7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump

<b>Background/Objectives:</b> Previously, we reported that 3-<i>O</i>-alkyl difluoroquercetins (di-F-Q) potentiates the antimicrobial activity of aztreonam (ATM) against metallo-β-lactamase (MBL)-producing <i>P. aeruginosa</i> through simultaneous inhibition of MB...

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Main Authors: Seongyeon Lee, Taegum Lee, Mi Kyoung Kim, Joong Hoon Ahn, Seri Jeong, Ki-Ho Park, Youhoon Chong
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Antibiotics
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Online Access:https://www.mdpi.com/2079-6382/13/12/1202
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author Seongyeon Lee
Taegum Lee
Mi Kyoung Kim
Joong Hoon Ahn
Seri Jeong
Ki-Ho Park
Youhoon Chong
author_facet Seongyeon Lee
Taegum Lee
Mi Kyoung Kim
Joong Hoon Ahn
Seri Jeong
Ki-Ho Park
Youhoon Chong
author_sort Seongyeon Lee
collection DOAJ
description <b>Background/Objectives:</b> Previously, we reported that 3-<i>O</i>-alkyl difluoroquercetins (di-F-Q) potentiates the antimicrobial activity of aztreonam (ATM) against metallo-β-lactamase (MBL)-producing <i>P. aeruginosa</i> through simultaneous inhibition of MBLs and efflux pumps. However, the ATM-potentiating activity of the 3-<i>O</i>-alkyl di-F-Q was observed only at high and potentially toxic concentrations (32 mg/L). <b>Methods:</b> As both MBLs and efflux pumps reside in the periplasm of Gram-negative bacteria, their inhibitors should accumulate in the periplasmic space. However, the outer membrane porins, the major entry pathway in Gram-negative bacteria, allow the passive diffusion of hydrophilic polar molecules across the outer membrane. Thus, we reasoned that the introduction of a polar substituent at 7-OH position of 3-<i>O</i>-alkyl di-F-Q would enhance its periplasmic concentration to result in potentiation of ATM at lower concentrations. <b>Results:</b> The title compound <b>5</b> exhibited inhibitory activity against NDM-1 as well as the efflux pump of <i>P. aeruginosa</i>, which resulted in synergistical potentiation of ATM. A combination of ATM (8 mg/L) and <b>5</b> (8 mg/L) inhibited 80% of the ATM-resistant CPPA, while ATM alone did not show any inhibition. In addition, only 4 mg/L of <b>5</b> was needed to reduce the MIC<sub>90</sub> of ATM four-fold in ATM-resistant CPPA (n = 15). The time–kill data further supported the effectiveness of the combined treatment of ATM with <b>5</b>, and the combination of ATM (1xMIC) with 8 mg/L of <b>5</b> showed bactericidal effects in every bacterial strain tested (PA-002, <i>bla</i><sub>IMP</sub>, PA-003, <i>bla</i><sub>VIM</sub>, PA-014, <i>bla</i><sub>GES</sub>, and PA-017, <i>bla</i><sub>NDM</sub>) by reducing the bacterial loads by 5.1 log<sub>10</sub>~8.9 log<sub>10</sub>. <b>Conclusions:</b> The title compound <b>5</b> exhibited inhibitory activity against NDM-1 as well as the efflux pump of <i>P. aeruginosa</i>, and the combined inhibitory activity resulted in synergistical potentiation of ATM. It should be noted that most CPPA isolates tested were sensitized to 8 mg/L of ATM upon combination with 4~8 mg/L of <b>5</b>.
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spelling doaj-art-e495719ca49346848ca92af1177105212025-08-20T02:53:41ZengMDPI AGAntibiotics2079-63822024-12-011312120210.3390/antibiotics131212027-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux PumpSeongyeon Lee0Taegum Lee1Mi Kyoung Kim2Joong Hoon Ahn3Seri Jeong4Ki-Ho Park5Youhoon Chong6Department of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University, Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of KoreaDepartment of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University, Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of KoreaDepartment of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University, Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of KoreaDepartment of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University, Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of KoreaDepartment of Laboratory Medicine, Hallym University College of Medicine, Chuncheon 24252, Republic of KoreaDepartment of Infectious Disease, Kyung Hee University School of Medicine, Seoul 02447, Republic of KoreaDepartment of Bioscience and Biotechnology, Bio/Molecular Informatics Center, Konkuk University, Hwayang-dong, Gwangjin-gu, Seoul 143-701, Republic of Korea<b>Background/Objectives:</b> Previously, we reported that 3-<i>O</i>-alkyl difluoroquercetins (di-F-Q) potentiates the antimicrobial activity of aztreonam (ATM) against metallo-β-lactamase (MBL)-producing <i>P. aeruginosa</i> through simultaneous inhibition of MBLs and efflux pumps. However, the ATM-potentiating activity of the 3-<i>O</i>-alkyl di-F-Q was observed only at high and potentially toxic concentrations (32 mg/L). <b>Methods:</b> As both MBLs and efflux pumps reside in the periplasm of Gram-negative bacteria, their inhibitors should accumulate in the periplasmic space. However, the outer membrane porins, the major entry pathway in Gram-negative bacteria, allow the passive diffusion of hydrophilic polar molecules across the outer membrane. Thus, we reasoned that the introduction of a polar substituent at 7-OH position of 3-<i>O</i>-alkyl di-F-Q would enhance its periplasmic concentration to result in potentiation of ATM at lower concentrations. <b>Results:</b> The title compound <b>5</b> exhibited inhibitory activity against NDM-1 as well as the efflux pump of <i>P. aeruginosa</i>, which resulted in synergistical potentiation of ATM. A combination of ATM (8 mg/L) and <b>5</b> (8 mg/L) inhibited 80% of the ATM-resistant CPPA, while ATM alone did not show any inhibition. In addition, only 4 mg/L of <b>5</b> was needed to reduce the MIC<sub>90</sub> of ATM four-fold in ATM-resistant CPPA (n = 15). The time–kill data further supported the effectiveness of the combined treatment of ATM with <b>5</b>, and the combination of ATM (1xMIC) with 8 mg/L of <b>5</b> showed bactericidal effects in every bacterial strain tested (PA-002, <i>bla</i><sub>IMP</sub>, PA-003, <i>bla</i><sub>VIM</sub>, PA-014, <i>bla</i><sub>GES</sub>, and PA-017, <i>bla</i><sub>NDM</sub>) by reducing the bacterial loads by 5.1 log<sub>10</sub>~8.9 log<sub>10</sub>. <b>Conclusions:</b> The title compound <b>5</b> exhibited inhibitory activity against NDM-1 as well as the efflux pump of <i>P. aeruginosa</i>, and the combined inhibitory activity resulted in synergistical potentiation of ATM. It should be noted that most CPPA isolates tested were sensitized to 8 mg/L of ATM upon combination with 4~8 mg/L of <b>5</b>.https://www.mdpi.com/2079-6382/13/12/1202<i>Pseudomonas aeruginosa</i>metallo-β-lactamaseefflux pumpsimultaneous inhibitionaztreonampotentiation
spellingShingle Seongyeon Lee
Taegum Lee
Mi Kyoung Kim
Joong Hoon Ahn
Seri Jeong
Ki-Ho Park
Youhoon Chong
7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump
Antibiotics
<i>Pseudomonas aeruginosa</i>
metallo-β-lactamase
efflux pump
simultaneous inhibition
aztreonam
potentiation
title 7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump
title_full 7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump
title_fullStr 7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump
title_full_unstemmed 7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump
title_short 7-<i>O</i>-Carboxylic Acid-Substituted 3-<i>O</i>-Alkyl Difluoroquercetin; An Aztreonam-Potentiating Agent Against Carbapenemase-Producing <i>Pseudomonas aeruginosa</i> Through Simultaneous Inhibition of Metallo-β-Lactamase and Efflux Pump
title_sort 7 i o i carboxylic acid substituted 3 i o i alkyl difluoroquercetin an aztreonam potentiating agent against carbapenemase producing i pseudomonas aeruginosa i through simultaneous inhibition of metallo β lactamase and efflux pump
topic <i>Pseudomonas aeruginosa</i>
metallo-β-lactamase
efflux pump
simultaneous inhibition
aztreonam
potentiation
url https://www.mdpi.com/2079-6382/13/12/1202
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AT taegumlee 7ioicarboxylicacidsubstituted3ioialkyldifluoroquercetinanaztreonampotentiatingagentagainstcarbapenemaseproducingipseudomonasaeruginosaithroughsimultaneousinhibitionofmetalloblactamaseandeffluxpump
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