The iron–sulfur protein subunit of succinate dehydrogenase is critical in driving mitochondrial reactive oxygen species generation in Apostichopus japonicus

Succinate dehydrogenase (SDH) is a mitochondrial enzyme with the unique ability to participate in both the tricarboxylic acid cycle and the electron transport chain to produce reactive oxygen species (ROS). The B subunit of SDH is required for succinate oxidation, which is critical for pro-inflammat...

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Veröffentlicht in:Fish & shellfish immunology 2020-07, Vol.102, p.350-360
Hauptverfasser: Sun, Lianlian, Zhou, Fangyuan, Shao, Yina, Lv, Zhimeng, Li, Chenghua
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Zhou, Fangyuan
Shao, Yina
Lv, Zhimeng
Li, Chenghua
description Succinate dehydrogenase (SDH) is a mitochondrial enzyme with the unique ability to participate in both the tricarboxylic acid cycle and the electron transport chain to produce reactive oxygen species (ROS). The B subunit of SDH is required for succinate oxidation, which is critical for pro-inflammatory response. In this study, we cloned the iron–sulfur protein subunit of SDH from Apostichopus japonicus (denoted as AjSDHB) via RACE technology and explored its role in the immune system as a response to pathogen infection. The full-length cDNA of AjSDHB was 1442 bp with a complete open reading frame of 858 bp encoding 286 amino acids. Simple modular architecture research tool analysis revealed that AjSDHB contained two conserved domains, including a 2Fe–2S iron–sulfur cluster binding domain and a 4Fe–4S dicluster domain, without a signal peptide. Multiple sequence alignment demonstrated that AjSDHB shared a high degree of structural conservation and sequence identities with other counterparts from invertebrates and vertebrates. Phylogenetic analysis supported the finding that AjSDHB is a new member of the SDHB protein subfamily. Tissue distribution analysis revealed that AjSDHB was expressed in all examined tissues and particularly highly expressed in the muscles. AjSDHB transcripts were markedly induced in coelomocytes both by Vibrio splendidus challenge in vivo and lipopolysaccharide exposure in vitro. Function analysis showed that siRNA-mediated AjSDHB knockdown could substantially reduce the mitochondrial membrane potential (ΔΨm) and further decrease mitochondrial ROS production in A. japonicus coelomocytes. By contrast, AjSDHB overexpression considerably increased ΔΨm and mitochondrial ROS production of A. japonicus coelomocytes. These results supported the idea that AjSDHB is involved in the innate immunity of A. japonicus through its participation in mitochondrial ROS generation. •The full-length cDNA of AjSDHB was cloned and characterized in Apostichopus japonicus.•AjSDHB interference blocks the mitochondrial membrane potential.•AjSDHB participates in driving the mitochondrial ROS production.
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Tissue distribution analysis revealed that AjSDHB was expressed in all examined tissues and particularly highly expressed in the muscles. AjSDHB transcripts were markedly induced in coelomocytes both by Vibrio splendidus challenge in vivo and lipopolysaccharide exposure in vitro. Function analysis showed that siRNA-mediated AjSDHB knockdown could substantially reduce the mitochondrial membrane potential (ΔΨm) and further decrease mitochondrial ROS production in A. japonicus coelomocytes. By contrast, AjSDHB overexpression considerably increased ΔΨm and mitochondrial ROS production of A. japonicus coelomocytes. 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shellfish immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sun, Lianlian</au><au>Zhou, Fangyuan</au><au>Shao, Yina</au><au>Lv, Zhimeng</au><au>Li, Chenghua</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The iron–sulfur protein subunit of succinate dehydrogenase is critical in driving mitochondrial reactive oxygen species generation in Apostichopus japonicus</atitle><jtitle>Fish &amp; shellfish immunology</jtitle><addtitle>Fish Shellfish Immunol</addtitle><date>2020-07</date><risdate>2020</risdate><volume>102</volume><spage>350</spage><epage>360</epage><pages>350-360</pages><issn>1050-4648</issn><eissn>1095-9947</eissn><abstract>Succinate dehydrogenase (SDH) is a mitochondrial enzyme with the unique ability to participate in both the tricarboxylic acid cycle and the electron transport chain to produce reactive oxygen species (ROS). The B subunit of SDH is required for succinate oxidation, which is critical for pro-inflammatory response. In this study, we cloned the iron–sulfur protein subunit of SDH from Apostichopus japonicus (denoted as AjSDHB) via RACE technology and explored its role in the immune system as a response to pathogen infection. The full-length cDNA of AjSDHB was 1442 bp with a complete open reading frame of 858 bp encoding 286 amino acids. Simple modular architecture research tool analysis revealed that AjSDHB contained two conserved domains, including a 2Fe–2S iron–sulfur cluster binding domain and a 4Fe–4S dicluster domain, without a signal peptide. Multiple sequence alignment demonstrated that AjSDHB shared a high degree of structural conservation and sequence identities with other counterparts from invertebrates and vertebrates. Phylogenetic analysis supported the finding that AjSDHB is a new member of the SDHB protein subfamily. Tissue distribution analysis revealed that AjSDHB was expressed in all examined tissues and particularly highly expressed in the muscles. AjSDHB transcripts were markedly induced in coelomocytes both by Vibrio splendidus challenge in vivo and lipopolysaccharide exposure in vitro. Function analysis showed that siRNA-mediated AjSDHB knockdown could substantially reduce the mitochondrial membrane potential (ΔΨm) and further decrease mitochondrial ROS production in A. japonicus coelomocytes. By contrast, AjSDHB overexpression considerably increased ΔΨm and mitochondrial ROS production of A. japonicus coelomocytes. These results supported the idea that AjSDHB is involved in the innate immunity of A. japonicus through its participation in mitochondrial ROS generation. •The full-length cDNA of AjSDHB was cloned and characterized in Apostichopus japonicus.•AjSDHB interference blocks the mitochondrial membrane potential.•AjSDHB participates in driving the mitochondrial ROS production.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>32371258</pmid><doi>10.1016/j.fsi.2020.04.060</doi><tpages>11</tpages></addata></record>
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subjects Amino Acid Sequence
Animals
Apostichopus japonicus
Base Sequence
Iron-Sulfur Proteins - genetics
Iron-Sulfur Proteins - metabolism
Iron–sulfur protein subunit of succinate dehydrogenase
Lipopolysaccharides - pharmacology
Mitochondria - metabolism
Mitochondrial membrane potential
Mitochondrial ROS
Phylogeny
Reactive Oxygen Species - metabolism
Sequence Alignment
Stichopus - enzymology
Stichopus - genetics
Stichopus - immunology
Stichopus - metabolism
Succinate Dehydrogenase - genetics
Succinate Dehydrogenase - metabolism
Vibrio - physiology
title The iron–sulfur protein subunit of succinate dehydrogenase is critical in driving mitochondrial reactive oxygen species generation in Apostichopus japonicus
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