Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress

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 a...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 2024-02, Vol.270, p.110927-110927, Article 110927
Hauptverfasser: Wang, Lin, Jiang, Yan, Fang, Lu, Guan, Changtao, Xu, Yongjiang
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 110927
container_issue
container_start_page 110927
container_title Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology
container_volume 270
creator Wang, Lin
Jiang, Yan
Fang, Lu
Guan, Changtao
Xu, Yongjiang
description 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. [Display omitted] •Two Hsp90 isoforms were identified in Seriola aureovittata: SaHsp90α and SaHsp90β.•Heat stress induced SaHsp90α and SaHsp90β transcripts expression in liver.•SaHsp90s knockdown exacerbated oxidative stress and apoptosis during heat stress.•SaHsp90s might directly interact with SOD and survivin in Seriola aureovittata.
doi_str_mv 10.1016/j.cbpb.2023.110927
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2896808658</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S1096495923001021</els_id><sourcerecordid>2896808658</sourcerecordid><originalsourceid>FETCH-LOGICAL-c356t-7319d9b6b923e697fdd679452fff7e462d9998e77603338d7bfa537422c02e0c3</originalsourceid><addsrcrecordid>eNp9kctu1DAYRi1ERS_wAiyQl2WRqS-JLxIbVJUWqRILYG059p-Op5k42M6UvgsPW49mYMnKtny-z5eD0HtKVpRQcbVZuX7uV4wwvqKUaCZfoTOqpG7qSr6uc6JF0-pOn6LznDeEcEU5fYNOuSIt4UyeoT93YEuT19E94jnFAmHCmmA7jrALtkDG8XfwtoQd4FwS5Izt5HECv7i6aec4l5hDxjU3VijhOODvkEIcLbZLgrgLpdhi8eUzjGN8KjaM-DFMD0PI6494mXzNrMPDuimwnSHZUkPHo96ik8GOGd4dxwv088vNj-u75v7b7dfrz_eN450ojeRUe92LXjMOQsvBeyF127FhGCS0gnmttQIpBeGcKy_7wXZctow5woA4foEuD731B34tkIvZhuzqde0EccmGKS0UUaJTFWUH1KWYc4LBzClsbXo2lJi9FbMxeytmb8UcrNTQh2P_0m_B_4v81VCBTwcA6it3AZLJLsDkwIcErhgfw__6XwBqb6Ds</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2896808658</pqid></control><display><type>article</type><title>Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress</title><source>MEDLINE</source><source>Elsevier ScienceDirect Journals</source><creator>Wang, Lin ; Jiang, Yan ; Fang, Lu ; Guan, Changtao ; Xu, Yongjiang</creator><creatorcontrib>Wang, Lin ; Jiang, Yan ; Fang, Lu ; Guan, Changtao ; Xu, Yongjiang</creatorcontrib><description>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. [Display omitted] •Two Hsp90 isoforms were identified in Seriola aureovittata: SaHsp90α and SaHsp90β.•Heat stress induced SaHsp90α and SaHsp90β transcripts expression in liver.•SaHsp90s knockdown exacerbated oxidative stress and apoptosis during heat stress.•SaHsp90s might directly interact with SOD and survivin in Seriola aureovittata.</description><identifier>ISSN: 1096-4959</identifier><identifier>EISSN: 1879-1107</identifier><identifier>DOI: 10.1016/j.cbpb.2023.110927</identifier><identifier>PMID: 38040327</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Amino Acids - metabolism ; Animals ; Apoptosis ; Heat shock protein ; Heat-Shock Proteins - metabolism ; High-temperature stress ; Liver - metabolism ; Oxidative Stress ; Peptides - metabolism ; Perciformes - genetics ; Perciformes - metabolism ; Seriola aureovittata ; Superoxide Dismutase - metabolism ; Temperature</subject><ispartof>Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 2024-02, Vol.270, p.110927-110927, Article 110927</ispartof><rights>2023</rights><rights>Copyright © 2023. Published by Elsevier Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c356t-7319d9b6b923e697fdd679452fff7e462d9998e77603338d7bfa537422c02e0c3</citedby><cites>FETCH-LOGICAL-c356t-7319d9b6b923e697fdd679452fff7e462d9998e77603338d7bfa537422c02e0c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1096495923001021$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3537,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38040327$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wang, Lin</creatorcontrib><creatorcontrib>Jiang, Yan</creatorcontrib><creatorcontrib>Fang, Lu</creatorcontrib><creatorcontrib>Guan, Changtao</creatorcontrib><creatorcontrib>Xu, Yongjiang</creatorcontrib><title>Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress</title><title>Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology</title><addtitle>Comp Biochem Physiol B Biochem Mol Biol</addtitle><description>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. [Display omitted] •Two Hsp90 isoforms were identified in Seriola aureovittata: SaHsp90α and SaHsp90β.•Heat stress induced SaHsp90α and SaHsp90β transcripts expression in liver.•SaHsp90s knockdown exacerbated oxidative stress and apoptosis during heat stress.•SaHsp90s might directly interact with SOD and survivin in Seriola aureovittata.</description><subject>Amino Acids - metabolism</subject><subject>Animals</subject><subject>Apoptosis</subject><subject>Heat shock protein</subject><subject>Heat-Shock Proteins - metabolism</subject><subject>High-temperature stress</subject><subject>Liver - metabolism</subject><subject>Oxidative Stress</subject><subject>Peptides - metabolism</subject><subject>Perciformes - genetics</subject><subject>Perciformes - metabolism</subject><subject>Seriola aureovittata</subject><subject>Superoxide Dismutase - metabolism</subject><subject>Temperature</subject><issn>1096-4959</issn><issn>1879-1107</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kctu1DAYRi1ERS_wAiyQl2WRqS-JLxIbVJUWqRILYG059p-Op5k42M6UvgsPW49mYMnKtny-z5eD0HtKVpRQcbVZuX7uV4wwvqKUaCZfoTOqpG7qSr6uc6JF0-pOn6LznDeEcEU5fYNOuSIt4UyeoT93YEuT19E94jnFAmHCmmA7jrALtkDG8XfwtoQd4FwS5Izt5HECv7i6aec4l5hDxjU3VijhOODvkEIcLbZLgrgLpdhi8eUzjGN8KjaM-DFMD0PI6494mXzNrMPDuimwnSHZUkPHo96ik8GOGd4dxwv088vNj-u75v7b7dfrz_eN450ojeRUe92LXjMOQsvBeyF127FhGCS0gnmttQIpBeGcKy_7wXZctow5woA4foEuD731B34tkIvZhuzqde0EccmGKS0UUaJTFWUH1KWYc4LBzClsbXo2lJi9FbMxeytmb8UcrNTQh2P_0m_B_4v81VCBTwcA6it3AZLJLsDkwIcErhgfw__6XwBqb6Ds</recordid><startdate>202402</startdate><enddate>202402</enddate><creator>Wang, Lin</creator><creator>Jiang, Yan</creator><creator>Fang, Lu</creator><creator>Guan, Changtao</creator><creator>Xu, Yongjiang</creator><general>Elsevier Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>202402</creationdate><title>Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress</title><author>Wang, Lin ; Jiang, Yan ; Fang, Lu ; Guan, Changtao ; Xu, Yongjiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c356t-7319d9b6b923e697fdd679452fff7e462d9998e77603338d7bfa537422c02e0c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Amino Acids - metabolism</topic><topic>Animals</topic><topic>Apoptosis</topic><topic>Heat shock protein</topic><topic>Heat-Shock Proteins - metabolism</topic><topic>High-temperature stress</topic><topic>Liver - metabolism</topic><topic>Oxidative Stress</topic><topic>Peptides - metabolism</topic><topic>Perciformes - genetics</topic><topic>Perciformes - metabolism</topic><topic>Seriola aureovittata</topic><topic>Superoxide Dismutase - metabolism</topic><topic>Temperature</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wang, Lin</creatorcontrib><creatorcontrib>Jiang, Yan</creatorcontrib><creatorcontrib>Fang, Lu</creatorcontrib><creatorcontrib>Guan, Changtao</creatorcontrib><creatorcontrib>Xu, Yongjiang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wang, Lin</au><au>Jiang, Yan</au><au>Fang, Lu</au><au>Guan, Changtao</au><au>Xu, Yongjiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress</atitle><jtitle>Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology</jtitle><addtitle>Comp Biochem Physiol B Biochem Mol Biol</addtitle><date>2024-02</date><risdate>2024</risdate><volume>270</volume><spage>110927</spage><epage>110927</epage><pages>110927-110927</pages><artnum>110927</artnum><issn>1096-4959</issn><eissn>1879-1107</eissn><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. [Display omitted] •Two Hsp90 isoforms were identified in Seriola aureovittata: SaHsp90α and SaHsp90β.•Heat stress induced SaHsp90α and SaHsp90β transcripts expression in liver.•SaHsp90s knockdown exacerbated oxidative stress and apoptosis during heat stress.•SaHsp90s might directly interact with SOD and survivin in Seriola aureovittata.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>38040327</pmid><doi>10.1016/j.cbpb.2023.110927</doi><tpages>1</tpages></addata></record>
fulltext fulltext
identifier ISSN: 1096-4959
ispartof Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 2024-02, Vol.270, p.110927-110927, Article 110927
issn 1096-4959
1879-1107
language eng
recordid cdi_proquest_miscellaneous_2896808658
source MEDLINE; Elsevier ScienceDirect Journals
subjects Amino Acids - metabolism
Animals
Apoptosis
Heat shock protein
Heat-Shock Proteins - metabolism
High-temperature stress
Liver - metabolism
Oxidative Stress
Peptides - metabolism
Perciformes - genetics
Perciformes - metabolism
Seriola aureovittata
Superoxide Dismutase - metabolism
Temperature
title Heat-shock protein 90 alleviates oxidative stress and reduces apoptosis in liver of Seriola aureovittata (yellowtail kingfish) under high-temperature stress
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-28T01%3A07%3A37IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Heat-shock%20protein%2090%20alleviates%20oxidative%20stress%20and%20reduces%20apoptosis%20in%20liver%20of%20Seriola%20aureovittata%20(yellowtail%20kingfish)%20under%20high-temperature%20stress&rft.jtitle=Comparative%20Biochemistry%20and%20Physiology%20Part%20B:%20Biochemistry%20and%20Molecular%20Biology&rft.au=Wang,%20Lin&rft.date=2024-02&rft.volume=270&rft.spage=110927&rft.epage=110927&rft.pages=110927-110927&rft.artnum=110927&rft.issn=1096-4959&rft.eissn=1879-1107&rft_id=info:doi/10.1016/j.cbpb.2023.110927&rft_dat=%3Cproquest_cross%3E2896808658%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2896808658&rft_id=info:pmid/38040327&rft_els_id=S1096495923001021&rfr_iscdi=true