DnaJC16, the molecular chaperone, is implicated in hemocyte apoptosis and facilitates of WSSV infection in shrimp

Chaperone proteins, including heat shock proteins (HSPs) and DnaJ proteins, are highly conserved and well known for their quick responses to environmental stresses and pathogen infections, especially viruses. However, how DnaJ, an HSP family member, in Penaeus vannamei responds to viral invasion has...

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Veröffentlicht in:Fish & shellfish immunology 2023-06, Vol.137, p.108770-108770, Article 108770
Hauptverfasser: Jaree, Phattarunda, Somboonwiwat, Kunlaya
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description Chaperone proteins, including heat shock proteins (HSPs) and DnaJ proteins, are highly conserved and well known for their quick responses to environmental stresses and pathogen infections, especially viruses. However, how DnaJ, an HSP family member, in Penaeus vannamei responds to viral invasion has not been reported. In this research, the novel DnaJ homolog subfamily C member 16-like, or DnaJC16, was characterized in P. vannamei. It contains the DnaJ and thioredoxin domains. Phylogenetic tree analysis demonstrated the conservation of DnaJC16 among penaeid shrimp, where PvDnaJC16 was found to be closely related to DnaJC16 from Fenneropenaeus chinensis and Marsupenaeus japonicus. The transcripts of PvDnaJC16 were expressed in all the tissues tested, and the highest expression was in the lymphoid organs. As hemocytes are major immune tissue, we found significant upregulation of PvDnaJC16 in shrimp hemocytes after white spot syndrome virus (WSSV) infection. Furthermore, the suppression of PvDnaJC16 expression by RNA interference in WSSV-infected shrimp showed a decrease in replication and WSSV copy number. Interestingly, a dramatically high cumulative survival rate following the WSSV challenge (over 60%) was observed in PvDnaJC16-silenced shrimp. Meanwhile, the total hemocyte number was significantly increased in PvDnaJC16 knockdown. In addition, the expression of caspase-3 was reduced, as was the caspase-3/7 activity in PvDnaJC16 silencing. Additionally, the percentage of late apoptotic hemocytes diminished after PvDnaJC16 reduction, whereas the percentage of hemocyte viability increased. Our data reflect the fact that the upregulation of PvDnaJC16 expression upon WSSV infection enhances hemocyte apoptosis, which can accelerate viral spreading in shrimp. •The Penaeus vannamei DnaJC16 transcript was upregulated upon WSSV infection.•WSSV-infected shrimp had a high survival rate after PvDnaJC16 silencing.•The THC index significantly increased after the PvDnaJC16 knockdown.•Suppression of PvDnaJC16 reduced the percentage of apoptotic hemocytes.•PvDnaJC16 aids WSSV infection by enhancing hemocyte apoptosis.
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Interestingly, a dramatically high cumulative survival rate following the WSSV challenge (over 60%) was observed in PvDnaJC16-silenced shrimp. Meanwhile, the total hemocyte number was significantly increased in PvDnaJC16 knockdown. In addition, the expression of caspase-3 was reduced, as was the caspase-3/7 activity in PvDnaJC16 silencing. Additionally, the percentage of late apoptotic hemocytes diminished after PvDnaJC16 reduction, whereas the percentage of hemocyte viability increased. 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However, how DnaJ, an HSP family member, in Penaeus vannamei responds to viral invasion has not been reported. In this research, the novel DnaJ homolog subfamily C member 16-like, or DnaJC16, was characterized in P. vannamei. It contains the DnaJ and thioredoxin domains. Phylogenetic tree analysis demonstrated the conservation of DnaJC16 among penaeid shrimp, where PvDnaJC16 was found to be closely related to DnaJC16 from Fenneropenaeus chinensis and Marsupenaeus japonicus. The transcripts of PvDnaJC16 were expressed in all the tissues tested, and the highest expression was in the lymphoid organs. As hemocytes are major immune tissue, we found significant upregulation of PvDnaJC16 in shrimp hemocytes after white spot syndrome virus (WSSV) infection. Furthermore, the suppression of PvDnaJC16 expression by RNA interference in WSSV-infected shrimp showed a decrease in replication and WSSV copy number. Interestingly, a dramatically high cumulative survival rate following the WSSV challenge (over 60%) was observed in PvDnaJC16-silenced shrimp. Meanwhile, the total hemocyte number was significantly increased in PvDnaJC16 knockdown. In addition, the expression of caspase-3 was reduced, as was the caspase-3/7 activity in PvDnaJC16 silencing. Additionally, the percentage of late apoptotic hemocytes diminished after PvDnaJC16 reduction, whereas the percentage of hemocyte viability increased. Our data reflect the fact that the upregulation of PvDnaJC16 expression upon WSSV infection enhances hemocyte apoptosis, which can accelerate viral spreading in shrimp. •The Penaeus vannamei DnaJC16 transcript was upregulated upon WSSV infection.•WSSV-infected shrimp had a high survival rate after PvDnaJC16 silencing.•The THC index significantly increased after the PvDnaJC16 knockdown.•Suppression of PvDnaJC16 reduced the percentage of apoptotic hemocytes.•PvDnaJC16 aids WSSV infection by enhancing hemocyte apoptosis.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Apoptosis - genetics</subject><subject>Arthropod Proteins</subject><subject>Caspase 3 - genetics</subject><subject>Chaperone</subject><subject>DnaJC16</subject><subject>Hemocytes</subject><subject>Molecular Chaperones - genetics</subject><subject>Penaeidae</subject><subject>Penaeus vannamei</subject><subject>Phylogeny</subject><subject>White spot syndrome virus</subject><subject>White spot syndrome virus 1 - physiology</subject><issn>1050-4648</issn><issn>1095-9947</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kMlOBCEURYnROH-AG8PSRVfLVANxZdo5Ji6cloSGR5pOVVFCtYl_L51Wl6545J17AwehE0qmlNDqfDl1yU8ZYTzfm7omW2ifElkWUop6ez2XpBCVaPbQQUpLQkjFK7KL9nidV4KV--jjqtcPM1pN8LgA3IUWzKrVEZuFHiCGHibYJ-y7ofVGj2Cx7_ECumC-RsB6CMMYUgZ0b7HTxrd-zFTCweH35-e3TDswow_9OpcWMRcdoR2n2wTHP-cher25fpndFY9Pt_ezy8fC8JKPheNWC6BSWjsXtAbQVjDtSgPMmUZYaQwl8zkXsqmEpJzTRlpiK8o1s5oBP0Rnm94hho8VpFF1PhloW91DWCXFGlJLKlnNMko3qIkhpQhODfmlOn4pStTatFqqbFqtTauN6Zw5_alfzTuwf4lftRm42ACQP_npIapkPPQGrI_ZibLB_1P_DX7AjyU</recordid><startdate>202306</startdate><enddate>202306</enddate><creator>Jaree, Phattarunda</creator><creator>Somboonwiwat, Kunlaya</creator><general>Elsevier Ltd</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><orcidid>https://orcid.org/0000-0002-0241-8238</orcidid></search><sort><creationdate>202306</creationdate><title>DnaJC16, the molecular chaperone, is implicated in hemocyte apoptosis and facilitates of WSSV infection in shrimp</title><author>Jaree, Phattarunda ; Somboonwiwat, Kunlaya</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c353t-f3da4e199ddb417eead42af5ce2fc84d9cc10bb3498649133189d0d613a2da2e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Apoptosis - genetics</topic><topic>Arthropod Proteins</topic><topic>Caspase 3 - genetics</topic><topic>Chaperone</topic><topic>DnaJC16</topic><topic>Hemocytes</topic><topic>Molecular Chaperones - genetics</topic><topic>Penaeidae</topic><topic>Penaeus vannamei</topic><topic>Phylogeny</topic><topic>White spot syndrome virus</topic><topic>White spot syndrome virus 1 - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jaree, Phattarunda</creatorcontrib><creatorcontrib>Somboonwiwat, Kunlaya</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>Fish &amp; shellfish immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jaree, Phattarunda</au><au>Somboonwiwat, Kunlaya</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>DnaJC16, the molecular chaperone, is implicated in hemocyte apoptosis and facilitates of WSSV infection in shrimp</atitle><jtitle>Fish &amp; shellfish immunology</jtitle><addtitle>Fish Shellfish Immunol</addtitle><date>2023-06</date><risdate>2023</risdate><volume>137</volume><spage>108770</spage><epage>108770</epage><pages>108770-108770</pages><artnum>108770</artnum><issn>1050-4648</issn><eissn>1095-9947</eissn><abstract>Chaperone proteins, including heat shock proteins (HSPs) and DnaJ proteins, are highly conserved and well known for their quick responses to environmental stresses and pathogen infections, especially viruses. However, how DnaJ, an HSP family member, in Penaeus vannamei responds to viral invasion has not been reported. In this research, the novel DnaJ homolog subfamily C member 16-like, or DnaJC16, was characterized in P. vannamei. It contains the DnaJ and thioredoxin domains. Phylogenetic tree analysis demonstrated the conservation of DnaJC16 among penaeid shrimp, where PvDnaJC16 was found to be closely related to DnaJC16 from Fenneropenaeus chinensis and Marsupenaeus japonicus. The transcripts of PvDnaJC16 were expressed in all the tissues tested, and the highest expression was in the lymphoid organs. As hemocytes are major immune tissue, we found significant upregulation of PvDnaJC16 in shrimp hemocytes after white spot syndrome virus (WSSV) infection. Furthermore, the suppression of PvDnaJC16 expression by RNA interference in WSSV-infected shrimp showed a decrease in replication and WSSV copy number. Interestingly, a dramatically high cumulative survival rate following the WSSV challenge (over 60%) was observed in PvDnaJC16-silenced shrimp. Meanwhile, the total hemocyte number was significantly increased in PvDnaJC16 knockdown. In addition, the expression of caspase-3 was reduced, as was the caspase-3/7 activity in PvDnaJC16 silencing. Additionally, the percentage of late apoptotic hemocytes diminished after PvDnaJC16 reduction, whereas the percentage of hemocyte viability increased. Our data reflect the fact that the upregulation of PvDnaJC16 expression upon WSSV infection enhances hemocyte apoptosis, which can accelerate viral spreading in shrimp. •The Penaeus vannamei DnaJC16 transcript was upregulated upon WSSV infection.•WSSV-infected shrimp had a high survival rate after PvDnaJC16 silencing.•The THC index significantly increased after the PvDnaJC16 knockdown.•Suppression of PvDnaJC16 reduced the percentage of apoptotic hemocytes.•PvDnaJC16 aids WSSV infection by enhancing hemocyte apoptosis.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>37105425</pmid><doi>10.1016/j.fsi.2023.108770</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-0241-8238</orcidid></addata></record>
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subjects Animals
Apoptosis
Apoptosis - genetics
Arthropod Proteins
Caspase 3 - genetics
Chaperone
DnaJC16
Hemocytes
Molecular Chaperones - genetics
Penaeidae
Penaeus vannamei
Phylogeny
White spot syndrome virus
White spot syndrome virus 1 - physiology
title DnaJC16, the molecular chaperone, is implicated in hemocyte apoptosis and facilitates of WSSV infection in shrimp
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