4a and the complete list of resistant strains generated and the sequences of their QRDR is shown in Supplementary Fig. Quinolones, coumarins, cyclothialidines, CcdB and microcin B17 inhibit DNA gyrase. 23, 10361040 (2000). The pellet was washed three times with sterile saline (0.9% NaCl in water) by repeated gentle suspension and centrifugation. Three independent replicates of each compound were performed. Blackwell Science Ltd, Oxford. All other author declare no competing financial interests. Concentrations were 0.01, 0.04, 0.017, 0.68, 2.7 and 10.8M, except for DNM, which was 8.9M for the highest concentration. Fluoroquinolone antibiotics. How many fluoroquinolones are approved for human use? J. Vet. MeSH Furthermore, no homologue of topoisomerase IV has been identified in the M. tuberculosis and Mycobacterium leprae genomes, indicating that the sole target of the quinolone family of inhibitors in these organisms is DNA gyrase. Chen, S. H., Chan, N. L. & Hsieh, T. S. New mechanistic and functional insights into DNA topoisomerases. Wang, S., Wang, Y., Shen, J., Wu, Y. In addition, the N-terminal half of GyrB hydrolyses ATP, and the C-terminal half is involved in binding to GyrA and DNA. Chemotherapy 57, 363371 (2011). Similarly, Bacillus anthracis, E. coli and A. baumannii also have the analogous serine mutated to leucine43,44,45. . At specified time points, mice were killed and blood was collected, centrifuged and the serum was frozen at 80C until analysis. The reaction mixtures were resolved on a 0.8% agarose gel in 40 mM Trisacetate buffer containing 1 mM EDTA. The animal studies (PK, in-vivo toxicity and in-vivo efficacy) were carried out in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. As representatives of cyclothialidines, the compound Ro 09-1437 and its derivative Ro 48-2865 were tested for their ability to inhibit the enzyme activity (Figure 1). DNA gyrase cleavage assays were performed as previously described with minor changes12,37,54. } Parkinson, E. I., Bair, J. S., Cismesia, M. & Hergenrother, P. J. Gyrase Docking 1. However, in mycobacteria, DNA gyrase is the only type II topoisomerase identified so far. When the effect of ciprofloxacin was tested on the supercoiling reaction, detectable inhibition (MIC) required 1.3 M of the drug, in agreement with earlier reports.38 In contrast, cleavage was doubled at concentrations (CC2) as low as 0.17 M (Figure 2 and Table 2). designed and executed the biological experiments including MIC determinations, sequencing of the QRDR of clinical isolates, in vitro analysis of DNA gyrase inhibition and development of resistant mutants. Biol. DNA gyrase, or simply gyrase, is an enzyme within the class of topoisomerase and is a subclass of Type II topoisomerases that reduces topological strain in an ATP dependent manner while double-stranded DNA is being unwound by elongating RNA-polymerase or by helicase in front of the progressing replication fork. (1998) J. Biol. Finally, we discovered a strong correlation between the nimB-promoter variant and a Thr82Ile mutation in DNA Gyrase A (GyrA), which confers fluoroquinolone resistance and has been linked to the . Mechanisms of Action and Resistance of Older and Newer Fluoroquinolones Expression of WT E. coli gyrase A and gyrase B was performed as previously described53. Extended spectrum of quinolone resistance, even to a potential latter third-generation agent, as a result of a minimum of two GrlA and two GyrA alterations in quinolone-resistant Staphylococcus aureus. DNA gyrase and topoisomerase IV control bacterial DNA topology by breaking DNA, passing duplex DNA through the break, and then resealing the break. The site is secure. Jacoby, G. A. Mechanisms of resistance to quinolones. Relative cleavage is the amount of cleavage product seen in the presence of CcdB normalized to the intrinsic cleavage produced by the enzyme alone. 38, 24772479 (1994). Bair, J. S., Palchaudhuri, R. & Hergenrother, P. J. Chemistry and biology of deoxynyboquinone, a potent inducer of cancer cell death. Fluoroquinolones inhibit the ability of the enzymes to ligate cleaved DNA and result in single-and double-stranded DNA breaks. Ciprofloxacin (Cipro)/ofloxacin (Floxin): gonococcal infection. Inhibition of DNA synthesis by quinolones requires the targeted topoisomerase to have DNA cleavage capability, and collisions of the replication fork with reversible quinolone-DNA-topoisomerase complexes convert them to an irreversible form. A. they are proteins B. they have turnover numbers that can be in the thousands and more C. they form 68, 27662772 (2013). 3b. Further modifications of these compounds would be needed to enhance their potency. Deoxynybomycins inhibit mutant DNA gyrase and rescue mice infected with fluoroquinolone-resistant bacteria. 2022 Dec 20;66(12):e0092122. 95, 50035013 (1973). These ternary complexes, called cleaved complexes because the DNA moiety is broken, block replication, transcription, and bacterial growth. J. These enzymes catalyse the introduction of negative supercoils and the decatenation of interlinked chromosomes, respectively6,7,8. Therefore, a thorough evaluation of the effects of a range of inhibitors on DNA gyrase from a Gram-positive bacterium is imperative. effective in treating soft-tissue, bone, and [PMC free article] . 9 and Supplementary Table 5). return null; 1998 Apr 14;95(8):4652-7 Vila, J., Ruiz, J., Goni, P., Marcos, A. The site is secure. Interestingly, M. smegmatis gyrase was refractory to the plasmid-borne proteinaceous inhibitors CcdB and microcin B17. Unlike FQs that bind within the two active sites, it binds between the active sites stabilizing either an uncleaved or a single-stranded cleaved DNA. The mice received vehicle alone, 50mgkg1 CIP, or 50mgkg1 DNM-2 by oral gavage once daily for 10 days; n=15 for each group. 83, 37293731 (1961). Why is resistance to quinolones important? Werner, G. et al. HHS Vulnerability Disclosure, Help DNM was evaluated against both FQ-sensitive S. aureus (ATCC 29213) and FQR MRSA (NRS3, which has GyrA S84L and ParC S80F). A brief overview of the DNA gyrase structure is provided. CcdB and microcin B17 are both plasmid-encoded proteinaceous inhibitors produced by Gram-negative bacteria.16,17 CcdB has been shown to bind to GyrA of E. coli and stabilize the gyraseDNA complex in a manner reminiscent of, but not identical to, the quinolones.18 In agreement with this, mutations conferring resistance to CcdB map to GyrA.19 Like CcdB, microcin B17 also acts by stabilizing the gyraseDNA covalent complex; however, the exact mode of inhibition remains to be elucidated.20 In contrast to CcdB and quinolones, the only mutation in E. coli conferring resistance to microcin B17 maps to Trp-751 in GyrB. The pellet was dissolved in and dialysed against TGEM, and loaded on to a novobiocinSepharose column. 2019 Apr;85:308-318. doi: 10.1016/j.bioorg.2019.01.009. (c) Doseresponse curves for FQS S. aureus (ATCC 29213) and FQR S. aureus (NRS3) treated with DNM. The authors thank J. C. Wang and A. Maxwell for overexpressing constructs of E. coli topoisomerase I and DNA gyrase, respectively. 2022 Feb;148(2):461-473. doi: 10.1007/s00432-021-03625-3. 6). After 30 min, the reaction was stopped with 0.6% SDS. Both E. coli and M. smegmatis gyrase were susceptible to etoposide. FOIA 4b). Expression of S83L and S83R GyrA was performed identically to expression of the WT GyrA. Would you like email updates of new search results? generally resistant. 2). The highest concentration of the inhibitor that failed to show any detectable inhibition of the supercoiling activity was termed the maximal non-effective concentration (MNEC), whereas the minimum concentration that produced complete inhibition was termed the IC100. 39, 12011203 (1995). 2). Recent progress in the discovery and development of DNA gyrase B inhibitors. Paul J. Hergenrother. Because they may affect the development of cartilage, all fluoroquinolones are contraindicated in children, adolescents, and pregnant or breast-feeding women. E. coli strains ZK4 and ZK650 were the microcin B17 susceptible and producer strains, respectively.30, Novobiocin and ciprofloxacin (Sigma, St Louis, MO, USA) were dissolved in water and 0.1 M NaOH, respectively. inhibited;Anaerobes: Site-directed mutagenesis was carried out with the QuikChange Lightning Site-Directed Mutagenesis Kit (Agilent), according to the manufacturers instructions, with the modification that NEB Turbo Competent E. coli were used as the host strain. CC2 was defined as the concentration of inhibitor required to stimulate basal cleavage by two-fold while maximum cleavage represents the fold increase in cleavage in the presence of saturating concentrations of the inhibitor. Microbiol. nausea vomiting diarrhea. Despite this similarity in binding position, the phenotype of DNM in the DNA cleavage assay (that is, the buildup of OC DNA) suggests that its overall mode of inhibition is more similar to that of GSK299423. Antimicrob Agents Chemother 37: 126-127. Dis. Fractions containing pure protein were pooled and dialysed against TDEN buffer (50mM Tris-HCl pH 7.5, 5mM dithiothreitol (DTT), 1mM EDTA, 150mM NaCl) overnight at 4C, using a Slide-A-Lyzer Dialysis Cassette, 10 000 MWCO (Thermo Scientific) and concentrated to 0.51ml, using an Amicon Ultra-15 50K Centrifugal Filter Device. The proteins were renatured by step dialysis against TGEM containing 4, 3, 2, 1 and 0 M urea. listed as inventors. National Library of Medicine doi: 10.1128/mBio.01093-21. for(m=0; mEffect of different classes of inhibitors on DNA gyrase from Clipboard, Search History, and several other advanced features are temporarily unavailable. Article Am. Epub 2018 May 22. Accessibility Activity is from three independent replicates of the microdilution broth assay and is reported as the MIC ingml1. 2023 Jul 8. doi: 10.1007/s11030-023-10676-w. Online ahead of print. It was found to be well tolerated when dosed either subcutaneously, orally or by intraperitoneal injection27. Mar. The column was washed sequentially with 10% and 20% ethanol, then microcin B17 was eluted with 30% ethanol. Dosage adjustments for renal and hepatic dysfunction vary among the quinolones. Natl Acad. Cleaved complexes; DNA gyrase; DNA topoisomerase; Fluoroquinolone; Plasmid DNA isolation; Quinolone. Although M. smegmatis DNA gyrase had lower affinity for etoposide, it showed higher levels of cleavage under saturating concentrations of the drug. 2000 Aug;31 Suppl 2:S24-8. The proteinDNA adducts thus generated also act as blocks for DNA tracking enzymes like RNA and DNA polymerases.15 Point mutations conferring resistance to quinolones primarily map to the N-terminal region of GyrA whereas a few map to the C-terminal half of GyrB.6. Med. Bethesda, MD 20894, Web Policies volume6, Articlenumber:6947 (2015) Overcoming target-mediated quinolone resistance in topoisomerase IV by introducing metal-ion-independent drug-enzyme interactions. DNM or DNM-2 inhibition of S83R also led to a buildup of OC DNA similar to that seen with S83L DNA gyrase only at a slightly higher concentration or longer time points, consistent with the activity of these compounds against VRE with the S83R DNA gyrase. Pharmacokinetic studies were next performed on DNM, DNM-2 and DNM-3. 1.211.52. The .gov means its official. Epub 2019 Jul 10. The overnight culture was then used to inoculate 1litre LB with 50gml1 ampicillin. However, alterations in the primary sequence of DNA gyrase between different organisms appear to modulate the susceptibility of the enzyme to specific inhibitors. When these strains were found, they showed dramatically improved sensitivity to CIP (MIC=0.258.0gml1). Comparison of the Diagnostic Performance of MeltPro and Next - PubMed Infect. The existence of two fluoroquinolone targets and stepwise accumulation of resistance suggested that new quinolones could be found that would require cells to obtain two topoisomerase mutations to display resistance. This leads to cell death and turns out to be a very effective way of killing bacteria. Antimicrob. Pharm. Kidney, brain, lung, liver, spleen, heart, and stomach sample examinations also did not reveal any evidence of toxicity. used as a substitute for consultation with practicing medical or Intercalation assays were performed as previously described34. Tricyclic GyrB/ParE (TriBE) inhibitors: a new class of broad-spectrum dual-targeting antibacterial agents. designed the synthesis of derivative 5. 1b). Treatment of red blood cells (RBCs) with DNM and key derivatives indicated that none of these compounds induce haemolysis (Supplementary Fig. Challa AP, Beam AL, Shen M, Peryea T, Lavieri RR, Lippmann ES, Aronoff DM. Cleaved complexes readily form in vitro when gyrase, plasmid DNA, and quinolone are combined and incubated; complexes are detected by the linearization of plasmid DNA, generally assayed by gel electrophoresis. However, no colonies were observed on co-treatment (resistance frequency <1.0 1010). in bacteria, namely topoisomerase IV and DNA gyrase. Baba, K. et al. Negative control tubes contained 1l DMSO and 19l RBC buffer, and positive control tubes contained 1l DMSO and 19l sterile deionized water. Six-week-old male pathogen-free BALB/c mice were purchased from Taconics Biosciences (Albany, NY). As resistance to DNM emerges, the data predict that such bacteria would be sensitive to FQs. Agents Chemother. Li, S. et al. Front Pharmacol. Owing to the documented difficulty of isolating DNM from natural sources31, we aimed to develop an efficient, modular and flexible synthesis of DNM that could also be used to construct derivatives. After multiple rounds of selection against CIP, a FQR/DNM-sensitive strain was generated. The https:// ensures that you are connecting to the X-ray crystallography reveals that 34 occupies the classical quinolone binding site in the topoisomerase IV-DNA cleavage complex but does not form significant contacts with residues in the quinolone resistance determining region. Cleavage reactions were carried out with M. smegmatis gyrase in the presence of various ciprofloxacin concentrations (lanes 15). cases--pseudomonal infections in cystic fibrosis Microbiology, pharmacokinetics and clinical use. In addition, in this study we found that orally administered DNM-2 is effective in treating mice infected with MRSA, thus showing the first in-vivo efficacy for this class of compounds. official website and that any information you provide is encrypted Sci. However, isolation of NM and DNM from natural sources is non-trivial 31 and the only reported total synthesis of DNM is very low yielding32,33. The supernatant (S100) was subjected to an ammonium sulphate fractionation (70% saturation). (b) KaplanMeier curves showing the survival rates of mice infected with MRSA (NRS3, FQR). The evolution of GP6 resistance in both species was driven by a combination of two classes of mutational events: (i) . (, Sugino, A., Peebles, C. L., Kruezer, K. N. & Cozzarelli, N. R. (, Willmott, C. J. R., Critchlow, S. E., Eperon, I. C. & Maxwell, A. Nybomycin (NM) is a natural product first identified from a culture of a streptomycete isolated from a Missouri soil sample and found to have antibacterial activity27,28. Karunarathne WAHM, Molagoda IMN, Kim MS, Choi YH, Oren M, Park EK, Kim GY. Fluoroquinolones inhibit these enzymes by stabilizing either the DNA-DNA gyrase complex [1] or the DNA-topoisomerase IV complex. PMC Resistance development on co-treatment with CIP and DNM-2 was then explored (Supplementary Fig. In vitro activity of temafloxacin hydrochloride (TA-167 or A-62254), a new fluorinated 4-quinolone. Half-lives range from 3 h Antimicrob. ATP hydrolysis and the mechanism of DNA cleavage. // -->. Moreover, since gyrase has already been used as a molecular target for anti-mycobacterial therapy, the present investigation also gives direction to the development of modified compounds as better therapeutic agents.