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A New Animal Model of Gastric Lymphomagenesis: APRIL Transgenic Mice Infected by Helicobacter Species.

Identifieur interne : 000906 ( PubMed/Curation ); précédent : 000905; suivant : 000907

A New Animal Model of Gastric Lymphomagenesis: APRIL Transgenic Mice Infected by Helicobacter Species.

Auteurs : Pauline Floch [France] ; Julien Izotte [France] ; Julien Guillemaud [France] ; Elodie Sifré [France] ; Pierre Costet [France] ; Benoit Rousseau [France] ; Amandine Marine Laur [France] ; Alban Giese [France] ; Victoria Korolik [Australie] ; Francis Mégraud [France] ; Pierre Dubus [France] ; Michael Hahne [France] ; Philippe Lehours [France]

Source :

RBID : pubmed:28460208

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English descriptors

Abstract

APRIL is a member of the tumor necrosis factor cytokine family involved in the regulation of B-cell immunity. We present a study of the infection by Helicobacter species of transgenic (Tg) C57BL6 mice, ectopically expressing the human form of APRIL. Wild-type (WT) and APRIL Tg mice were infected with Helicobacter felis and Helicobacter pylori and compared with noninfected animals. Mice were euthanized 18 months after infection, and inflammatory responses and histologic alterations were analyzed. Flow cytometry results revealed that WT-infected mice had less leukocyte infiltration than APRIL Tg-infected mice. In WT-infected mice, infiltrates in gastric tissues were predominantly composed of T cells, mainly CD4(+) for H. pylori and CD8(+) for H. felis. In APRIL Tg-infected mice, leukocyte infiltrates were composed of B cells with few CD4(+) T cells for both species. B cells expressed B surface markers compatible with a marginal zone origin. These results were confirmed by immunohistochemistry. B cells in particular were involved in lymphoepithelial lesions, a hallmark of gastric MALT lymphoma. Monoclonality was observed in a few infiltrates in the presence of lymphoepithelial lesions. These results confirm the importance of APRIL in the development of gastric lymphoid infiltrates induced by Helicobacter species in vivo. We believe that APRIL Tg mice infected by Helicobacter species may represent a novel animal model of gastric lymphomagenesis.

DOI: 10.1016/j.ajpath.2017.03.004
PubMed: 28460208

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<name sortKey="Korolik, Victoria" sort="Korolik, Victoria" uniqKey="Korolik V" first="Victoria" last="Korolik">Victoria Korolik</name>
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<nlm:affiliation>Institute for Glycomics, Griffith University, Gold Coast, Queensland, Australia.</nlm:affiliation>
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<name sortKey="Megraud, Francis" sort="Megraud, Francis" uniqKey="Megraud F" first="Francis" last="Mégraud">Francis Mégraud</name>
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<name sortKey="Hahne, Michael" sort="Hahne, Michael" uniqKey="Hahne M" first="Michael" last="Hahne">Michael Hahne</name>
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<nlm:affiliation>Montpellier Institute of Molecular Genetics UMR5535, University of Montpellier, Montpellier, France.</nlm:affiliation>
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<name sortKey="Lehours, Philippe" sort="Lehours, Philippe" uniqKey="Lehours P" first="Philippe" last="Lehours">Philippe Lehours</name>
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<nlm:affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France. Electronic address: philippe.lehours@u-bordeaux.fr.</nlm:affiliation>
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<title level="j">The American journal of pathology</title>
<idno type="eISSN">1525-2191</idno>
<imprint>
<date when="2017" type="published">2017</date>
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<term>Animals</term>
<term>B-Lymphocytes (microbiology)</term>
<term>B-Lymphocytes (pathology)</term>
<term>Bacterial Load</term>
<term>CD4-Positive T-Lymphocytes (microbiology)</term>
<term>CD4-Positive T-Lymphocytes (pathology)</term>
<term>Disease Models, Animal</term>
<term>Female</term>
<term>Helicobacter Infections (immunology)</term>
<term>Helicobacter Infections (microbiology)</term>
<term>Helicobacter Infections (pathology)</term>
<term>Helicobacter pylori (immunology)</term>
<term>Humans</term>
<term>Immunohistochemistry</term>
<term>Inflammation</term>
<term>Lymphoid Tissue (microbiology)</term>
<term>Lymphoid Tissue (pathology)</term>
<term>Lymphoma, B-Cell, Marginal Zone (immunology)</term>
<term>Lymphoma, B-Cell, Marginal Zone (microbiology)</term>
<term>Lymphoma, B-Cell, Marginal Zone (pathology)</term>
<term>Lymphoma, Non-Hodgkin (immunology)</term>
<term>Lymphoma, Non-Hodgkin (microbiology)</term>
<term>Lymphoma, Non-Hodgkin (pathology)</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Transgenic</term>
<term>Stomach (microbiology)</term>
<term>Stomach (pathology)</term>
<term>Stomach Neoplasms (immunology)</term>
<term>Stomach Neoplasms (microbiology)</term>
<term>Stomach Neoplasms (pathology)</term>
<term>Tumor Necrosis Factor Ligand Superfamily Member 13 (genetics)</term>
<term>Tumor Necrosis Factor Ligand Superfamily Member 13 (immunology)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr">
<term>Animaux</term>
<term>Charge bactérienne</term>
<term>Estomac (anatomopathologie)</term>
<term>Estomac (microbiologie)</term>
<term>Femelle</term>
<term>Helicobacter pylori (immunologie)</term>
<term>Humains</term>
<term>Immunohistochimie</term>
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<term>Infections à Helicobacter (immunologie)</term>
<term>Infections à Helicobacter (microbiologie)</term>
<term>Inflammation</term>
<term>Lymphocytes B (anatomopathologie)</term>
<term>Lymphocytes B (microbiologie)</term>
<term>Lymphocytes T CD4+ (anatomopathologie)</term>
<term>Lymphocytes T CD4+ (microbiologie)</term>
<term>Lymphome B de la zone marginale (anatomopathologie)</term>
<term>Lymphome B de la zone marginale (immunologie)</term>
<term>Lymphome B de la zone marginale (microbiologie)</term>
<term>Lymphome malin non hodgkinien (anatomopathologie)</term>
<term>Lymphome malin non hodgkinien (immunologie)</term>
<term>Lymphome malin non hodgkinien (microbiologie)</term>
<term>Membre-13 de la superfamille du facteur de nécrose tumorale (génétique)</term>
<term>Membre-13 de la superfamille du facteur de nécrose tumorale (immunologie)</term>
<term>Modèles animaux de maladie humaine</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris transgéniques</term>
<term>Tissu lymphoïde (anatomopathologie)</term>
<term>Tissu lymphoïde (microbiologie)</term>
<term>Tumeurs de l'estomac (anatomopathologie)</term>
<term>Tumeurs de l'estomac (immunologie)</term>
<term>Tumeurs de l'estomac (microbiologie)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en">
<term>Tumor Necrosis Factor Ligand Superfamily Member 13</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr">
<term>Estomac</term>
<term>Infections à Helicobacter</term>
<term>Lymphocytes B</term>
<term>Lymphocytes T CD4+</term>
<term>Lymphome B de la zone marginale</term>
<term>Lymphome malin non hodgkinien</term>
<term>Tissu lymphoïde</term>
<term>Tumeurs de l'estomac</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr">
<term>Membre-13 de la superfamille du facteur de nécrose tumorale</term>
</keywords>
<keywords scheme="MESH" qualifier="immunologie" xml:lang="fr">
<term>Helicobacter pylori</term>
<term>Infections à Helicobacter</term>
<term>Lymphome B de la zone marginale</term>
<term>Lymphome malin non hodgkinien</term>
<term>Membre-13 de la superfamille du facteur de nécrose tumorale</term>
<term>Tumeurs de l'estomac</term>
</keywords>
<keywords scheme="MESH" qualifier="immunology" xml:lang="en">
<term>Helicobacter Infections</term>
<term>Helicobacter pylori</term>
<term>Lymphoma, B-Cell, Marginal Zone</term>
<term>Lymphoma, Non-Hodgkin</term>
<term>Stomach Neoplasms</term>
<term>Tumor Necrosis Factor Ligand Superfamily Member 13</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiologie" xml:lang="fr">
<term>Estomac</term>
<term>Infections à Helicobacter</term>
<term>Lymphocytes B</term>
<term>Lymphocytes T CD4+</term>
<term>Lymphome B de la zone marginale</term>
<term>Lymphome malin non hodgkinien</term>
<term>Tissu lymphoïde</term>
<term>Tumeurs de l'estomac</term>
</keywords>
<keywords scheme="MESH" qualifier="microbiology" xml:lang="en">
<term>B-Lymphocytes</term>
<term>CD4-Positive T-Lymphocytes</term>
<term>Helicobacter Infections</term>
<term>Lymphoid Tissue</term>
<term>Lymphoma, B-Cell, Marginal Zone</term>
<term>Lymphoma, Non-Hodgkin</term>
<term>Stomach</term>
<term>Stomach Neoplasms</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en">
<term>B-Lymphocytes</term>
<term>CD4-Positive T-Lymphocytes</term>
<term>Helicobacter Infections</term>
<term>Lymphoid Tissue</term>
<term>Lymphoma, B-Cell, Marginal Zone</term>
<term>Lymphoma, Non-Hodgkin</term>
<term>Stomach</term>
<term>Stomach Neoplasms</term>
</keywords>
<keywords scheme="MESH" xml:lang="en">
<term>Animals</term>
<term>Bacterial Load</term>
<term>Disease Models, Animal</term>
<term>Female</term>
<term>Humans</term>
<term>Immunohistochemistry</term>
<term>Inflammation</term>
<term>Mice</term>
<term>Mice, Inbred C57BL</term>
<term>Mice, Transgenic</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr">
<term>Animaux</term>
<term>Charge bactérienne</term>
<term>Femelle</term>
<term>Humains</term>
<term>Immunohistochimie</term>
<term>Inflammation</term>
<term>Modèles animaux de maladie humaine</term>
<term>Souris</term>
<term>Souris de lignée C57BL</term>
<term>Souris transgéniques</term>
</keywords>
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<front>
<div type="abstract" xml:lang="en">APRIL is a member of the tumor necrosis factor cytokine family involved in the regulation of B-cell immunity. We present a study of the infection by Helicobacter species of transgenic (Tg) C57BL6 mice, ectopically expressing the human form of APRIL. Wild-type (WT) and APRIL Tg mice were infected with Helicobacter felis and Helicobacter pylori and compared with noninfected animals. Mice were euthanized 18 months after infection, and inflammatory responses and histologic alterations were analyzed. Flow cytometry results revealed that WT-infected mice had less leukocyte infiltration than APRIL Tg-infected mice. In WT-infected mice, infiltrates in gastric tissues were predominantly composed of T cells, mainly CD4(+) for H. pylori and CD8(+) for H. felis. In APRIL Tg-infected mice, leukocyte infiltrates were composed of B cells with few CD4(+) T cells for both species. B cells expressed B surface markers compatible with a marginal zone origin. These results were confirmed by immunohistochemistry. B cells in particular were involved in lymphoepithelial lesions, a hallmark of gastric MALT lymphoma. Monoclonality was observed in a few infiltrates in the presence of lymphoepithelial lesions. These results confirm the importance of APRIL in the development of gastric lymphoid infiltrates induced by Helicobacter species in vivo. We believe that APRIL Tg mice infected by Helicobacter species may represent a novel animal model of gastric lymphomagenesis.</div>
</front>
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<MedlineCitation Status="MEDLINE" Owner="NLM">
<PMID Version="1">28460208</PMID>
<DateCreated>
<Year>2017</Year>
<Month>05</Month>
<Day>01</Day>
</DateCreated>
<DateCompleted>
<Year>2017</Year>
<Month>10</Month>
<Day>13</Day>
</DateCompleted>
<DateRevised>
<Year>2017</Year>
<Month>10</Month>
<Day>13</Day>
</DateRevised>
<Article PubModel="Print-Electronic">
<Journal>
<ISSN IssnType="Electronic">1525-2191</ISSN>
<JournalIssue CitedMedium="Internet">
<Volume>187</Volume>
<Issue>7</Issue>
<PubDate>
<Year>2017</Year>
<Month>Jul</Month>
</PubDate>
</JournalIssue>
<Title>The American journal of pathology</Title>
<ISOAbbreviation>Am. J. Pathol.</ISOAbbreviation>
</Journal>
<ArticleTitle>A New Animal Model of Gastric Lymphomagenesis: APRIL Transgenic Mice Infected by Helicobacter Species.</ArticleTitle>
<Pagination>
<MedlinePgn>1473-1484</MedlinePgn>
</Pagination>
<ELocationID EIdType="pii" ValidYN="Y">S0002-9440(17)30031-7</ELocationID>
<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.ajpath.2017.03.004</ELocationID>
<Abstract>
<AbstractText>APRIL is a member of the tumor necrosis factor cytokine family involved in the regulation of B-cell immunity. We present a study of the infection by Helicobacter species of transgenic (Tg) C57BL6 mice, ectopically expressing the human form of APRIL. Wild-type (WT) and APRIL Tg mice were infected with Helicobacter felis and Helicobacter pylori and compared with noninfected animals. Mice were euthanized 18 months after infection, and inflammatory responses and histologic alterations were analyzed. Flow cytometry results revealed that WT-infected mice had less leukocyte infiltration than APRIL Tg-infected mice. In WT-infected mice, infiltrates in gastric tissues were predominantly composed of T cells, mainly CD4(+) for H. pylori and CD8(+) for H. felis. In APRIL Tg-infected mice, leukocyte infiltrates were composed of B cells with few CD4(+) T cells for both species. B cells expressed B surface markers compatible with a marginal zone origin. These results were confirmed by immunohistochemistry. B cells in particular were involved in lymphoepithelial lesions, a hallmark of gastric MALT lymphoma. Monoclonality was observed in a few infiltrates in the presence of lymphoepithelial lesions. These results confirm the importance of APRIL in the development of gastric lymphoid infiltrates induced by Helicobacter species in vivo. We believe that APRIL Tg mice infected by Helicobacter species may represent a novel animal model of gastric lymphomagenesis.</AbstractText>
<CopyrightInformation>Copyright © 2017 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y">
<Author ValidYN="Y">
<LastName>Floch</LastName>
<ForeName>Pauline</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Izotte</LastName>
<ForeName>Julien</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Guillemaud</LastName>
<ForeName>Julien</ForeName>
<Initials>J</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Sifré</LastName>
<ForeName>Elodie</ForeName>
<Initials>E</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Costet</LastName>
<ForeName>Pierre</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>Animal Facilities, University of Bordeaux, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Rousseau</LastName>
<ForeName>Benoit</ForeName>
<Initials>B</Initials>
<AffiliationInfo>
<Affiliation>Animal Facilities, University of Bordeaux, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Laur</LastName>
<ForeName>Amandine Marine</ForeName>
<Initials>AM</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Giese</LastName>
<ForeName>Alban</ForeName>
<Initials>A</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Korolik</LastName>
<ForeName>Victoria</ForeName>
<Initials>V</Initials>
<AffiliationInfo>
<Affiliation>Institute for Glycomics, Griffith University, Gold Coast, Queensland, Australia.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Mégraud</LastName>
<ForeName>Francis</ForeName>
<Initials>F</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Dubus</LastName>
<ForeName>Pierre</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Hahne</LastName>
<ForeName>Michael</ForeName>
<Initials>M</Initials>
<AffiliationInfo>
<Affiliation>Montpellier Institute of Molecular Genetics UMR5535, University of Montpellier, Montpellier, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y">
<LastName>Lehours</LastName>
<ForeName>Philippe</ForeName>
<Initials>P</Initials>
<AffiliationInfo>
<Affiliation>INSERM UMR1053, Bordeaux Research in Translational Oncology, Bordeaux, France. Electronic address: philippe.lehours@u-bordeaux.fr.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList>
<PublicationType UI="D016428">Journal Article</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic">
<Year>2017</Year>
<Month>04</Month>
<Day>29</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo>
<Country>United States</Country>
<MedlineTA>Am J Pathol</MedlineTA>
<NlmUniqueID>0370502</NlmUniqueID>
<ISSNLinking>0002-9440</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D053300">Tumor Necrosis Factor Ligand Superfamily Member 13</NameOfSubstance>
</Chemical>
</ChemicalList>
<SupplMeshList>
<SupplMeshName Type="Disease" UI="C535648">Familial primary gastric lymphoma</SupplMeshName>
</SupplMeshList>
<CitationSubset>AIM</CitationSubset>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList>
<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D001402" MajorTopicYN="N">B-Lymphocytes</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D058491" MajorTopicYN="N">Bacterial Load</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D015496" MajorTopicYN="N">CD4-Positive T-Lymphocytes</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D004195" MajorTopicYN="N">Disease Models, Animal</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D005260" MajorTopicYN="N">Female</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016481" MajorTopicYN="N">Helicobacter Infections</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016480" MajorTopicYN="N">Helicobacter pylori</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="Y">immunology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D007150" MajorTopicYN="N">Immunohistochemistry</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D007249" MajorTopicYN="N">Inflammation</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008221" MajorTopicYN="N">Lymphoid Tissue</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D018442" MajorTopicYN="N">Lymphoma, B-Cell, Marginal Zone</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008228" MajorTopicYN="N">Lymphoma, Non-Hodgkin</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D051379" MajorTopicYN="N">Mice</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008810" MajorTopicYN="N">Mice, Inbred C57BL</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D008822" MajorTopicYN="N">Mice, Transgenic</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013270" MajorTopicYN="N">Stomach</DescriptorName>
<QualifierName UI="Q000382" MajorTopicYN="N">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D013274" MajorTopicYN="N">Stomach Neoplasms</DescriptorName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
<QualifierName UI="Q000382" MajorTopicYN="Y">microbiology</QualifierName>
<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D053300" MajorTopicYN="N">Tumor Necrosis Factor Ligand Superfamily Member 13</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
<QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
<PubmedData>
<History>
<PubMedPubDate PubStatus="received">
<Year>2017</Year>
<Month>01</Month>
<Day>06</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="revised">
<Year>2017</Year>
<Month>02</Month>
<Day>27</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted">
<Year>2017</Year>
<Month>03</Month>
<Day>09</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="pubmed">
<Year>2017</Year>
<Month>5</Month>
<Day>2</Day>
<Hour>6</Hour>
<Minute>0</Minute>
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<PubMedPubDate PubStatus="medline">
<Year>2017</Year>
<Month>10</Month>
<Day>14</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
<PubMedPubDate PubStatus="entrez">
<Year>2017</Year>
<Month>5</Month>
<Day>2</Day>
<Hour>6</Hour>
<Minute>0</Minute>
</PubMedPubDate>
</History>
<PublicationStatus>ppublish</PublicationStatus>
<ArticleIdList>
<ArticleId IdType="pubmed">28460208</ArticleId>
<ArticleId IdType="pii">S0002-9440(17)30031-7</ArticleId>
<ArticleId IdType="doi">10.1016/j.ajpath.2017.03.004</ArticleId>
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