Lupus-associated endogenous retroviral LTR polymorphism and epigenetic imprinting promote HRES-1/RAB4 expression and mTOR activation.
Identifieur interne : 000094 ( Main/Exploration ); précédent : 000093; suivant : 000095Lupus-associated endogenous retroviral LTR polymorphism and epigenetic imprinting promote HRES-1/RAB4 expression and mTOR activation.
Auteurs : Aparna Godavarthy ; Ryan Kelly ; John Jimah ; Miguel Beckford ; Tiffany Caza ; David Fernandez ; Nick Huang [États-Unis] ; Manuel Duarte ; Joshua Lewis ; Hind J. Fadel [États-Unis] ; Eric M. Poeschla [États-Unis] ; Katalin Banki [États-Unis] ; Andras Perl [États-Unis]Source :
- JCI insight [ 2379-3708 ] ; 2020.
Abstract
Overexpression and long terminal repeat (LTR) polymorphism of the HRES‑1/Rab4 human endogenous retrovirus locus have been associated with T cell activation and disease manifestations in systemic lupus erythematosus (SLE). Although genomic DNA methylation is diminished overall in SLE, its role in HRES-1/Rab4 expression is unknown. Therefore, we determined how lupus-associated polymorphic rs451401 alleles of the LTR regulate transcription from the HRES-1/Rab4 promoter and thus affect T cell activation. The results showed that cytosine-119 is hypermethylated while cytosine-51 of the promoter and the LTR enhancer are hypomethylated in SLE. Pharmacologic or genetic inactivation of DNA methyltransferase 1 augmented the expression of HRES-1/Rab4. The minimal promoter was selectively recognized by metabolic stress sensor NRF1 when cytosine-119 but not cytosine-51 was methylated, and NRF1 stimulated HRES-1/Rab4 expression in human T cells. In turn, IRF2 and PSIP1 bound to the LTR enhancer and exerted control over HRES-1/Rab4 expression in rs451401 genotype- and methylation-dependent manners. The LTR enhancer conferred markedly greater expression of HRES-1/Rab4 in subjects with rs451401CC over rs451401GG alleles that in turn promoted mechanistic target of rapamycin (mTOR) activation upon T cell receptor stimulation. HRES-1/Rab4 alone robustly activated mTOR in human T cells. These findings identify HRES-1/Rab4 as a methylation- and rs451401 allele-dependent transducer of environmental stress and controller of T cell activation.
DOI: 10.1172/jci.insight.134010
PubMed: 31805010
PubMed Central: PMC7030820
Affiliations:
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Poeschla</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Banki, Katalin" sort="Banki, Katalin" uniqKey="Banki K" first="Katalin" last="Banki">Katalin Banki</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pathology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York</wicri:regionArea><placeName><region type="state">État de New 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Godavarthy</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation></author><author><name sortKey="Kelly, Ryan" sort="Kelly, Ryan" uniqKey="Kelly R" first="Ryan" last="Kelly">Ryan Kelly</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation></author><author><name sortKey="Jimah, John" sort="Jimah, John" uniqKey="Jimah J" first="John" last="Jimah">John Jimah</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation></author><author><name sortKey="Beckford, Miguel" sort="Beckford, Miguel" uniqKey="Beckford M" first="Miguel" last="Beckford">Miguel Beckford</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation></author><author><name sortKey="Caza, Tiffany" sort="Caza, Tiffany" uniqKey="Caza T" first="Tiffany" last="Caza">Tiffany Caza</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation><affiliation><nlm:affiliation>Department of Microbiology and Immunology, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author><author><name sortKey="Fernandez, David" sort="Fernandez, David" uniqKey="Fernandez D" first="David" last="Fernandez">David Fernandez</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation><affiliation><nlm:affiliation>Department of Microbiology and Immunology, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation></author><author><name sortKey="Huang, Nick" sort="Huang, Nick" uniqKey="Huang N" first="Nick" last="Huang">Nick Huang</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Duarte, Manuel" sort="Duarte, Manuel" uniqKey="Duarte M" first="Manuel" last="Duarte">Manuel Duarte</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation></author><author><name sortKey="Lewis, Joshua" sort="Lewis, Joshua" uniqKey="Lewis J" first="Joshua" last="Lewis">Joshua Lewis</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation></author><author><name sortKey="Fadel, Hind J" sort="Fadel, Hind J" uniqKey="Fadel H" first="Hind J" last="Fadel">Hind J. Fadel</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Poeschla, Eric M" sort="Poeschla, Eric M" uniqKey="Poeschla E" first="Eric M" last="Poeschla">Eric M. Poeschla</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Banki, Katalin" sort="Banki, Katalin" uniqKey="Banki K" first="Katalin" last="Banki">Katalin Banki</name><affiliation wicri:level="2"><nlm:affiliation>Department of Pathology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Pathology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Perl, Andras" sort="Perl, Andras" uniqKey="Perl A" first="Andras" last="Perl">Andras Perl</name><affiliation><nlm:affiliation>Division of Rheumatology, Department of Medicine.</nlm:affiliation><wicri:noCountry code="subField">Department of Medicine</wicri:noCountry></affiliation><affiliation><nlm:affiliation>Department of Microbiology and Immunology, and.</nlm:affiliation><wicri:noCountry code="subField">and</wicri:noCountry></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry and Molecular Biology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry and Molecular Biology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author></analytic><series><title level="j">JCI insight</title><idno type="eISSN">2379-3708</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Overexpression and long terminal repeat (LTR) polymorphism of the HRES‑1/Rab4 human endogenous retrovirus locus have been associated with T cell activation and disease manifestations in systemic lupus erythematosus (SLE). Although genomic DNA methylation is diminished overall in SLE, its role in HRES-1/Rab4 expression is unknown. Therefore, we determined how lupus-associated polymorphic rs451401 alleles of the LTR regulate transcription from the HRES-1/Rab4 promoter and thus affect T cell activation. The results showed that cytosine-119 is hypermethylated while cytosine-51 of the promoter and the LTR enhancer are hypomethylated in SLE. Pharmacologic or genetic inactivation of DNA methyltransferase 1 augmented the expression of HRES-1/Rab4. The minimal promoter was selectively recognized by metabolic stress sensor NRF1 when cytosine-119 but not cytosine-51 was methylated, and NRF1 stimulated HRES-1/Rab4 expression in human T cells. In turn, IRF2 and PSIP1 bound to the LTR enhancer and exerted control over HRES-1/Rab4 expression in rs451401 genotype- and methylation-dependent manners. The LTR enhancer conferred markedly greater expression of HRES-1/Rab4 in subjects with rs451401CC over rs451401GG alleles that in turn promoted mechanistic target of rapamycin (mTOR) activation upon T cell receptor stimulation. HRES-1/Rab4 alone robustly activated mTOR in human T cells. These findings identify HRES-1/Rab4 as a methylation- and rs451401 allele-dependent transducer of environmental stress and controller of T cell activation.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">31805010</PMID><DateRevised><Year>2020</Year><Month>07</Month><Day>07</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2379-3708</ISSN><JournalIssue CitedMedium="Internet"><Volume>5</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>01</Month><Day>16</Day></PubDate></JournalIssue><Title>JCI insight</Title><ISOAbbreviation>JCI Insight</ISOAbbreviation></Journal><ArticleTitle>Lupus-associated endogenous retroviral LTR polymorphism and epigenetic imprinting promote HRES-1/RAB4 expression and mTOR activation.</ArticleTitle><ELocationID EIdType="doi" ValidYN="Y">10.1172/jci.insight.134010</ELocationID><ELocationID EIdType="pii" ValidYN="Y">134010</ELocationID><Abstract><AbstractText>Overexpression and long terminal repeat (LTR) polymorphism of the HRES‑1/Rab4 human endogenous retrovirus locus have been associated with T cell activation and disease manifestations in systemic lupus erythematosus (SLE). Although genomic DNA methylation is diminished overall in SLE, its role in HRES-1/Rab4 expression is unknown. Therefore, we determined how lupus-associated polymorphic rs451401 alleles of the LTR regulate transcription from the HRES-1/Rab4 promoter and thus affect T cell activation. The results showed that cytosine-119 is hypermethylated while cytosine-51 of the promoter and the LTR enhancer are hypomethylated in SLE. Pharmacologic or genetic inactivation of DNA methyltransferase 1 augmented the expression of HRES-1/Rab4. The minimal promoter was selectively recognized by metabolic stress sensor NRF1 when cytosine-119 but not cytosine-51 was methylated, and NRF1 stimulated HRES-1/Rab4 expression in human T cells. In turn, IRF2 and PSIP1 bound to the LTR enhancer and exerted control over HRES-1/Rab4 expression in rs451401 genotype- and methylation-dependent manners. The LTR enhancer conferred markedly greater expression of HRES-1/Rab4 in subjects with rs451401CC over rs451401GG alleles that in turn promoted mechanistic target of rapamycin (mTOR) activation upon T cell receptor stimulation. HRES-1/Rab4 alone robustly activated mTOR in human T cells. These findings identify HRES-1/Rab4 as a methylation- and rs451401 allele-dependent transducer of environmental stress and controller of T cell activation.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Godavarthy</LastName><ForeName>Aparna</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kelly</LastName><ForeName>Ryan</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Jimah</LastName><ForeName>John</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Beckford</LastName><ForeName>Miguel</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Caza</LastName><ForeName>Tiffany</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fernandez</LastName><ForeName>David</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, and.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Huang</LastName><ForeName>Nick</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Duarte</LastName><ForeName>Manuel</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lewis</LastName><ForeName>Joshua</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Fadel</LastName><ForeName>Hind J</ForeName><Initials>HJ</Initials><AffiliationInfo><Affiliation>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Poeschla</LastName><ForeName>Eric M</ForeName><Initials>EM</Initials><AffiliationInfo><Affiliation>Department of Molecular Medicine, Mayo Clinic College of Medicine, Rochester, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Banki</LastName><ForeName>Katalin</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Department of Pathology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Perl</LastName><ForeName>Andras</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Division of Rheumatology, Department of Medicine.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology and Immunology, and.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biochemistry and Molecular Biology, State University of New York, Upstate Medical University, College of Medicine, Syracuse, New York, 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Fadel</name><name sortKey="Perl, Andras" sort="Perl, Andras" uniqKey="Perl A" first="Andras" last="Perl">Andras Perl</name><name sortKey="Poeschla, Eric M" sort="Poeschla, Eric M" uniqKey="Poeschla E" first="Eric M" last="Poeschla">Eric M. Poeschla</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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