Serveur d'exploration sur les récepteurs immunitaires végétaux

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Immunobiotic Lactobacillus jensenii TL2937 Alleviates Dextran Sodium Sulfate-Induced Colitis by Differentially Modulating the Transcriptomic Response of Intestinal Epithelial Cells.

Identifieur interne : 000136 ( Main/Exploration ); précédent : 000135; suivant : 000137

Immunobiotic Lactobacillus jensenii TL2937 Alleviates Dextran Sodium Sulfate-Induced Colitis by Differentially Modulating the Transcriptomic Response of Intestinal Epithelial Cells.

Auteurs : Nana Sato [Japon] ; Valeria Garcia-Castillo [Japon, Chili] ; Mao Yuzawa [Japon] ; Md Aminul Islam [Japon, Bangladesh] ; Leonardo Albarracin [Japon, Argentine] ; Mikado Tomokiyo [Japon] ; Wakako Ikeda-Ohtsubo [Japon] ; Apolinaria Garcia-Cancino [Chili] ; Hideki Takahashi [Japon] ; Julio Villena [Japon, Bangladesh] ; Haruki Kitazawa [Japon]

Source :

RBID : pubmed:33042131

Abstract

Immunobiotics have emerged as a promising intervention to alleviate intestinal damage in inflammatory bowel disease (IBD). However, the beneficial properties of immunobiotics are strain dependent and, therefore, each strain has to be evaluated in order to demonstrate its potential application in IBD. Our previous in vitro and in vivo studies demonstrated that Lactobacillus jensenii TL2937 attenuates gut acute inflammatory response triggered by Toll-like receptor 4 activation. However, its effect on colitis has not been evaluated before. In this work, we studied whether the TL2937 strain was able to protect against the development of colitis in a dextran sodium sulfate (DSS)-induced mouse model and we delved into the mechanisms of action by evaluating the effect of the immunobiotic bacteria on the transcriptomic response of DSS-challenged intestinal epithelial cells. L. jensenii TL2937 was administered to adult BALB/c mice before the induction of colitis by the administration of DSS. Colitis and the associated inflammatory response were evaluated for 14 days. Mice fed with L. jensenii TL2937 had lower disease activity index and alterations of colon length when compared to control mice. Reduced myeloperoxidase activity, lower production of pro-inflammatory (TNF-α, IL-1, CXCL1, MCP-1, IL-15, and IL-17), and higher levels of immunoregulatory (IL-10 and IL-27) cytokines were found in the colon of TL2937-treated mice. In addition, the treatment of porcine intestinal epithelial (PIE) cells with L. jensenii TL2937 before the challenge with DSS differentially regulated the activation of the JNK pathway, leading to an increase in epithelial cell integrity and to a differential immunotranscriptomic response. TL2937-treated PIE cells had a significant reduction in the expression of inflammatory cytokines (TNF-α, IL-1α, IL-1β, IL-6, IL-15), chemokines (CCL2, CCL4, CCL8, CXCL4, CXCL5, CXCL9, CXCL10), adhesion molecules (SELE, SELL, EPCAM), and other immune factors (NCF1, NCF2, NOS2, SAA2) when compared to control cells after the challenge with DSS. The findings of this work indicate that (a) L. jensenii TL2937 is able to alleviate DSS-induced colitis suggesting a potential novel application for this immunobiotic strain, (b) the modulation of the transcriptomic response of intestinal epithelial cells would play a key role in the beneficial effects of the TL2937 strain on colitis, and (c) the in vitro PIE cell immunoassay system could be of value for the screening and selection of new immunobiotic strains for their application in IBD.

DOI: 10.3389/fimmu.2020.02174
PubMed: 33042131
PubMed Central: PMC7527445


Affiliations:


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<i>Lactobacillus jensenii</i>
TL2937 Alleviates Dextran Sodium Sulfate-Induced Colitis by Differentially Modulating the Transcriptomic Response of Intestinal Epithelial Cells.</title>
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<name sortKey="Sato, Nana" sort="Sato, Nana" uniqKey="Sato N" first="Nana" last="Sato">Nana Sato</name>
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<name sortKey="Garcia Castillo, Valeria" sort="Garcia Castillo, Valeria" uniqKey="Garcia Castillo V" first="Valeria" last="Garcia-Castillo">Valeria Garcia-Castillo</name>
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<nlm:affiliation>Laboratory of Bacterial Pathogenicity, Faculty of Biological Sciences, University of Concepcion, Concepción, Chile.</nlm:affiliation>
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<name sortKey="Islam, Md Aminul" sort="Islam, Md Aminul" uniqKey="Islam M" first="Md Aminul" last="Islam">Md Aminul Islam</name>
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<nlm:affiliation>Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.</nlm:affiliation>
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<name sortKey="Albarracin, Leonardo" sort="Albarracin, Leonardo" uniqKey="Albarracin L" first="Leonardo" last="Albarracin">Leonardo Albarracin</name>
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<nlm:affiliation>Laboratory of Immunobiotechnology, Reference Center for Lactobacilli (CERELA-National Council for Scientific and Technological Research), San Miguel de Tucumán, Argentina.</nlm:affiliation>
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<nlm:affiliation>Laboratory of Computing Science, Faculty of Exact Sciences and Technology, Tucuman University, San Miguel de Tucumán, Argentina.</nlm:affiliation>
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<name sortKey="Ikeda Ohtsubo, Wakako" sort="Ikeda Ohtsubo, Wakako" uniqKey="Ikeda Ohtsubo W" first="Wakako" last="Ikeda-Ohtsubo">Wakako Ikeda-Ohtsubo</name>
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<name sortKey="Garcia Cancino, Apolinaria" sort="Garcia Cancino, Apolinaria" uniqKey="Garcia Cancino A" first="Apolinaria" last="Garcia-Cancino">Apolinaria Garcia-Cancino</name>
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<nlm:affiliation>Laboratory of Bacterial Pathogenicity, Faculty of Biological Sciences, University of Concepcion, Concepción, Chile.</nlm:affiliation>
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<name sortKey="Takahashi, Hideki" sort="Takahashi, Hideki" uniqKey="Takahashi H" first="Hideki" last="Takahashi">Hideki Takahashi</name>
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<name sortKey="Villena, Julio" sort="Villena, Julio" uniqKey="Villena J" first="Julio" last="Villena">Julio Villena</name>
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<name sortKey="Kitazawa, Haruki" sort="Kitazawa, Haruki" uniqKey="Kitazawa H" first="Haruki" last="Kitazawa">Haruki Kitazawa</name>
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<title xml:lang="en">Immunobiotic
<i>Lactobacillus jensenii</i>
TL2937 Alleviates Dextran Sodium Sulfate-Induced Colitis by Differentially Modulating the Transcriptomic Response of Intestinal Epithelial Cells.</title>
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<name sortKey="Sato, Nana" sort="Sato, Nana" uniqKey="Sato N" first="Nana" last="Sato">Nana Sato</name>
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<orgName type="university">Université du Tōhoku</orgName>
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<nlm:affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</nlm:affiliation>
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<wicri:regionArea>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai</wicri:regionArea>
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<name sortKey="Garcia Castillo, Valeria" sort="Garcia Castillo, Valeria" uniqKey="Garcia Castillo V" first="Valeria" last="Garcia-Castillo">Valeria Garcia-Castillo</name>
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<wicri:regionArea>Laboratory of Bacterial Pathogenicity, Faculty of Biological Sciences, University of Concepcion, Concepción</wicri:regionArea>
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<name sortKey="Yuzawa, Mao" sort="Yuzawa, Mao" uniqKey="Yuzawa M" first="Mao" last="Yuzawa">Mao Yuzawa</name>
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<country xml:lang="fr">Japon</country>
<wicri:regionArea>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai</wicri:regionArea>
<orgName type="university">Université du Tōhoku</orgName>
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<settlement type="city">Sendai</settlement>
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<author>
<name sortKey="Islam, Md Aminul" sort="Islam, Md Aminul" uniqKey="Islam M" first="Md Aminul" last="Islam">Md Aminul Islam</name>
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<nlm:affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</nlm:affiliation>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai</wicri:regionArea>
<orgName type="university">Université du Tōhoku</orgName>
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<settlement type="city">Sendai</settlement>
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<nlm:affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</nlm:affiliation>
<country xml:lang="fr">Japon</country>
<wicri:regionArea>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai</wicri:regionArea>
<orgName type="university">Université du Tōhoku</orgName>
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<settlement type="city">Sendai</settlement>
<region type="province">Région de Tōhoku</region>
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<nlm:affiliation>Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.</nlm:affiliation>
<country xml:lang="fr">Bangladesh</country>
<wicri:regionArea>Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh</wicri:regionArea>
<wicri:noRegion>Mymensingh</wicri:noRegion>
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<author>
<name sortKey="Albarracin, Leonardo" sort="Albarracin, Leonardo" uniqKey="Albarracin L" first="Leonardo" last="Albarracin">Leonardo Albarracin</name>
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<nlm:affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</nlm:affiliation>
<country xml:lang="fr">Japon</country>
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<orgName type="university">Université du Tōhoku</orgName>
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<settlement type="city">Sendai</settlement>
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<nlm:affiliation>Laboratory of Computing Science, Faculty of Exact Sciences and Technology, Tucuman University, San Miguel de Tucumán, Argentina.</nlm:affiliation>
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<author>
<name sortKey="Garcia Cancino, Apolinaria" sort="Garcia Cancino, Apolinaria" uniqKey="Garcia Cancino A" first="Apolinaria" last="Garcia-Cancino">Apolinaria Garcia-Cancino</name>
<affiliation wicri:level="1">
<nlm:affiliation>Laboratory of Bacterial Pathogenicity, Faculty of Biological Sciences, University of Concepcion, Concepción, Chile.</nlm:affiliation>
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<region type="province">Région de Tōhoku</region>
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<wicri:regionArea>Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh</wicri:regionArea>
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<title level="j">Frontiers in immunology</title>
<idno type="eISSN">1664-3224</idno>
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<div type="abstract" xml:lang="en">Immunobiotics have emerged as a promising intervention to alleviate intestinal damage in inflammatory bowel disease (IBD). However, the beneficial properties of immunobiotics are strain dependent and, therefore, each strain has to be evaluated in order to demonstrate its potential application in IBD. Our previous
<i>in vitro</i>
and
<i>in vivo</i>
studies demonstrated that
<i>Lactobacillus jensenii</i>
TL2937 attenuates gut acute inflammatory response triggered by Toll-like receptor 4 activation. However, its effect on colitis has not been evaluated before. In this work, we studied whether the TL2937 strain was able to protect against the development of colitis in a dextran sodium sulfate (DSS)-induced mouse model and we delved into the mechanisms of action by evaluating the effect of the immunobiotic bacteria on the transcriptomic response of DSS-challenged intestinal epithelial cells.
<i>L. jensenii</i>
TL2937 was administered to adult BALB/c mice before the induction of colitis by the administration of DSS. Colitis and the associated inflammatory response were evaluated for 14 days. Mice fed with
<i>L. jensenii</i>
TL2937 had lower disease activity index and alterations of colon length when compared to control mice. Reduced myeloperoxidase activity, lower production of pro-inflammatory (TNF-α, IL-1, CXCL1, MCP-1, IL-15, and IL-17), and higher levels of immunoregulatory (IL-10 and IL-27) cytokines were found in the colon of TL2937-treated mice. In addition, the treatment of porcine intestinal epithelial (PIE) cells with
<i>L. jensenii</i>
TL2937 before the challenge with DSS differentially regulated the activation of the JNK pathway, leading to an increase in epithelial cell integrity and to a differential immunotranscriptomic response. TL2937-treated PIE cells had a significant reduction in the expression of inflammatory cytokines (
<i>TNF</i>
-α,
<i>IL-1</i>
α,
<i>IL-1</i>
β,
<i>IL-6, IL-15</i>
), chemokines (
<i>CCL2, CCL4, CCL8, CXCL4, CXCL5, CXCL9, CXCL10</i>
), adhesion molecules (
<i>SELE, SELL, EPCAM</i>
), and other immune factors (
<i>NCF1, NCF2, NOS2, SAA2</i>
) when compared to control cells after the challenge with DSS. The findings of this work indicate that (a)
<i>L. jensenii</i>
TL2937 is able to alleviate DSS-induced colitis suggesting a potential novel application for this immunobiotic strain, (b) the modulation of the transcriptomic response of intestinal epithelial cells would play a key role in the beneficial effects of the TL2937 strain on colitis, and (c) the
<i>in vitro</i>
PIE cell immunoassay system could be of value for the screening and selection of new immunobiotic strains for their application in IBD.</div>
</front>
</TEI>
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<Year>2020</Year>
<Month>10</Month>
<Day>13</Day>
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<Journal>
<ISSN IssnType="Electronic">1664-3224</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>11</Volume>
<PubDate>
<Year>2020</Year>
</PubDate>
</JournalIssue>
<Title>Frontiers in immunology</Title>
<ISOAbbreviation>Front Immunol</ISOAbbreviation>
</Journal>
<ArticleTitle>Immunobiotic
<i>Lactobacillus jensenii</i>
TL2937 Alleviates Dextran Sodium Sulfate-Induced Colitis by Differentially Modulating the Transcriptomic Response of Intestinal Epithelial Cells.</ArticleTitle>
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<Abstract>
<AbstractText>Immunobiotics have emerged as a promising intervention to alleviate intestinal damage in inflammatory bowel disease (IBD). However, the beneficial properties of immunobiotics are strain dependent and, therefore, each strain has to be evaluated in order to demonstrate its potential application in IBD. Our previous
<i>in vitro</i>
and
<i>in vivo</i>
studies demonstrated that
<i>Lactobacillus jensenii</i>
TL2937 attenuates gut acute inflammatory response triggered by Toll-like receptor 4 activation. However, its effect on colitis has not been evaluated before. In this work, we studied whether the TL2937 strain was able to protect against the development of colitis in a dextran sodium sulfate (DSS)-induced mouse model and we delved into the mechanisms of action by evaluating the effect of the immunobiotic bacteria on the transcriptomic response of DSS-challenged intestinal epithelial cells.
<i>L. jensenii</i>
TL2937 was administered to adult BALB/c mice before the induction of colitis by the administration of DSS. Colitis and the associated inflammatory response were evaluated for 14 days. Mice fed with
<i>L. jensenii</i>
TL2937 had lower disease activity index and alterations of colon length when compared to control mice. Reduced myeloperoxidase activity, lower production of pro-inflammatory (TNF-α, IL-1, CXCL1, MCP-1, IL-15, and IL-17), and higher levels of immunoregulatory (IL-10 and IL-27) cytokines were found in the colon of TL2937-treated mice. In addition, the treatment of porcine intestinal epithelial (PIE) cells with
<i>L. jensenii</i>
TL2937 before the challenge with DSS differentially regulated the activation of the JNK pathway, leading to an increase in epithelial cell integrity and to a differential immunotranscriptomic response. TL2937-treated PIE cells had a significant reduction in the expression of inflammatory cytokines (
<i>TNF</i>
-α,
<i>IL-1</i>
α,
<i>IL-1</i>
β,
<i>IL-6, IL-15</i>
), chemokines (
<i>CCL2, CCL4, CCL8, CXCL4, CXCL5, CXCL9, CXCL10</i>
), adhesion molecules (
<i>SELE, SELL, EPCAM</i>
), and other immune factors (
<i>NCF1, NCF2, NOS2, SAA2</i>
) when compared to control cells after the challenge with DSS. The findings of this work indicate that (a)
<i>L. jensenii</i>
TL2937 is able to alleviate DSS-induced colitis suggesting a potential novel application for this immunobiotic strain, (b) the modulation of the transcriptomic response of intestinal epithelial cells would play a key role in the beneficial effects of the TL2937 strain on colitis, and (c) the
<i>in vitro</i>
PIE cell immunoassay system could be of value for the screening and selection of new immunobiotic strains for their application in IBD.</AbstractText>
<CopyrightInformation>Copyright © 2020 Sato, Garcia-Castillo, Yuzawa, Islam, Albarracin, Tomokiyo, Ikeda-Ohtsubo, Garcia-Cancino, Takahashi, Villena and Kitazawa.</CopyrightInformation>
</Abstract>
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<LastName>Sato</LastName>
<ForeName>Nana</ForeName>
<Initials>N</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Garcia-Castillo</LastName>
<ForeName>Valeria</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Laboratory of Bacterial Pathogenicity, Faculty of Biological Sciences, University of Concepcion, Concepción, Chile.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Yuzawa</LastName>
<ForeName>Mao</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Islam</LastName>
<ForeName>Md Aminul</ForeName>
<Initials>MA</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Albarracin</LastName>
<ForeName>Leonardo</ForeName>
<Initials>L</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Laboratory of Immunobiotechnology, Reference Center for Lactobacilli (CERELA-National Council for Scientific and Technological Research), San Miguel de Tucumán, Argentina.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Laboratory of Computing Science, Faculty of Exact Sciences and Technology, Tucuman University, San Miguel de Tucumán, Argentina.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Tomokiyo</LastName>
<ForeName>Mikado</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Ikeda-Ohtsubo</LastName>
<ForeName>Wakako</ForeName>
<Initials>W</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Garcia-Cancino</LastName>
<ForeName>Apolinaria</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Bacterial Pathogenicity, Faculty of Biological Sciences, University of Concepcion, Concepción, Chile.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Takahashi</LastName>
<ForeName>Hideki</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Laboratory of Plant Pathology, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Plant Immunology Unit, International Education and Research Center for Food Agricultural Immunology, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
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<Author ValidYN="Y">
<LastName>Villena</LastName>
<ForeName>Julio</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Department of Medicine, Faculty of Veterinary Science, Bangladesh Agricultural University, Mymensingh, Bangladesh.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Kitazawa</LastName>
<ForeName>Haruki</ForeName>
<Initials>H</Initials>
<AffiliationInfo>
<Affiliation>Food and Feed Immunology Group, Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
<AffiliationInfo>
<Affiliation>Livestock Immunology Unit, International Education and Research Center for Food Agricultural Immunology (CFAI), Graduate School of Agricultural Science, Tohoku University, Sendai, Japan.</Affiliation>
</AffiliationInfo>
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