin: a novel broadspectrum antibiotic inhibiting bacterial topoisomerase. Chemistry, 2012, 18, 15772-15781.
108. Hossion, A.M.; Zamami, Y.; Kandahary, R.K.; Tsuchiya, T.; Ogawa, W.; Iwado, A.; Sasaki, K. Quercetin diacylglycoside analogues showing dual inhibition of DNA gyrase and topoisomerase IV as novel antibacterial agents. J. Med. Chem., 2011, 54, 3686-3703.
109. Brvar, M.; Perdih, A.; Oblak, M.; Mašić, L.P.; Šolmajer, T. In silico discovery of 2-amino-4-(2, 4-dihydroxyphenyl) thiazoles as novel inhibitors of DNA gyrase B. Bioorg. Med. Chem. Lett., 2010, 20, 958-962.
110. Brvar, M.; Perdih, A.; Hodnik, V.; Renko, M.; Anderluh, G.; Jerala, R.; Šolmajer, T. In silico discovery and biophysical evaluation of novel 5-(2-hydroxybenzylidene) rhodanine inhibitors of DNA gyrase B. Bioorg. Med. Chem., 2012, 20, 2572-2580.
111. Wolber, G.; Langer, T. LigandScout: 3-D pharmacophores derived from protein-bound ligands and their use as virtual screening filters. J. Chem. Inf. Model., 2005, 45, 160-169.
112. Irwin, J.J.; Shoichet, B.K. ZINC-a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model., 2005, 45, 177-182.
113. Gross, C.H.; Parsons, J.D.; Grossman, T.H.; Charifson, P.S.; Bellon, S.; Jernee, J.; Dwyer, M.; Chambers, S.P.; Markland, W.; Botfield, M.; Raybuck, S.A. Active-site residues of Escherichia coli DNA gyrase required in coupling ATP hydrolysis to DNA supercoiling and amino acid substitutions leading to novobiocin resistance. Antimicrob. Agents Chemother., 2003, 47, 1037-1046.
114. Charifson, P.S.; Grillot, A.L.; Grossman, T.H.; Parsons, J.D.; Badia, M.; Bellon, S.; Deininger, D.D.; Drumm, J.E.; Gross, C.H.; LeTiran, A.; Liao, Y.; Mani, N.; Nicolau, D.P.; Perola, E.; Ronkin, S.; Shannon, D.; Swenson, L.L.; Tang, Q.; Tessier, P.R.; Tian, S.K.; Trudeau, M.; Wang, T.; Wei, Y.; Zhang, H.; Stamos, D. 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., 2008, 51, 5243-5263.
115. Grossman, T.H.; Bartels, D.J.; Mullin, S.; Gross, C.H.; Parsons, J.D.; Liao, Y.; Grillot, A.L.; Stamos, D.; Olson, E.R.; Charifson, P.S.; Mani, N. Dual targeting of GyrB and ParE by a novel aminobenzimidazole class of antibacterial compounds. Antimicrob. Agents Chemother., 2007, 51, 657-666.
116. Mani, N.; Gross, C.H.; Parsons, J.D.; Hanzelka, B.; Muh, U.; Mullin, S.; Liao, Y.; Grillot, A.L.; Stamos, D.; Charifson, P.S.; Grossman, T.H. In vitro characterization of the antibacterial spectrum of novel bacterial type II topoisomerase inhibitors of the aminobenzimidazole class. Antimicrob. Agents Chemother., 2006, 50, 1228-1237.
117. Vertex Pharmaceuticals Inc. Pyrimidine gyrase and topoisomerase IV inhibitors. WO2012097269; 2012.
118. East, S.P.; White, C.B.; Barker, O.; Barker, S.; Bennett, J.; Brown, D.; Boyd, E.A.; Brennan, C.; Chowdhury, C.; Collins, I.; Convers-Reignier, E.; Dymock, B.W.; Fletcher, R.; Haydon, D.J.; Gardiner, M.; Hatcher, S.; Ingram, P.; Lancett, P.; Mortenson, P.; Papadopoulos, K.; Smee, C.; Thomaides-Brears, H.B.; Tye, H.; Workman, J.; Czaplewski, L.G. DNA gyrase (GyrB) /topoiso merase IV (ParE) inhibitors: synthesis and antibacterial activity. Bioorg. Med. Chem. Lett., 2009, 19, 894-899.
119. Starr, J.T.; Sciotti, R.J.; Hanna, D.L.; Huband, M.D.; Mullins, L.M.; Cai, H.; Gage, J.W.; Lockard, M.; Rauckhorst, M.R.; Owen, R.M.; Lall, M.S.; Tomilo, M.; Chen, H.; McCurdy, S.P.; Barbachyn, M.R. 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., 2009, 19, 5302-5306.
120. Congreve, M.; Chessari, G.; Tisi, D.; Woodhead, A.J. Recent developments in fragment-based drug discovery. J. Med. Chem., 2008, 51, 3661-3680.
121. Lubbers, T.; Angehrn, P.; Gmunder, H.; Herzig, S. Design, synthesis, and structure-activity relationship studies of new phenolic DNA gyrase inhibitors. Bioorg. Med. Chem. Lett., 2007, 17, 4708-4714.
122. Manchester, J.I.; Dussault, D.D.; Rose, J.A.; Boriack-Sjodin, P.A.; Uria-Nickelsen, M.; Ioannidis, G.; Bist, S.; Fleming, P.; Hull, K.G. Discovery of a novel azaindole class of antibacterial agents targeting the ATPase domains of DNA gyrase and topoisomerase IV. Bioorg. Med. Chem. Lett., 2012, 22, 5150-5156.
123. Uria-Nickelsen, M.; Neckermann, G.; Sriram, S.; Andrews, B.; Manchester, J.I.; Carcanague, D.; Stokes, S.; Hull, K.G. Novel topoisomerase inhibitors: microbiological characterisation and in vivo efficacy of pyrimidines. Int. J. Antimicrob. Agents, 2013, 41, 363-371.
124. Uria-Nickelsen, M.; Blodgett, A.; Kamp, H.; Eakin, A.; Sherer, B.; Green, O. Novel DNA gyrase inhibitors: microbiological characterisation of pyrrolamides. Int. J. Antimicrob. Agents, 2013, 41, 28-35.
125. Mdluli, K.; Ma, Z. Mycobacterium tuberculosis DNA gyrase as a target for drug discovery. Infect. Disord. Drug Targets, 2007, 7, 159-168.
126. Koul, A.; Arnoult, E.; Lounis, N.; Guillemont, J.; Andries, K. The challenge of new drug discovery for tuberculosis. Nature, 2011, 469, 483-490.
127. Dong, Y.; Zhao, X.; Kreiswirth, B.N.; Drlica, K. Mutant prevention concentration as a measure of antibiotic potency: studies with clinical isolates of Mycobacterium tuberculosis. Antimicrob. Agents Chemother., 2000, 44, 2581-2584.
128. Zhao, B.Y.; Pine, R.; Domagala, J.; Drlica, K. Fluoroquinolone action against clinical isolates of Mycobacterium tuberculosis: effects of a C-8 methoxyl group on survival in liquid media and in human macrophages. Antimicrob. Agents Chemother., 1999, 43, 661-666.
129. Pantel, A.; Petrella, S.; Veziris, N.; Brossier, F.; Bastian, S.; Jarlier, V.; Mayer, C.; Aubry, A. Extending the definition of the GyrB quinolone resistance-determining region in Mycobacterium tuberculosis DNA gyrase for assessing fluoroquinolone resistance in M. tuberculosis. Antimicrob. Agents Chemother., 2012, 56, 1990-1996.
130. Pantel, A.; Petrella, S.; Matrat, S.; Brossier, F.; Bastian, S.; Reitter, D.; Jarlier, V.; Mayer, C.; Aubry, A. DNA gyrase inhibition assays are necessary to demonstrate fluoroquinolone resistance secondary to gyrB mutations in Mycobacterium tuberculosis. Antimicrob. Agents Chemother., 2011, 55, 4524-4529.
131. Aubry, A.; Pan, X.S.; Fisher, L.M.; Jarlier, V.; Cambau, E. Mycobacterium tuberculosis DNA gyrase: interaction with quinolones and correlation with antimycobacterial drug activity. Antimicrob. Agents Chemother., 2004, 48, 1281-1288.
132. Gomez, C.; Ponien, P.; Serradji, N.; Lamouri, A.; Pantel, A.; Capton, E.; Jarlier, V.; Anquetin, G.; Aubry, A. Synthesis of gatifloxacin derivatives and their biological activities against Mycobacterium leprae and Mycobacterium tuberculosis. Bioorg. Med. Chem., 2013, 21, 948-956.
133. Malik, M.; Marks, K.R.; Mustaev, A.; Zhao, X.; Chavda, K.; Kerns, R.J.; Drlica, K. Fluoroquinolone and quinazolinedione activities against wild-type and gyrase mutant strains of Mycobacterium smegmatis. Antimicrob. Agents Chemother., 2011, 55, 2335-2343.
134. Minovski, N.; Perdih, A.; Šolmajer, T. Combinatorially-generated library of 6-fluoroquinolone analogs as potential novel antitubercular agents: a chemometric and molecular modeling assessment. J. Mol. Model., 2012, 18, 1735-1753.
135. Minovski, N.; Perdih, A.; Novič, M.; Šolmajer, T. Cluster-based molecular docking study for in silico identification of novel 6-fluoroquinolones as potential inhibitors against Mycobacterium tuberculosis. J. Comput. Chem., 2013, 34, 790-801.
136. Chopra, S.; Matsuyama, K.; Tran, T.; Malerich, J.P.; Wan, B.; Franzblau, S.G.; Lun, S.; Guo, H.; Maiga, M.C.; Bishai, W.R.; Madrid, P.B. Evaluation of gyrase B as a drug target in Mycobacterium tuberculosis. J. Antimicrob. Chemother., 2012, 67, 415-421.
137. Karkare, S.; Chung, T.T.; Collin, F.; Mitchenall, L.A.; McKay, A.R.; Greive, S.J.; Meyer, J.J.; Lall, N.; Maxwell, A. The naphthoquinone diospyrin is an inhibitor of DNA gyrase with a novel mechanism of action. J. Biol. Chem., 2013, 288, 5149-5156.
138. Lipinski, C.A.; Lombardo, F.; Dominy, B.W.; Feeney, P.J. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Delivery Rev., 2001, 46, 3-26.
139. O'Shea, R.; Moser, H.E. Physicochemical properties of antibacterial compounds: implications for drug discovery. J. Med. Chem., 2008, 51, 2871-2878.
140. Manchester, J.I.; Buurman, E.T.; Bisacchi, G.S.; McLaughlin, R.E. Molecular determinants of AcrB-mediated bacterial efflux implications for drug discovery. J. Med. Chem., 2012, 55, 2532-2537.