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Proteomic analysis of carp seminal plasma provides insights into the immune response to bacterial infection of the male reproductive system
Aeromonas salmonicida is recognized as a significant bacterial pathogen in ulcerative disease of cyprinid fish. However, the mechanism of immunity to these bacteria in common carp is still not well understood, especially the immune regulation in the gonad to bacterial infection. The aims of our stud...
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Published in: | Fish & shellfish immunology 2022-08, Vol.127, p.822-835 |
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creator | Dietrich, Mariola A. Adamek, Mikołaj Teitge, Felix Teich, Lukas Jung-Schroers, Verena Malinowska, Agata Świderska, Bianka Rakus, Krzysztof Kodzik, Natalia Chadzińska, Magdalena Karol, Halina Liszewska, Ewa Ciereszko, Andrzej |
description | Aeromonas salmonicida is recognized as a significant bacterial pathogen in ulcerative disease of cyprinid fish. However, the mechanism of immunity to these bacteria in common carp is still not well understood, especially the immune regulation in the gonad to bacterial infection. The aims of our study were to analyze changes in the seminal plasma proteome following A. salmonicida infection in carp males. The observed pathological changes in the tissue (liver, spleen, kidney and testis) morphology and upregulation of immune-related genes (tnfa2, il6a) confirmed the successful infection challenge. Using mass spectrometry-based label-free quantitative proteomics, we identified 1402 seminal plasma proteins, and 44 proteins (20 up- and 24 downregulated) were found to be differentially abundant between infected and control males. Most differentially abundant proteins were involved in the immune response mechanisms, such as acute phase response, complement activation and coagulation, inflammation, lipid metabolism, cell-cell and cell-matrix adhesion, creatine-phosphate biosynthesis and germ cell-Sertoli cell junction signaling. Bacterial infection also caused profound changes in expression of selected genes in the testis and hematopoietic organs, which contributed to changes in seminal proteins. The altered seminal proteins and bacterial proteins in seminal plasma may serve as valuable markers of infection in the testis.
•A. salmonicida infection affects carp seminal plasma proteome.•Infection alters proteins involved in innate immunity, lipid and energy metabolism.•Infection causes changes in gene expression in the testis and hematopoietic organs.•A. salmonicida and/or its components cross the blood-testis barrier and enter the testis.•The altered proteins may serve as valuable markers of infection in the testis. |
doi_str_mv | 10.1016/j.fsi.2022.07.019 |
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•A. salmonicida infection affects carp seminal plasma proteome.•Infection alters proteins involved in innate immunity, lipid and energy metabolism.•Infection causes changes in gene expression in the testis and hematopoietic organs.•A. salmonicida and/or its components cross the blood-testis barrier and enter the testis.•The altered proteins may serve as valuable markers of infection in the testis.</description><identifier>ISSN: 1050-4648</identifier><identifier>EISSN: 1095-9947</identifier><identifier>DOI: 10.1016/j.fsi.2022.07.019</identifier><language>eng</language><publisher>Elsevier Ltd</publisher><subject>Aeromonas salmonicida ; Fish ; Infection ; Proteome ; Reproductive tract ; Semen</subject><ispartof>Fish & shellfish immunology, 2022-08, Vol.127, p.822-835</ispartof><rights>2022 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c303t-dd1ebe4318eeeaabde6e92525235d34fdf47de274c65675eaeebec11327eefad3</citedby><cites>FETCH-LOGICAL-c303t-dd1ebe4318eeeaabde6e92525235d34fdf47de274c65675eaeebec11327eefad3</cites><orcidid>0000-0002-2525-0941 ; 0000-0001-6599-901X ; 0000-0003-4890-3164 ; 0000-0002-2628-2611 ; 0000-0002-9373-4008</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids></links><search><creatorcontrib>Dietrich, Mariola A.</creatorcontrib><creatorcontrib>Adamek, Mikołaj</creatorcontrib><creatorcontrib>Teitge, Felix</creatorcontrib><creatorcontrib>Teich, Lukas</creatorcontrib><creatorcontrib>Jung-Schroers, Verena</creatorcontrib><creatorcontrib>Malinowska, Agata</creatorcontrib><creatorcontrib>Świderska, Bianka</creatorcontrib><creatorcontrib>Rakus, Krzysztof</creatorcontrib><creatorcontrib>Kodzik, Natalia</creatorcontrib><creatorcontrib>Chadzińska, Magdalena</creatorcontrib><creatorcontrib>Karol, Halina</creatorcontrib><creatorcontrib>Liszewska, Ewa</creatorcontrib><creatorcontrib>Ciereszko, Andrzej</creatorcontrib><title>Proteomic analysis of carp seminal plasma provides insights into the immune response to bacterial infection of the male reproductive system</title><title>Fish & shellfish immunology</title><description>Aeromonas salmonicida is recognized as a significant bacterial pathogen in ulcerative disease of cyprinid fish. However, the mechanism of immunity to these bacteria in common carp is still not well understood, especially the immune regulation in the gonad to bacterial infection. The aims of our study were to analyze changes in the seminal plasma proteome following A. salmonicida infection in carp males. The observed pathological changes in the tissue (liver, spleen, kidney and testis) morphology and upregulation of immune-related genes (tnfa2, il6a) confirmed the successful infection challenge. Using mass spectrometry-based label-free quantitative proteomics, we identified 1402 seminal plasma proteins, and 44 proteins (20 up- and 24 downregulated) were found to be differentially abundant between infected and control males. Most differentially abundant proteins were involved in the immune response mechanisms, such as acute phase response, complement activation and coagulation, inflammation, lipid metabolism, cell-cell and cell-matrix adhesion, creatine-phosphate biosynthesis and germ cell-Sertoli cell junction signaling. Bacterial infection also caused profound changes in expression of selected genes in the testis and hematopoietic organs, which contributed to changes in seminal proteins. The altered seminal proteins and bacterial proteins in seminal plasma may serve as valuable markers of infection in the testis.
•A. salmonicida infection affects carp seminal plasma proteome.•Infection alters proteins involved in innate immunity, lipid and energy metabolism.•Infection causes changes in gene expression in the testis and hematopoietic organs.•A. salmonicida and/or its components cross the blood-testis barrier and enter the testis.•The altered proteins may serve as valuable markers of infection in the testis.</description><subject>Aeromonas salmonicida</subject><subject>Fish</subject><subject>Infection</subject><subject>Proteome</subject><subject>Reproductive tract</subject><subject>Semen</subject><issn>1050-4648</issn><issn>1095-9947</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kM1O7DAMhSsEEr8PwC5LNi1J06ZTsUKIPwmJu7iso0zigkdNU-LMSPMMvDSp5q6vsohln3Nkf0VxLXgluFC3m2ogrGpe1xXvKi76o-JM8L4t-77pjpe65WWjmtVpcU604ZwrqfhZ8fMnhgTBo2VmMuOekFgYmDVxZgQec4_NoyFv2BzDDh0Qw4nw8ystRQosfQFD77cTsAg0h4mA5fba2AQRsx2nAWzCMC3Bi9qbcdHmPLfNgx0w2lMCf1mcDGYkuPr3XxQfT49_H17Kt_fn14f7t9JKLlPpnIA1NFKsAMCYtQMFfd3mJ1snm8ENTeeg7hqrWtW1YCDLrRCy7gAG4-RFcXPIzRt8b4GS9kgWxtFMELaka9UL3qyUklkqDlIbA1GEQc8RvYl7LbhewOuNzuD1Al7zTmfw2XN38EC-YYcQNVmEyYLDmEFoF_A_7l9d55DN</recordid><startdate>202208</startdate><enddate>202208</enddate><creator>Dietrich, Mariola A.</creator><creator>Adamek, Mikołaj</creator><creator>Teitge, Felix</creator><creator>Teich, Lukas</creator><creator>Jung-Schroers, Verena</creator><creator>Malinowska, Agata</creator><creator>Świderska, Bianka</creator><creator>Rakus, Krzysztof</creator><creator>Kodzik, Natalia</creator><creator>Chadzińska, Magdalena</creator><creator>Karol, Halina</creator><creator>Liszewska, Ewa</creator><creator>Ciereszko, Andrzej</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-2525-0941</orcidid><orcidid>https://orcid.org/0000-0001-6599-901X</orcidid><orcidid>https://orcid.org/0000-0003-4890-3164</orcidid><orcidid>https://orcid.org/0000-0002-2628-2611</orcidid><orcidid>https://orcid.org/0000-0002-9373-4008</orcidid></search><sort><creationdate>202208</creationdate><title>Proteomic analysis of carp seminal plasma provides insights into the immune response to bacterial infection of the male reproductive system</title><author>Dietrich, Mariola A. ; Adamek, Mikołaj ; Teitge, Felix ; Teich, Lukas ; Jung-Schroers, Verena ; Malinowska, Agata ; Świderska, Bianka ; Rakus, Krzysztof ; Kodzik, Natalia ; Chadzińska, Magdalena ; Karol, Halina ; Liszewska, Ewa ; Ciereszko, Andrzej</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c303t-dd1ebe4318eeeaabde6e92525235d34fdf47de274c65675eaeebec11327eefad3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aeromonas salmonicida</topic><topic>Fish</topic><topic>Infection</topic><topic>Proteome</topic><topic>Reproductive tract</topic><topic>Semen</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dietrich, Mariola A.</creatorcontrib><creatorcontrib>Adamek, Mikołaj</creatorcontrib><creatorcontrib>Teitge, Felix</creatorcontrib><creatorcontrib>Teich, Lukas</creatorcontrib><creatorcontrib>Jung-Schroers, Verena</creatorcontrib><creatorcontrib>Malinowska, Agata</creatorcontrib><creatorcontrib>Świderska, Bianka</creatorcontrib><creatorcontrib>Rakus, Krzysztof</creatorcontrib><creatorcontrib>Kodzik, Natalia</creatorcontrib><creatorcontrib>Chadzińska, Magdalena</creatorcontrib><creatorcontrib>Karol, Halina</creatorcontrib><creatorcontrib>Liszewska, Ewa</creatorcontrib><creatorcontrib>Ciereszko, Andrzej</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Fish & shellfish immunology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dietrich, Mariola A.</au><au>Adamek, Mikołaj</au><au>Teitge, Felix</au><au>Teich, Lukas</au><au>Jung-Schroers, Verena</au><au>Malinowska, Agata</au><au>Świderska, Bianka</au><au>Rakus, Krzysztof</au><au>Kodzik, Natalia</au><au>Chadzińska, Magdalena</au><au>Karol, Halina</au><au>Liszewska, Ewa</au><au>Ciereszko, Andrzej</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Proteomic analysis of carp seminal plasma provides insights into the immune response to bacterial infection of the male reproductive system</atitle><jtitle>Fish & shellfish immunology</jtitle><date>2022-08</date><risdate>2022</risdate><volume>127</volume><spage>822</spage><epage>835</epage><pages>822-835</pages><issn>1050-4648</issn><eissn>1095-9947</eissn><abstract>Aeromonas salmonicida is recognized as a significant bacterial pathogen in ulcerative disease of cyprinid fish. However, the mechanism of immunity to these bacteria in common carp is still not well understood, especially the immune regulation in the gonad to bacterial infection. The aims of our study were to analyze changes in the seminal plasma proteome following A. salmonicida infection in carp males. The observed pathological changes in the tissue (liver, spleen, kidney and testis) morphology and upregulation of immune-related genes (tnfa2, il6a) confirmed the successful infection challenge. Using mass spectrometry-based label-free quantitative proteomics, we identified 1402 seminal plasma proteins, and 44 proteins (20 up- and 24 downregulated) were found to be differentially abundant between infected and control males. Most differentially abundant proteins were involved in the immune response mechanisms, such as acute phase response, complement activation and coagulation, inflammation, lipid metabolism, cell-cell and cell-matrix adhesion, creatine-phosphate biosynthesis and germ cell-Sertoli cell junction signaling. Bacterial infection also caused profound changes in expression of selected genes in the testis and hematopoietic organs, which contributed to changes in seminal proteins. The altered seminal proteins and bacterial proteins in seminal plasma may serve as valuable markers of infection in the testis.
•A. salmonicida infection affects carp seminal plasma proteome.•Infection alters proteins involved in innate immunity, lipid and energy metabolism.•Infection causes changes in gene expression in the testis and hematopoietic organs.•A. salmonicida and/or its components cross the blood-testis barrier and enter the testis.•The altered proteins may serve as valuable markers of infection in the testis.</abstract><pub>Elsevier Ltd</pub><doi>10.1016/j.fsi.2022.07.019</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-2525-0941</orcidid><orcidid>https://orcid.org/0000-0001-6599-901X</orcidid><orcidid>https://orcid.org/0000-0003-4890-3164</orcidid><orcidid>https://orcid.org/0000-0002-2628-2611</orcidid><orcidid>https://orcid.org/0000-0002-9373-4008</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aeromonas salmonicida Fish Infection Proteome Reproductive tract Semen |
title | Proteomic analysis of carp seminal plasma provides insights into the immune response to bacterial infection of the male reproductive system |
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