Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection
Macrophage polarization affects the progression of pathogenic bacterial infections. Lactobacillus is widely used to interact with macrophages and to exert specific immunomodulatory activities. In this study, we investigated the regulation of macrophage polarization against Salmonella enterica seroty...
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| Format: | Article |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.933550/full |
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| author | Bingjie Duan Bingjie Duan Bingjie Duan Ruihan Liu Ruihan Liu Ruihan Liu Yumeng Shi Yumeng Shi Yumeng Shi Anqi Sun Anqi Sun Anqi Sun Zhengxu Tang Zhengxu Tang Zhengxu Tang Chunfeng Wang Chunfeng Wang Chunfeng Wang Jingtao Hu Jingtao Hu Jingtao Hu |
| author_facet | Bingjie Duan Bingjie Duan Bingjie Duan Ruihan Liu Ruihan Liu Ruihan Liu Yumeng Shi Yumeng Shi Yumeng Shi Anqi Sun Anqi Sun Anqi Sun Zhengxu Tang Zhengxu Tang Zhengxu Tang Chunfeng Wang Chunfeng Wang Chunfeng Wang Jingtao Hu Jingtao Hu Jingtao Hu |
| author_sort | Bingjie Duan |
| collection | DOAJ |
| description | Macrophage polarization affects the progression of pathogenic bacterial infections. Lactobacillus is widely used to interact with macrophages and to exert specific immunomodulatory activities. In this study, we investigated the regulation of macrophage polarization against Salmonella enterica serotype Typhimurium (STM) by Lactobacillus plantarum JL01 (LP), to explore prevention and treatment strategies for salmonellosis. We assessed the in vitro differential polarization of RAW 264.7 macrophages and mouse bone marrow macrophages (BMMs) by LP against STM, by measuring protein and cytokine levels, and bactericidal activity. In addition, we assessed the protective effects of LP against STM by evaluating weight loss, survival, the burden of STM in tissues, the polarization of macrophages in the spleen and mesenteric lymph nodes (MLNs), intestinal histopathology, and cytokine production. LP slightly affected the polarization of RAW 264.7, a slight M1-skewing. LP promoted the RAW 264.7 bactericidal activity against STM. In BMMs, M1 polarization induced by LP was significantly lower than the M1-positive phenotype. The combination of LP with M1 synergistically improved M1 polarization and bactericidal activity against STM compared to the individual effects. LP promoted the activation of the NF-κB signaling pathway. Supplementation with the NF-κB inhibitor decreased M1 polarization induced by LP. We observed the protective effect of LP against STM in C57BL/6 mice, through a decrease in weight loss, mortality, STM burden in the liver, and promotion of macrophage M1 and M2 polarization in the spleen and MLNs; though M1 was higher, it did not cause inflammatory damage. In summary, LP can synergistically promote M1 polarization in combination with the M1 phenotype through the NF-κB signaling pathway and increases resistance against S. Typhimurium infection. These findings will lay the foundation for the prevention and treatment of S. Typhimurium infections in the future. |
| first_indexed | 2024-04-13T23:36:25Z |
| format | Article |
| id | doaj.art-a541c9bb22804e0eb93625ebeab0d9e8 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-04-13T23:36:25Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-a541c9bb22804e0eb93625ebeab0d9e82022-12-22T02:24:45ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-10-011310.3389/fmicb.2022.933550933550Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infectionBingjie Duan0Bingjie Duan1Bingjie Duan2Ruihan Liu3Ruihan Liu4Ruihan Liu5Yumeng Shi6Yumeng Shi7Yumeng Shi8Anqi Sun9Anqi Sun10Anqi Sun11Zhengxu Tang12Zhengxu Tang13Zhengxu Tang14Chunfeng Wang15Chunfeng Wang16Chunfeng Wang17Jingtao Hu18Jingtao Hu19Jingtao Hu20College of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaCollege of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaCollege of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaCollege of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaCollege of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaCollege of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaCollege of Animal Science and Technology, Jilin Agricultural University, Changchun, ChinaJilin Provincial Key Laboratory of Animal Microecology and Health Breeding, Changchun, ChinaKey Laboratory of Animal Production and Product Quality Safety of Ministry of Education, Changchun, ChinaMacrophage polarization affects the progression of pathogenic bacterial infections. Lactobacillus is widely used to interact with macrophages and to exert specific immunomodulatory activities. In this study, we investigated the regulation of macrophage polarization against Salmonella enterica serotype Typhimurium (STM) by Lactobacillus plantarum JL01 (LP), to explore prevention and treatment strategies for salmonellosis. We assessed the in vitro differential polarization of RAW 264.7 macrophages and mouse bone marrow macrophages (BMMs) by LP against STM, by measuring protein and cytokine levels, and bactericidal activity. In addition, we assessed the protective effects of LP against STM by evaluating weight loss, survival, the burden of STM in tissues, the polarization of macrophages in the spleen and mesenteric lymph nodes (MLNs), intestinal histopathology, and cytokine production. LP slightly affected the polarization of RAW 264.7, a slight M1-skewing. LP promoted the RAW 264.7 bactericidal activity against STM. In BMMs, M1 polarization induced by LP was significantly lower than the M1-positive phenotype. The combination of LP with M1 synergistically improved M1 polarization and bactericidal activity against STM compared to the individual effects. LP promoted the activation of the NF-κB signaling pathway. Supplementation with the NF-κB inhibitor decreased M1 polarization induced by LP. We observed the protective effect of LP against STM in C57BL/6 mice, through a decrease in weight loss, mortality, STM burden in the liver, and promotion of macrophage M1 and M2 polarization in the spleen and MLNs; though M1 was higher, it did not cause inflammatory damage. In summary, LP can synergistically promote M1 polarization in combination with the M1 phenotype through the NF-κB signaling pathway and increases resistance against S. Typhimurium infection. These findings will lay the foundation for the prevention and treatment of S. Typhimurium infections in the future.https://www.frontiersin.org/articles/10.3389/fmicb.2022.933550/fullLactobacillus plantarumS. Typhimuriummacrophage polarizationBMMsM1 |
| spellingShingle | Bingjie Duan Bingjie Duan Bingjie Duan Ruihan Liu Ruihan Liu Ruihan Liu Yumeng Shi Yumeng Shi Yumeng Shi Anqi Sun Anqi Sun Anqi Sun Zhengxu Tang Zhengxu Tang Zhengxu Tang Chunfeng Wang Chunfeng Wang Chunfeng Wang Jingtao Hu Jingtao Hu Jingtao Hu Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection Frontiers in Microbiology Lactobacillus plantarum S. Typhimurium macrophage polarization BMMs M1 |
| title | Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection |
| title_full | Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection |
| title_fullStr | Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection |
| title_full_unstemmed | Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection |
| title_short | Lactobacillus plantarum synergistically regulates M1 macrophage polarization in resistance against Salmonella enterica serovar Typhimurium infection |
| title_sort | lactobacillus plantarum synergistically regulates m1 macrophage polarization in resistance against salmonella enterica serovar typhimurium infection |
| topic | Lactobacillus plantarum S. Typhimurium macrophage polarization BMMs M1 |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.933550/full |
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