Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy

Abstract Formic acid, a toxic one-carbon metabolite formed from methanol and formaldehyde in the body, can cause neuronal dysfunctions. It was recently hypothesized that metabolic formation of toxic one-carbon metabolites (particularly formic acid) under hyperglycemic conditions may contribute to th...

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Main Authors: Tian Hao Xiao, Bao Ting Zhu
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-11312-3
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author Tian Hao Xiao
Bao Ting Zhu
author_facet Tian Hao Xiao
Bao Ting Zhu
author_sort Tian Hao Xiao
collection DOAJ
description Abstract Formic acid, a toxic one-carbon metabolite formed from methanol and formaldehyde in the body, can cause neuronal dysfunctions. It was recently hypothesized that metabolic formation of toxic one-carbon metabolites (particularly formic acid) under hyperglycemic conditions may contribute to the pathogenesis of diabetic complications in humans. The present study aims to investigate the mechanism of formic acid-induced neurotoxicity using immortalized HT22 mouse hippocampal neurons as an in-vitro model. We found that treatment of cells with sodium formate (SF, a salt form of formic acid) causes a concentration-dependent loss of cell viability (based on MTT assay), whereas the cell number is reduced to a lesser degree when SF is present at lower concentrations. In addition, SF at the lower concentrations decreases cell proliferation by suppressing DNA synthesis, but at higher concentrations, SF induces cell death through apoptosis. SF can preferentially cause accumulation of mitochondrial ROS, disruption of mitochondrial structure, and suppression of mitochondrial functions (including ATP production). SF-induced mitochondrial ROS accumulation subsequently leads to the depletion of cellular glutathione, along with the buildup of cellular ROS and lipid-ROS. These changes jointly lead to increased permeability of both cytoplasmic and mitochondrial membranes, and ultimately the induction of apoptotic cell death. Analysis of the cellular transcriptomics revealed that the expression of genes for the relevant enzymes and proteins involved in mitochondrial function, energy metabolism and other cellular processes is altered in SF-treated cells. These findings highlight mitochondria as a crucial target in mediating SF-induced cytotoxicity, and also shed mechanistic lights on how formic acid accumulation may contribute to the pathogenesis of diabetic neuropathy and other diabetic complications.
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spelling doaj-art-a977cb9b368c4e87b62aeadaf4bc4ef82025-08-20T04:01:51ZengNature PortfolioScientific Reports2045-23222025-07-0115112610.1038/s41598-025-11312-3Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathyTian Hao Xiao0Bao Ting Zhu1Shenzhen Key Laboratory of Steroid Drug Discovery and Development, School of Medicine, The Chinese University of Hong KongShenzhen Key Laboratory of Steroid Drug Discovery and Development, School of Medicine, The Chinese University of Hong KongAbstract Formic acid, a toxic one-carbon metabolite formed from methanol and formaldehyde in the body, can cause neuronal dysfunctions. It was recently hypothesized that metabolic formation of toxic one-carbon metabolites (particularly formic acid) under hyperglycemic conditions may contribute to the pathogenesis of diabetic complications in humans. The present study aims to investigate the mechanism of formic acid-induced neurotoxicity using immortalized HT22 mouse hippocampal neurons as an in-vitro model. We found that treatment of cells with sodium formate (SF, a salt form of formic acid) causes a concentration-dependent loss of cell viability (based on MTT assay), whereas the cell number is reduced to a lesser degree when SF is present at lower concentrations. In addition, SF at the lower concentrations decreases cell proliferation by suppressing DNA synthesis, but at higher concentrations, SF induces cell death through apoptosis. SF can preferentially cause accumulation of mitochondrial ROS, disruption of mitochondrial structure, and suppression of mitochondrial functions (including ATP production). SF-induced mitochondrial ROS accumulation subsequently leads to the depletion of cellular glutathione, along with the buildup of cellular ROS and lipid-ROS. These changes jointly lead to increased permeability of both cytoplasmic and mitochondrial membranes, and ultimately the induction of apoptotic cell death. Analysis of the cellular transcriptomics revealed that the expression of genes for the relevant enzymes and proteins involved in mitochondrial function, energy metabolism and other cellular processes is altered in SF-treated cells. These findings highlight mitochondria as a crucial target in mediating SF-induced cytotoxicity, and also shed mechanistic lights on how formic acid accumulation may contribute to the pathogenesis of diabetic neuropathy and other diabetic complications.https://doi.org/10.1038/s41598-025-11312-3Formic acidCytotoxicityATP synthesis deficiencyMitochondrial damage
spellingShingle Tian Hao Xiao
Bao Ting Zhu
Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
Scientific Reports
Formic acid
Cytotoxicity
ATP synthesis deficiency
Mitochondrial damage
title Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
title_full Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
title_fullStr Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
title_full_unstemmed Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
title_short Sodium formate-induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
title_sort sodium formate induced mitochondrial impairment and cytotoxicity in neuronal cells reveal crucial pathogenic mechanisms underlying diabetic neuropathy and retinopathy
topic Formic acid
Cytotoxicity
ATP synthesis deficiency
Mitochondrial damage
url https://doi.org/10.1038/s41598-025-11312-3
work_keys_str_mv AT tianhaoxiao sodiumformateinducedmitochondrialimpairmentandcytotoxicityinneuronalcellsrevealcrucialpathogenicmechanismsunderlyingdiabeticneuropathyandretinopathy
AT baotingzhu sodiumformateinducedmitochondrialimpairmentandcytotoxicityinneuronalcellsrevealcrucialpathogenicmechanismsunderlyingdiabeticneuropathyandretinopathy