Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro
Memory-like responses in innate immune cells confer nonspecific protection against secondary exposures. A number of microbial agents have been found to induce enhanced or diminished recall responses in innate cells, however, studies investigating the ability of probiotic bacteria to trigger such eff...
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Taylor & Francis Group
2022-12-01
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| Series: | Gut Microbes |
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| Online Access: | https://www.tandfonline.com/doi/10.1080/19490976.2022.2045046 |
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| author | Gintare Lasaviciute Myriam Barz Marieke van der Heiden Claudia Arasa Kanwal Tariq Jaclyn Quin Ann-Kristin Östlund Farrants Eva Sverremark-Ekström |
| author_facet | Gintare Lasaviciute Myriam Barz Marieke van der Heiden Claudia Arasa Kanwal Tariq Jaclyn Quin Ann-Kristin Östlund Farrants Eva Sverremark-Ekström |
| author_sort | Gintare Lasaviciute |
| collection | DOAJ |
| description | Memory-like responses in innate immune cells confer nonspecific protection against secondary exposures. A number of microbial agents have been found to induce enhanced or diminished recall responses in innate cells, however, studies investigating the ability of probiotic bacteria to trigger such effects are lacking. Here, we show that priming of human monocytes with a secretome from the gut probiotic bacterium Limosilactobacillus (L.) reuteri induces a mixed secondary response phenotype in monocyte-derived dendritic cells (mo-DCs), with a strong IL-6 and IL-1β response but low TNFα, IL-23 and IL-27 secretion. Instead, blood DC priming with L. reuteri-secretome resembles a tolerant state upon secondary exposure. A similar pattern was found in conventional and gut-like (retinoic acid exposed) DCs, although retinoic acid hampered TNFα and IL-6 production and enrichment of histone modifications in L. reuteri-secretome primed mo-DC cultures. Further, we show that the memory-like phenotype of mo-DCs, induced by priming stimuli, is important for subsequent T helper (Th) cell differentiation pathways and might determine the inflammatory nature of Th cells. We also show enhanced recall responses characterized by robust inflammatory cytokines and lactate production in the gut-like mo-DCs derived from β-glucan primed monocytes. Such responses were accompanied with enriched histone modifications at the promoter of genes associated with a trained phenotype in myeloid cells. Altogether, we demonstrate that a gut commensal-derived secretome prompts recall responses in human DCs which differ from that induced by classical training agents such as β-glucan. Our results could be beneficial for future therapeutic interventions where T cell responses are needed to be modulated. |
| format | Article |
| id | doaj-art-ce3c1d59cc6347eebb7d495674185fd4 |
| institution | OA Journals |
| issn | 1949-0976 1949-0984 |
| language | English |
| publishDate | 2022-12-01 |
| publisher | Taylor & Francis Group |
| record_format | Article |
| series | Gut Microbes |
| spelling | doaj-art-ce3c1d59cc6347eebb7d495674185fd42025-08-20T02:38:10ZengTaylor & Francis GroupGut Microbes1949-09761949-09842022-12-0114110.1080/19490976.2022.2045046Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitroGintare Lasaviciute0Myriam Barz1Marieke van der Heiden2Claudia Arasa3Kanwal Tariq4Jaclyn Quin5Ann-Kristin Östlund Farrants6Eva Sverremark-Ekström7Department of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenCentral European Institute of Technology, Masaryk University, Brno, Czech RepublicDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm University, Stockholm, SwedenMemory-like responses in innate immune cells confer nonspecific protection against secondary exposures. A number of microbial agents have been found to induce enhanced or diminished recall responses in innate cells, however, studies investigating the ability of probiotic bacteria to trigger such effects are lacking. Here, we show that priming of human monocytes with a secretome from the gut probiotic bacterium Limosilactobacillus (L.) reuteri induces a mixed secondary response phenotype in monocyte-derived dendritic cells (mo-DCs), with a strong IL-6 and IL-1β response but low TNFα, IL-23 and IL-27 secretion. Instead, blood DC priming with L. reuteri-secretome resembles a tolerant state upon secondary exposure. A similar pattern was found in conventional and gut-like (retinoic acid exposed) DCs, although retinoic acid hampered TNFα and IL-6 production and enrichment of histone modifications in L. reuteri-secretome primed mo-DC cultures. Further, we show that the memory-like phenotype of mo-DCs, induced by priming stimuli, is important for subsequent T helper (Th) cell differentiation pathways and might determine the inflammatory nature of Th cells. We also show enhanced recall responses characterized by robust inflammatory cytokines and lactate production in the gut-like mo-DCs derived from β-glucan primed monocytes. Such responses were accompanied with enriched histone modifications at the promoter of genes associated with a trained phenotype in myeloid cells. Altogether, we demonstrate that a gut commensal-derived secretome prompts recall responses in human DCs which differ from that induced by classical training agents such as β-glucan. Our results could be beneficial for future therapeutic interventions where T cell responses are needed to be modulated.https://www.tandfonline.com/doi/10.1080/19490976.2022.2045046Limosilactobacillus reuteridendritic cellsT helper cellsinnate immune memoryepigenetics |
| spellingShingle | Gintare Lasaviciute Myriam Barz Marieke van der Heiden Claudia Arasa Kanwal Tariq Jaclyn Quin Ann-Kristin Östlund Farrants Eva Sverremark-Ekström Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro Gut Microbes Limosilactobacillus reuteri dendritic cells T helper cells innate immune memory epigenetics |
| title | Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro |
| title_full | Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro |
| title_fullStr | Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro |
| title_full_unstemmed | Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro |
| title_short | Gut commensal Limosilactobacillus reuteri induces atypical memory-like phenotype in human dendritic cells in vitro |
| title_sort | gut commensal limosilactobacillus reuteri induces atypical memory like phenotype in human dendritic cells in vitro |
| topic | Limosilactobacillus reuteri dendritic cells T helper cells innate immune memory epigenetics |
| url | https://www.tandfonline.com/doi/10.1080/19490976.2022.2045046 |
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