Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice
The impacts of metabolomic changes (reduced short-chain-fatty acids; SCFAs) in uremic condition is not fully understood. Once daily Candida gavage with or without probiotics (different times of administration) for 1 week prior to bilateral nephrectomy (Bil Nep) in 8-week-old C57BL6 mice as the possi...
Main Authors: | , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2023-03-01
|
Series: | Frontiers in Immunology |
Subjects: | |
Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1131447/full |
_version_ | 1811157731040559104 |
---|---|
author | Wiwat Chancharoenthana Wiwat Chancharoenthana Supitcha Kamolratanakul Supitcha Kamolratanakul Peerapat Visitchanakun Supistha Sontidejkul Thanya Cheibchalard Thanya Cheibchalard Naraporn Somboonna Naraporn Somboonna Sarn Settachaimongkon Asada Leelahavanichkul |
author_facet | Wiwat Chancharoenthana Wiwat Chancharoenthana Supitcha Kamolratanakul Supitcha Kamolratanakul Peerapat Visitchanakun Supistha Sontidejkul Thanya Cheibchalard Thanya Cheibchalard Naraporn Somboonna Naraporn Somboonna Sarn Settachaimongkon Asada Leelahavanichkul |
author_sort | Wiwat Chancharoenthana |
collection | DOAJ |
description | The impacts of metabolomic changes (reduced short-chain-fatty acids; SCFAs) in uremic condition is not fully understood. Once daily Candida gavage with or without probiotics (different times of administration) for 1 week prior to bilateral nephrectomy (Bil Nep) in 8-week-old C57BL6 mice as the possible models more resemble human conditions were performed. Candida-administered Bil Nep mice demonstrated more severe conditions than Bil Nep alone as indicated by mortality (n = 10/group) and other 48 h parameters (n = 6-8/group), including serum cytokines, leaky gut (FITC-dextran assay, endotoxemia, serum beta-glucan, and loss of Zona-occludens-1), and dysbiosis (increased Enterobacteriaceae with decreased diversity in microbiome analysis) (n = 3/group for fecal microbiome) without the difference in uremia (serum creatinine). With nuclear magnetic resonance metabolome analysis (n = 3-5/group), Bil Nep reduced fecal butyric (and propionic) acid and blood 3-hydroxy butyrate compared with sham and Candida-Bil Nep altered metabolomic patterns compared with Bil Nep alone. Then, Lacticaseibacillus rhamnosus dfa1 (SCFA-producing Lacticaseibacilli) (n = 8/group) attenuated the model severity (mortality, leaky gut, serum cytokines, and increased fecal butyrate) of Bil Nep mice (n = 6/group) (regardless of Candida). In enterocytes (Caco-2 cells), butyrate attenuated injury induced by indoxyl sulfate (a gut-derived uremic toxin) as indicated by transepithelial electrical resistance, supernatant IL-8, NFκB expression, and cell energy status (mitochondria and glycolysis activities by extracellular flux analysis). In conclusion, the reduced butyrate by uremia was not enhanced by Candida administration; however, the presence of Candida in the gut induced a leaky gut that was attenuated by SCFA-producing probiotics. Our data support the use of probiotics in uremia. |
first_indexed | 2024-04-10T05:12:16Z |
format | Article |
id | doaj.art-0e621195c9b349819498eb5b489a373b |
institution | Directory Open Access Journal |
issn | 1664-3224 |
language | English |
last_indexed | 2024-04-10T05:12:16Z |
publishDate | 2023-03-01 |
publisher | Frontiers Media S.A. |
record_format | Article |
series | Frontiers in Immunology |
spelling | doaj.art-0e621195c9b349819498eb5b489a373b2023-03-09T06:26:11ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-03-011410.3389/fimmu.2023.11314471131447Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy miceWiwat Chancharoenthana0Wiwat Chancharoenthana1Supitcha Kamolratanakul2Supitcha Kamolratanakul3Peerapat Visitchanakun4Supistha Sontidejkul5Thanya Cheibchalard6Thanya Cheibchalard7Naraporn Somboonna8Naraporn Somboonna9Sarn Settachaimongkon10Asada Leelahavanichkul11Department of Clinical Tropical Medicine, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandTropical Immunology and Translational Research Unit (TITRU), Department of Clinical Tropical Medicine, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandDepartment of Clinical Tropical Medicine, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandTropical Immunology and Translational Research Unit (TITRU), Department of Clinical Tropical Medicine, Faculty of Tropical Medicine, Mahidol University, Bangkok, ThailandCenter of Excellence on Translational Research in Inflammatory and Immunology (CETRII), Department of Microbiology, Chulalongkorn University, Bangkok, ThailandCenter of Excellence on Translational Research in Inflammatory and Immunology (CETRII), Department of Microbiology, Chulalongkorn University, Bangkok, ThailandProgram in Biotechnology, Faculty of Science, Chulalongkorn University, Bangkok, ThailandDepartment of Microbiology, Faculty of Science, Chulalongkorn University, Bangkok, ThailandDepartment of Microbiology, Faculty of Science, Chulalongkorn University, Bangkok, ThailandMicrobiome Research Unit for Probiotics in Food and Cosmetics, Chulalongkorn University, Bangkok, ThailandDepartment of Food Technology, Faculty of Science, Chulalongkorn University, Bangkok, ThailandCenter of Excellence on Translational Research in Inflammatory and Immunology (CETRII), Department of Microbiology, Chulalongkorn University, Bangkok, ThailandThe impacts of metabolomic changes (reduced short-chain-fatty acids; SCFAs) in uremic condition is not fully understood. Once daily Candida gavage with or without probiotics (different times of administration) for 1 week prior to bilateral nephrectomy (Bil Nep) in 8-week-old C57BL6 mice as the possible models more resemble human conditions were performed. Candida-administered Bil Nep mice demonstrated more severe conditions than Bil Nep alone as indicated by mortality (n = 10/group) and other 48 h parameters (n = 6-8/group), including serum cytokines, leaky gut (FITC-dextran assay, endotoxemia, serum beta-glucan, and loss of Zona-occludens-1), and dysbiosis (increased Enterobacteriaceae with decreased diversity in microbiome analysis) (n = 3/group for fecal microbiome) without the difference in uremia (serum creatinine). With nuclear magnetic resonance metabolome analysis (n = 3-5/group), Bil Nep reduced fecal butyric (and propionic) acid and blood 3-hydroxy butyrate compared with sham and Candida-Bil Nep altered metabolomic patterns compared with Bil Nep alone. Then, Lacticaseibacillus rhamnosus dfa1 (SCFA-producing Lacticaseibacilli) (n = 8/group) attenuated the model severity (mortality, leaky gut, serum cytokines, and increased fecal butyrate) of Bil Nep mice (n = 6/group) (regardless of Candida). In enterocytes (Caco-2 cells), butyrate attenuated injury induced by indoxyl sulfate (a gut-derived uremic toxin) as indicated by transepithelial electrical resistance, supernatant IL-8, NFκB expression, and cell energy status (mitochondria and glycolysis activities by extracellular flux analysis). In conclusion, the reduced butyrate by uremia was not enhanced by Candida administration; however, the presence of Candida in the gut induced a leaky gut that was attenuated by SCFA-producing probiotics. Our data support the use of probiotics in uremia.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1131447/fulluremiamicrobiomeshort-chain fatty acidfungikidney |
spellingShingle | Wiwat Chancharoenthana Wiwat Chancharoenthana Supitcha Kamolratanakul Supitcha Kamolratanakul Peerapat Visitchanakun Supistha Sontidejkul Thanya Cheibchalard Thanya Cheibchalard Naraporn Somboonna Naraporn Somboonna Sarn Settachaimongkon Asada Leelahavanichkul Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice Frontiers in Immunology uremia microbiome short-chain fatty acid fungi kidney |
title | Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice |
title_full | Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice |
title_fullStr | Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice |
title_full_unstemmed | Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice |
title_short | Lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in Candida-administered bilateral nephrectomy mice |
title_sort | lacticaseibacilli attenuated fecal dysbiosis and metabolome changes in candida administered bilateral nephrectomy mice |
topic | uremia microbiome short-chain fatty acid fungi kidney |
url | https://www.frontiersin.org/articles/10.3389/fimmu.2023.1131447/full |
work_keys_str_mv | AT wiwatchancharoenthana lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT wiwatchancharoenthana lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT supitchakamolratanakul lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT supitchakamolratanakul lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT peerapatvisitchanakun lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT supisthasontidejkul lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT thanyacheibchalard lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT thanyacheibchalard lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT narapornsomboonna lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT narapornsomboonna lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT sarnsettachaimongkon lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice AT asadaleelahavanichkul lacticaseibacilliattenuatedfecaldysbiosisandmetabolomechangesincandidaadministeredbilateralnephrectomymice |