Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa

In addition to its role as an iron storage protein, ferritin can function as a major detoxification component in the innate immune defense, and Cu2+ ions can also play crucial antibacterial roles in the blood clam, Tegillarca granosa. However, the mechanism of interaction between iron and copper in...

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Main Authors: Tinghong Ming, Qinqin Jiang, Chunheng Huo, Hengshang Huan, Yan Wu, Chang Su, Xiaoting Qiu, Chenyang Lu, Jun Zhou, Ye Li, Jiaojiao Han, Zhen Zhang, Xiurong Su
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-03-01
Series:Frontiers in Molecular Biosciences
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmolb.2022.800008/full
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author Tinghong Ming
Tinghong Ming
Qinqin Jiang
Qinqin Jiang
Chunheng Huo
Chunheng Huo
Hengshang Huan
Hengshang Huan
Yan Wu
Yan Wu
Chang Su
Xiaoting Qiu
Chenyang Lu
Chenyang Lu
Jun Zhou
Jun Zhou
Ye Li
Ye Li
Jiaojiao Han
Jiaojiao Han
Zhen Zhang
Zhen Zhang
Xiurong Su
Xiurong Su
author_facet Tinghong Ming
Tinghong Ming
Qinqin Jiang
Qinqin Jiang
Chunheng Huo
Chunheng Huo
Hengshang Huan
Hengshang Huan
Yan Wu
Yan Wu
Chang Su
Xiaoting Qiu
Chenyang Lu
Chenyang Lu
Jun Zhou
Jun Zhou
Ye Li
Ye Li
Jiaojiao Han
Jiaojiao Han
Zhen Zhang
Zhen Zhang
Xiurong Su
Xiurong Su
author_sort Tinghong Ming
collection DOAJ
description In addition to its role as an iron storage protein, ferritin can function as a major detoxification component in the innate immune defense, and Cu2+ ions can also play crucial antibacterial roles in the blood clam, Tegillarca granosa. However, the mechanism of interaction between iron and copper in recombinant Tegillarca granosa ferritin (TgFer) remains to be investigated. In this study, we investigated the crystal structure of TgFer and examined the effects of Fe2+ and Cu2+ ions on the TgFer structure and catalytic activity. The crystal structure revealed that TgFer presented a typically 4–3–2 symmetry in a cage-like, spherical shell composed of 24 identical subunits, featuring highly conserved organization in both the ferroxidase center and the 3-fold channel. Structural and biochemical analyses indicated that the 4-fold channel of TgFer could be serviced as potential binding sites of metal ions. Cu2+ ions appear to bind preferentially with the 3-fold channel as well as ferroxidase site over Fe2+ ions, possibly inhibiting the ferroxidase activity of TgFer. Our results present a structural and functional characterization of TgFer, providing mechanistic insight into the interactions between TgFer and both Fe2+ and Cu2+ ions.
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spelling doaj.art-3fe674f1825247bf9c2a86ae53cb32a92022-12-22T01:10:29ZengFrontiers Media S.A.Frontiers in Molecular Biosciences2296-889X2022-03-01910.3389/fmolb.2022.800008800008Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosaTinghong Ming0Tinghong Ming1Qinqin Jiang2Qinqin Jiang3Chunheng Huo4Chunheng Huo5Hengshang Huan6Hengshang Huan7Yan Wu8Yan Wu9Chang Su10Xiaoting Qiu11Chenyang Lu12Chenyang Lu13Jun Zhou14Jun Zhou15Ye Li16Ye Li17Jiaojiao Han18Jiaojiao Han19Zhen Zhang20Zhen Zhang21Xiurong Su22Xiurong Su23State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaCollege of Food and Pharmaceutical Sciences, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaCollege of Food and Pharmaceutical Sciences, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaCollege of Food and Pharmaceutical Sciences, Ningbo University, Ningbo, ChinaZhejiang Collaborative Innovation Center for High Value Utilization of Byproducts from Ethylene Project, Ningbo Polytechnic College, Ningbo, ChinaCollege of Food and Pharmaceutical Sciences, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaState Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-products, Ningbo University, Ningbo, ChinaSchool of Marine Science, Ningbo University, Ningbo, ChinaIn addition to its role as an iron storage protein, ferritin can function as a major detoxification component in the innate immune defense, and Cu2+ ions can also play crucial antibacterial roles in the blood clam, Tegillarca granosa. However, the mechanism of interaction between iron and copper in recombinant Tegillarca granosa ferritin (TgFer) remains to be investigated. In this study, we investigated the crystal structure of TgFer and examined the effects of Fe2+ and Cu2+ ions on the TgFer structure and catalytic activity. The crystal structure revealed that TgFer presented a typically 4–3–2 symmetry in a cage-like, spherical shell composed of 24 identical subunits, featuring highly conserved organization in both the ferroxidase center and the 3-fold channel. Structural and biochemical analyses indicated that the 4-fold channel of TgFer could be serviced as potential binding sites of metal ions. Cu2+ ions appear to bind preferentially with the 3-fold channel as well as ferroxidase site over Fe2+ ions, possibly inhibiting the ferroxidase activity of TgFer. Our results present a structural and functional characterization of TgFer, providing mechanistic insight into the interactions between TgFer and both Fe2+ and Cu2+ ions.https://www.frontiersin.org/articles/10.3389/fmolb.2022.800008/fullblood clam Tegillarca granosaferritincrystal structureFe2+ ionCu2+ ioncatalytic activity
spellingShingle Tinghong Ming
Tinghong Ming
Qinqin Jiang
Qinqin Jiang
Chunheng Huo
Chunheng Huo
Hengshang Huan
Hengshang Huan
Yan Wu
Yan Wu
Chang Su
Xiaoting Qiu
Chenyang Lu
Chenyang Lu
Jun Zhou
Jun Zhou
Ye Li
Ye Li
Jiaojiao Han
Jiaojiao Han
Zhen Zhang
Zhen Zhang
Xiurong Su
Xiurong Su
Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa
Frontiers in Molecular Biosciences
blood clam Tegillarca granosa
ferritin
crystal structure
Fe2+ ion
Cu2+ ion
catalytic activity
title Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa
title_full Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa
title_fullStr Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa
title_full_unstemmed Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa
title_short Structural Insights Into the Effects of Interactions With Iron and Copper Ions on Ferritin From the Blood Clam Tegillarca granosa
title_sort structural insights into the effects of interactions with iron and copper ions on ferritin from the blood clam tegillarca granosa
topic blood clam Tegillarca granosa
ferritin
crystal structure
Fe2+ ion
Cu2+ ion
catalytic activity
url https://www.frontiersin.org/articles/10.3389/fmolb.2022.800008/full
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