SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions

Zinc (Zn) is a crucial trace element in vertebrates, fulfilling a range of physiological functions, whose metabolism and homeostasis are manipulated by Zn transporter proteins. SUMOylation, a reversible post-translational modification (PTM), extensively participates in various biological processes i...

Full description

Saved in:
Bibliographic Details
Main Authors: Tao Liu, Chang-Chun Song, Fu-Xuan Duan, Chong-Chao Zhong, Sheng-Zan Liu, Jia-Cheng Guo, An-Gen Yu, Zhi Luo
Format: Article
Language:English
Published: MDPI AG 2025-06-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/14/6/750
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849433014944137216
author Tao Liu
Chang-Chun Song
Fu-Xuan Duan
Chong-Chao Zhong
Sheng-Zan Liu
Jia-Cheng Guo
An-Gen Yu
Zhi Luo
author_facet Tao Liu
Chang-Chun Song
Fu-Xuan Duan
Chong-Chao Zhong
Sheng-Zan Liu
Jia-Cheng Guo
An-Gen Yu
Zhi Luo
author_sort Tao Liu
collection DOAJ
description Zinc (Zn) is a crucial trace element in vertebrates, fulfilling a range of physiological functions, whose metabolism and homeostasis are manipulated by Zn transporter proteins. SUMOylation, a reversible post-translational modification (PTM), extensively participates in various biological processes in the body, yet its underlying mechanism in regulating Zn transporters remains unexplored. Our findings indicate that high dietary Zn substantially elevated intestinal Zn content and modulated the expression profiles of Zn transporter-related genes and proteins, including ZIP8 transporter. In addition, high Zn diet tended to inhibit the SUMOylation modification and upregulate deSUMOylation modification in the intestine and intestinal epithelial cells. Furthermore, we found that the ZIP8 protein undergoes SUMOylation modification; UBC9 upregulated but SENP1 and Zn downregulated the SUMOylation level of ZIP8, and the K24 and K222 positions are the primary SUMOylation modification sites of ZIP8 protein in yellow catfish. Mechanistically, SENP1 modulates the deSUMOylation modification of ZIP8 by sensing Zn-induced oxidative stress. In summary, for the first time, we have uncovered a unique regulatory mechanism of ZIP8 mediated by SUMOylation modification in vertebrates and demonstrate that SENP1 is capable of sensing oxidative stress to reduce the SUMOylation modification of ZIP8 at K24 and K222 sites.
format Article
id doaj-art-68b7adcad53a468db5bb66d996d2d2f6
institution Kabale University
issn 2076-3921
language English
publishDate 2025-06-01
publisher MDPI AG
record_format Article
series Antioxidants
spelling doaj-art-68b7adcad53a468db5bb66d996d2d2f62025-08-20T03:27:11ZengMDPI AGAntioxidants2076-39212025-06-0114675010.3390/antiox14060750SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport FunctionsTao Liu0Chang-Chun Song1Fu-Xuan Duan2Chong-Chao Zhong3Sheng-Zan Liu4Jia-Cheng Guo5An-Gen Yu6Zhi Luo7Hubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaHubei Hongshan Laboratory, Fishery College, Huazhong Agriculture University, Wuhan 430070, ChinaZinc (Zn) is a crucial trace element in vertebrates, fulfilling a range of physiological functions, whose metabolism and homeostasis are manipulated by Zn transporter proteins. SUMOylation, a reversible post-translational modification (PTM), extensively participates in various biological processes in the body, yet its underlying mechanism in regulating Zn transporters remains unexplored. Our findings indicate that high dietary Zn substantially elevated intestinal Zn content and modulated the expression profiles of Zn transporter-related genes and proteins, including ZIP8 transporter. In addition, high Zn diet tended to inhibit the SUMOylation modification and upregulate deSUMOylation modification in the intestine and intestinal epithelial cells. Furthermore, we found that the ZIP8 protein undergoes SUMOylation modification; UBC9 upregulated but SENP1 and Zn downregulated the SUMOylation level of ZIP8, and the K24 and K222 positions are the primary SUMOylation modification sites of ZIP8 protein in yellow catfish. Mechanistically, SENP1 modulates the deSUMOylation modification of ZIP8 by sensing Zn-induced oxidative stress. In summary, for the first time, we have uncovered a unique regulatory mechanism of ZIP8 mediated by SUMOylation modification in vertebrates and demonstrate that SENP1 is capable of sensing oxidative stress to reduce the SUMOylation modification of ZIP8 at K24 and K222 sites.https://www.mdpi.com/2076-3921/14/6/750ZincZinc transportersSUMOylation modificationZn homeostasisoxidative stress
spellingShingle Tao Liu
Chang-Chun Song
Fu-Xuan Duan
Chong-Chao Zhong
Sheng-Zan Liu
Jia-Cheng Guo
An-Gen Yu
Zhi Luo
SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions
Antioxidants
Zinc
Zinc transporters
SUMOylation modification
Zn homeostasis
oxidative stress
title SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions
title_full SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions
title_fullStr SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions
title_full_unstemmed SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions
title_short SENP1 Senses Oxidative Stress to Regulate the SUMOylation Modification of ZIP8 and Maintain Zinc Transport Functions
title_sort senp1 senses oxidative stress to regulate the sumoylation modification of zip8 and maintain zinc transport functions
topic Zinc
Zinc transporters
SUMOylation modification
Zn homeostasis
oxidative stress
url https://www.mdpi.com/2076-3921/14/6/750
work_keys_str_mv AT taoliu senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT changchunsong senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT fuxuanduan senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT chongchaozhong senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT shengzanliu senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT jiachengguo senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT angenyu senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions
AT zhiluo senp1sensesoxidativestresstoregulatethesumoylationmodificationofzip8andmaintainzinctransportfunctions