TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions

Abstract Despite the high incidence of dry mouth in postmenopausal women, its underlying mechanisms and therapeutic interventions remain underexplored. Using ovariectomized (OVX) mouse models, here this study identifies ferroptosis, an iron‐dependent regulated cell death, as a central mechanism driv...

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Main Authors: Su‐Jeong Oh, Ye Young Shin, Ji‐Su Ahn, Hee‐Jeong Park, Min‐Jung Kang, Tae‐Hoon Shin, Byung‐Chul Lee, Won Kyu Kim, Jung‐Min Oh, Dongjun Lee, Yun Hak Kim, Ji Min Kim, Eui‐Suk Sung, Eun‐Woo Lee, Jee‐Heon Jeong, Byung‐Joo Lee, Yoojin Seo, Hyung‐Sik Kim
Format: Article
Language:English
Published: Wiley 2024-12-01
Series:Advanced Science
Subjects:
Online Access:https://doi.org/10.1002/advs.202400660
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author Su‐Jeong Oh
Ye Young Shin
Ji‐Su Ahn
Hee‐Jeong Park
Min‐Jung Kang
Tae‐Hoon Shin
Byung‐Chul Lee
Won Kyu Kim
Jung‐Min Oh
Dongjun Lee
Yun Hak Kim
Ji Min Kim
Eui‐Suk Sung
Eun‐Woo Lee
Jee‐Heon Jeong
Byung‐Joo Lee
Yoojin Seo
Hyung‐Sik Kim
author_facet Su‐Jeong Oh
Ye Young Shin
Ji‐Su Ahn
Hee‐Jeong Park
Min‐Jung Kang
Tae‐Hoon Shin
Byung‐Chul Lee
Won Kyu Kim
Jung‐Min Oh
Dongjun Lee
Yun Hak Kim
Ji Min Kim
Eui‐Suk Sung
Eun‐Woo Lee
Jee‐Heon Jeong
Byung‐Joo Lee
Yoojin Seo
Hyung‐Sik Kim
author_sort Su‐Jeong Oh
collection DOAJ
description Abstract Despite the high incidence of dry mouth in postmenopausal women, its underlying mechanisms and therapeutic interventions remain underexplored. Using ovariectomized (OVX) mouse models, here this study identifies ferroptosis, an iron‐dependent regulated cell death, as a central mechanism driving postmenopausal salivary gland (SG) dysfunction. In the OVX‐SGs, TGFβ signaling pathway is enhanced with the aberrant TGFβ2 expression in SG mesenchymal cells. Intriguingly, TGFβ2 treatment reduces iron‐storing ferritin levels, leading to lipid peroxidation and ferroptotic death in SG epithelial organoids (SGOs). Mechanistically, TGFβ2 promotes the autophagy‐mediated ferritin degradation, so‐called ferritinophagy. A notable overexpression of the type III TGFβ receptor (TβRIII) is found in the OVX‐SGs and TGFβ2‐treated SGOs, while the silencing of TβRIII mitigates the ferroptosis‐mediated deleterious effects of TGFβ2 on SGOs. Finally, administration of ferroptosis inhibitor, Liproxstatin‐1 (Lip‐1), improves saliva secretion in OVX mice. Present findings collectively suggest a link between TGFβ signaling, ferroptosis, and SG injury, offering new therapeutic avenues for postmenopausal xerostomia.
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spelling doaj-art-7ba0b6f787f741d1820472fa17c7037c2025-08-20T01:58:42ZengWileyAdvanced Science2198-38442024-12-011147n/an/a10.1002/advs.202400660TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal ConditionsSu‐Jeong Oh0Ye Young Shin1Ji‐Su Ahn2Hee‐Jeong Park3Min‐Jung Kang4Tae‐Hoon Shin5Byung‐Chul Lee6Won Kyu Kim7Jung‐Min Oh8Dongjun Lee9Yun Hak Kim10Ji Min Kim11Eui‐Suk Sung12Eun‐Woo Lee13Jee‐Heon Jeong14Byung‐Joo Lee15Yoojin Seo16Hyung‐Sik Kim17Department of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Laboratory Animal Medicine College of Veterinary Medicine and Veterinary Medical Research Institute Jeju National University Jeju‐si 63243 Republic of KoreaDepartment of Biological Sciences Sookmyung Women's University Seoul 04310 Republic of KoreaNatural Product Research Center Korea Institute of Science andTechnology (KIST) Gangneung 25451 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Convergence Medicine Pusan National University School of Medicine Yangsan 50612 Republic of KoreaDepartment of Anatomy Pusan National University School of Medicine Yangsan 50612 Republic of KoreaDepartment of Otorhinolaryngology‐Head and Neck Surgery Pusan National University School of Medicine and Biomedical Research Institute Pusan National University Hospital Busan 49241 Republic of KoreaDepartment of Otorhinolaryngology‐Head and Neck Surgery Biomedical Research Institute Pusan National University School of Medicine Yangsan Pusan National University Hospital Yangsan 50612 Republic of KoreaMetabolic Regulation Research Center Korea Research Institute of Bioscience and Biotechnology (KRIBB) Daejeon 34141 Republic of KoreaDepartment of Precision Medicine School of Medicine Sungkyunkwan University Suwon 16419 Republic of KoreaDepartment of Otorhinolaryngology‐Head and Neck Surgery Pusan National University School of Medicine and Biomedical Research Institute Pusan National University Hospital Busan 49241 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaDepartment of Oral Biochemistry, Dental and Life Science Institute, School of Dentistry Pusan National University Yangsan 50612 Republic of KoreaAbstract Despite the high incidence of dry mouth in postmenopausal women, its underlying mechanisms and therapeutic interventions remain underexplored. Using ovariectomized (OVX) mouse models, here this study identifies ferroptosis, an iron‐dependent regulated cell death, as a central mechanism driving postmenopausal salivary gland (SG) dysfunction. In the OVX‐SGs, TGFβ signaling pathway is enhanced with the aberrant TGFβ2 expression in SG mesenchymal cells. Intriguingly, TGFβ2 treatment reduces iron‐storing ferritin levels, leading to lipid peroxidation and ferroptotic death in SG epithelial organoids (SGOs). Mechanistically, TGFβ2 promotes the autophagy‐mediated ferritin degradation, so‐called ferritinophagy. A notable overexpression of the type III TGFβ receptor (TβRIII) is found in the OVX‐SGs and TGFβ2‐treated SGOs, while the silencing of TβRIII mitigates the ferroptosis‐mediated deleterious effects of TGFβ2 on SGOs. Finally, administration of ferroptosis inhibitor, Liproxstatin‐1 (Lip‐1), improves saliva secretion in OVX mice. Present findings collectively suggest a link between TGFβ signaling, ferroptosis, and SG injury, offering new therapeutic avenues for postmenopausal xerostomia.https://doi.org/10.1002/advs.202400660estrogenferroptosisorganoidssalivary glandTGFβ2xerostomia
spellingShingle Su‐Jeong Oh
Ye Young Shin
Ji‐Su Ahn
Hee‐Jeong Park
Min‐Jung Kang
Tae‐Hoon Shin
Byung‐Chul Lee
Won Kyu Kim
Jung‐Min Oh
Dongjun Lee
Yun Hak Kim
Ji Min Kim
Eui‐Suk Sung
Eun‐Woo Lee
Jee‐Heon Jeong
Byung‐Joo Lee
Yoojin Seo
Hyung‐Sik Kim
TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions
Advanced Science
estrogen
ferroptosis
organoids
salivary gland
TGFβ2
xerostomia
title TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions
title_full TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions
title_fullStr TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions
title_full_unstemmed TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions
title_short TGFβ2‐Driven Ferritin Degradation and Subsequent Ferroptosis Underlie Salivary Gland Dysfunction in Postmenopausal Conditions
title_sort tgfβ2 driven ferritin degradation and subsequent ferroptosis underlie salivary gland dysfunction in postmenopausal conditions
topic estrogen
ferroptosis
organoids
salivary gland
TGFβ2
xerostomia
url https://doi.org/10.1002/advs.202400660
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