Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice
Influenza is a serious respiratory disease that continues to threaten global health. Mucosa-associated invariant T (MAIT) cells use T-cell receptors (TCRs) that recognize microbial riboflavin derived intermediates presented by the major histocompatibility complex (MHC) class I-like protein MR1. Ribo...
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Frontiers Media S.A.
2022-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.916580/full |
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| author | Ying Li Ying Li Ying Li Ying Li Chun-Wei Shi Chun-Wei Shi Chun-Wei Shi Chun-Wei Shi Yu-Ting Zhang Yu-Ting Zhang Yu-Ting Zhang Yu-Ting Zhang Hai-Bin Huang Hai-Bin Huang Hai-Bin Huang Hai-Bin Huang Yan-Long Jiang Yan-Long Jiang Yan-Long Jiang Yan-Long Jiang Jian-Zhong Wang Jian-Zhong Wang Jian-Zhong Wang Jian-Zhong Wang Xin Cao Xin Cao Xin Cao Xin Cao Nan Wang Nan Wang Nan Wang Nan Wang Yan Zeng Yan Zeng Yan Zeng Yan Zeng Gui-Lian Yang Gui-Lian Yang Gui-Lian Yang Gui-Lian Yang Wen-Tao Yang Wen-Tao Yang Wen-Tao Yang Wen-Tao Yang Chun-Feng Wang Chun-Feng Wang Chun-Feng Wang Chun-Feng Wang |
| author_facet | Ying Li Ying Li Ying Li Ying Li Chun-Wei Shi Chun-Wei Shi Chun-Wei Shi Chun-Wei Shi Yu-Ting Zhang Yu-Ting Zhang Yu-Ting Zhang Yu-Ting Zhang Hai-Bin Huang Hai-Bin Huang Hai-Bin Huang Hai-Bin Huang Yan-Long Jiang Yan-Long Jiang Yan-Long Jiang Yan-Long Jiang Jian-Zhong Wang Jian-Zhong Wang Jian-Zhong Wang Jian-Zhong Wang Xin Cao Xin Cao Xin Cao Xin Cao Nan Wang Nan Wang Nan Wang Nan Wang Yan Zeng Yan Zeng Yan Zeng Yan Zeng Gui-Lian Yang Gui-Lian Yang Gui-Lian Yang Gui-Lian Yang Wen-Tao Yang Wen-Tao Yang Wen-Tao Yang Wen-Tao Yang Chun-Feng Wang Chun-Feng Wang Chun-Feng Wang Chun-Feng Wang |
| author_sort | Ying Li |
| collection | DOAJ |
| description | Influenza is a serious respiratory disease that continues to threaten global health. Mucosa-associated invariant T (MAIT) cells use T-cell receptors (TCRs) that recognize microbial riboflavin derived intermediates presented by the major histocompatibility complex (MHC) class I-like protein MR1. Riboflavin synthesis is broadly conserved, but the roles or mechanisms of riboflavin in MR1–/– mouse influenza infection are not well understood. In our study, immunofluorescence techniques were applied to analyze the number and distribution of viruses in lung tissue. The amount of cytokine expression was assessed by flow cytometry (FCM), ELISA, and qPCR. The changes in the fecal flora of mice were evaluated based on amplicon sequencing of the 16S V3-V4 region. Our study showed that MAIT cell deficiency increased mortality and that riboflavin altered these effects in microbiota-depleted mice. The oral administration of riboflavin inhibited IL-1β, IL-17A, and IL-18 production but significantly increased the expression of IFN-γ, TNF-α, CCL2, CCL3, and CCL4 in a mouse model. The analysis of the mouse flora revealed that riboflavin treatment significantly increased the relative abundance of Akkermansia and Lactobacillus (p < 0.05) and decreased that of Bacteroides. In contrast, MR1–/– mice exhibited a concentrated aggregation of Bacteroides (p < 0.01), which indicated that MAIT cell deficiency reduced the diversity of the bacterial population. Our results define the functions of MAIT cells and riboflavin in resistance to influenza virus and suggest a potential role for riboflavin in enhancing MAIT cell immunity and the intestinal flora diversity. Gut populations can be expanded to enhance host resistance to influenza, and the results indicate novel interactions among viruses, MAIT cells, and the gut microbiota. |
| first_indexed | 2024-04-13T21:07:58Z |
| format | Article |
| id | doaj.art-d8be2f258483491390e0fccdc346340e |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T21:07:58Z |
| publishDate | 2022-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-d8be2f258483491390e0fccdc346340e2022-12-22T02:29:56ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-06-011310.3389/fmicb.2022.916580916580Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency MiceYing Li0Ying Li1Ying Li2Ying Li3Chun-Wei Shi4Chun-Wei Shi5Chun-Wei Shi6Chun-Wei Shi7Yu-Ting Zhang8Yu-Ting Zhang9Yu-Ting Zhang10Yu-Ting Zhang11Hai-Bin Huang12Hai-Bin Huang13Hai-Bin Huang14Hai-Bin Huang15Yan-Long Jiang16Yan-Long Jiang17Yan-Long Jiang18Yan-Long Jiang19Jian-Zhong Wang20Jian-Zhong Wang21Jian-Zhong Wang22Jian-Zhong Wang23Xin Cao24Xin Cao25Xin Cao26Xin Cao27Nan Wang28Nan Wang29Nan Wang30Nan Wang31Yan Zeng32Yan Zeng33Yan Zeng34Yan Zeng35Gui-Lian Yang36Gui-Lian Yang37Gui-Lian Yang38Gui-Lian Yang39Wen-Tao Yang40Wen-Tao Yang41Wen-Tao Yang42Wen-Tao Yang43Chun-Feng Wang44Chun-Feng Wang45Chun-Feng Wang46Chun-Feng Wang47College of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaCollege of Veterinary Medicine, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Healthy Breeding, Jilin Agricultural University, Changchun, ChinaJilin Provincial Engineering Research Center of Animal Probiotics, Jilin Agricultural University, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Jilin Agricultural University, Changchun, ChinaInfluenza is a serious respiratory disease that continues to threaten global health. Mucosa-associated invariant T (MAIT) cells use T-cell receptors (TCRs) that recognize microbial riboflavin derived intermediates presented by the major histocompatibility complex (MHC) class I-like protein MR1. Riboflavin synthesis is broadly conserved, but the roles or mechanisms of riboflavin in MR1–/– mouse influenza infection are not well understood. In our study, immunofluorescence techniques were applied to analyze the number and distribution of viruses in lung tissue. The amount of cytokine expression was assessed by flow cytometry (FCM), ELISA, and qPCR. The changes in the fecal flora of mice were evaluated based on amplicon sequencing of the 16S V3-V4 region. Our study showed that MAIT cell deficiency increased mortality and that riboflavin altered these effects in microbiota-depleted mice. The oral administration of riboflavin inhibited IL-1β, IL-17A, and IL-18 production but significantly increased the expression of IFN-γ, TNF-α, CCL2, CCL3, and CCL4 in a mouse model. The analysis of the mouse flora revealed that riboflavin treatment significantly increased the relative abundance of Akkermansia and Lactobacillus (p < 0.05) and decreased that of Bacteroides. In contrast, MR1–/– mice exhibited a concentrated aggregation of Bacteroides (p < 0.01), which indicated that MAIT cell deficiency reduced the diversity of the bacterial population. Our results define the functions of MAIT cells and riboflavin in resistance to influenza virus and suggest a potential role for riboflavin in enhancing MAIT cell immunity and the intestinal flora diversity. Gut populations can be expanded to enhance host resistance to influenza, and the results indicate novel interactions among viruses, MAIT cells, and the gut microbiota.https://www.frontiersin.org/articles/10.3389/fmicb.2022.916580/fullMAIT cellsriboflavincytokinesinfluenzagut microbiota |
| spellingShingle | Ying Li Ying Li Ying Li Ying Li Chun-Wei Shi Chun-Wei Shi Chun-Wei Shi Chun-Wei Shi Yu-Ting Zhang Yu-Ting Zhang Yu-Ting Zhang Yu-Ting Zhang Hai-Bin Huang Hai-Bin Huang Hai-Bin Huang Hai-Bin Huang Yan-Long Jiang Yan-Long Jiang Yan-Long Jiang Yan-Long Jiang Jian-Zhong Wang Jian-Zhong Wang Jian-Zhong Wang Jian-Zhong Wang Xin Cao Xin Cao Xin Cao Xin Cao Nan Wang Nan Wang Nan Wang Nan Wang Yan Zeng Yan Zeng Yan Zeng Yan Zeng Gui-Lian Yang Gui-Lian Yang Gui-Lian Yang Gui-Lian Yang Wen-Tao Yang Wen-Tao Yang Wen-Tao Yang Wen-Tao Yang Chun-Feng Wang Chun-Feng Wang Chun-Feng Wang Chun-Feng Wang Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice Frontiers in Microbiology MAIT cells riboflavin cytokines influenza gut microbiota |
| title | Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice |
| title_full | Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice |
| title_fullStr | Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice |
| title_full_unstemmed | Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice |
| title_short | Riboflavin Attenuates Influenza Virus Through Cytokine-Mediated Effects on the Diversity of the Gut Microbiota in MAIT Cell Deficiency Mice |
| title_sort | riboflavin attenuates influenza virus through cytokine mediated effects on the diversity of the gut microbiota in mait cell deficiency mice |
| topic | MAIT cells riboflavin cytokines influenza gut microbiota |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.916580/full |
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