Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress
Lin Wang , Yan Jiang , Lu Fang , Changtao Guan , Yongjiang Xu
{"title":"Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress","authors":"Lin Wang , Yan Jiang , Lu Fang , Changtao Guan , Yongjiang Xu","doi":"10.1016/j.cbpb.2023.110927","DOIUrl":null,"url":null,"abstract":"<div><p>Hsp90s are molecular chaperones that enhance fish tolerance to high-temperature stress. However, the function of Hsp90s in <em>Seriola aureovittata</em> (yellowtail kingfish) under high-temperature stress remains largely unknown. Here, two <span><em>Hsp90</em></span><span> isoforms were identified in </span><em>S. aureovittata</em> by bioinformatics analysis: <em>SaHsp90α</em> and <em>SaHsp90β</em>. The coding sequence of <em>SaHsp90α</em><span> was 2193-bp long and encoded a polypeptide of 730 amino acids; </span><em>SaHsp90β</em> was 2178-bp long and encoded a polypeptide of 725 amino acids. <em>Sa</em>Hsp90α and <em>Sa</em>Hsp90β both contained a HATPase domain and a HSP90 domain. Their transcripts were detected in all examined <em>S. aureovittata</em> tissues, with relatively high levels in the gonads, head kidney, and intestine. During high-temperature stress at 28 °C, the expression levels of <em>SaHsp90α</em> and <em>SaHsp90β</em> transcripts were significantly increased in liver. After simultaneously knocking down the expression of the <em>SaHsp90</em><span>s, there was a significant decrease in liver superoxide dismutase (SOD) activity and a remarkable increase of malondialdehyde content in liver after high-temperature stress. The expression levels of the key caspase<span> family genes </span></span><em>caspase-3</em> and <em>caspase-7</em> were also significantly upregulated by high-temperature stress in <em>SaHsp90</em><span>-knockdown liver. TUNEL labeling demonstrated that the number of apoptotic cells significantly increased in the </span><em>SaHsp90</em>-knockdown group when high-temperature treatment lasted for 48 h. Protein–protein docking analysis predicted that <em>Sa</em>Hsp90α and <em>Sa</em>Hsp90β can bind to <em>S. aureovittata</em><span> SOD and survivin<span>, which are key proteins for maintenance of redox homeostasis and inhibition of apoptosis. These findings demonstrate that </span></span><em>Sa</em>Hsp90α and <em>Sa</em>Hsp90β play a crucial role in resistance to high-temperature stress by regulating redox homeostasis and apoptosis in yellowtail kingfish.</p></div>","PeriodicalId":55236,"journal":{"name":"Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology","volume":"270 ","pages":"Article 110927"},"PeriodicalIF":1.9000,"publicationDate":"2023-11-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1096495923001021","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q4","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Hsp90s are molecular chaperones that enhance fish tolerance to high-temperature stress. However, the function of Hsp90s in Seriola aureovittata (yellowtail kingfish) under high-temperature stress remains largely unknown. Here, two Hsp90 isoforms were identified in S. aureovittata by bioinformatics analysis: SaHsp90α and SaHsp90β. The coding sequence of SaHsp90α was 2193-bp long and encoded a polypeptide of 730 amino acids; SaHsp90β was 2178-bp long and encoded a polypeptide of 725 amino acids. SaHsp90α and SaHsp90β both contained a HATPase domain and a HSP90 domain. Their transcripts were detected in all examined S. aureovittata tissues, with relatively high levels in the gonads, head kidney, and intestine. During high-temperature stress at 28 °C, the expression levels of SaHsp90α and SaHsp90β transcripts were significantly increased in liver. After simultaneously knocking down the expression of the SaHsp90s, there was a significant decrease in liver superoxide dismutase (SOD) activity and a remarkable increase of malondialdehyde content in liver after high-temperature stress. The expression levels of the key caspase family genes caspase-3 and caspase-7 were also significantly upregulated by high-temperature stress in SaHsp90-knockdown liver. TUNEL labeling demonstrated that the number of apoptotic cells significantly increased in the SaHsp90-knockdown group when high-temperature treatment lasted for 48 h. Protein–protein docking analysis predicted that SaHsp90α and SaHsp90β can bind to S. aureovittata SOD and survivin, which are key proteins for maintenance of redox homeostasis and inhibition of apoptosis. These findings demonstrate that SaHsp90α and SaHsp90β play a crucial role in resistance to high-temperature stress by regulating redox homeostasis and apoptosis in yellowtail kingfish.
期刊介绍:
Comparative Biochemistry & Physiology (CBP) publishes papers in comparative, environmental and evolutionary physiology.
Part B: Biochemical and Molecular Biology (CBPB), focuses on biochemical physiology, primarily bioenergetics/energy metabolism, cell biology, cellular stress responses, enzymology, intermediary metabolism, macromolecular structure and function, gene regulation, evolutionary genetics. Most studies focus on biochemical or molecular analyses that have clear ramifications for physiological processes.