HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy

Abstract Iron accumulation causes cell death and disrupts tissue functions, which necessitates chelation therapy to reduce iron overload. However, clinical utilization of deferoxamine (DFO), an iron chelator, has been documented to give rise to systemic adverse effects, including ocular toxicity. Th...

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Main Authors: Yang Kong, Pei‐Kang Liu, Yao Li, Nicholas D Nolan, Peter M J Quinn, Chun‐Wei Hsu, Laura A Jenny, Jin Zhao, Xuan Cui, Ya‐Ju Chang, Katherine J Wert, Janet R Sparrow, Nan‐Kai Wang, Stephen H Tsang
Format: Article
Language:English
Published: Springer Nature 2023-01-01
Series:EMBO Molecular Medicine
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Online Access:https://doi.org/10.15252/emmm.202216525
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author Yang Kong
Pei‐Kang Liu
Yao Li
Nicholas D Nolan
Peter M J Quinn
Chun‐Wei Hsu
Laura A Jenny
Jin Zhao
Xuan Cui
Ya‐Ju Chang
Katherine J Wert
Janet R Sparrow
Nan‐Kai Wang
Stephen H Tsang
author_facet Yang Kong
Pei‐Kang Liu
Yao Li
Nicholas D Nolan
Peter M J Quinn
Chun‐Wei Hsu
Laura A Jenny
Jin Zhao
Xuan Cui
Ya‐Ju Chang
Katherine J Wert
Janet R Sparrow
Nan‐Kai Wang
Stephen H Tsang
author_sort Yang Kong
collection DOAJ
description Abstract Iron accumulation causes cell death and disrupts tissue functions, which necessitates chelation therapy to reduce iron overload. However, clinical utilization of deferoxamine (DFO), an iron chelator, has been documented to give rise to systemic adverse effects, including ocular toxicity. This study provided the pathogenic and molecular basis for DFO‐related retinopathy and identified retinal pigment epithelium (RPE) as the target tissue in DFO‐related retinopathy. Our modeling demonstrated the susceptibility of RPE to DFO compared with the neuroretina. Intriguingly, we established upregulation of hypoxia inducible factor (HIF) 2α and mitochondrial deficit as the most prominent pathogenesis underlying the RPE atrophy. Moreover, suppressing hyperactivity of HIF2α and preserving mitochondrial dysfunction by α‐ketoglutarate (AKG) protects the RPE against lesions both in vitro and in vivo. This supported our observation that AKG supplementation alleviates visual impairment in a patient undergoing DFO‐chelation therapy. Overall, our study established a significant role of iron deficiency in initiating DFO‐related RPE atrophy. Inhibiting HIF2α and rescuing mitochondrial function by AKG protect RPE cells and can potentially ameliorate patients' visual function.
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spelling doaj-art-dad16b5228fa4f2aae01a11f4bb1e21e2025-08-24T11:43:51ZengSpringer NatureEMBO Molecular Medicine1757-46761757-46842023-01-0115212010.15252/emmm.202216525HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophyYang Kong0Pei‐Kang Liu1Yao Li2Nicholas D Nolan3Peter M J Quinn4Chun‐Wei Hsu5Laura A Jenny6Jin Zhao7Xuan Cui8Ya‐Ju Chang9Katherine J Wert10Janet R Sparrow11Nan‐Kai Wang12Stephen H Tsang13Department of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartments of Ophthalmology and Molecular Biology, University of Texas Southwestern Medical CenterDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityDepartment of Ophthalmology, Vagelos College of Physicians and Surgeons, Columbia UniversityAbstract Iron accumulation causes cell death and disrupts tissue functions, which necessitates chelation therapy to reduce iron overload. However, clinical utilization of deferoxamine (DFO), an iron chelator, has been documented to give rise to systemic adverse effects, including ocular toxicity. This study provided the pathogenic and molecular basis for DFO‐related retinopathy and identified retinal pigment epithelium (RPE) as the target tissue in DFO‐related retinopathy. Our modeling demonstrated the susceptibility of RPE to DFO compared with the neuroretina. Intriguingly, we established upregulation of hypoxia inducible factor (HIF) 2α and mitochondrial deficit as the most prominent pathogenesis underlying the RPE atrophy. Moreover, suppressing hyperactivity of HIF2α and preserving mitochondrial dysfunction by α‐ketoglutarate (AKG) protects the RPE against lesions both in vitro and in vivo. This supported our observation that AKG supplementation alleviates visual impairment in a patient undergoing DFO‐chelation therapy. Overall, our study established a significant role of iron deficiency in initiating DFO‐related RPE atrophy. Inhibiting HIF2α and rescuing mitochondrial function by AKG protect RPE cells and can potentially ameliorate patients' visual function.https://doi.org/10.15252/emmm.202216525HIF2α upregulationiron deficiencymitochondrial deficitRPE atrophyα‐ketoglutarate
spellingShingle Yang Kong
Pei‐Kang Liu
Yao Li
Nicholas D Nolan
Peter M J Quinn
Chun‐Wei Hsu
Laura A Jenny
Jin Zhao
Xuan Cui
Ya‐Ju Chang
Katherine J Wert
Janet R Sparrow
Nan‐Kai Wang
Stephen H Tsang
HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
EMBO Molecular Medicine
HIF2α upregulation
iron deficiency
mitochondrial deficit
RPE atrophy
α‐ketoglutarate
title HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
title_full HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
title_fullStr HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
title_full_unstemmed HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
title_short HIF2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
title_sort hif2α activation and mitochondrial deficit due to iron chelation cause retinal atrophy
topic HIF2α upregulation
iron deficiency
mitochondrial deficit
RPE atrophy
α‐ketoglutarate
url https://doi.org/10.15252/emmm.202216525
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