Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes
IntroductionImmune function changes across the life course; the fetal immune system is characterised by tolerance while that of seniors is less able to respond effectively to antigens and is more pro-inflammatory than in younger adults. Lipids are involved centrally in immune function but there is l...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1079642/full |
| _version_ | 1811293594561019904 |
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| author | Annette L. West Johanna von Gerichten Nicola A. Irvine Elizabeth A. Miles Karen A. Lillycrop Philip C. Calder Philip C. Calder Barbara A. Fielding Graham C. Burdge |
| author_facet | Annette L. West Johanna von Gerichten Nicola A. Irvine Elizabeth A. Miles Karen A. Lillycrop Philip C. Calder Philip C. Calder Barbara A. Fielding Graham C. Burdge |
| author_sort | Annette L. West |
| collection | DOAJ |
| description | IntroductionImmune function changes across the life course; the fetal immune system is characterised by tolerance while that of seniors is less able to respond effectively to antigens and is more pro-inflammatory than in younger adults. Lipids are involved centrally in immune function but there is limited information about how T cell lipid metabolism changes during the life course.Methods and ResultsWe investigated whether life stage alters fatty acid composition, lipid droplet content and α-linolenic acid (18:3ω-3) metabolism in human fetal CD3+ T lymphocytes and in CD3+ T lymphocytes from adults (median 41 years) and seniors (median 70 years). Quiescent fetal T cells had higher saturated (SFA), monounsaturated fatty acid (MUFA), and ω-6 polyunsaturated fatty acid (PUFA) contents than adults or seniors. Activation-induced changes in fatty acid composition differed between life stages. The principal metabolic fates of [13C]18:3ω-3 were constitutive hydroxyoctadecatrienoic acid synthesis and β-oxidation and carbon recycling into SFA and MUFA. These processes declined progressively across the life course. Longer chain ω-3 PUFA synthesis was a relatively minor metabolic fate of 18:3ω-3 at all life stages. Fetal and adult T lymphocytes had similar lipid droplet contents, which were lower than in T cells from seniors. Variation in the lipid droplet content of adult T cells accounted for 62% of the variation in mitogen-induced CD69 expression, but there was no significant relationship in fetal cells or lymphocytes from seniors.DiscussionTogether these findings show that fatty acid metabolism in human T lymphocytes changes across the life course in a manner that may facilitate the adaptation of immune function to different life stages. |
| first_indexed | 2024-04-13T05:03:46Z |
| format | Article |
| id | doaj.art-adc829dcb3514a6e9c3b6ff1a052bb6a |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-13T05:03:46Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-adc829dcb3514a6e9c3b6ff1a052bb6a2022-12-22T03:01:14ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-12-011310.3389/fimmu.2022.10796421079642Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytesAnnette L. West0Johanna von Gerichten1Nicola A. Irvine2Elizabeth A. Miles3Karen A. Lillycrop4Philip C. Calder5Philip C. Calder6Barbara A. Fielding7Graham C. Burdge8School of Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, Hampshire, United KingdomDepartment of Nutritional Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, Surrey, United KingdomSchool of Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, Hampshire, United KingdomSchool of Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, Hampshire, United KingdomCentre for Biological Sciences, Faculty of Natural and Environmental Sciences, University of Southampton, Southampton, Hampshire, United KingdomSchool of Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, Hampshire, United KingdomNational Institute for Health and Care Research (NIHR) Southampton Biomedical Research Centre, University Hospital Southampton National Health Service (NHS) Foundation Trust and University of Southampton, Southampton, Hampshire, United KingdomDepartment of Nutritional Sciences, Faculty of Health and Medical Sciences, University of Surrey, Guildford, Surrey, United KingdomSchool of Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, Hampshire, United KingdomIntroductionImmune function changes across the life course; the fetal immune system is characterised by tolerance while that of seniors is less able to respond effectively to antigens and is more pro-inflammatory than in younger adults. Lipids are involved centrally in immune function but there is limited information about how T cell lipid metabolism changes during the life course.Methods and ResultsWe investigated whether life stage alters fatty acid composition, lipid droplet content and α-linolenic acid (18:3ω-3) metabolism in human fetal CD3+ T lymphocytes and in CD3+ T lymphocytes from adults (median 41 years) and seniors (median 70 years). Quiescent fetal T cells had higher saturated (SFA), monounsaturated fatty acid (MUFA), and ω-6 polyunsaturated fatty acid (PUFA) contents than adults or seniors. Activation-induced changes in fatty acid composition differed between life stages. The principal metabolic fates of [13C]18:3ω-3 were constitutive hydroxyoctadecatrienoic acid synthesis and β-oxidation and carbon recycling into SFA and MUFA. These processes declined progressively across the life course. Longer chain ω-3 PUFA synthesis was a relatively minor metabolic fate of 18:3ω-3 at all life stages. Fetal and adult T lymphocytes had similar lipid droplet contents, which were lower than in T cells from seniors. Variation in the lipid droplet content of adult T cells accounted for 62% of the variation in mitogen-induced CD69 expression, but there was no significant relationship in fetal cells or lymphocytes from seniors.DiscussionTogether these findings show that fatty acid metabolism in human T lymphocytes changes across the life course in a manner that may facilitate the adaptation of immune function to different life stages.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1079642/fullT lymphocyteessential fatty acidα-linolenic acidhydroxyoctadecadienoic acidslife courselipid droplet |
| spellingShingle | Annette L. West Johanna von Gerichten Nicola A. Irvine Elizabeth A. Miles Karen A. Lillycrop Philip C. Calder Philip C. Calder Barbara A. Fielding Graham C. Burdge Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes Frontiers in Immunology T lymphocyte essential fatty acid α-linolenic acid hydroxyoctadecadienoic acids life course lipid droplet |
| title | Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes |
| title_full | Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes |
| title_fullStr | Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes |
| title_full_unstemmed | Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes |
| title_short | Fatty acid composition and metabolic partitioning of α-linolenic acid are contingent on life stage in human CD3+ T lymphocytes |
| title_sort | fatty acid composition and metabolic partitioning of α linolenic acid are contingent on life stage in human cd3 t lymphocytes |
| topic | T lymphocyte essential fatty acid α-linolenic acid hydroxyoctadecadienoic acids life course lipid droplet |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1079642/full |
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