Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context

Summary: Background: The global emergence and spread of carbapenem-resistant Enterobacteriaceae in clinical settings have driven the search for inhibitors that can counteract carbapenemases. These enzymes include several serine β-lactamases (SBLs, such as KPC) and metallo-β-lactamases (MBLs, such a...

Full description

Saved in:
Bibliographic Details
Main Authors: Yan Zhang, Siyuan Yang, Zhaoju Deng, Huangwei Song, Ning Xie, Yunrui Tian, Shangshang Qin, Jifeng Liu, Yong Guo, Dongli Wang, Junfeng Liu, Congming Wu, Jianzhong Shen, Shizhen Ma, Yang Wang, Dejun Liu
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:EBioMedicine
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2352396425001987
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849322013540220928
author Yan Zhang
Siyuan Yang
Zhaoju Deng
Huangwei Song
Ning Xie
Yunrui Tian
Shangshang Qin
Jifeng Liu
Yong Guo
Dongli Wang
Junfeng Liu
Congming Wu
Jianzhong Shen
Shizhen Ma
Yang Wang
Dejun Liu
author_facet Yan Zhang
Siyuan Yang
Zhaoju Deng
Huangwei Song
Ning Xie
Yunrui Tian
Shangshang Qin
Jifeng Liu
Yong Guo
Dongli Wang
Junfeng Liu
Congming Wu
Jianzhong Shen
Shizhen Ma
Yang Wang
Dejun Liu
author_sort Yan Zhang
collection DOAJ
description Summary: Background: The global emergence and spread of carbapenem-resistant Enterobacteriaceae in clinical settings have driven the search for inhibitors that can counteract carbapenemases. These enzymes include several serine β-lactamases (SBLs, such as KPC) and metallo-β-lactamases (MBLs, such as NDM) that hydrolyse almost all β-lactams including carbapenems. This endeavour has successful developed some SBL inhibitors, including the boron-containing compound vaborbactam. However, the challenge posed by MBLs remains unresolved. Methods: A high-throughput screening was conducted on 1718 FDA-approved drugs as potential adjuvants to meropenem. The synergistic effect was determined by checkerboard assay. The underlying mechanisms were elucidated using enzyme inhibition assays, molecular docking and dynamics simulations. The safety and efficacy were evaluated using a murine model. Findings: We have identified another boron-containing broad-spectrum serine and metallo-β-lactamase inhibitor, the benzoxaborole antifungal agent tavaborole. In vitro, tavaborole enhances the antibacterial activity of multiple β-lactam antibiotics against bacteria producing either SBLs or MBLs. In vivo, injectable administration of tavaborole has demonstrated good safety in mice and has restored the efficacy of meropenem against blaNDM-5 and blaKPC-2-positive bacterial infection in a mouse intraperitoneal model. Tavaborole may effectively inhibit the activity of SBLs and MBLs by covalently bonding with the active serine residue of SBLs and chelating the Zn2+ at the active center of MBLs. Interpretation: Tavaborole shows good potential as an agent for use in combination with β-lactam antibiotics for treating multidrug-resistant Gram-negative bacterial infections. Funding: National Key Research and Development Program of China, National Natural Science Foundation of China, Pinduoduo-China Agricultural University Research Fund.
format Article
id doaj-art-321b8b2f40e34b3ba6ab61b090d279f7
institution Kabale University
issn 2352-3964
language English
publishDate 2025-06-01
publisher Elsevier
record_format Article
series EBioMedicine
spelling doaj-art-321b8b2f40e34b3ba6ab61b090d279f72025-08-20T03:49:33ZengElsevierEBioMedicine2352-39642025-06-0111610575410.1016/j.ebiom.2025.105754Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in contextYan Zhang0Siyuan Yang1Zhaoju Deng2Huangwei Song3Ning Xie4Yunrui Tian5Shangshang Qin6Jifeng Liu7Yong Guo8Dongli Wang9Junfeng Liu10Congming Wu11Jianzhong Shen12Shizhen Ma13Yang Wang14Dejun Liu15National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China; School of Pharmaceutical Science and Technology, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China; Ministry of Agriculture Key Laboratory for Crop Pest Monitoring and Green Control, College of Plant Protection, China Agricultural University, Beijing, ChinaSchool of Pharmaceutical Sciences, Key Laboratory of Advanced Drug Preparation Technologies, Ministry of Education, Zhengzhou University, Zhengzhou, ChinaSchool of Pharmaceutical Sciences, Key Laboratory of Advanced Drug Preparation Technologies, Ministry of Education, Zhengzhou University, Zhengzhou, ChinaHunan Province Cooperative Innovation Center for Molecular Target New Drug Study, School of Pharmaceutical Science, Hengyang Medical School, University of South China, Hengyang, ChinaMinistry of Agriculture Key Laboratory for Crop Pest Monitoring and Green Control, College of Plant Protection, China Agricultural University, Beijing, ChinaMinistry of Agriculture Key Laboratory for Crop Pest Monitoring and Green Control, College of Plant Protection, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, ChinaNational Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China; Corresponding author.National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China; Corresponding author.National Key Laboratory of Veterinary Public Health and Safety, College of Veterinary Medicine, China Agricultural University, Beijing, China; Corresponding author.Summary: Background: The global emergence and spread of carbapenem-resistant Enterobacteriaceae in clinical settings have driven the search for inhibitors that can counteract carbapenemases. These enzymes include several serine β-lactamases (SBLs, such as KPC) and metallo-β-lactamases (MBLs, such as NDM) that hydrolyse almost all β-lactams including carbapenems. This endeavour has successful developed some SBL inhibitors, including the boron-containing compound vaborbactam. However, the challenge posed by MBLs remains unresolved. Methods: A high-throughput screening was conducted on 1718 FDA-approved drugs as potential adjuvants to meropenem. The synergistic effect was determined by checkerboard assay. The underlying mechanisms were elucidated using enzyme inhibition assays, molecular docking and dynamics simulations. The safety and efficacy were evaluated using a murine model. Findings: We have identified another boron-containing broad-spectrum serine and metallo-β-lactamase inhibitor, the benzoxaborole antifungal agent tavaborole. In vitro, tavaborole enhances the antibacterial activity of multiple β-lactam antibiotics against bacteria producing either SBLs or MBLs. In vivo, injectable administration of tavaborole has demonstrated good safety in mice and has restored the efficacy of meropenem against blaNDM-5 and blaKPC-2-positive bacterial infection in a mouse intraperitoneal model. Tavaborole may effectively inhibit the activity of SBLs and MBLs by covalently bonding with the active serine residue of SBLs and chelating the Zn2+ at the active center of MBLs. Interpretation: Tavaborole shows good potential as an agent for use in combination with β-lactam antibiotics for treating multidrug-resistant Gram-negative bacterial infections. Funding: National Key Research and Development Program of China, National Natural Science Foundation of China, Pinduoduo-China Agricultural University Research Fund.http://www.sciencedirect.com/science/article/pii/S2352396425001987β-lactamase inhibitorsSerine β-lactamasesMetallo-β-lactamasesTavaborole
spellingShingle Yan Zhang
Siyuan Yang
Zhaoju Deng
Huangwei Song
Ning Xie
Yunrui Tian
Shangshang Qin
Jifeng Liu
Yong Guo
Dongli Wang
Junfeng Liu
Congming Wu
Jianzhong Shen
Shizhen Ma
Yang Wang
Dejun Liu
Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context
EBioMedicine
β-lactamase inhibitors
Serine β-lactamases
Metallo-β-lactamases
Tavaborole
title Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context
title_full Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context
title_fullStr Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context
title_full_unstemmed Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context
title_short Antifungal agent tavaborole as a potential broad-spectrum serine and metallo-β-lactamases inhibitorResearch in context
title_sort antifungal agent tavaborole as a potential broad spectrum serine and metallo β lactamases inhibitorresearch in context
topic β-lactamase inhibitors
Serine β-lactamases
Metallo-β-lactamases
Tavaborole
url http://www.sciencedirect.com/science/article/pii/S2352396425001987
work_keys_str_mv AT yanzhang antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT siyuanyang antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT zhaojudeng antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT huangweisong antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT ningxie antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT yunruitian antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT shangshangqin antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT jifengliu antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT yongguo antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT dongliwang antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT junfengliu antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT congmingwu antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT jianzhongshen antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT shizhenma antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT yangwang antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext
AT dejunliu antifungalagenttavaboroleasapotentialbroadspectrumserineandmetalloblactamasesinhibitorresearchincontext