The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo

Abstract Homocysteine (Hcy), a sulfur-containing amino acid derived from methionine, has been shown to be a significant and modifiable risk factor for various neurological disorders, including stroke, Parkinson’s disease, Alzheimer’s disease, and elderly depression. However, there is currently a lac...

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Main Authors: Meng Wang, Xiaoshan Liang, Keqing Jin, Yinyue Liu, Suhui Luo, Qiang Zhang, Xuan Wang, Zhiping Dong, Xumei zhang
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-98306-3
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author Meng Wang
Xiaoshan Liang
Keqing Jin
Yinyue Liu
Suhui Luo
Qiang Zhang
Xuan Wang
Zhiping Dong
Xumei zhang
author_facet Meng Wang
Xiaoshan Liang
Keqing Jin
Yinyue Liu
Suhui Luo
Qiang Zhang
Xuan Wang
Zhiping Dong
Xumei zhang
author_sort Meng Wang
collection DOAJ
description Abstract Homocysteine (Hcy), a sulfur-containing amino acid derived from methionine, has been shown to be a significant and modifiable risk factor for various neurological disorders, including stroke, Parkinson’s disease, Alzheimer’s disease, and elderly depression. However, there is currently a lack of comprehensive understanding regarding the molecular mechanisms underlying Hcy-induced neurotoxicity. Therefore, this study aimed to establish rat and cell models of Hcy intervention in order to elucidate the underlying mechanism of neurotoxicity. Our research findings demonstrate that Hcy induces depressive - like symptoms in normal Sprague-Dawley rats. Pathological damage and apoptosis were detected in the DG, CA3, and CA1 regions of the hippocampus, along with the cortical area. Moreover, synaptic structural impairment was observed within the hippocampal. Simultaneously, Hcy promotes neuronal apoptosis and LDH leakage in mouse neuroblastoma (N2a) cells. Furthermore, we conducted mRNA microarray analysis to investigate differences in mRNA expressions and utilized Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis for gene function annotations in Hcy-treated N2a cells. The results highlighted significant alterations in 457 mRNAs in the Hcy-treated group compared to the Control group. Among the differentially expressed genes (DEGs), a total of 155 were found to be significantly up-regulated, while the remaining 302 were down-regulated. Furthermore, it was observed that four genes (snap25, cplx1, slc32a1 and atp6v1e2) related to the synaptic vesicle cycle exhibited decreased expression in Hcy-treated N2a cells compared to the Control group. The expression levels of these four genes, as well as their corresponding proteins, were subsequently confirmed using RT-qPCR and western blot analysis, respectively. In conclusion, this study shed light on the detrimental impact of hyperhomocysteinemia on the nervous system, particularly with regard to the synaptic vesicle cycle.
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spelling doaj-art-5b5cf62c5aed4bccb531848e69422c862025-08-20T01:59:57ZengNature PortfolioScientific Reports2045-23222025-05-0115111410.1038/s41598-025-98306-3The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivoMeng Wang0Xiaoshan Liang1Keqing Jin2Yinyue Liu3Suhui Luo4Qiang Zhang5Xuan Wang6Zhiping Dong7Xumei zhang8Department of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityTianjin Key Laboratory of Environment, Nutrition and Public Health, Center for International Collaborative Research on Environment, Nutrition and Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityDepartment of Nutrition and Food Science, School of Public Health, Tianjin Medical UniversityAbstract Homocysteine (Hcy), a sulfur-containing amino acid derived from methionine, has been shown to be a significant and modifiable risk factor for various neurological disorders, including stroke, Parkinson’s disease, Alzheimer’s disease, and elderly depression. However, there is currently a lack of comprehensive understanding regarding the molecular mechanisms underlying Hcy-induced neurotoxicity. Therefore, this study aimed to establish rat and cell models of Hcy intervention in order to elucidate the underlying mechanism of neurotoxicity. Our research findings demonstrate that Hcy induces depressive - like symptoms in normal Sprague-Dawley rats. Pathological damage and apoptosis were detected in the DG, CA3, and CA1 regions of the hippocampus, along with the cortical area. Moreover, synaptic structural impairment was observed within the hippocampal. Simultaneously, Hcy promotes neuronal apoptosis and LDH leakage in mouse neuroblastoma (N2a) cells. Furthermore, we conducted mRNA microarray analysis to investigate differences in mRNA expressions and utilized Gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis for gene function annotations in Hcy-treated N2a cells. The results highlighted significant alterations in 457 mRNAs in the Hcy-treated group compared to the Control group. Among the differentially expressed genes (DEGs), a total of 155 were found to be significantly up-regulated, while the remaining 302 were down-regulated. Furthermore, it was observed that four genes (snap25, cplx1, slc32a1 and atp6v1e2) related to the synaptic vesicle cycle exhibited decreased expression in Hcy-treated N2a cells compared to the Control group. The expression levels of these four genes, as well as their corresponding proteins, were subsequently confirmed using RT-qPCR and western blot analysis, respectively. In conclusion, this study shed light on the detrimental impact of hyperhomocysteinemia on the nervous system, particularly with regard to the synaptic vesicle cycle.https://doi.org/10.1038/s41598-025-98306-3HomocysteineN2a cellsMicroarray analysisSynaptic vesicle cycleNeurotoxicity
spellingShingle Meng Wang
Xiaoshan Liang
Keqing Jin
Yinyue Liu
Suhui Luo
Qiang Zhang
Xuan Wang
Zhiping Dong
Xumei zhang
The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
Scientific Reports
Homocysteine
N2a cells
Microarray analysis
Synaptic vesicle cycle
Neurotoxicity
title The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
title_full The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
title_fullStr The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
title_full_unstemmed The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
title_short The involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
title_sort involvement of the synaptic vesicle cycle in homocysteine induced neurotoxicity in vitro and in vivo
topic Homocysteine
N2a cells
Microarray analysis
Synaptic vesicle cycle
Neurotoxicity
url https://doi.org/10.1038/s41598-025-98306-3
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