Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells

In lactic acid bacteria, the synthesis of exopolysaccharides (EPS) has been associated with some favorable technological properties as well as health-promoting benefits. Research works have shown the potential of EPS produced by lactobacilli to differentially modulate immune responses. However, most...

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Main Authors: Paulraj Kanmani, Leonardo Albarracin, Hisakazu Kobayashi, Elvira Maria Hebert, Lucila Saavedra, Ryoya Komatsu, Brian Gatica, Ayako Miyazaki, Wakako Ikeda-Ohtsubo, Yoshihito Suda, Hisashi Aso, Shintaro Egusa, Takashi Mishima, Alexis Salas-Burgos, Hideki Takahashi, Julio Villena, Haruki Kitazawa
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-09-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2018.02178/full
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author Paulraj Kanmani
Paulraj Kanmani
Leonardo Albarracin
Leonardo Albarracin
Leonardo Albarracin
Hisakazu Kobayashi
Hisakazu Kobayashi
Elvira Maria Hebert
Lucila Saavedra
Ryoya Komatsu
Ryoya Komatsu
Brian Gatica
Ayako Miyazaki
Wakako Ikeda-Ohtsubo
Wakako Ikeda-Ohtsubo
Yoshihito Suda
Hisashi Aso
Hisashi Aso
Shintaro Egusa
Takashi Mishima
Alexis Salas-Burgos
Hideki Takahashi
Hideki Takahashi
Julio Villena
Julio Villena
Haruki Kitazawa
Haruki Kitazawa
author_facet Paulraj Kanmani
Paulraj Kanmani
Leonardo Albarracin
Leonardo Albarracin
Leonardo Albarracin
Hisakazu Kobayashi
Hisakazu Kobayashi
Elvira Maria Hebert
Lucila Saavedra
Ryoya Komatsu
Ryoya Komatsu
Brian Gatica
Ayako Miyazaki
Wakako Ikeda-Ohtsubo
Wakako Ikeda-Ohtsubo
Yoshihito Suda
Hisashi Aso
Hisashi Aso
Shintaro Egusa
Takashi Mishima
Alexis Salas-Burgos
Hideki Takahashi
Hideki Takahashi
Julio Villena
Julio Villena
Haruki Kitazawa
Haruki Kitazawa
author_sort Paulraj Kanmani
collection DOAJ
description In lactic acid bacteria, the synthesis of exopolysaccharides (EPS) has been associated with some favorable technological properties as well as health-promoting benefits. Research works have shown the potential of EPS produced by lactobacilli to differentially modulate immune responses. However, most studies were performed in immune cells and few works have concentrated in the immunomodulatory activities of EPS in non-immune cells such as intestinal epithelial cells. In addition, the cellular and molecular mechanisms involved in the immunoregulatory effects of EPS have not been studied in detail. In this work, we have performed a genomic characterization of Lactobacillus delbrueckii subsp. delbrueckii TUA4408L and evaluated the immunomodulatory and antiviral properties of its acidic (APS) and neutral (NPS) EPS in porcine intestinal epithelial (PIE) cells. Whole genome sequencing allowed the analysis of the general features of L. delbrueckii TUA4408L genome as well as the characterization of its EPS genes. A typical EPS gene cluster was found in the TUA4408L genome consisting in five highly conserved genes epsA-E, and a variable region, which includes the genes for the polymerase wzy, the flippase wzx, and seven glycosyltransferases. In addition, we demonstrated here for the first time that L. delbrueckii TUA4408L and its EPS are able to improve the resistance of PIE cells against rotavirus infection by reducing viral replication and regulating inflammatory response. Moreover, studies in PIE cells demonstrated that the TUA4408L strain and its EPS differentially modulate the antiviral innate immune response triggered by the activation of Toll-like receptor 3 (TLR3). L. delbrueckii TUA4408L and its EPS are capable of increasing the activation of interferon regulatory factor (IRF)-3 and nuclear factor κB (NF-κB) signaling pathways leading to an improved expression of the antiviral factors interferon (IFN)-β, Myxovirus resistance gene A (MxA) and RNaseL.
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spelling doaj.art-8505c63785204a818e78e766ad521bfc2022-12-22T01:37:40ZengFrontiers Media S.A.Frontiers in Immunology1664-32242018-09-01910.3389/fimmu.2018.02178384503Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial CellsPaulraj Kanmani0Paulraj Kanmani1Leonardo Albarracin2Leonardo Albarracin3Leonardo Albarracin4Hisakazu Kobayashi5Hisakazu Kobayashi6Elvira Maria Hebert7Lucila Saavedra8Ryoya Komatsu9Ryoya Komatsu10Brian Gatica11Ayako Miyazaki12Wakako Ikeda-Ohtsubo13Wakako Ikeda-Ohtsubo14Yoshihito Suda15Hisashi Aso16Hisashi Aso17Shintaro Egusa18Takashi Mishima19Alexis Salas-Burgos20Hideki Takahashi21Hideki Takahashi22Julio Villena23Julio Villena24Haruki Kitazawa25Haruki Kitazawa26Food and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLivestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanFood and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanReference Centre for Lactobacilli (CERELA-CONICET), Tucuman, ArgentinaScientific Computing Laboratory, Computer Science Department, Faculty of Exact Sciences and Technology, National University of Tucuman, Tucuman, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLivestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanReference Centre for Lactobacilli (CERELA-CONICET), Tucuman, ArgentinaReference Centre for Lactobacilli (CERELA-CONICET), Tucuman, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLivestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanDepartment of Pharmacology, University of Concepcion, Concepcion, ChileViral Diseases and Epidemiology Research Division, National Institute of Animal Health, NARO, Tsukuba, JapanFood and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLivestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanDepartment of Food, Agriculture, and Environment, Miyagi University, Sendai, JapanLivestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanCell Biology Laboratory, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanResearch & Development Division, Marusan-Ai Co., Ltd., Okazaki, Japan0Graduate School of Regional Innovation Studies, Mie University, Tsu, JapanDepartment of Pharmacology, University of Concepcion, Concepcion, Chile1Laboratory of Plant Pathology, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan2Plant Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanFood and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanReference Centre for Lactobacilli (CERELA-CONICET), Tucuman, ArgentinaFood and Feed Immunology Group, Laboratory of Animal Products Chemistry, Graduate School of Agricultural Science, Tohoku University, Sendai, JapanLivestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, JapanIn lactic acid bacteria, the synthesis of exopolysaccharides (EPS) has been associated with some favorable technological properties as well as health-promoting benefits. Research works have shown the potential of EPS produced by lactobacilli to differentially modulate immune responses. However, most studies were performed in immune cells and few works have concentrated in the immunomodulatory activities of EPS in non-immune cells such as intestinal epithelial cells. In addition, the cellular and molecular mechanisms involved in the immunoregulatory effects of EPS have not been studied in detail. In this work, we have performed a genomic characterization of Lactobacillus delbrueckii subsp. delbrueckii TUA4408L and evaluated the immunomodulatory and antiviral properties of its acidic (APS) and neutral (NPS) EPS in porcine intestinal epithelial (PIE) cells. Whole genome sequencing allowed the analysis of the general features of L. delbrueckii TUA4408L genome as well as the characterization of its EPS genes. A typical EPS gene cluster was found in the TUA4408L genome consisting in five highly conserved genes epsA-E, and a variable region, which includes the genes for the polymerase wzy, the flippase wzx, and seven glycosyltransferases. In addition, we demonstrated here for the first time that L. delbrueckii TUA4408L and its EPS are able to improve the resistance of PIE cells against rotavirus infection by reducing viral replication and regulating inflammatory response. Moreover, studies in PIE cells demonstrated that the TUA4408L strain and its EPS differentially modulate the antiviral innate immune response triggered by the activation of Toll-like receptor 3 (TLR3). L. delbrueckii TUA4408L and its EPS are capable of increasing the activation of interferon regulatory factor (IRF)-3 and nuclear factor κB (NF-κB) signaling pathways leading to an improved expression of the antiviral factors interferon (IFN)-β, Myxovirus resistance gene A (MxA) and RNaseL.https://www.frontiersin.org/article/10.3389/fimmu.2018.02178/fullporcine intestinal epithelial cellsimmunobioticsTLR3Rotavirusantiviral activitygenome sequence
spellingShingle Paulraj Kanmani
Paulraj Kanmani
Leonardo Albarracin
Leonardo Albarracin
Leonardo Albarracin
Hisakazu Kobayashi
Hisakazu Kobayashi
Elvira Maria Hebert
Lucila Saavedra
Ryoya Komatsu
Ryoya Komatsu
Brian Gatica
Ayako Miyazaki
Wakako Ikeda-Ohtsubo
Wakako Ikeda-Ohtsubo
Yoshihito Suda
Hisashi Aso
Hisashi Aso
Shintaro Egusa
Takashi Mishima
Alexis Salas-Burgos
Hideki Takahashi
Hideki Takahashi
Julio Villena
Julio Villena
Haruki Kitazawa
Haruki Kitazawa
Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells
Frontiers in Immunology
porcine intestinal epithelial cells
immunobiotics
TLR3
Rotavirus
antiviral activity
genome sequence
title Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells
title_full Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells
title_fullStr Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells
title_full_unstemmed Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells
title_short Genomic Characterization of Lactobacillus delbrueckii TUA4408L and Evaluation of the Antiviral Activities of its Extracellular Polysaccharides in Porcine Intestinal Epithelial Cells
title_sort genomic characterization of lactobacillus delbrueckii tua4408l and evaluation of the antiviral activities of its extracellular polysaccharides in porcine intestinal epithelial cells
topic porcine intestinal epithelial cells
immunobiotics
TLR3
Rotavirus
antiviral activity
genome sequence
url https://www.frontiersin.org/article/10.3389/fimmu.2018.02178/full
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