The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation

Clostridium butyricum is known as a probiotic butyric acid bacterium that can improve the intestinal environment. In this study, we isolated a new strain of C. butyricum from infant feces and evaluated its physiological characteristics and antiviral efficacy by modulating the innate immune responses...

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Main Authors: Kiramage Chathuranga, Yeseul Shin, Md Bashir Uddin, Jayoung Paek, W. A. Gayan Chathuranga, Yebin Seong, Lu Bai, Hongik Kim, Jeong Hwan Shin, Young-Hyo Chang, Jong-Soo Lee
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1242183/full
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author Kiramage Chathuranga
Yeseul Shin
Md Bashir Uddin
Md Bashir Uddin
Md Bashir Uddin
Jayoung Paek
W. A. Gayan Chathuranga
Yebin Seong
Lu Bai
Hongik Kim
Jeong Hwan Shin
Young-Hyo Chang
Jong-Soo Lee
author_facet Kiramage Chathuranga
Yeseul Shin
Md Bashir Uddin
Md Bashir Uddin
Md Bashir Uddin
Jayoung Paek
W. A. Gayan Chathuranga
Yebin Seong
Lu Bai
Hongik Kim
Jeong Hwan Shin
Young-Hyo Chang
Jong-Soo Lee
author_sort Kiramage Chathuranga
collection DOAJ
description Clostridium butyricum is known as a probiotic butyric acid bacterium that can improve the intestinal environment. In this study, we isolated a new strain of C. butyricum from infant feces and evaluated its physiological characteristics and antiviral efficacy by modulating the innate immune responses in vitro and in vivo. The isolated C. butyricum S-45-5 showed typical characteristics of C. butyricum including bile acid resistance, antibacterial ability, and growth promotion of various lactic acid bacteria. As an antiviral effect, C. butyricum S-45-5 markedly reduced the replication of influenza A virus (PR8), Newcastle Disease Virus (NDV), and Herpes Simplex Virus (HSV) in RAW264.7 cells in vitro. This suppression can be explained by the induction of antiviral state in cells by the induction of antiviral, IFN-related genes and secretion of IFNs and pro-inflammatory cytokines. In vivo, oral administration of C. butyricum S-45-5 exhibited prophylactic effects on BALB/c mice against fatal doses of highly pathogenic mouse-adapted influenza A subtypes (H1N1, H3N2, and H9N2). Before challenge with influenza virus, C. butyricum S-45-5-treated BALB/c mice showed increased levels of IFN-β, IFN-γ, IL-6, and IL-12 in serum, the small intestine, and bronchoalveolar lavage fluid (BALF), which correlated with observed prophylactic effects. Interestingly, after challenge with influenza virus, C. butyricum S-45-5-treated BALB/c mice showed reduced levels of pro-inflammatory cytokines and relatively higher levels of anti-inflammatory cytokines at day 7 post-infection. Taken together, these findings suggest that C. butyricum S-45-5 plays an antiviral role in vitro and in vivo by inducing an antiviral state and affects immune modulation to alleviate local and systemic inflammatory responses caused by influenza virus infection. Our study provides the beneficial effects of the new C. butyricum S-45-5 with antiviral effects as a probiotic.
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spelling doaj.art-4a7a8b8cdaa6437d845f6e4a58d49a6d2023-10-10T04:57:38ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-10-011410.3389/fimmu.2023.12421831242183The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulationKiramage Chathuranga0Yeseul Shin1Md Bashir Uddin2Md Bashir Uddin3Md Bashir Uddin4Jayoung Paek5W. A. Gayan Chathuranga6Yebin Seong7Lu Bai8Hongik Kim9Jeong Hwan Shin10Young-Hyo Chang11Jong-Soo Lee12College of Veterinary Medicine, Chungnam National University, Daejeon, Republic of KoreaAccess to Genetic Resources and Benefit-Sharing (ABS) Research Support Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, Republic of KoreaCollege of Veterinary Medicine, Chungnam National University, Daejeon, Republic of KoreaDepartment of Medicine, Sylhet Agricultural University, Sylhet, BangladeshDepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, TX, United StatesAccess to Genetic Resources and Benefit-Sharing (ABS) Research Support Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, Republic of KoreaCollege of Veterinary Medicine, Chungnam National University, Daejeon, Republic of KoreaCollege of Veterinary Medicine, Chungnam National University, Daejeon, Republic of KoreaAccess to Genetic Resources and Benefit-Sharing (ABS) Research Support Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, Republic of KoreaResearch and Development Division, Vitabio, Inc., Daejeon, Republic of KoreaDepartment of Laboratory Medicine, Inje University College of Medicine, Busan, Republic of KoreaAccess to Genetic Resources and Benefit-Sharing (ABS) Research Support Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB), Daejeon, Republic of KoreaCollege of Veterinary Medicine, Chungnam National University, Daejeon, Republic of KoreaClostridium butyricum is known as a probiotic butyric acid bacterium that can improve the intestinal environment. In this study, we isolated a new strain of C. butyricum from infant feces and evaluated its physiological characteristics and antiviral efficacy by modulating the innate immune responses in vitro and in vivo. The isolated C. butyricum S-45-5 showed typical characteristics of C. butyricum including bile acid resistance, antibacterial ability, and growth promotion of various lactic acid bacteria. As an antiviral effect, C. butyricum S-45-5 markedly reduced the replication of influenza A virus (PR8), Newcastle Disease Virus (NDV), and Herpes Simplex Virus (HSV) in RAW264.7 cells in vitro. This suppression can be explained by the induction of antiviral state in cells by the induction of antiviral, IFN-related genes and secretion of IFNs and pro-inflammatory cytokines. In vivo, oral administration of C. butyricum S-45-5 exhibited prophylactic effects on BALB/c mice against fatal doses of highly pathogenic mouse-adapted influenza A subtypes (H1N1, H3N2, and H9N2). Before challenge with influenza virus, C. butyricum S-45-5-treated BALB/c mice showed increased levels of IFN-β, IFN-γ, IL-6, and IL-12 in serum, the small intestine, and bronchoalveolar lavage fluid (BALF), which correlated with observed prophylactic effects. Interestingly, after challenge with influenza virus, C. butyricum S-45-5-treated BALB/c mice showed reduced levels of pro-inflammatory cytokines and relatively higher levels of anti-inflammatory cytokines at day 7 post-infection. Taken together, these findings suggest that C. butyricum S-45-5 plays an antiviral role in vitro and in vivo by inducing an antiviral state and affects immune modulation to alleviate local and systemic inflammatory responses caused by influenza virus infection. Our study provides the beneficial effects of the new C. butyricum S-45-5 with antiviral effects as a probiotic.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1242183/fullClostridium butyricum S-45-5probioticsantiviral activityinterferoninfluenza virus
spellingShingle Kiramage Chathuranga
Yeseul Shin
Md Bashir Uddin
Md Bashir Uddin
Md Bashir Uddin
Jayoung Paek
W. A. Gayan Chathuranga
Yebin Seong
Lu Bai
Hongik Kim
Jeong Hwan Shin
Young-Hyo Chang
Jong-Soo Lee
The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation
Frontiers in Immunology
Clostridium butyricum S-45-5
probiotics
antiviral activity
interferon
influenza virus
title The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation
title_full The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation
title_fullStr The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation
title_full_unstemmed The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation
title_short The novel immunobiotic Clostridium butyricum S-45-5 displays broad-spectrum antiviral activity in vitro and in vivo by inducing immune modulation
title_sort novel immunobiotic clostridium butyricum s 45 5 displays broad spectrum antiviral activity in vitro and in vivo by inducing immune modulation
topic Clostridium butyricum S-45-5
probiotics
antiviral activity
interferon
influenza virus
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1242183/full
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