IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon
B cells of teleost fish differentiate in the head kidney, and spleen, and either remain in the lymphatic organs or move to the blood and peripheral tissues. There is limited knowledge about piscine B cell traffic to sites of vaccination and infection and their functional roles at these sites. In thi...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2020-08-01
|
| Series: | Vaccines |
| Subjects: | |
| Online Access: | https://www.mdpi.com/2076-393X/8/3/493 |
| _version_ | 1797555079295795200 |
|---|---|
| author | Anne Flore Bakke Håvard Bjørgen Erling Olaf Koppang Petter Frost Sergey Afanasyev Preben Boysen Aleksei Krasnov Hege Lund |
| author_facet | Anne Flore Bakke Håvard Bjørgen Erling Olaf Koppang Petter Frost Sergey Afanasyev Preben Boysen Aleksei Krasnov Hege Lund |
| author_sort | Anne Flore Bakke |
| collection | DOAJ |
| description | B cells of teleost fish differentiate in the head kidney, and spleen, and either remain in the lymphatic organs or move to the blood and peripheral tissues. There is limited knowledge about piscine B cell traffic to sites of vaccination and infection and their functional roles at these sites. In this work, we examined the traffic of B cells in Atlantic salmon challenged with salmonid alphavirus (SAV). In situ hybridization (RNAScope) showed increased numbers of immunoglobin (Ig)M<sup>+</sup> and IgT<sup>+</sup> B cells in the heart in response to SAV challenge, with IgM<sup>+</sup> B cells being most abundant. An increase in IgT<sup>+</sup> B cells was also evident, indicating a role of IgT<sup>+</sup> B cells in nonmucosal tissues and systemic viral infections. After infection, B cells were mainly found in the <i>stratum spongiosum</i> of the cardiac ventricle, colocalizing with virus-infected myocardial-like cells. From sequencing the variable region of IgM in the main target organ (heart) and comparing it with a major lymphatic organ (the spleen), co-occurrence in antibody repertoires indicated a transfer of B cells from the spleen to the heart, as well as earlier recruitment of B cells to the heart in vaccinated fish compared to those that were unvaccinated. Transcriptome analyses performed at 21 days post-challenge suggested higher expression of multiple mediators of inflammation and lymphocyte-specific genes in unvaccinated compared to vaccinated fish, in parallel with a massive suppression of genes involved in heart contraction, metabolism, and development of tissue. The adaptive responses to SAV in vaccinated salmon appeared to alleviate the disease. Altogether, these results suggest that migration of B cells from lymphatic organs to sites of infection is an important part of the adaptive immune response of Atlantic salmon to SAV. |
| first_indexed | 2024-03-10T16:41:13Z |
| format | Article |
| id | doaj.art-d6528940a0d4480887432ec06c442397 |
| institution | Directory Open Access Journal |
| issn | 2076-393X |
| language | English |
| last_indexed | 2024-03-10T16:41:13Z |
| publishDate | 2020-08-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Vaccines |
| spelling | doaj.art-d6528940a0d4480887432ec06c4423972023-11-20T12:02:19ZengMDPI AGVaccines2076-393X2020-08-018349310.3390/vaccines8030493IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic SalmonAnne Flore Bakke0Håvard Bjørgen1Erling Olaf Koppang2Petter Frost3Sergey Afanasyev4Preben Boysen5Aleksei Krasnov6Hege Lund7Faculty of Veterinary Medicine, Norwegian University of Life Sciences (NMBU), Ullevålsveien 72, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences (NMBU), Ullevålsveien 72, 0454 Oslo, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences (NMBU), Ullevålsveien 72, 0454 Oslo, NorwayMSD Animal Health Innovation AD, Thormøhlens Gate 55, 5006 Bergen, NorwayI. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Torez 44, Saint-Petersburg 194223, RussiaFaculty of Veterinary Medicine, Norwegian University of Life Sciences (NMBU), Ullevålsveien 72, 0454 Oslo, NorwayNofima AS, Osloveien 1, 1433 Ås, NorwayFaculty of Veterinary Medicine, Norwegian University of Life Sciences (NMBU), Ullevålsveien 72, 0454 Oslo, NorwayB cells of teleost fish differentiate in the head kidney, and spleen, and either remain in the lymphatic organs or move to the blood and peripheral tissues. There is limited knowledge about piscine B cell traffic to sites of vaccination and infection and their functional roles at these sites. In this work, we examined the traffic of B cells in Atlantic salmon challenged with salmonid alphavirus (SAV). In situ hybridization (RNAScope) showed increased numbers of immunoglobin (Ig)M<sup>+</sup> and IgT<sup>+</sup> B cells in the heart in response to SAV challenge, with IgM<sup>+</sup> B cells being most abundant. An increase in IgT<sup>+</sup> B cells was also evident, indicating a role of IgT<sup>+</sup> B cells in nonmucosal tissues and systemic viral infections. After infection, B cells were mainly found in the <i>stratum spongiosum</i> of the cardiac ventricle, colocalizing with virus-infected myocardial-like cells. From sequencing the variable region of IgM in the main target organ (heart) and comparing it with a major lymphatic organ (the spleen), co-occurrence in antibody repertoires indicated a transfer of B cells from the spleen to the heart, as well as earlier recruitment of B cells to the heart in vaccinated fish compared to those that were unvaccinated. Transcriptome analyses performed at 21 days post-challenge suggested higher expression of multiple mediators of inflammation and lymphocyte-specific genes in unvaccinated compared to vaccinated fish, in parallel with a massive suppression of genes involved in heart contraction, metabolism, and development of tissue. The adaptive responses to SAV in vaccinated salmon appeared to alleviate the disease. Altogether, these results suggest that migration of B cells from lymphatic organs to sites of infection is an important part of the adaptive immune response of Atlantic salmon to SAV.https://www.mdpi.com/2076-393X/8/3/493Atlantic salmonB cellssalmon alphavirusin situ hybridizationIgM sequencingtranscriptome |
| spellingShingle | Anne Flore Bakke Håvard Bjørgen Erling Olaf Koppang Petter Frost Sergey Afanasyev Preben Boysen Aleksei Krasnov Hege Lund IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon Vaccines Atlantic salmon B cells salmon alphavirus in situ hybridization IgM sequencing transcriptome |
| title | IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon |
| title_full | IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon |
| title_fullStr | IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon |
| title_full_unstemmed | IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon |
| title_short | IgM+ and IgT+ B Cell Traffic to the Heart during SAV Infection in Atlantic Salmon |
| title_sort | igm and igt b cell traffic to the heart during sav infection in atlantic salmon |
| topic | Atlantic salmon B cells salmon alphavirus in situ hybridization IgM sequencing transcriptome |
| url | https://www.mdpi.com/2076-393X/8/3/493 |
| work_keys_str_mv | AT anneflorebakke igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT havardbjørgen igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT erlingolafkoppang igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT petterfrost igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT sergeyafanasyev igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT prebenboysen igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT alekseikrasnov igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon AT hegelund igmandigtbcelltraffictotheheartduringsavinfectioninatlanticsalmon |