Loss of ferroportin induces memory impairment by promoting ferroptosis in Alzheimer’s disease
Iron homeostasis disturbance has been implicated in Alzheimer’s disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD rema...
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| Published in | Cell death and differentiation Vol. 28; no. 5; pp. 1548 - 1562 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.05.2021
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Iron homeostasis disturbance has been implicated in Alzheimer’s disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD remains elusive. Here, we report that ferroportin1 (Fpn), the only identified mammalian nonheme iron exporter, was downregulated in the brains of APPswe/PS1dE9 mice as an Alzheimer’s mouse model and Alzheimer’s patients. Genetic deletion of Fpn in principal neurons of the neocortex and hippocampus by breeding Fpn
fl/fl
mice with NEX-Cre mice led to AD-like hippocampal atrophy and memory deficits. Interestingly, the canonical morphological and molecular characteristics of ferroptosis were observed in both Fpn
fl/fl/NEXcre
and AD mice. Gene set enrichment analysis (GSEA) of ferroptosis-related RNA-seq data showed that the differentially expressed genes were highly enriched in gene sets associated with AD. Furthermore, administration of specific inhibitors of ferroptosis effectively reduced the neuronal death and memory impairments induced by Aβ aggregation in vitro and in vivo. In addition, restoring Fpn ameliorated ferroptosis and memory impairment in APPswe/PS1dE9 mice. Our study demonstrates the critical role of Fpn and ferroptosis in the progression of AD, thus provides promising therapeutic approaches for this disease. |
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| AbstractList | Iron homeostasis disturbance has been implicated in Alzheimer's disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD remains elusive. Here, we report that ferroportin1 (Fpn), the only identified mammalian nonheme iron exporter, was downregulated in the brains of APPswe/PS1dE9 mice as an Alzheimer's mouse model and Alzheimer's patients. Genetic deletion of Fpn in principal neurons of the neocortex and hippocampus by breeding Fpnfl/fl mice with NEX-Cre mice led to AD-like hippocampal atrophy and memory deficits. Interestingly, the canonical morphological and molecular characteristics of ferroptosis were observed in both Fpnfl/fl/NEXcre and AD mice. Gene set enrichment analysis (GSEA) of ferroptosis-related RNA-seq data showed that the differentially expressed genes were highly enriched in gene sets associated with AD. Furthermore, administration of specific inhibitors of ferroptosis effectively reduced the neuronal death and memory impairments induced by Aβ aggregation in vitro and in vivo. In addition, restoring Fpn ameliorated ferroptosis and memory impairment in APPswe/PS1dE9 mice. Our study demonstrates the critical role of Fpn and ferroptosis in the progression of AD, thus provides promising therapeutic approaches for this disease.Iron homeostasis disturbance has been implicated in Alzheimer's disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD remains elusive. Here, we report that ferroportin1 (Fpn), the only identified mammalian nonheme iron exporter, was downregulated in the brains of APPswe/PS1dE9 mice as an Alzheimer's mouse model and Alzheimer's patients. Genetic deletion of Fpn in principal neurons of the neocortex and hippocampus by breeding Fpnfl/fl mice with NEX-Cre mice led to AD-like hippocampal atrophy and memory deficits. Interestingly, the canonical morphological and molecular characteristics of ferroptosis were observed in both Fpnfl/fl/NEXcre and AD mice. Gene set enrichment analysis (GSEA) of ferroptosis-related RNA-seq data showed that the differentially expressed genes were highly enriched in gene sets associated with AD. Furthermore, administration of specific inhibitors of ferroptosis effectively reduced the neuronal death and memory impairments induced by Aβ aggregation in vitro and in vivo. In addition, restoring Fpn ameliorated ferroptosis and memory impairment in APPswe/PS1dE9 mice. Our study demonstrates the critical role of Fpn and ferroptosis in the progression of AD, thus provides promising therapeutic approaches for this disease. Iron homeostasis disturbance has been implicated in Alzheimer’s disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD remains elusive. Here, we report that ferroportin1 (Fpn), the only identified mammalian nonheme iron exporter, was downregulated in the brains of APPswe/PS1dE9 mice as an Alzheimer’s mouse model and Alzheimer’s patients. Genetic deletion of Fpn in principal neurons of the neocortex and hippocampus by breeding Fpnfl/fl mice with NEX-Cre mice led to AD-like hippocampal atrophy and memory deficits. Interestingly, the canonical morphological and molecular characteristics of ferroptosis were observed in both Fpnfl/fl/NEXcre and AD mice. Gene set enrichment analysis (GSEA) of ferroptosis-related RNA-seq data showed that the differentially expressed genes were highly enriched in gene sets associated with AD. Furthermore, administration of specific inhibitors of ferroptosis effectively reduced the neuronal death and memory impairments induced by Aβ aggregation in vitro and in vivo. In addition, restoring Fpn ameliorated ferroptosis and memory impairment in APPswe/PS1dE9 mice. Our study demonstrates the critical role of Fpn and ferroptosis in the progression of AD, thus provides promising therapeutic approaches for this disease. Iron homeostasis disturbance has been implicated in Alzheimer’s disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD remains elusive. Here, we report that ferroportin1 (Fpn), the only identified mammalian nonheme iron exporter, was downregulated in the brains of APPswe/PS1dE9 mice as an Alzheimer’s mouse model and Alzheimer’s patients. Genetic deletion of Fpn in principal neurons of the neocortex and hippocampus by breeding Fpn fl/fl mice with NEX-Cre mice led to AD-like hippocampal atrophy and memory deficits. Interestingly, the canonical morphological and molecular characteristics of ferroptosis were observed in both Fpn fl/fl/NEXcre and AD mice. Gene set enrichment analysis (GSEA) of ferroptosis-related RNA-seq data showed that the differentially expressed genes were highly enriched in gene sets associated with AD. Furthermore, administration of specific inhibitors of ferroptosis effectively reduced the neuronal death and memory impairments induced by Aβ aggregation in vitro and in vivo. In addition, restoring Fpn ameliorated ferroptosis and memory impairment in APPswe/PS1dE9 mice. Our study demonstrates the critical role of Fpn and ferroptosis in the progression of AD, thus provides promising therapeutic approaches for this disease. Iron homeostasis disturbance has been implicated in Alzheimer's disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis is a nonapoptotic form of cell death dependent upon intracellular iron. However, the involvement of ferroptosis in the pathogenesis of AD remains elusive. Here, we report that ferroportin1 (Fpn), the only identified mammalian nonheme iron exporter, was downregulated in the brains of APPswe/PS1dE9 mice as an Alzheimer's mouse model and Alzheimer's patients. Genetic deletion of Fpn in principal neurons of the neocortex and hippocampus by breeding Fpn mice with NEX-Cre mice led to AD-like hippocampal atrophy and memory deficits. Interestingly, the canonical morphological and molecular characteristics of ferroptosis were observed in both Fpn and AD mice. Gene set enrichment analysis (GSEA) of ferroptosis-related RNA-seq data showed that the differentially expressed genes were highly enriched in gene sets associated with AD. Furthermore, administration of specific inhibitors of ferroptosis effectively reduced the neuronal death and memory impairments induced by Aβ aggregation in vitro and in vivo. In addition, restoring Fpn ameliorated ferroptosis and memory impairment in APPswe/PS1dE9 mice. Our study demonstrates the critical role of Fpn and ferroptosis in the progression of AD, thus provides promising therapeutic approaches for this disease. |
| Author | Lu, Youming Xie, Dong Xiong, Wan Bao, Wen-Dai Wang, Fudi Zhang, Hong-Hong Hu, Ya-Zhuo Wang, Jing Nelson, Peter T. Liu, Dan Zhou, Xiao-Ting Man, Heng-Ye Hu, Fan Zhu, Ling-Qiang Pang, Pei Chen, Kai Wang, Wang-Xia Han, Zhi-Tao Chen, Jian-Guo |
| Author_xml | – sequence: 1 givenname: Wen-Dai surname: Bao fullname: Bao, Wen-Dai organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 2 givenname: Pei surname: Pang fullname: Pang, Pei organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 3 givenname: Xiao-Ting surname: Zhou fullname: Zhou, Xiao-Ting organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 4 givenname: Fan surname: Hu fullname: Hu, Fan organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 5 givenname: Wan surname: Xiong fullname: Xiong, Wan organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 6 givenname: Kai surname: Chen fullname: Chen, Kai organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 7 givenname: Jing surname: Wang fullname: Wang, Jing organization: Department of Radiology, Union Hospital, Tongji Medical College, Huazhong University of Science and Technology – sequence: 8 givenname: Fudi orcidid: 0000-0001-8730-0003 surname: Wang fullname: Wang, Fudi organization: Department of Nutrition, School of Public Health, Zhejiang University – sequence: 9 givenname: Dong surname: Xie fullname: Xie, Dong organization: Institute of Nutritional Science, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences – sequence: 10 givenname: Ya-Zhuo surname: Hu fullname: Hu, Ya-Zhuo organization: Beijing Key Laboratory of Aging and Geriatrics, National Clinical Research Center for Geriatric Disease, Institute of Geriatrics, Chinese PLA General Hospital and Chinese PLA Medical Academy – sequence: 11 givenname: Zhi-Tao surname: Han fullname: Han, Zhi-Tao organization: Beijing Key Laboratory of Aging and Geriatrics, National Clinical Research Center for Geriatric Disease, Institute of Geriatrics, Chinese PLA General Hospital and Chinese PLA Medical Academy – sequence: 12 givenname: Hong-Hong surname: Zhang fullname: Zhang, Hong-Hong organization: Beijing Key Laboratory of Aging and Geriatrics, National Clinical Research Center for Geriatric Disease, Institute of Geriatrics, Chinese PLA General Hospital and Chinese PLA Medical Academy – sequence: 13 givenname: Wang-Xia orcidid: 0000-0002-8104-3779 surname: Wang fullname: Wang, Wang-Xia organization: Sanders Brown Center on Aging, Pathology and Laboratory Medicine, University of Kentucky – sequence: 14 givenname: Peter T. surname: Nelson fullname: Nelson, Peter T. organization: Sanders Brown Center on Aging, Pathology and Laboratory Medicine, University of Kentucky – sequence: 15 givenname: Jian-Guo surname: Chen fullname: Chen, Jian-Guo organization: The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 16 givenname: Youming surname: Lu fullname: Lu, Youming organization: The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 17 givenname: Heng-Ye orcidid: 0000-0002-3530-3066 surname: Man fullname: Man, Heng-Ye organization: Department of Biology, Boston University – sequence: 18 givenname: Dan surname: Liu fullname: Liu, Dan email: liudan_echo@mail.hust.edu.cn organization: The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology – sequence: 19 givenname: Ling-Qiang orcidid: 0000-0001-9964-9229 surname: Zhu fullname: Zhu, Ling-Qiang email: zhulq@mail.hust.edu.cn organization: Department of Pathophysiology, Key Lab of Neurological Disorder of Education Ministry, School of Basic Medicine, Tongji Medical College, Huazhong University of Science and Technology, The Institute of Brain Research, Collaborative Innovation Center for Brain Science, Huazhong University of Science and Technology |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33398092$$D View this record in MEDLINE/PubMed |
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| Snippet | Iron homeostasis disturbance has been implicated in Alzheimer’s disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis... Iron homeostasis disturbance has been implicated in Alzheimer's disease (AD), and excess iron exacerbates oxidative damage and cognitive defects. Ferroptosis... |
| SourceID | pubmedcentral proquest pubmed crossref springer |
| SourceType | Open Access Repository Aggregation Database Index Database Enrichment Source Publisher |
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| SubjectTerms | 13/1 13/105 13/89 13/95 14/19 14/28 38/22 38/77 38/90 59/57 631/378/2611 631/443/7 64/110 64/60 82/29 82/51 Alzheimer Disease - genetics Alzheimer's disease Animals Apoptosis Atrophy Biochemistry Biomedical and Life Sciences Cell Biology Cell Cycle Analysis Cell death Cognitive ability Disease Models, Animal Ferroptosis Ferroptosis - physiology Gene set enrichment analysis Hippocampus Homeostasis Humans Iron Life Sciences Memory Memory Disorders - genetics Mice Neocortex Neurodegenerative diseases Physical characteristics Stem Cells |
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| Title | Loss of ferroportin induces memory impairment by promoting ferroptosis in Alzheimer’s disease |
| URI | https://link.springer.com/article/10.1038/s41418-020-00685-9 https://www.ncbi.nlm.nih.gov/pubmed/33398092 https://www.proquest.com/docview/2534802956 https://www.proquest.com/docview/2475403842 https://pubmed.ncbi.nlm.nih.gov/PMC8166828 |
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