The Histone Demethylases JMJD1A and JMJD2B Are Transcriptional Targets of Hypoxia-inducible Factor HIF

Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these m...

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Published in	The Journal of biological chemistry Vol. 283; no. 52; pp. 36542 - 36552
Main Authors	Beyer, Sophie, Kristensen, Malene Maag, Jensen, Kim Steen, Johansen, Jens Vilstrup, Staller, Peter
Format	Journal Article
Language	English
Published	United States Elsevier Inc 26.12.2008 American Society for Biochemistry and Molecular Biology
Subjects	Arginine - chemistry Base Sequence Gene Expression Regulation HeLa Cells Histone Deacetylases - metabolism Histones - chemistry Humans Hypoxia Hypoxia-Inducible Factor 1 - metabolism Jumonji Domain-Containing Histone Demethylases Kidney - embryology Lysine - chemistry Microscopy, Fluorescence Molecular Sequence Data Oxidoreductases, N-Demethylating - physiology Transcription Factors - physiology Transcription, Chromatin, and Epigenetics
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Abstract	Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1α binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program.
AbstractList	Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1α binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program. Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1Î± binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program. Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1α binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program. Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1alpha binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program. Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1alpha binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program.Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1alpha binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program. Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins. Histone methylation occurs on arginine and lysine residues and is involved in the regulation of gene transcription. A dynamic control of these modifications is exerted by histone methyltransferases and the recently discovered histone demethylases. Here we show that the hypoxia-inducible factor HIF-1Î± binds to specific recognition sites in the genes encoding the jumonji family histone demethylases JMJD1A and JMJD2B and induces their expression. Accordingly, hypoxic cells express elevated levels of JMJD1A and JMJD2B mRNA and protein. Furthermore, we find increased expression of JMJD1A and JMJD2B in renal cancer cells that have lost the von Hippel Lindau tumor suppressor protein VHL and therefore display a deregulated expression of hypoxia-inducible factor. Studies on ectopically expressed JMJD1A and JMJD2B indicate that both proteins retain their histone lysine demethylase activity in hypoxia and thereby might impact the hypoxic gene expression program.
Author	Beyer, Sophie Jensen, Kim Steen Staller, Peter Johansen, Jens Vilstrup Kristensen, Malene Maag
AuthorAffiliation	Biotech Research and Innovation Centre and the § Bioinformatics Centre, University of Copenhagen, DK-2200, Copenhagen Denmark
AuthorAffiliation_xml	– name: Biotech Research and Innovation Centre and the § Bioinformatics Centre, University of Copenhagen, DK-2200, Copenhagen Denmark
Author_xml	– sequence: 1 givenname: Sophie surname: Beyer fullname: Beyer, Sophie organization: Biotech Research and Innovation Centre, University of Copenhagen, DK-2200, Copenhagen Denmark – sequence: 2 givenname: Malene Maag surname: Kristensen fullname: Kristensen, Malene Maag organization: Biotech Research and Innovation Centre, University of Copenhagen, DK-2200, Copenhagen Denmark – sequence: 3 givenname: Kim Steen surname: Jensen fullname: Jensen, Kim Steen organization: Biotech Research and Innovation Centre, University of Copenhagen, DK-2200, Copenhagen Denmark – sequence: 4 givenname: Jens Vilstrup surname: Johansen fullname: Johansen, Jens Vilstrup organization: Biotech Research and Innovation Centre, University of Copenhagen, DK-2200, Copenhagen Denmark – sequence: 5 givenname: Peter surname: Staller fullname: Staller, Peter email: peter.staller@bric.ku.dk organization: Biotech Research and Innovation Centre, University of Copenhagen, DK-2200, Copenhagen Denmark
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/18984585$$D View this record in MEDLINE/PubMed
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 This work was supported by the Biotech Research and Innovation Centre, the Danish Cancer Society, the Danish Cancer Research Foundation, Lykfeldts Legat, and the Novo Nordisk Foundation. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. To whom correspondence should be addressed: Ole Maaløes Vej 5, DK-2200 Copenhagen, Denmark. Tel.: 45-3532-5682; Fax: 45-3532-5669; E-mail: peter.staller@bric.ku.dk. The on-line version of this article (available at http://www.jbc.org) contains supplemental Fig. S1 and Tables S2 and S2.
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Snippet	Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins.... Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins.... Posttranslational histone modifications serve to store epigenetic information and control both nucleosome assembly and recruitment of non-histone proteins....
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SubjectTerms	Arginine - chemistry Base Sequence Gene Expression Regulation HeLa Cells Histone Deacetylases - metabolism Histones - chemistry Humans Hypoxia Hypoxia-Inducible Factor 1 - metabolism Jumonji Domain-Containing Histone Demethylases Kidney - embryology Lysine - chemistry Microscopy, Fluorescence Molecular Sequence Data Oxidoreductases, N-Demethylating - physiology Transcription Factors - physiology Transcription, Chromatin, and Epigenetics
Title	The Histone Demethylases JMJD1A and JMJD2B Are Transcriptional Targets of Hypoxia-inducible Factor HIF
URI	https://dx.doi.org/10.1074/jbc.M804578200 http://www.jbc.org/content/283/52/36542.abstract https://www.ncbi.nlm.nih.gov/pubmed/18984585 https://www.proquest.com/docview/48190664 https://www.proquest.com/docview/69904611 https://pubmed.ncbi.nlm.nih.gov/PMC2662309
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