Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus

Abstract Disulfiram (Antabuse®) is a prescription alcohol sobriety aid that has shown repurposing potential as an antibacterial drug for infections due to Gram-positive bacteria. In this investigation, we sought to define the principal mechanisms that disulfiram operates as a growth inhibitor of Sta...

Full description

Saved in:
Bibliographic Details
Main Authors: Timothy E. Long, Surya Teja Naidu, Emily G. Hissom, Yogesh Meka, Hasitha Chavva, Kathleen C. Brown, Meagan E. Valentine, Jun Fan, James Denvir, Donald A. Primerano, Hongwei D. Yu, Monica A. Valentovic
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-00078-3
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849387865973194752
author Timothy E. Long
Surya Teja Naidu
Emily G. Hissom
Yogesh Meka
Hasitha Chavva
Kathleen C. Brown
Meagan E. Valentine
Jun Fan
James Denvir
Donald A. Primerano
Hongwei D. Yu
Monica A. Valentovic
author_facet Timothy E. Long
Surya Teja Naidu
Emily G. Hissom
Yogesh Meka
Hasitha Chavva
Kathleen C. Brown
Meagan E. Valentine
Jun Fan
James Denvir
Donald A. Primerano
Hongwei D. Yu
Monica A. Valentovic
author_sort Timothy E. Long
collection DOAJ
description Abstract Disulfiram (Antabuse®) is a prescription alcohol sobriety aid that has shown repurposing potential as an antibacterial drug for infections due to Gram-positive bacteria. In this investigation, we sought to define the principal mechanisms that disulfiram operates as a growth inhibitor of Staphylococcus aureus using differential transcriptomic, metabolomic, bioenergetic, and phenotypic growth analyses. The RNA-seq transcriptome analysis revealed that disulfiram induces oxidative stress, redox imbalance, metal acquisition, and the biosynthesis of pantothenate, coenzyme A, thiamine, menaquinone, siderophores/metallophores, and bacillithiol. The metabolomic analysis indicated that disulfiram depletes coenzyme A and attenuates the catabolism of glucose, pyruvate, and NADH. Conversely, disulfiram appeared to up-regulate arginine catabolism for ATP production and accelerate citrate consumption that was attributed to induction of siderophore biosynthesis (i.e., staphyloferrin). The bioenergetic studies further revealed that the primary metabolite of disulfiram (i.e., diethyldithiocarbamate) is likely involved in the mechanism of action as an inhibitor of oxidative phosphorylation and chelating agent of iron and other metals. In the final analysis, disulfiram inhibits the growth of S. aureus by inducing perturbations in central glucose catabolism and redox imbalance (e.g., oxidative stress). Moreover, the chelation of metal ions and antagonism of the respiratory chain by diethyldithiocarbamate are believed to contribute to the inhibition of cell replication.
format Article
id doaj-art-ade8359b7ebe43bfb667a06da8b18100
institution Kabale University
issn 2045-2322
language English
publishDate 2025-05-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-ade8359b7ebe43bfb667a06da8b181002025-08-20T03:42:27ZengNature PortfolioScientific Reports2045-23222025-05-0115111510.1038/s41598-025-00078-3Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureusTimothy E. Long0Surya Teja Naidu1Emily G. Hissom2Yogesh Meka3Hasitha Chavva4Kathleen C. Brown5Meagan E. Valentine6Jun Fan7James Denvir8Donald A. Primerano9Hongwei D. Yu10Monica A. Valentovic11Department of Pharmaceutical Sciences, School of Pharmacy, Marshall UniversityDepartment of Pharmaceutical Sciences, School of Pharmacy, Marshall UniversityDepartment of Pharmaceutical Sciences, School of Pharmacy, Marshall UniversityDepartment of Pharmaceutical Sciences, School of Pharmacy, Marshall UniversityDepartment of Pharmaceutical Sciences, School of Pharmacy, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityDepartment of Biomedical Sciences, Joan C. Edwards School of Medicine, Marshall UniversityAbstract Disulfiram (Antabuse®) is a prescription alcohol sobriety aid that has shown repurposing potential as an antibacterial drug for infections due to Gram-positive bacteria. In this investigation, we sought to define the principal mechanisms that disulfiram operates as a growth inhibitor of Staphylococcus aureus using differential transcriptomic, metabolomic, bioenergetic, and phenotypic growth analyses. The RNA-seq transcriptome analysis revealed that disulfiram induces oxidative stress, redox imbalance, metal acquisition, and the biosynthesis of pantothenate, coenzyme A, thiamine, menaquinone, siderophores/metallophores, and bacillithiol. The metabolomic analysis indicated that disulfiram depletes coenzyme A and attenuates the catabolism of glucose, pyruvate, and NADH. Conversely, disulfiram appeared to up-regulate arginine catabolism for ATP production and accelerate citrate consumption that was attributed to induction of siderophore biosynthesis (i.e., staphyloferrin). The bioenergetic studies further revealed that the primary metabolite of disulfiram (i.e., diethyldithiocarbamate) is likely involved in the mechanism of action as an inhibitor of oxidative phosphorylation and chelating agent of iron and other metals. In the final analysis, disulfiram inhibits the growth of S. aureus by inducing perturbations in central glucose catabolism and redox imbalance (e.g., oxidative stress). Moreover, the chelation of metal ions and antagonism of the respiratory chain by diethyldithiocarbamate are believed to contribute to the inhibition of cell replication.https://doi.org/10.1038/s41598-025-00078-3
spellingShingle Timothy E. Long
Surya Teja Naidu
Emily G. Hissom
Yogesh Meka
Hasitha Chavva
Kathleen C. Brown
Meagan E. Valentine
Jun Fan
James Denvir
Donald A. Primerano
Hongwei D. Yu
Monica A. Valentovic
Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus
Scientific Reports
title Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus
title_full Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus
title_fullStr Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus
title_full_unstemmed Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus
title_short Disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of Staphylococcus aureus
title_sort disulfiram induces redox imbalance and perturbations in central glucose catabolism and metal homeostasis to inhibit the growth of staphylococcus aureus
url https://doi.org/10.1038/s41598-025-00078-3
work_keys_str_mv AT timothyelong disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT suryatejanaidu disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT emilyghissom disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT yogeshmeka disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT hasithachavva disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT kathleencbrown disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT meaganevalentine disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT junfan disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT jamesdenvir disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT donaldaprimerano disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT hongweidyu disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus
AT monicaavalentovic disulfiraminducesredoximbalanceandperturbationsincentralglucosecatabolismandmetalhomeostasistoinhibitthegrowthofstaphylococcusaureus