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Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.

Identifieur interne : 002647 ( PubMed/Curation ); précédent : 002646; suivant : 002648

Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.

Auteurs : Mary J. Van Helden [Belgique] ; Steven Goossens [Belgique] ; Cécile Daussy [France] ; Anne-Laure Mathieu [France] ; Fabrice Faure [France] ; Antoine Marçais [France] ; Niels Vandamme [Belgique] ; Natalie Farla [Belgique] ; Katia Mayol [France] ; Sébastien Viel [France] ; Sophie Degouve [France] ; Emilie Debien [France] ; Eve Seuntjens [Belgique] ; Andrea Conidi [Pays-Bas] ; Julie Chaix [France] ; Philippe Mangeot [France] ; Simon De Bernard [France] ; Laurent Buffat [France] ; Jody J. Haigh [Australie] ; Danny Huylebroeck [Pays-Bas] ; Bart N. Lambrecht [Pays-Bas] ; Geert Berx [Belgique] ; Thierry Walzer [France]

Source :

The Journal of experimental medicine [ 1540-9538 ] ; 2015.

RBID : pubmed:26503444

Descripteurs français

English descriptors

KwdEn :
- Animals, Bone Marrow (immunology), Bone Marrow (metabolism), Cell Line, Tumor, Cell Survival (genetics), Cell Survival (immunology), Cells, Cultured, Cytokines (immunology), Cytokines (secretion), Flow Cytometry, Gene Expression (immunology), Homeodomain Proteins (genetics), Homeodomain Proteins (immunology), Homeodomain Proteins (metabolism), Humans, Killer Cells, Natural (immunology), Killer Cells, Natural (metabolism), Melanoma, Experimental (genetics), Melanoma, Experimental (immunology), Melanoma, Experimental (metabolism), Mice, Inbred C57BL, Mice, Knockout, Mice, Transgenic, Repressor Proteins (genetics), Repressor Proteins (immunology), Repressor Proteins (metabolism), Reverse Transcriptase Polymerase Chain Reaction, T-Box Domain Proteins (genetics), T-Box Domain Proteins (immunology), T-Box Domain Proteins (metabolism).
MESH :
- chemical , genetics : Homeodomain Proteins, Repressor Proteins, T-Box Domain Proteins.
- chemical , immunology : Cytokines, Homeodomain Proteins, Repressor Proteins, T-Box Domain Proteins.
- genetics : Cell Survival, Melanoma, Experimental.
- immunology : Bone Marrow, Cell Survival, Gene Expression, Killer Cells, Natural, Melanoma, Experimental.
- metabolism : Bone Marrow, Homeodomain Proteins, Killer Cells, Natural, Melanoma, Experimental, Repressor Proteins, T-Box Domain Proteins.
- chemical , secretion : Cytokines.
- Animals, Cell Line, Tumor, Cells, Cultured, Flow Cytometry, Humans, Mice, Inbred C57BL, Mice, Knockout, Mice, Transgenic, Reverse Transcriptase Polymerase Chain Reaction.

Abstract

Natural killer (NK) cell maturation is a tightly controlled process that endows NK cells with functional competence and the capacity to recognize target cells. Here, we found that the transcription factor (TF) Zeb2 was the most highly induced TF during NK cell maturation. Zeb2 is known to control epithelial to mesenchymal transition, but its role in immune cells is mostly undefined. Targeted deletion of Zeb2 resulted in impaired NK cell maturation, survival, and exit from the bone marrow. NK cell function was preserved, but mice lacking Zeb2 in NK cells were more susceptible to B16 melanoma lung metastases. Reciprocally, ectopic expression of Zeb2 resulted in a higher frequency of mature NK cells in all organs. Moreover, the immature phenotype of Zeb2(-/-) NK cells closely resembled that of Tbx21(-/-) NK cells. This was caused by both a dependence of Zeb2 expression on T-bet and a probable cooperation of these factors in gene regulation. Transgenic expression of Zeb2 in Tbx21(-/-) NK cells partially restored a normal maturation, establishing that timely induction of Zeb2 by T-bet is an essential event during NK cell differentiation. Finally, this novel transcriptional cascade could also operate in human as T-bet and Zeb2 are similarly regulated in mouse and human NK cells.

DOI: 10.1084/jem.20150809
PubMed: 26503444

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<author><name sortKey="Debien, Emilie" sort="Debien, Emilie" uniqKey="Debien E" first="Emilie" last="Debien">Emilie Debien</name>
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<author><name sortKey="Buffat, Laurent" sort="Buffat, Laurent" uniqKey="Buffat L" first="Laurent" last="Buffat">Laurent Buffat</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en">Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.</title>
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<author><name sortKey="Goossens, Steven" sort="Goossens, Steven" uniqKey="Goossens S" first="Steven" last="Goossens">Steven Goossens</name>
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<author><name sortKey="Mathieu, Anne Laure" sort="Mathieu, Anne Laure" uniqKey="Mathieu A" first="Anne-Laure" last="Mathieu">Anne-Laure Mathieu</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon</wicri:regionArea>
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<author><name sortKey="Faure, Fabrice" sort="Faure, Fabrice" uniqKey="Faure F" first="Fabrice" last="Faure">Fabrice Faure</name>
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<country xml:lang="fr">France</country>
<wicri:regionArea>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon</wicri:regionArea>
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</affiliation>
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<country xml:lang="fr">Pays-Bas</country>
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</affiliation>
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<author><name sortKey="Lambrecht, Bart N" sort="Lambrecht, Bart N" uniqKey="Lambrecht B" first="Bart N" last="Lambrecht">Bart N. Lambrecht</name>
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<country xml:lang="fr">Pays-Bas</country>
<wicri:regionArea>Laboratory of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center, 9052 Ghent, Belgium GROUP-ID Consortium, Ghent University, 9000 Ghent, Belgium Department of Pulmonary Medicine, Erasmus MC, 3015 CN Rotterdam</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Berx, Geert" sort="Berx, Geert" uniqKey="Berx G" first="Geert" last="Berx">Geert Berx</name>
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<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Unit of Molecular and Cellular Oncology, VIB Inflammation Research Center, 9052 Ghent, Belgium Department for Biomedical Molecular Biology, Ghent University, 9052 Ghent</wicri:regionArea>
</affiliation>
</author>
<author><name sortKey="Walzer, Thierry" sort="Walzer, Thierry" uniqKey="Walzer T" first="Thierry" last="Walzer">Thierry Walzer</name>
<affiliation wicri:level="1"><nlm:affiliation>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon, France Thierry.walzer@inserm.fr.</nlm:affiliation>
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</affiliation>
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<series><title level="j">The Journal of experimental medicine</title>
<idno type="eISSN">1540-9538</idno>
<imprint><date when="2015" type="published">2015</date>
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<term>Repressor Proteins (metabolism)</term>
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<front><div type="abstract" xml:lang="en">Natural killer (NK) cell maturation is a tightly controlled process that endows NK cells with functional competence and the capacity to recognize target cells. Here, we found that the transcription factor (TF) Zeb2 was the most highly induced TF during NK cell maturation. Zeb2 is known to control epithelial to mesenchymal transition, but its role in immune cells is mostly undefined. Targeted deletion of Zeb2 resulted in impaired NK cell maturation, survival, and exit from the bone marrow. NK cell function was preserved, but mice lacking Zeb2 in NK cells were more susceptible to B16 melanoma lung metastases. Reciprocally, ectopic expression of Zeb2 resulted in a higher frequency of mature NK cells in all organs. Moreover, the immature phenotype of Zeb2(-/-) NK cells closely resembled that of Tbx21(-/-) NK cells. This was caused by both a dependence of Zeb2 expression on T-bet and a probable cooperation of these factors in gene regulation. Transgenic expression of Zeb2 in Tbx21(-/-) NK cells partially restored a normal maturation, establishing that timely induction of Zeb2 by T-bet is an essential event during NK cell differentiation. Finally, this novel transcriptional cascade could also operate in human as T-bet and Zeb2 are similarly regulated in mouse and human NK cells.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">26503444</PMID>
<DateCreated><Year>2015</Year>
<Month>11</Month>
<Day>17</Day>
</DateCreated>
<DateCompleted><Year>2016</Year>
<Month>04</Month>
<Day>12</Day>
</DateCompleted>
<DateRevised><Year>2017</Year>
<Month>11</Month>
<Day>16</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1540-9538</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>212</Volume>
<Issue>12</Issue>
<PubDate><Year>2015</Year>
<Month>Nov</Month>
<Day>16</Day>
</PubDate>
</JournalIssue>
<Title>The Journal of experimental medicine</Title>
<ISOAbbreviation>J. Exp. Med.</ISOAbbreviation>
</Journal>
<ArticleTitle>Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.</ArticleTitle>
<Pagination><MedlinePgn>2015-25</MedlinePgn>
</Pagination>
<ELocationID EIdType="doi" ValidYN="Y">10.1084/jem.20150809</ELocationID>
<Abstract><AbstractText>Natural killer (NK) cell maturation is a tightly controlled process that endows NK cells with functional competence and the capacity to recognize target cells. Here, we found that the transcription factor (TF) Zeb2 was the most highly induced TF during NK cell maturation. Zeb2 is known to control epithelial to mesenchymal transition, but its role in immune cells is mostly undefined. Targeted deletion of Zeb2 resulted in impaired NK cell maturation, survival, and exit from the bone marrow. NK cell function was preserved, but mice lacking Zeb2 in NK cells were more susceptible to B16 melanoma lung metastases. Reciprocally, ectopic expression of Zeb2 resulted in a higher frequency of mature NK cells in all organs. Moreover, the immature phenotype of Zeb2(-/-) NK cells closely resembled that of Tbx21(-/-) NK cells. This was caused by both a dependence of Zeb2 expression on T-bet and a probable cooperation of these factors in gene regulation. Transgenic expression of Zeb2 in Tbx21(-/-) NK cells partially restored a normal maturation, establishing that timely induction of Zeb2 by T-bet is an essential event during NK cell differentiation. Finally, this novel transcriptional cascade could also operate in human as T-bet and Zeb2 are similarly regulated in mouse and human NK cells.</AbstractText>
<CopyrightInformation>© 2015 van Helden et al.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>van Helden</LastName>
<ForeName>Mary J</ForeName>
<Initials>MJ</Initials>
<AffiliationInfo><Affiliation>Laboratory of Immunoregulation and Mucosal Immunology, VIB Inflammation Research Center, 9052 Ghent, Belgium GROUP-ID Consortium, Ghent University, 9000 Ghent, Belgium Department of Respiratory Medicine, Ghent University, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Goossens</LastName>
<ForeName>Steven</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Unit of Molecular and Cellular Oncology, VIB Inflammation Research Center, 9052 Ghent, Belgium Department for Biomedical Molecular Biology, Ghent University, 9052 Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Daussy</LastName>
<ForeName>Cécile</ForeName>
<Initials>C</Initials>
<AffiliationInfo><Affiliation>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Mathieu</LastName>
<ForeName>Anne-Laure</ForeName>
<Initials>AL</Initials>
<AffiliationInfo><Affiliation>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Faure</LastName>
<ForeName>Fabrice</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Marçais</LastName>
<ForeName>Antoine</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Université de Lyon, 69007 Lyon, France Institut National de la Santé et de la Recherche Médicale, U1111, 69342 Lyon, France Ecole Normale Supérieure de Lyon, 69007 Lyon, France Centre International de Recherche en Infectiologie, 69007 Lyon, France Centre National de la Recherche Scientifique, UMR5308, 69342 Lyon, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Vandamme</LastName>
<ForeName>Niels</ForeName>
<Initials>N</Initials>
<AffiliationInfo><Affiliation>Unit of Molecular and Cellular Oncology, VIB Inflammation Research Center, 9052 Ghent, Belgium Department for Biomedical Molecular Biology, Ghent University, 9052 Ghent, Belgium.</Affiliation>
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   |texte=   Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.
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Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.

Terminal NK cell maturation is controlled by concerted actions of T-bet and Zeb2 and is essential for melanoma rejection.

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