Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти

The pyrazolone-based 4-(furan-2-yl)benzoic acids have been synthesized and studied as xanthine oxidase inhibitors. This enzyme is one of the therapeutic targets for the treatment of hyperuricemia and related diseases. The compounds studied have found to exhibit low micromolar IC50 values relative to...

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Published in:Журнал органічної та фармацевтичної хімії
Date:2023
Volume:21
Issue:4
Pages:27-35
ISSN:2518-1548
Author Affiliations:
  • Alona V. Beiko — V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine
  • Oleksandr L. Kobzar — V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine
  • Maryna V. Kachaeva — V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine
  • Stepan G. Pilyo — V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine — ORCID: 0000-0003-1072-2990
  • Vsevolod Yu. Tanchuk — V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine
  • Andriy I. Vovk — V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine
Main Authors: Beiko, Alona V., Kobzar, Oleksandr L., Kachaeva, Maryna V., Pilyo, Stepan G., Tanchuk, Vsevolod Yu., Vovk, Andriy I.
Format: Article
Language:English
Published: National University of Pharmacy 2023
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Online Access:https://ophcj.nuph.edu.ua/article/view/298726
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Journal of Organic and Pharmaceutical Chemistry
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author Beiko, Alona V.
Kobzar, Oleksandr L.
Kachaeva, Maryna V.
Pilyo, Stepan G.
Tanchuk, Vsevolod Yu.
Vovk, Andriy I.
author_facet Beiko, Alona V.
Kobzar, Oleksandr L.
Kachaeva, Maryna V.
Pilyo, Stepan G.
Tanchuk, Vsevolod Yu.
Vovk, Andriy I.
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author_orcid_str_mv 0000-0003-1072-2990
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container_title Журнал органічної та фармацевтичної хімії
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description The pyrazolone-based 4-(furan-2-yl)benzoic acids have been synthesized and studied as xanthine oxidase inhibitors. This enzyme is one of the therapeutic targets for the treatment of hyperuricemia and related diseases. The compounds studied have found to exhibit low micromolar IC50 values relative to the enzyme in vitro, depending on substituents in position 3 of the pyrazolone ring. However, the inhibitory effects observed are reduced in the presence of bovine serum albumin or Tween-80. Among the pyrazolone derivatives synthesized, 4-(5-((3-methyl-5-oxo-1-phenyl-1,5-dihydro-4H-pyrazol-4-ylidene)methyl)furan-2-yl)benzoic acid has been found to be the most potent inhibitor of xanthine oxidase. Kinetic results have shown that this compound is a mixed-type inhibitor with higher affinity to the free enzyme than to the enzyme-substrate complex. The results of the molecular docking and molecular dynamics show that the carboxylic group of the inhibitor can form a salt bridge with Arg880 and a hydrogen bond with Thr1010. These interactions can be key factors in the enzyme-inhibitor complex stabilization.
doi_str_mv 10.24959/ophcj.23.298726
first_indexed 2025-07-23T04:43:25Z
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fulltext ISSN 2308-8303 (Print) / 2518-1548 (Online) 27 Original Research http://ophcj.nuph.edu.ua UDC 547.775+547.722+577.152.1 A. V. Beiko, O. L. Kobzar, M. V. Kachaeva, S. G. Pilyo, V. Yu. Tanchuk, A. I. Vovk V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the National Academy of Sciences of Ukraine, 1 Academician Kukhar str., 02094 Kyiv, Ukraine Inhibition of Xanthine Oxidase by Pyrazolone Derivatives Bearing a 4-(Furan-2-yl)benzoic Acid Moiety Abstract The pyrazolone-based 4-(furan-2-yl)benzoic acids have been synthesized and studied as xanthine oxidase inhibitors. This en- zyme is one of the therapeutic targets for the treatment of hyperuricemia and related diseases. The compounds studied have found to exhibit low micromolar IC50 values relative to the enzyme in vitro, depending on substituents in position 3 of the pyrazolone ring. However, the inhibitory effects observed are reduced in the presence of bovine serum albumin or Tween-80. Among the pyrazolone derivatives synthesized, 4-(5-((3-methyl-5-oxo-1-phenyl-1,5-dihydro-4H-pyrazol-4-ylidene)methyl)furan- 2-yl)benzoic acid has been found to be the most potent inhibitor of xanthine oxidase. Kinetic results have shown that this compound is a mixed-type inhibitor with higher affinity to the free enzyme than to the enzyme-substrate complex. The re- sults of the molecular docking and molecular dynamics show that the carboxylic group of the inhibitor can form a salt bridge with Arg880 and a hydrogen bond with Thr1010. These interactions can be key factors in the enzyme-inhibitor complex stabilization. Keywords: xanthine oxidase; inhibition; pyrazolone; benzoic acid; molecular docking; molecular dynamics А. В. Бейко, О. Л. Кобзар, М. В. Качаєва, С. Г. Пільо, В. Ю. Танчук, А. І. Вовк Інститут біоорганічної хімії та нафтохімії ім. В. П. Кухаря Національної академії наук України, вул. Академіка Кухаря, 1, Київ, 02094, Україна Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти Анотація 4-(Фуран-2-іл)бензойні кислоти з фрагментом піразолону було синтезовано та досліджено як інгібітори ксантиноксидази. Цей ензим є однією з терапевтичних мішеней для лікування гіперурикемії та супутніх захворювань. Вивчені сполуки демонстрували низькомікромолярні значення IC50 щодо ензиму in vitro, залежно від замісників у положенні 3 піра- золонового кільця. Однак спостережувані інгібувальні ефекти знижувались за наявності бичачого сироваткового аль- буміну або твіну-80. Серед синтезованих похідних піразолону 4-(5-((3-метил-5-оксо-1-феніл-1,5-дигідро-4H-піразол- 4-іліден)метил)фуран-2-іл)бензойна кислота виявилась найпотужнішим інгібітором ксантиноксидази. Кінетичні до- слідження засвідчили, що ця сполука є інгібітором змішаного типу з більшою спорідненістю до вільного ензиму, ніж до ензим-субстратного комплексу. Результати молекулярного докінгу і молекулярної динаміки свідчать про те, що карбоксильна група інгібітора може формувати сольовий місток із залишком Arg880 і водневий зв’язок із залишком Thr1010. Ці взаємодії можуть бути ключовими факторами стабілізації комплексу ензим-інгібітор. Ключові слова: ксантиноксидаза; інгібування; піразолони; бензойна кислота; молекулярний докінг; молекулярна динаміка Citation: Beiko, A. V.; Kobzar, O. L.; Kachaeva, M. V.; Pilyo, S. G.; Tanchuk, V. Yu.; Vovk, A. I. Inhibition of xanthine oxidase by pyrazolone derivatives bearing a 4-(furan-2-yl)benzoic acid moiety. Journal of Organic and Pharmaceutical Chemistry 2023, 21 (4), 27 – 35. https://doi.org/10.24959/ophcj.23.298726 Received: 1 October 2023; Revised: 23 October 2023; Accepted: 28 October 2023 Copyright© 2023, A. V. Beiko, O. L. Kobzar, M. V. Kachaeva, S. G. Pilyo, V. Yu. Tanchuk, A. I. Vovk. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0). Funding: The work was founded by the National Academy of Sciences of Ukraine. Conflict of interests: The authors have no conflict of interests to declare. ISSN 2308-8303 (Print) / 2518-1548 (Online) 28 Журнал органічної та фармацевтичної хімії 2023, 21 (4) ■ Introduction Xanthine oxidase (XO) is the main cytosolic molybdenum-containing enzyme of the purine ca- tabolism that catalyzes the transformation of hy- poxanthine to xanthine and uric acid. Increased xanthine oxidase activity is not only the cause of hyperuricemia and gout, but also the cause of hy- peruricemia-related disorders, such as metabolic syndrome, renal and cardiovascular diseases, dia- betes, hypertension, and cancer. In addition, the enzymatic reaction is accompanied by the forma- tion of reactive oxygen species causing oxidative stress and systemic inflammation [1]. Current- ly, FDA-approved drugs, such as allopurinol and febuxostat (as well as topiroxostat approved in Japan), are widely used in the treatment of the di- seases associated with the enhanced XO activity. However, these drugs possess significant adver- se effects and are not suitable for a long-term treat- ment of asymptomatic hyperuricemia. Thus, the development of new XO inhibitors is needed [2]. For this reason, the derivatives of imidazole, py- razole, thiazole, selenazole, isoxazole, pyrimidine, quinolone, purine, pyrazolopyrimidine, pyrazolo- quinazoline, and some other heterocyclic compounds have been previously synthesized and studied as XO inhibitors [3]. Among them, compounds bearing the carboxyl group like febuxostat appeared to be effective inhibitors of the enzyme. The binding mechanisms of such compounds to the XO active site include the interactions of their carboxylate groups with Arg880 and Thr1011 [3]. The present study is aimed to synthesize the pyrazolone-based 4-(furan-2-yl)benzoic acids for their evaluation as XO inhibitors. It should be no- ted that structurally similar compounds namely pyrazolone-based phenylfuran-2-yl derivatives were described previously as inhibitors of SARS-CoV and MERS-CoV 3C-like protease [4], heptosyl- transferase WaaC [5], and neuraminidase [6]. ■ Results and discussion Compounds 3a – i were synthesized with a yield of 80 – 87 % according to Scheme by the Knoeve- nagel condensation of pyrazolones 1 with 4-(5-for- mylfuran-2-yl)benzoic acid (2). The pyrazolones 1 bearing various substituents in positions 3 and 5 were obtained by the condensation of β-keto- carboxylic esters with hydrazine derivatives (Knorr synthesis) [7]. 4-(5-Formylfuran-2-yl)benzoic acid was obtained via the arylation of 2-furancarbox- aldehyde by a diazonium salt of p-aminobenzoic acid (Meerwein arylation method) [8]. 1H NMR, IR, and mass-spectra confirmed the structures of the compounds 3a – i synthesized. In 1H NMR spectra, the methyne proton (–CH=) signals ap- pear in the range from 8.06 to 6.87 ppm, overlap- ping with the signals from the aryl substituents (except compound 3g with the chemical shift of the methine proton singlet of 7.85 ppm). The 1H NMR signals of the carboxylic groups were observed at 12.17 – 13.11 ppm. In the IR spectra, the inten- sive absorption bands of carbonyl groups were found at 1679 – 1696 cm–1. The synthesized compounds 3a – i can exist as E- or Z-isomers. It was shown previously that (5-phenylfuran-2-yl)methylene-containing pyra- zolone derivatives synthesized by the same route were a mixture of E-Z-isomers with a Z-isomer as a major product [5, 6]. The pyrazolone derivatives 3a – i were studied in vitro as inhibitors of xanthine oxidase from bovine milk. This enzyme was characterized by 90 % amino acid sequence identity to XO from the human liver [9]. The IC50 values determined from the dose-dependent curves of the enzyme inhibition (Figure 1) are presented in Table 1. These values are inhibitor concentrations, at which the XO activity was decreased by 50 %. According to the results obtained, compounds 3a – i exhibited low micromolar IC50 values towards O HO O N N O Ar R H2N OH , AcOH reflux, 2h O OH O N NO R ArO 1a i– 3a i– 1d 3d, : Ar = Ph, R = 4-FC6H4 1e 3e, : Ar = Ph, R = 4-ClC6H4 1f 3f, : Ar = Ph, R = 4-O2NC6H4 1g 3g, : Ar = Ph, R = thiophen-2-yl 1h 3h, : Ar = Ph, R = pyridin-4-yl 1i 3i, : Ar = 4-MeC6H4, R = Ph 2 + 1a 3a, : Ar = Ph, R = Me 1b 3b, : Ar = Ph, R = CF3 1c 3c, : Ar = Ph, R = Ph Scheme. The synthesis of pyrazolone-based 4-(furan-2-yl)benzoic acids 3a – i ISSN 2308-8303 (Print) / 2518-1548 (Online) 29 Journal of Organic and Pharmaceutical Chemistry 2023, 21 (4) XO in vitro. Compound 3a bearing 3-methyl-5- phenyl pyrazolone part had an IC50 value of 36 nM; it was the closest to that for the inhibition by febuxostat (Table 1) and significantly exceeded the IC50 value (4.5 µM) of 4-(5-formylfuran-2-yl) benzoic acid (2) observed. This indicates that the inhibition efficiency of compound 3a was ensured due to a pyrazolone scaffold. The replacement of the methyl group in the structure of compound 3a on the trifluoromethyl substituent (derivati- ve 3b) led to a 14-fold loss of the XO inhibition activity. Compounds 3c – h with phenyl, 4-fluoro- phenyl, 4-chlorophenyl, 4-nitrophenyl, thiophen- 2-yl, or pyridin-4-yl substituents in position 3 of the pyrazolone ring, as well as compound 3i bear- ing the 1-(4-tolyl)-3-phenyl-substituted pyrazolo- ne moiety were characterized by low differences in the IC50 values ranging from 0.058 to 0.22 µM. The inhibition effects of most of the compounds studied here were found to be significantly re- duced (up to 80-fold) by bovine serum albumin (BSA) or Tween-80 (Table 1). The inhibitory ac- tivity in the presence of BSA and a detergent was less changed for compound 3a bearing a methyl group at position 3 of the pyrazolone ring and de- creased most strongly for 3-(thiophen-2-yl)-sub- stituted compound 3g. In contrast to this, BSA or Tween-80 almost did not change the inhibi- tory potency of febuxostat as a reference com- pound against XO. Taking into account that the decrease of the XO inhibition can be related to the binding of the inhibitors to BSA, a spectral study was per- formed. It was found that compound 3i quenched the fluorescence of BSA (Figure 2). The BSA fluorescence spectra were measured at different temperatures (298 K, 303 K, 308 K, and 313 K) in the presence of 0.5 µM, 1 µM, 2 µM, and 3 µM of compound 3i. The Stern-Volmer quenching constants (KSV) obtained from plots of F0/F vs. the quencher concentration were 2.55×105 M–1 (R2 = 0.98), 3.42×105 M–1 (R2 = 0.96), 5.36×105 M–1 (R2 = 1.00), 6.42×105 M–1 (R2 = 0.99), respectively. The KSV values increased with an in- crease in temperature. This dependence can indi- cate a dynamic quenching process. However, further analysis showed that the apparent bimolecular quenching rate constants (kq) were three orders of magnitude larger than the value of the maximum scatter collision quenching constant of various quen- chers with biopolymers (2.0×1010 M–1 sec–1) [10]. The calculated values of kq were 4.39×1013 M–1 sec–1, 5.90×1013 M–1 sec–1, 9.25×1013 M–1 sec–1, and 1.11×1014 M–1 sec–1 for 298 K, 303 K, 308 K, and 313 K, respectively. Thus, the fluorescence quen- ching of BSA by compound 3i can be also caused by the complex formation. The results of kinetic studies were analyzed to elucidate the mechanism of the XO inhibition Table 1. Pyrazolone-based 4-(furan-2-yl)benzoic acids as xanthine oxidase inhibitors* Compound IC50, µM IC50, µM (in the presence of BSA) IC50, µM (in the presence of Tween-80) 3a 0.036 ± 0.0025 0.09 ± 0.02 0.11 ± 0.01 3b 0.52 ± 0.09 2.54 ± 0.69 2.44 ± 0.37 3c 0.096 ± 0.006 2.16 ± 0.48 3.74 ± 0.43 3d 0.15 ± 0.03 2.32 ± 0.10 2.55 ± 0.12 3e 0.17 ± 0.04 3.30 ± 0.68 7.48 ± 1.04 3f 0.22 ± 0.015 3.77 ± 0.09 7.88 ± 1.42 3g 0.058 ± 0.012 4.66 ± 0.91 2.58 ± 0.25 3h 0.22 ± 0.02 1.87 ± 0.51 2.20 ± 0.29 3i 0.06 ± 0.014 0.63 ± 0.18 2.08 ± 0.33 Febuxostat 0.0062 ± 0.0007 0.0075 ± 0.0001 0.0056 ± 0.0005 Note: *IC50 values were determined from 2-3 series of experiments and shown as an average value ± standard deviation. The concentrations of BSA or Tween-80 in the model systems were 2 µM and 0.025 vol.  %, respectively Figure 1. Dose-dependent curves of xanthine oxidase inhibition by compounds 3a (○), 3c (□) and 3i (∆) ISSN 2308-8303 (Print) / 2518-1548 (Online) 30 Журнал органічної та фармацевтичної хімії 2023, 21 (4) by pyrazolone derivative 3a. The double recipro- cal Lineweaver-Burk plots shown in Figure 3 demonstrate that compound 3a is a mixed-type inhibitor of the enzyme. The competitive and non- competitive inhibition constants (Ki and Ki’) cal- culated were 7.11 ± 1.27 nM and 66.5 ± 15.4 nM, respectively. The Ki value being one order of mag- nitude lower than the Ki’ value indicates that the affinity of the compound is higher to the free en- zyme than to the enzyme-substrate complex. Molecular docking calculations were carried out using the AutoDock Vina software [11]. The affi- nity of compound 3a (Z-isomer) to XO was cha- racterized by a docking energy of -10.8 kcal mol–1. According to the results obtained, the 4-(furan- 2-yl)benzoic acid fragment of compound 3a is located in the substrate binding region near the molybdopterin cofactor. The carboxylic group of the inhibitor has a salt-bridge interaction with Arg880, as well as hydrogen bonds with Thr1010 and a water molecule (HOH1457), which interacts with Glu1261. The phenyl group of the 4-(furan-2- yl)benzoic acid part of the inhibitor forms face-to- face and edge-to-face π-π-stacking interactions with Phe914 and Phe1009. The furan linker that con- nects the benzoic acid and pyrazolone fragments of the inhibitor is sandwiched between hydropho- bic amino acid residues Leu873, Leu1014, and Pro1076. The pyrazolone fragment bearing phenyl and methyl groups in position 1 and 3, respec- tively, is located near Leu648, Phe649, Lys771, His875, Ser876, Val1011, and Phe1013. The oxy- gen atom of the pyrazolone carbonyl group forms a hydrogen bond with Ser876 (Figure 4 (A)). Figure 2. Fluorescence emission spectra of BSA in the absence (a) and presence (b → h) of compound 3i measured at a temperature of 298 K, λex of 280 nm, and slits of 5 nm. The BSA concentration was 2 µM. The concentrations of compound 3i were 0 µM, 1 µM, 2 µM, 4 µM, 5 µM, 6 µM, 8 µM, and 10 µM Figure 3. Lineweaver-Burke plots for the XO inhibition by compound 3a. The inhibitor concentrations were 0 (○), 15 nM (□), 30 nM (∆), and 45 nM (◊) Figure 4. Binding modes of the Z-isomer of compound 3a in the active site of XO predicted by the molecular docking calculation (A) and the subsequent molecular dynamic simulation (B). All the hydrogens are hidden for clarity, and the oxygen atoms shown as red spheres represent water molecules ISSN 2308-8303 (Print) / 2518-1548 (Online) 31 Journal of Organic and Pharmaceutical Chemistry 2023, 21 (4) The molecular dynamic simulation was per- formed by the NAMD software [12] to verify the stability of the enzyme-inhibitor complex model obtained, as well as for a more detailed analy- sis of the interactions that could occur between inhibitor 3a and the enzyme active site. The cal- culations were performed with the complex of the chain C of the enzyme containing molybdopterin and the inhibitor (XO-Moco-3a), as well as with the complex of the chain C of XO containing only a molybdopterin cofactor (XO-Moco). The time- dependent changes of the root mean square de- viation (RMSD) values for the enzyme backbone atoms for both model systems are shown in Figu- re 5 (A). As can be seen, the RMSD of XO-Moco and XO-Moco-3a complexes reached equilibration approximately after 10 ns and 14 ns, respectively. The XO-Moco-3a model system has higher RMSD values compared to those for the XO-Moco com- plex. This suggests that the binding of the ligand leads to a change in the structure of the enzyme. Despite this, the root mean square fluctuation (RMSF) revealed that compound 3a only slightly affected the fluctuation of the nearby amino acid residues (Figure 5 (B)). The negative effect of the ligand on the compactness and folding of XO is indicated by the increased values of the radius of gyration (RoG) and solvent-accessible surface area (SASA) which are shown in Figure 5 (C) and Figure 5 (D), respectively. The binding mode of inhibitor 3a in the ac- tive site of the XO obtained after 20 ns of the MD simulation is given in Figure 4 (B). The ligand is more deeply located in the active site of the en- zyme as compared with its location after the mole- cular docking (Figure 4 (A)). This is especially noticeable from the changed locations of the furan ring and the 3-methyl-5-phenyl substituted pyra- zolone moiety, which showed π-π-stacking and π-cation interactions with Phe914 and Lys771, respectively. Such position of the inhibitor can be caused by the solvent action of water forming hyd- rogen bonds with the carbonyl oxygen of the pyra- zolone ring. The changes in the structure of the enzyme detected by the plots in Figure 5 can be re- lated to the changes in the position of the inhibitor. According to several studies [13, 14, 15] and the check of the amino acid residues protonation states by the PROPKA software [16], Glu802 was proto- nated, and therefore, was represented as Glu802. Figure 5. The values of the root mean square deviation of the enzyme backbone (A), the root mean square fluctuation of the amino acid residues (B), the radius of gyration (C), and the solvent accessible surface area (D) obtained from the MD simulation for the XO-Moco and XO-Moco-3a model systems ISSN 2308-8303 (Print) / 2518-1548 (Online) 32 Журнал органічної та фармацевтичної хімії 2023, 21 (4) The free binding energy of compound 3a in the active site of the XO was studied from the MD simulation results using the MMPBSA me- thod. As seen from Table 2, the VDWAALS, EEL, and ENPOLAR energies contribute to stabiliza- tion of the enzyme-inhibitor complex, while the EPB and EDISPER energies lead to its destabi- lization. The free energy decomposed by the MMPBSA method per amino acid residues located within 4 Å from the ligand in the enzyme active site at the last frame of the MD simulation are shown in Table 3. Currently, the method cannot be used for the decomposition of the non-polar solvation component. According to the total energies, the interactions of the benzoic acid moiety of the li- gand with the amino acid residues Arg880, Phe1009, and Thr1010 are key factor for the enzyme-inhi- bitor complex stabilization. As can be seen, the electrostatic energies make the greatest contri- bution to these interactions. ■ Conclusions Thus, pyrazolone-based 4-(furan-2-yl)benzoic acids 3a – i can inhibit XO with IC50 values in the submicromolar range. The inhibitory properties of the compounds are affected by the nature of substituents in position 3 of the pyrazolone ring. The inhibition of XO by most of the compounds synthesized is significantly reduced in the pre- sence of bovine serum albumin or Tween-80, ex- cluding 3-methyl-1-phenyl pyrazolone-based de- rivative 3a. Among the 4-(furan-2-yl)benzoic acids synthesized, compound 3a has proven to be a po- tent inhibitor of xanthine oxidase. Kinetic studies have shown that the 3-methyl-1-phenyl pyrazo- lone-based 4-(furan-2-yl)benzoic acid 3a is a mixed- type inhibitor of the enzyme. The inhibition con- stants calculated suggest that the affinity of the inhibitor to the free enzyme is higher than that to the enzyme-substrate complex. Molecular dock- ing and molecular dynamic simulations have shown that the salt-bridge and the hydrogen bond for- med between the carboxylic group of the inhibi- tor and the residues Arg880 and Thr1010 can be responsible for the stability of the enzyme- inhibitor complex. ■ Experimental part Commercially available chemical reagents and solvents were purchased and used without puri- fication. The TCL method was applied to moni- tor the reaction progress. The Fisher-Johns ap- paratus was used for the melting point determi- nation. 1H NMR spectra were taken on a Varian Mercury (500 MHz) spectrometer in DMSO-d6 or CF3C(O)OD solution using the signal of residual Table 2. The calculated energies of MMPBSA components of the free binding energy of compound 3a bound at the XO active site* MMPBSA component Energy ± SD, kcal mol–1 VDWAALS -34.5398 ± 3.1316 EEL -101.2729 ± 14.6772 EPB 106.1432 ± 10.5794 ENPOLAR -28.9013 ± 1.6140 EDISPER 49.3169 ± 1.9125 ∆Gtotal -11.3089 ± 6.7691 Note: *VDWAALS is a van der Waals energy contribution from MM; EEL is the electrostatic energy as calculated by the MM force field; EPB is an electrostatic contribution to the solvation free energy calculated by PB; ENPOLAR is a nonpolar contribution to the solvation free energy calculated by an empirical model; EDISPER is dispersion energy; ∆Gtotal is the free binding energy. Table 3. The free energy decomposed per amino acid residues Residue Energy ± SD, kcal mol–1 van der Waals Electrostatic Polar solvation TOTAL Leu648 -1.64 ± 0.57 -0.03 ± 0.30 0.65 ± 0.48 -1.02 ± 0.44 Asn768 -0.37 ± 0.15 -0.16 ± 0.27 0.88 ± 0.43 0.35 ± 0.44 Lys771 -1.05 ± 0.41 -15.21 ± 2.196 17.21 ± 2.97 0.94 ± 0.92 Glh802 -0.90 ± 0.33 -0.51 ± 0.24 1.78 ± 0.47 0.37 ± 0.46 Thr803 -0.21 ± 0.12 -0.18 ± 0.08 0.24 ± 0.11 -0.15 ± 0.11 Leu873 -1.83 ± 0.30 0.85 ± 0.17 -0.59 ± 0.16 -1.57 ± 0.33 Ser876 -1.37 ± 0.20 -0.12 ± 1.16 1.97 ± 1.10 0.47 ± 0.49 Arg880 0.13 ± 0.78 -39.28 ± 5.73 32.42 ± 2.62 -6.74 ± 3.77 Ala910 -0.18 ± 0.10 -0.57 ± 0.08 0.56 ± 0.11 -0.19 ± 0.15 Phe914 -1.30 ± 0.34 0.11 ± 0.24 0.23 ± 0.29 -0.96 ± 0.28 Phe1009 -2.03 ± 0.37 -5.35 ± 0.87 4.27 ± 0.35 -3.12 ± 0.94 Thr1010 0.43 ± 0.83 -12.82 ± 3.65 6.80 ± 1.68 -5.59 ± 1.92 Ala1078 -0.87 ± 0.24 -0.80 ± 0.37 1.00 ± 0.28 -0.68 ± 0.35 Ala1079 -1.09 ± 0.33 -0.38 ± 0.58 1.13 ± 0.49 -0.34 ± 0.46 ISSN 2308-8303 (Print) / 2518-1548 (Online) 33 Journal of Organic and Pharmaceutical Chemistry 2023, 21 (4) solvent protons as a standard. IR spectra were recorded on a Vertex-70 spectrometer in KBr tablets. LC-MS spectra were obtained using an Agilent 1200 Series high-performance liquid chromatograph. 4-(5-Formyl-2-furanyl)benzoic acid 2 was ob- tained by the method described previously [17]. The general procedure for the synthesis of compounds 3a – i A solution of 0.005 mol of corresponding py- razolone 1 in 15 – 20 mL of acetic acid was added to a hot solution of 0.005 mol of 4-(5-formyl-2-fu- ranyl)benzoic acid 2 in 20 – 30 mL of acetic acid followed by addition of 0.005 mol of ethanolamine. The reaction mixture was refluxed for 2 hours and then left at 20 – 25 °C for 12 hours. The pre- cipitate formed was filtered, washed with etha- nol, dried, and recrystallized from a mixture of MeCN/DMF. 4-[5-(3-Methyl-5-oxo-1-phenyl-1,5-dihydropy- razol-4-ylidenemethyl)-furan-2-yl]-benzoic acid (3a) E/Z – 1:3. Burgundy solid. Yield – 86%. M. p. > 250 °С. Anal. Calcd for C22H16N2O4, %: C 70.96, H 4.33, N 7.52. Found, %: C 70.90, H 4.38, N 7.44. IR (KBr), νmax, cm−1: 2873, 1680 (C=O), 1604, 1319, 1273, 1027. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 2.31 (0.75H, s, Me), 2.68 (0.25H, s, Me), 7.18 (1H, t, JHH = 8.0 Hz, Ar), 7.49 – 7.66 (2Н, m, Ar), 7.75 – 8.00 (4Н, m, Ar, –CH=), 8.00 – 8.05 (4H, m, Ar), 8.64 (1H, d, JHH = 4.0 Hz, Ar), 13.03 (1Н, br. s, C(O)OH). LC-MS, m/z (Irel, %): 373 [M+H]+ (100). 4-[5-(5-Oxo-1-phenyl-3-trifluoromethyl-1,5-di- hydro-pyrazol-4-ylidenemethyl)-furan-2-yl]-ben- zoic acid (3b) Z-isomer. Burgundy solid. Yield – 82 %. M. p. > 250 °С. Anal. Calcd for C22H13F3N2O4, %: C 61.98, H 3.07, N 6.57. Found, %: C 62.04, H 3.16, N 6.50. IR (KBr), νmax, cm−1: 2535, 1692 (C=O), 1590, 1510, 1470, 1427, 1276, 1116, 954, 808. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 7.33 (1H, t, JHH = 8.0 Hz, Ar), 7.50 – 7.53 (2H, m, Ar, –CH=), 7.68 – 7.72 (1H, m, Ar), 7.82 – 7.87 (3Н, m, Ar), 8.07 – 8.17 (4Н, m, Ar), 8.80 – 8.82 (1H, m, Ar), 13.09 (1H, br. s, C(O)OH). LC-MS, m/z (Irel, %): 427 [M+H]+ (100). 4-[5-(5-Oxo-1,3-diphenyl-1,5-dihydro-pyrazol- 4-ylidenemethyl)-furan-2-yl]-benzoic acid (3c) E/Z – 1:5. Burgundy solid. Yield – 85 %. M. p. > 250 °С. Anal. Calcd for C27H18N2O4, %: C 74.65, H 4.18, N 6.45. Found, %: C 74.74, H 4.22, N 6.40. IR (KBr), νmax, cm−1: 2545, 1696 (C=O), 1591, 1275, 942, 802. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 7.00 (1Н, d, JHH = 8.0 Hz, Ar), 7.25 (1Н, t, JHH = 8.0 Hz, Ar), 7.48 (2Н, q, JHH = 8.0 Hz, Ar), 7.61 – 7.79 (6Н, m, Ar, –CH=), 7.78 (2Н, d, JHH = 8.0 Hz, Ar), 8.76 – 7.96 (5Н, m, Ar), 12.17 (1H, br. s, C(O)OH). LC-MS, m/z (Irel, %): 436 [M+H]+ (100). 4-{5-[3-(4-Fluoro-phenyl)-5-oxo-1-phenyl-1,5- dihydro-pyrazol-4-ylidenemethyl]-furan-2-yl}- benzoic acid (3d) E/Z – 1:5. Burgundy solid. Yield – 85 %. M. p. > 250 °С. Anal. Calcd for C27H17FN2O4, %: C 71.68, H 3.79, N 6.19. Found, %: C 71.72, H 3.82, N 6.12. IR (KBr), νmax, cm−1: 2989, 1696 (C=O), 1591, 1496, 1275, 944, 810. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 7.01 (1Н, d, JHH = 8.0 Hz, Ar), 7.22 – 7.32 (2Н, m, Ar), 7.43 – 7.51 (4Н, m, Ar), 7.64 – 7.86 (4Н, m, Ar, –CH=), 7.95 – 8.76 (5Н, m, Ar), 12.12 (1Н, br. s, C(O)OH). LC-MS, m/z (Irel, %): 453 [M+H]+ (100). 4-{5-[3-(4-Chloro-phenyl)-5-oxo-1-phenyl-1,5- dihydro-pyrazol-4-ylidenemethyl]-furan-2-yl}- benzoic acid (3e) E/Z – 1:3. Burgundy solid. Yield – 80 %. M. p. > 250 °С. Anal. Calcd for C27H17ClN2O4, %: C 69.16, H 3.65, Cl 7.56, N 5.97. Found, %: C 69.34, H 3.72, Cl 7.60, N 5.94. IR (KBr), νmax, cm−1: 2536, 1683 (C=O), 1592, 1274, 941, 803, 771. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 6.96 – 7.27 (1H, m, Ar), 7.46 – 7.52 (3H, m, Ar), 7.61 – 7.86 (6H, m, Ar, –CH=), 7.94 – 8.08 (5Н, m, Ar), 8.75 (1Н, d, JHH = 4.0 Hz, Ar), 13.08 (1Н, br. s, C(O)OH). LC-MS, m/z (Irel, %): 470 [M+H]+ (100). 4-{5-[3-(4-Nitro-phenyl)-5-oxo-1-phenyl-1,5- dihydro-pyrazol-4-ylidenemethyl]-furan-2-yl}- benzoic acid (3f) E/Z – 1:5. Burgundy solid. Yield – 80 %. M. p. > 250 °С. Anal. Calcd for C27H17N3O6, %: C 67.64, H 3.57, N 8.76. Found, %: C 67.68, H 3.64, N 8.72. IR (KBr), νmax, cm−1: 2535, 1687 (C=O), 1592, 1516, 1348, 1273, 803. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 6.87-8.06 (6H, m, Ar, –CH=), 8.22 – 8.41 (2Н, m, Ar), 8.74 (8Н, m, Ar), 13.05 (br. s, 1Н, C(O)OH). LC-MS, m/z (Irel, %): 480 [M+H]+ (100). 4-[5-(5-Oxo-1-phenyl-3-thiophen-2-yl-1,5-dihyd- ro-pyrazol-4-ylidenemethyl)-furan-2-yl]-benzoic acid (3g) Z-izomer. Burgundy solid. Yield – 80 %. M. p. > 250 °С. Anal. Calcd for C25H16N2O4S, %: C 68.17, H 3.66, N 6.36, S 7.28. Found, %: C 68.24, H 3.76, N 6.46, S 7.32. IR (KBr), νmax, cm−1: 2531, 1682 (C=O), 1593, 1422, 1277, 693. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 7.22 (2Н, t, JHH = 8.0 Hz, Ar), 7.30 (1Н, t, JHH = 4.0 Hz, Ar), 7.45 (2Н, t, JHH = 8.0 Hz, Ar), 7.58 (1Н, d, JHH = 4.0 Hz, Ar), 7.76 – 7.85 (3Н, m, Ar, –CH=), 7.91 – 8.03 (5Н, m, Ar), 8.72 (1Н, d, JHH = 4.0 Hz, Ar), 13.40 (1Н, br. s, C(O)OH). LC-MS, m/z (Irel, %): 441 [M+1]+ (100). ISSN 2308-8303 (Print) / 2518-1548 (Online) 34 Журнал органічної та фармацевтичної хімії 2023, 21 (4) 4-[5-(5-Oxo-1-phenyl-3-pyridin-4-yl-1,5-di- hydro-pyrazol-4-ylidenemethyl)-furan-2-yl]-ben- zoic acid (3h) E/Z – 1:5. Burgundy solid. Yield – 85%. M. p. > 250 °С. Anal. Calcd for C26H17N3O4, %: C 71.72, H 3.94, N 9.65. Found, %: C 71.86, H 4.00, N 9.60. IR (KBr), νmax, cm−1: 2920, 2567, 1670 (C=O), 1602, 1510, 1400, 1265, 931, 807. 1H NMR (500 MHz, CF3C(O)OD), δ, ppm: 7.42 – 7.80 (7H, m, Ar, –CH=), 8.21 – 8.75 (7Н, m, Ar), 9.22 – 9.30 (2Н, m, Ar). LC-MS, m/z (Irel, %): 436 [M+H]+ (100). 4-[5-(5-Oxo-3-phenyl-1-p-tolyl-1,5-dihydro- pyrazol-4-ylidenemethyl)-furan-2-yl]-benzoic acid (3i) E/Z – 1:5. Burgundy solid. Yield – 87%. M. p. > 250 °С. Anal. Calcd for C28H20N2O4, %: C 74.99, H 4.50, N 6.25. Found, %: C 74.90, H 4.67, N 6.30. IR (KBr), νmax, cm−1: 2923, 2536, 1679 (C=O), 1603, 1513, 1424, 1276, 943, 812. 1H NMR (500 MHz, DMSO-d6), δ, ppm: 2.33 (3H, s, Me), 7.29 (2Н, d, JHH = 8.0 Hz, Ar), 7.60 – 7.64 (5H, m, Ar, –CH=), 7.78 (2Н, d, JHH = 8.0 Hz, Ar), 7.88 (2Н, t, JHH = 8.0 Hz, Ar), 8.05 – 8.77 (5Н, m, Ar), 13.11 (1Н, br. s, C(O)OH). LC-MS, m/z (Irel, %): 449 [M+H]+ (100). The in vitro study of pyrazolone-contain- ing 4-(furan-2-yl)benzoic acids as xanthine oxidase inhibitors XO from bovine milk and xanthine as a sub- strate were purchased from Sigma-Aldrich. In the case of pyrazolone-based 4-(furan-2-yl)benzoic acids 3a – i, the system contained a sodium-phos- phate buffer (50 mM, pH 7.4), xanthine (50 µM), EDTA (0.1 mM), DMSO (1 %), and an inhibitor. To study the specificity of the XO inhibition by com- pounds 3a – i, the reaction mixture additionally contained 2 µM of BSA or 0.025 vol.  % Tween-80. The reaction was initiated by the enzyme addi- tion after preincubation of the mixture for 5 min. The total volume of the system was 2 mL. The ac- tivity of XO was monitored spectrophotometri- cally at 293 nm. The uric acid molar extinction coefficient of 12.2 mM–1 cm–1 was used for calcu- lations. The value of the calculated Michaelis- Menten constant (Km) was 5.7 µM. The fluorescence quenching experiment The fluorescence quenching studies were per- formed on the example of compound 3i to confirm the interaction of pyrazolone-based 4-(furan-2-yl) benzoic acids with bovine serum albumin (BSA). The reaction mixture consisted of sodium phos- phate buffer (50 mM, pH 7.4), 2 µM BSA, DMSO (1 %), and a quencher (compound 3i). The total vo- lume of the reaction mixture was 2 mL. The Stern- Volmer quenching constants were obtained from plots of F0/F vs. the quencher concentration de- scribed by the Stern-Volmer equation: F0 / F = 1 + kqτ0 = 1 + KSV[Q] where F0 and F are the BSA fluorescence intensi- ties observed without and with the quencher in the model systems, respectively; [Q] is the con- centration of the quencher; kq is the apparent bi- molecular quenching rate constant; τ0 is the life- time of unquenched tryptophan in BSA; KSV is the Stern-Volmer quenching constant. Molecular docking calculation Compound 3a was docked into the active site (chain C) of XO from bovine milk (PDB code 1FIQ [9]) using the protocol described in [18]. The cal- culation was performed by the AutoDock Vina software [11]. The enzyme-inhibitor model com- plex was analyzed by Discovery Studio 3.5 (Ac- celrys, San Diego, CA, USA). Molecular dynamic simulation The molecular dynamic simulations were per- formed using the NAMD software [12] according to the previously described protocol [19]. The pre- paration of the model system for the calculation was carried out using the conda environment. The VMD 1.9.3 [20] was used for the calculation of RMSD, RMSF, RoG, and SASA. The binding free energy and its decomposition per amino acid residues were performed by MMPBSA.py [21] ac- cording to the protocol described in [19]. ■ Acknowledgements We would like to thank Enamine Ltd for sup- porting the synthesis of compounds. ■ References 1. Chen, C.; Lü, J.-M.; Yao, Q. Hyperuricemia-related diseases and xanthine oxidoreductase (XOR) inhibitors: an overview. Med. Sci. Monit. 2016, 22, 2501 – 2512. https://doi.org/10.12659/msm.899852. 2. Singh, A.; Singh, K.; Sharma, A.; Kaur, K.; Chadha, R.; Bedi, P. M. S. 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Graphics 1996, 14, 33 – 38. https://doi.org/10.1016/0263-7855(96)00018-5. 21. Miller, B. R.; McGee, T. D.; Swails, J. M.; Homeyer, N.; Gohlke, H.; Roitberg, A. E. MMPBSA.py: an efficient program for end-state free energy calculations. J. Chem. Theory Comput. 2012, 8 (9), 3314 – 3321. https://doi.org/10.1021/ct300418h. Information about the authors: Alona V. Beiko, Ph.D. Student, V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine; https://orcid.org/0000-0003-1119-988X. Oleksandr L. Kobzar, Ph.D. in Chemistry; Senior Researcher of the Department of Bioorganic Mechanisms, V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine; https://orcid.org/0000-0003-4370-7041. Maryna V. Kachaeva, Ph.D. in Chemistry; Researcher of the Department of Chemistry of Bioactive Nitrogen-Containing Heterocyclic Bases, V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine; https://orcid.org/0000-0003-1517-4807. Stepan G. Pilyo, Ph.D. in Chemistry; Senior Researcher of the Department of Chemistry of Bioactive Nitrogen-Containing Heterocyclic Bases, V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine; https://orcid.org/0000-0002-7089-1393. Vsevolod Yu. Tanchuk, Ph.D. in Chemistry; Senior Researcher of the Department of Bioorganic Mechanisms, V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine; https://orcid.org/0000-0001-9055-870X. Andriy I. Vovk (corresponding author), Dr. Sci. in Chemistry, Professor, Head of the Department of Bioorganic Mechanisms, Director of V. P. Kukhar Institute of Bioorganic Chemistry and Petrochemistry of the NAS of Ukraine; https://orcid.org/0000-0001-6167-076X; e-mail for correspondence: vovk@bpci.kiev.ua.
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spelling oai:ojs.journals.uran.ua:article-2987262026-08-23T18:33:04Z Inhibition of Xanthine Oxidase by Pyrazolone Derivatives Bearing a 4-(Furan-2-yl)benzoic Acid Moiety Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти Beiko, Alona V. Kobzar, Oleksandr L. Kachaeva, Maryna V. Pilyo, Stepan G. Tanchuk, Vsevolod Yu. Vovk, Andriy I. ксантиноксидаза інгібування піразолони бензойна кислота молекулярний докінг молекулярна динаміка xanthine oxidase inhibition pyrazolone benzoic acid molecular docking molecular dynamics The pyrazolone-based 4-(furan-2-yl)benzoic acids have been synthesized and studied as xanthine oxidase inhibitors. This enzyme is one of the therapeutic targets for the treatment of hyperuricemia and related diseases. The compounds studied have found to exhibit low micromolar IC50 values relative to the enzyme in vitro, depending on substituents in position 3 of the pyrazolone ring. However, the inhibitory effects observed are reduced in the presence of bovine serum albumin or Tween-80. Among the pyrazolone derivatives synthesized, 4-(5-((3-methyl-5-oxo-1-phenyl-1,5-dihydro-4H-pyrazol-4-ylidene)methyl)furan-2-yl)benzoic acid has been found to be the most potent inhibitor of xanthine oxidase. Kinetic results have shown that this compound is a mixed-type inhibitor with higher affinity to the free enzyme than to the enzyme-substrate complex. The results of the molecular docking and molecular dynamics show that the carboxylic group of the inhibitor can form a salt bridge with Arg880 and a hydrogen bond with Thr1010. These interactions can be key factors in the enzyme-inhibitor complex stabilization. 4-(Фуран-2-іл)бензойні кислоти з фрагментом піразолону було синтезовано та досліджено як інгібітори ксантиноксидази. Цей ензим є однією з терапевтичних мішеней для лікування гіперурикемії та супутніх захворювань. Вивчені сполуки демонстрували низькомікромолярні значення IC50 щодо ензиму in vitro, залежно від замісників у положенні 3 піразолонового кільця. Однак спостережувані інгібувальні ефекти знижувались за наявності бичачого сироваткового альбуміну або твіну-80. Серед синтезованих похідних піразолону 4-(5-((3-метил-5-оксо-1-феніл-1,5-дигідро-4H-піразол-4-іліден)метил)фуран-2-іл)бензойна кислота виявилась найпотужнішим інгібітором ксантиноксидази. Кінетичні дослідження засвідчили, що ця сполука є інгібітором змішаного типу з більшою спорідненістю до вільного ензиму, ніж до ензим-субстратного комплексу. Результати молекулярного докінгу і молекулярної динаміки свідчать про те, що карбоксильна група інгібітора може формувати сольовий місток із залишком Arg880 і водневий зв’язок із залишком Thr1010. Ці взаємодії можуть бути ключовими факторами стабілізації комплексу ензим-інгібітор. National University of Pharmacy 2023-12-09 Article Article application/pdf https://ophcj.nuph.edu.ua/article/view/298726 10.24959/ophcj.23.298726 Journal of Organic and Pharmaceutical Chemistry; Vol. 21 No. 4 (2023); 27-35 Журнал органической и фармацевтической химии; Том 21 № 4 (2023); 27-35 Журнал органічної та фармацевтичної хімії; Том 21 № 4 (2023); 27-35 2518-1548 2308-8303 en https://ophcj.nuph.edu.ua/article/view/298726/292485 Copyright (c) 2024 Alona V. Beiko, Oleksandr L. Kobzar, Maryna V. Kachaeva, Stepan G. Pilyo, Vsevolod Yu. Tanchuk, Andriy I. Vovk http://creativecommons.org/licenses/by/4.0
spellingShingle ксантиноксидаза
інгібування
піразолони
бензойна кислота
молекулярний докінг
молекулярна динаміка
Beiko, Alona V.
Kobzar, Oleksandr L.
Kachaeva, Maryna V.
Pilyo, Stepan G.
Tanchuk, Vsevolod Yu.
Vovk, Andriy I.
Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
title Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
title_alt Inhibition of Xanthine Oxidase by Pyrazolone Derivatives Bearing a 4-(Furan-2-yl)benzoic Acid Moiety
title_full Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
title_fullStr Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
title_full_unstemmed Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
title_short Інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
title_sort інгібування ксантиноксидази похідними піразолону, що містять фрагмент 4-(фуран-2-іл)бензойної кислоти
topic ксантиноксидаза
інгібування
піразолони
бензойна кислота
молекулярний докінг
молекулярна динаміка
topic_facet ксантиноксидаза
інгібування
піразолони
бензойна кислота
молекулярний докінг
молекулярна динаміка
xanthine oxidase
inhibition
pyrazolone
benzoic acid
molecular docking
molecular dynamics
url https://ophcj.nuph.edu.ua/article/view/298726
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