RapamycinFungusV1, Main, Exploration, bibRecord, 000516

Promoter-associated proteins of EPAS1 identified by enChIP-MS - A putative role of HDX as a negative regulator.

Identifieur interne : 000516 ( Main/Exploration ); précédent : 000515; suivant : 000517

Promoter-associated proteins of EPAS1 identified by enChIP-MS - A putative role of HDX as a negative regulator.

Auteurs : Arash Hamidian [Suède] ; Marica Vaapil [Suède] ; Kristoffer Von Stedingk [Suède] ; Toshitsugu Fujita [Japon] ; Camilla U. Persson [Suède] ; Pontus Eriksson [Suède] ; Srinivas Veerla [Suède] ; Katleen De Preter [Belgique] ; Frank Speleman [Belgique] ; Hodaka Fujii [Japon] ; Sven P Hlman [Suède] ; Sofie Mohlin [Suède]

Source :

Biochemical and biophysical research communications [ 1090-2104 ] ; 2018.

RBID : pubmed:29577908

Descripteurs français

English descriptors

Abstract

Presence of perivascular neuroblastoma cells with high expression of hypoxia inducible factor (HIF)-2α correlates with distant metastasis and aggressive disease. Regulation of HIFs are traditionally considered to occur post-translationally, but we have recently shown that HIF-2α is unconventionally regulated also at the transcriptional level in neuroblastoma cells. Regulatory factors binding directly to EPAS1 (encoding HIF-2α) to promote transcription are yet to be defined. Here, we employ the novel CRISPR/Cas9-based engineered DNA-binding molecule-mediated chromatin immunoprecipitation (enChIP) - mass spectrometry (MS) methodology to, in an unbiased fashion, identify proteins that associate with the EPAS1 promoter under normoxic and hypoxic conditions. Our enChIP analysis resulted in 27 proteins binding to the EPAS1 promoter in neuroblastoma cells. In agreement with a general hypoxia-driven downregulation of gene transcription, the majority (24 out of 27) of proteins dissociate from the promoter at hypoxia. Among them were several nucleosome-associated proteins suggesting a general opening of chromatin as one explanation to induced EPAS1 transcription at hypoxia. Of particular interest from the list of released factors at hypoxia was the highly divergent homeobox (HDX) transcription factor, that we show inversely correlates with HIF-2α in neuroblastoma cells. We propose a putative model where HDX negatively regulates EPAS1 expression through a release-of-inhibition mechanism.

DOI: 10.1016/j.bbrc.2018.03.150
PubMed: 29577908

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<author><name sortKey="De Preter, Katleen" sort="De Preter, Katleen" uniqKey="De Preter K" first="Katleen" last="De Preter">Katleen De Preter</name>
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<country xml:lang="fr">Belgique</country>
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<author><name sortKey="Speleman, Frank" sort="Speleman, Frank" uniqKey="Speleman F" first="Frank" last="Speleman">Frank Speleman</name>
<affiliation wicri:level="4"><nlm:affiliation>Center for Medical Genetics, Ghent University, Ghent, B-9000, Belgium; Cancer Research Institute Ghent (CRIG), Ghent University, B-9000, Ghent, Belgium.</nlm:affiliation>
<country xml:lang="fr">Belgique</country>
<wicri:regionArea>Center for Medical Genetics, Ghent University, Ghent, B-9000, Belgium; Cancer Research Institute Ghent (CRIG), Ghent University, B-9000, Ghent</wicri:regionArea>
<orgName type="university">Université de Gand</orgName>
<placeName><settlement type="city">Gand</settlement>
<region>Région flamande</region>
<region type="district" nuts="2">Province de Flandre-Orientale</region>
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<author><name sortKey="Fujii, Hodaka" sort="Fujii, Hodaka" uniqKey="Fujii H" first="Hodaka" last="Fujii">Hodaka Fujii</name>
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<country xml:lang="fr">Japon</country>
<wicri:regionArea>Combined Program on Microbiology and Immunology, Research Institute for Microbial Diseases, Osaka University, Yamadaoka 3-1, Suita City, Osaka, 565-0871, Japan; Department of Biochemistry and Genome Biology, Hirosaki University Graduate School of Medicine, Zaifu-cho 5, Hirosaki, Aomori Prefecture, 036-8562</wicri:regionArea>
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<country xml:lang="fr">Suède</country>
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<profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Animals (MeSH)</term>
<term>Base Sequence (MeSH)</term>
<term>Basic Helix-Loop-Helix Transcription Factors (genetics)</term>
<term>Basic Helix-Loop-Helix Transcription Factors (metabolism)</term>
<term>Cell Hypoxia (genetics)</term>
<term>Cell Line, Tumor (MeSH)</term>
<term>Chromatin (metabolism)</term>
<term>Chromatin Immunoprecipitation (methods)</term>
<term>DNA (metabolism)</term>
<term>Gene Expression Regulation, Neoplastic (MeSH)</term>
<term>Gene Regulatory Networks (MeSH)</term>
<term>Genetic Engineering (MeSH)</term>
<term>Homeodomain Proteins (genetics)</term>
<term>Homeodomain Proteins (metabolism)</term>
<term>Humans (MeSH)</term>
<term>Mass Spectrometry (methods)</term>
<term>Mice (MeSH)</term>
<term>Neuroblastoma (genetics)</term>
<term>Neuroblastoma (pathology)</term>
<term>Promoter Regions, Genetic (MeSH)</term>
<term>Proto-Oncogene Proteins c-myc (metabolism)</term>
<term>RNA, Guide (metabolism)</term>
<term>RNA, Messenger (genetics)</term>
<term>RNA, Messenger (metabolism)</term>
<term>Rapamycin-Insensitive Companion of mTOR Protein (genetics)</term>
<term>Rapamycin-Insensitive Companion of mTOR Protein (metabolism)</term>
<term>Reproducibility of Results (MeSH)</term>
<term>Transcription Factors (genetics)</term>
<term>Transcription Factors (metabolism)</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>ADN (métabolisme)</term>
<term>ARN guide (métabolisme)</term>
<term>ARN messager (génétique)</term>
<term>ARN messager (métabolisme)</term>
<term>Animaux (MeSH)</term>
<term>Chromatine (métabolisme)</term>
<term>Compagnon de mTOR insensible à la rapamycine (génétique)</term>
<term>Compagnon de mTOR insensible à la rapamycine (métabolisme)</term>
<term>Facteurs de transcription (génétique)</term>
<term>Facteurs de transcription (métabolisme)</term>
<term>Facteurs de transcription à motif basique hélice-boucle-hélice (génétique)</term>
<term>Facteurs de transcription à motif basique hélice-boucle-hélice (métabolisme)</term>
<term>Génie génétique (MeSH)</term>
<term>Humains (MeSH)</term>
<term>Hypoxie cellulaire (génétique)</term>
<term>Immunoprécipitation de la chromatine (méthodes)</term>
<term>Lignée cellulaire tumorale (MeSH)</term>
<term>Neuroblastome (anatomopathologie)</term>
<term>Neuroblastome (génétique)</term>
<term>Protéines proto-oncogènes c-myc (métabolisme)</term>
<term>Protéines à homéodomaine (génétique)</term>
<term>Protéines à homéodomaine (métabolisme)</term>
<term>Reproductibilité des résultats (MeSH)</term>
<term>Régions promotrices (génétique) (MeSH)</term>
<term>Régulation de l'expression des gènes tumoraux (MeSH)</term>
<term>Réseaux de régulation génique (MeSH)</term>
<term>Souris (MeSH)</term>
<term>Spectrométrie de masse (méthodes)</term>
<term>Séquence nucléotidique (MeSH)</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>Basic Helix-Loop-Helix Transcription Factors</term>
<term>Homeodomain Proteins</term>
<term>RNA, Messenger</term>
<term>Rapamycin-Insensitive Companion of mTOR Protein</term>
<term>Transcription Factors</term>
</keywords>
<keywords scheme="MESH" type="chemical" qualifier="metabolism" xml:lang="en"><term>Basic Helix-Loop-Helix Transcription Factors</term>
<term>Chromatin</term>
<term>DNA</term>
<term>Homeodomain Proteins</term>
<term>Proto-Oncogene Proteins c-myc</term>
<term>RNA, Guide</term>
<term>RNA, Messenger</term>
<term>Rapamycin-Insensitive Companion of mTOR Protein</term>
<term>Transcription Factors</term>
</keywords>
<keywords scheme="MESH" qualifier="anatomopathologie" xml:lang="fr"><term>Neuroblastome</term>
</keywords>
<keywords scheme="MESH" qualifier="genetics" xml:lang="en"><term>Cell Hypoxia</term>
<term>Neuroblastoma</term>
</keywords>
<keywords scheme="MESH" qualifier="génétique" xml:lang="fr"><term>ARN messager</term>
<term>Compagnon de mTOR insensible à la rapamycine</term>
<term>Facteurs de transcription</term>
<term>Facteurs de transcription à motif basique hélice-boucle-hélice</term>
<term>Hypoxie cellulaire</term>
<term>Neuroblastome</term>
<term>Protéines à homéodomaine</term>
</keywords>
<keywords scheme="MESH" qualifier="methods" xml:lang="en"><term>Chromatin Immunoprecipitation</term>
<term>Mass Spectrometry</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>ADN</term>
<term>ARN guide</term>
<term>ARN messager</term>
<term>Chromatine</term>
<term>Compagnon de mTOR insensible à la rapamycine</term>
<term>Facteurs de transcription</term>
<term>Facteurs de transcription à motif basique hélice-boucle-hélice</term>
<term>Protéines proto-oncogènes c-myc</term>
<term>Protéines à homéodomaine</term>
</keywords>
<keywords scheme="MESH" qualifier="méthodes" xml:lang="fr"><term>Immunoprécipitation de la chromatine</term>
<term>Spectrométrie de masse</term>
</keywords>
<keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>Neuroblastoma</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Animals</term>
<term>Base Sequence</term>
<term>Cell Line, Tumor</term>
<term>Gene Expression Regulation, Neoplastic</term>
<term>Gene Regulatory Networks</term>
<term>Genetic Engineering</term>
<term>Humans</term>
<term>Mice</term>
<term>Promoter Regions, Genetic</term>
<term>Reproducibility of Results</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Génie génétique</term>
<term>Humains</term>
<term>Lignée cellulaire tumorale</term>
<term>Reproductibilité des résultats</term>
<term>Régions promotrices (génétique)</term>
<term>Régulation de l'expression des gènes tumoraux</term>
<term>Réseaux de régulation génique</term>
<term>Souris</term>
<term>Séquence nucléotidique</term>
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<front><div type="abstract" xml:lang="en">Presence of perivascular neuroblastoma cells with high expression of hypoxia inducible factor (HIF)-2α correlates with distant metastasis and aggressive disease. Regulation of HIFs are traditionally considered to occur post-translationally, but we have recently shown that HIF-2α is unconventionally regulated also at the transcriptional level in neuroblastoma cells. Regulatory factors binding directly to EPAS1 (encoding HIF-2α) to promote transcription are yet to be defined. Here, we employ the novel CRISPR/Cas9-based engineered DNA-binding molecule-mediated chromatin immunoprecipitation (enChIP) - mass spectrometry (MS) methodology to, in an unbiased fashion, identify proteins that associate with the EPAS1 promoter under normoxic and hypoxic conditions. Our enChIP analysis resulted in 27 proteins binding to the EPAS1 promoter in neuroblastoma cells. In agreement with a general hypoxia-driven downregulation of gene transcription, the majority (24 out of 27) of proteins dissociate from the promoter at hypoxia. Among them were several nucleosome-associated proteins suggesting a general opening of chromatin as one explanation to induced EPAS1 transcription at hypoxia. Of particular interest from the list of released factors at hypoxia was the highly divergent homeobox (HDX) transcription factor, that we show inversely correlates with HIF-2α in neuroblastoma cells. We propose a putative model where HDX negatively regulates EPAS1 expression through a release-of-inhibition mechanism.</div>
</front>
</TEI>
<pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">29577908</PMID>
<DateCompleted><Year>2018</Year>
<Month>10</Month>
<Day>09</Day>
</DateCompleted>
<DateRevised><Year>2018</Year>
<Month>12</Month>
<Day>02</Day>
</DateRevised>
<Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1090-2104</ISSN>
<JournalIssue CitedMedium="Internet"><Volume>499</Volume>
<Issue>2</Issue>
<PubDate><Year>2018</Year>
<Month>05</Month>
<Day>05</Day>
</PubDate>
</JournalIssue>
<Title>Biochemical and biophysical research communications</Title>
<ISOAbbreviation>Biochem Biophys Res Commun</ISOAbbreviation>
</Journal>
<ArticleTitle>Promoter-associated proteins of EPAS1 identified by enChIP-MS - A putative role of HDX as a negative regulator.</ArticleTitle>
<Pagination><MedlinePgn>291-298</MedlinePgn>
</Pagination>
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<ELocationID EIdType="doi" ValidYN="Y">10.1016/j.bbrc.2018.03.150</ELocationID>
<Abstract><AbstractText>Presence of perivascular neuroblastoma cells with high expression of hypoxia inducible factor (HIF)-2α correlates with distant metastasis and aggressive disease. Regulation of HIFs are traditionally considered to occur post-translationally, but we have recently shown that HIF-2α is unconventionally regulated also at the transcriptional level in neuroblastoma cells. Regulatory factors binding directly to EPAS1 (encoding HIF-2α) to promote transcription are yet to be defined. Here, we employ the novel CRISPR/Cas9-based engineered DNA-binding molecule-mediated chromatin immunoprecipitation (enChIP) - mass spectrometry (MS) methodology to, in an unbiased fashion, identify proteins that associate with the EPAS1 promoter under normoxic and hypoxic conditions. Our enChIP analysis resulted in 27 proteins binding to the EPAS1 promoter in neuroblastoma cells. In agreement with a general hypoxia-driven downregulation of gene transcription, the majority (24 out of 27) of proteins dissociate from the promoter at hypoxia. Among them were several nucleosome-associated proteins suggesting a general opening of chromatin as one explanation to induced EPAS1 transcription at hypoxia. Of particular interest from the list of released factors at hypoxia was the highly divergent homeobox (HDX) transcription factor, that we show inversely correlates with HIF-2α in neuroblastoma cells. We propose a putative model where HDX negatively regulates EPAS1 expression through a release-of-inhibition mechanism.</AbstractText>
<CopyrightInformation>Copyright © 2018 Elsevier Inc. All rights reserved.</CopyrightInformation>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Hamidian</LastName>
<ForeName>Arash</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Translational Cancer Research, Lund University Cancer Center at Medicon Village, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Vaapil</LastName>
<ForeName>Marica</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Translational Cancer Research, Lund University Cancer Center at Medicon Village, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>von Stedingk</LastName>
<ForeName>Kristoffer</ForeName>
<Initials>K</Initials>
<AffiliationInfo><Affiliation>Department of Pediatrics, Clinical Sciences, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Fujita</LastName>
<ForeName>Toshitsugu</ForeName>
<Initials>T</Initials>
<AffiliationInfo><Affiliation>Combined Program on Microbiology and Immunology, Research Institute for Microbial Diseases, Osaka University, Yamadaoka 3-1, Suita City, Osaka, 565-0871, Japan; Department of Biochemistry and Genome Biology, Hirosaki University Graduate School of Medicine, Zaifu-cho 5, Hirosaki, Aomori Prefecture, 036-8562, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Persson</LastName>
<ForeName>Camilla U</ForeName>
<Initials>CU</Initials>
<AffiliationInfo><Affiliation>Translational Cancer Research, Lund University Cancer Center at Medicon Village, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Eriksson</LastName>
<ForeName>Pontus</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>Department of Oncology and Pathology, Clinical Sciences Lund, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Veerla</LastName>
<ForeName>Srinivas</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Department of Oncology and Pathology, Clinical Sciences Lund, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>De Preter</LastName>
<ForeName>Katleen</ForeName>
<Initials>K</Initials>
<AffiliationInfo><Affiliation>Center for Medical Genetics, Ghent University, Ghent, B-9000, Belgium; Cancer Research Institute Ghent (CRIG), Ghent University, B-9000, Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Speleman</LastName>
<ForeName>Frank</ForeName>
<Initials>F</Initials>
<AffiliationInfo><Affiliation>Center for Medical Genetics, Ghent University, Ghent, B-9000, Belgium; Cancer Research Institute Ghent (CRIG), Ghent University, B-9000, Ghent, Belgium.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Fujii</LastName>
<ForeName>Hodaka</ForeName>
<Initials>H</Initials>
<AffiliationInfo><Affiliation>Combined Program on Microbiology and Immunology, Research Institute for Microbial Diseases, Osaka University, Yamadaoka 3-1, Suita City, Osaka, 565-0871, Japan; Department of Biochemistry and Genome Biology, Hirosaki University Graduate School of Medicine, Zaifu-cho 5, Hirosaki, Aomori Prefecture, 036-8562, Japan.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Påhlman</LastName>
<ForeName>Sven</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Translational Cancer Research, Lund University Cancer Center at Medicon Village, Lund University, Lund, Sweden.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Mohlin</LastName>
<ForeName>Sofie</ForeName>
<Initials>S</Initials>
<AffiliationInfo><Affiliation>Department of Pediatrics, Clinical Sciences, Lund University, Lund, Sweden. Electronic address: sofie.mohlin@med.lu.se.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2018</Year>
<Month>03</Month>
<Day>26</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>Biochem Biophys Res Commun</MedlineTA>
<NlmUniqueID>0372516</NlmUniqueID>
<ISSNLinking>0006-291X</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D051792">Basic Helix-Loop-Helix Transcription Factors</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D002843">Chromatin</NameOfSubstance>
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<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D018398">Homeodomain Proteins</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D016271">Proto-Oncogene Proteins c-myc</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="C492571">RICTOR protein, human</NameOfSubstance>
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<Chemical><RegistryNumber>0</RegistryNumber>
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<Chemical><RegistryNumber>0</RegistryNumber>
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</Chemical>
<Chemical><RegistryNumber>1B37H0967P</RegistryNumber>
<NameOfSubstance UI="C105713">endothelial PAS domain-containing protein 1</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>9007-49-2</RegistryNumber>
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<MeshHeadingList><MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001483" MajorTopicYN="N">Base Sequence</DescriptorName>
</MeshHeading>
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<QualifierName UI="Q000235" MajorTopicYN="Y">genetics</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D015687" MajorTopicYN="N">Cell Hypoxia</DescriptorName>
<QualifierName UI="Q000235" MajorTopicYN="N">genetics</QualifierName>
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<MeshHeading><DescriptorName UI="D015972" MajorTopicYN="N">Gene Expression Regulation, Neoplastic</DescriptorName>
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<MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
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<QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName>
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<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
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<KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="Y">HDX</Keyword>
<Keyword MajorTopicYN="Y">HIF-2α</Keyword>
<Keyword MajorTopicYN="Y">Hypoxia</Keyword>
<Keyword MajorTopicYN="Y">MYCN</Keyword>
<Keyword MajorTopicYN="Y">Neuroblastoma</Keyword>
<Keyword MajorTopicYN="Y">enChIP</Keyword>
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Promoter-associated proteins of EPAS1 identified by enChIP-MS - A putative role of HDX as a negative regulator.

Promoter-associated proteins of EPAS1 identified by enChIP-MS - A putative role of HDX as a negative regulator.

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