L-methionine supplementation modulates IgM+ B cell responses in rainbow trout
The interest in dietary amino acids (AAs) as potential immunomodulators has been growing the recent years, since specific AAs are known to regulate key metabolic pathways of the immune response or increase the synthesis of some immune-related proteins. Methionine, tryptophan and lysine are among the...
| Main Authors: | , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-10-01
|
| Series: | Frontiers in Immunology |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1264228/full |
| _version_ | 1797662906646528000 |
|---|---|
| author | Diana Martín M. Camino Ordás Inês Carvalho Inês Carvalho Patricia Díaz-Rosales Noelia Nuñez-Ortiz Samuel Vicente-Gil Aitor Arrogante Carlos Zarza Marina Machado Benjamín Costas Benjamín Costas Carolina Tafalla |
| author_facet | Diana Martín M. Camino Ordás Inês Carvalho Inês Carvalho Patricia Díaz-Rosales Noelia Nuñez-Ortiz Samuel Vicente-Gil Aitor Arrogante Carlos Zarza Marina Machado Benjamín Costas Benjamín Costas Carolina Tafalla |
| author_sort | Diana Martín |
| collection | DOAJ |
| description | The interest in dietary amino acids (AAs) as potential immunomodulators has been growing the recent years, since specific AAs are known to regulate key metabolic pathways of the immune response or increase the synthesis of some immune-related proteins. Methionine, tryptophan and lysine are among the ten essential AAs for fish, meaning that they cannot be produced endogenously and must be provided through the diet. To date, although dietary supplementation of fish with some of these AAs has been shown to have positive effects on some innate immune parameters and disease resistance, the effects that these AAs provoke on cells of the adaptive immune system remained unexplored. Hence, in the current study, we have investigated the effects of these three AAs on the functionality of rainbow trout (Oncorhynchus mykiss) IgM+ B cells. For this, splenic leukocytes were isolated from untreated adult rainbow trout and incubated in culture media additionally supplemented with different doses of methionine, tryptophan or lysine in the presence or absence of the model antigen TNP-LPS (2,4,6-trinitrophenyl hapten conjugated to lipopolysaccharide). The survival, IgM secreting capacity and proliferation of IgM+ B cells was then studied. In the case of methionine, the phagocytic capacity of IgM+ B cells was also determined. Our results demonstrate that methionine supplementation significantly increases the proliferative effects provoked by TNP-LPS and also up-regulates the number of cells secreting IgM, whereas tryptophan or lysine have either minor or even negative effects on rainbow trout IgM+ B cells. This increase in the number of IgM-secreting cells in response to methionine surplus was further verified in a feeding experiment, in which the beneficial effects of methionine on the specific response to anal immunization were also confirmed. The results presented demonstrate the beneficial effects of dietary supplementation with methionine on the adaptive immune responses of fish. |
| first_indexed | 2024-03-11T19:06:53Z |
| format | Article |
| id | doaj.art-041ab9a452b14436b0156e56eaa46c4b |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-03-11T19:06:53Z |
| publishDate | 2023-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-041ab9a452b14436b0156e56eaa46c4b2023-10-10T06:54:42ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-10-011410.3389/fimmu.2023.12642281264228L-methionine supplementation modulates IgM+ B cell responses in rainbow troutDiana Martín0M. Camino Ordás1Inês Carvalho2Inês Carvalho3Patricia Díaz-Rosales4Noelia Nuñez-Ortiz5Samuel Vicente-Gil6Aitor Arrogante7Carlos Zarza8Marina Machado9Benjamín Costas10Benjamín Costas11Carolina Tafalla12Fish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainFish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainCentro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR), Universidade do Porto, Matosinhos, PortugalInstituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Porto, PortugalFish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainFish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainFish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainFish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainSkretting Aquaculture Innovation, Stavanger, NorwayCentro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR), Universidade do Porto, Matosinhos, PortugalCentro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR), Universidade do Porto, Matosinhos, PortugalInstituto de Ciências Biomédicas Abel Salazar (ICBAS), Universidade do Porto, Porto, PortugalFish Immunology and Pathology Laboratory, Animal Health and Research Center (CISA), National Institute for Agricultural and Food Research and Technology (INIA), Spanish National Research Council (CSIC), Madrid, SpainThe interest in dietary amino acids (AAs) as potential immunomodulators has been growing the recent years, since specific AAs are known to regulate key metabolic pathways of the immune response or increase the synthesis of some immune-related proteins. Methionine, tryptophan and lysine are among the ten essential AAs for fish, meaning that they cannot be produced endogenously and must be provided through the diet. To date, although dietary supplementation of fish with some of these AAs has been shown to have positive effects on some innate immune parameters and disease resistance, the effects that these AAs provoke on cells of the adaptive immune system remained unexplored. Hence, in the current study, we have investigated the effects of these three AAs on the functionality of rainbow trout (Oncorhynchus mykiss) IgM+ B cells. For this, splenic leukocytes were isolated from untreated adult rainbow trout and incubated in culture media additionally supplemented with different doses of methionine, tryptophan or lysine in the presence or absence of the model antigen TNP-LPS (2,4,6-trinitrophenyl hapten conjugated to lipopolysaccharide). The survival, IgM secreting capacity and proliferation of IgM+ B cells was then studied. In the case of methionine, the phagocytic capacity of IgM+ B cells was also determined. Our results demonstrate that methionine supplementation significantly increases the proliferative effects provoked by TNP-LPS and also up-regulates the number of cells secreting IgM, whereas tryptophan or lysine have either minor or even negative effects on rainbow trout IgM+ B cells. This increase in the number of IgM-secreting cells in response to methionine surplus was further verified in a feeding experiment, in which the beneficial effects of methionine on the specific response to anal immunization were also confirmed. The results presented demonstrate the beneficial effects of dietary supplementation with methionine on the adaptive immune responses of fish.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1264228/fullamino acidsmethioninetryptophanlysineIgM + B cellsrainbow trout |
| spellingShingle | Diana Martín M. Camino Ordás Inês Carvalho Inês Carvalho Patricia Díaz-Rosales Noelia Nuñez-Ortiz Samuel Vicente-Gil Aitor Arrogante Carlos Zarza Marina Machado Benjamín Costas Benjamín Costas Carolina Tafalla L-methionine supplementation modulates IgM+ B cell responses in rainbow trout Frontiers in Immunology amino acids methionine tryptophan lysine IgM + B cells rainbow trout |
| title | L-methionine supplementation modulates IgM+ B cell responses in rainbow trout |
| title_full | L-methionine supplementation modulates IgM+ B cell responses in rainbow trout |
| title_fullStr | L-methionine supplementation modulates IgM+ B cell responses in rainbow trout |
| title_full_unstemmed | L-methionine supplementation modulates IgM+ B cell responses in rainbow trout |
| title_short | L-methionine supplementation modulates IgM+ B cell responses in rainbow trout |
| title_sort | l methionine supplementation modulates igm b cell responses in rainbow trout |
| topic | amino acids methionine tryptophan lysine IgM + B cells rainbow trout |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1264228/full |
| work_keys_str_mv | AT dianamartin lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT mcaminoordas lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT inescarvalho lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT inescarvalho lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT patriciadiazrosales lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT noelianunezortiz lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT samuelvicentegil lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT aitorarrogante lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT carloszarza lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT marinamachado lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT benjamincostas lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT benjamincostas lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout AT carolinatafalla lmethioninesupplementationmodulatesigmbcellresponsesinrainbowtrout |