ArticleMolecular cell2023
RANK ligand converts the NCoR/HDAC3 co-repressor to a PGC1β- and RNA-dependent co-activator of osteoclast gene expression.
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Article in Molecular cell, 2023. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 23 papers.
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23 citing papers in PubMed, 19 citations in OpenAlex.
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Authors and funding
28 authors at 6 institutions in 3 countries.
Yohei AbeDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Eric R KofmanDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA; Stem Cell Program, University of California San Diego, La Jolla, CA 92093, USA; Institute for Genomic Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Maria AlmeidaDivision of Endocrinology and Metabolism, Center for Osteoporosis and Metabolic Bone Diseases, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA; Department of Orthopedic Surgery, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA; Central Arkansas Veterans Healthcare System, Little Rock, AR 72205, USA.
Zhengyu OuyangDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Filipa PonteDivision of Endocrinology and Metabolism, Center for Osteoporosis and Metabolic Bone Diseases, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA.
Jasmine R MuellerDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA; Stem Cell Program, University of California San Diego, La Jolla, CA 92093, USA; Institute for Genomic Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Grisel Cruz-BecerraDepartment of Molecular Biology, University of California San Diego, La Jolla, CA 92093, USA.
Mashito SakaiDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA; Biochemistry and Molecular Biology, Nippon Medical School Hospital, Tokyo 113-8602, Japan.
Thomas A ProhaskaDepartment of Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Nathanael J SpannDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Ana Resende-CoelhoDivision of Endocrinology and Metabolism, Center for Osteoporosis and Metabolic Bone Diseases, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA.
Jason S SeidmanDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Joshua D StenderDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Havilah TaylorDepartment of Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Weiwei FanGene Expression Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
Verena M LinkDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA; Faculty of Biology, Department II, Ludwig-Maximilians Universität München, Planegg-Martinsried 82152, Germany.
Isidoro CoboDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Johannes C M SchlachetzkiDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Takao HamakuboDepartment of Protein-Protein Interaction Research, Institute for Advanced Medical Sciences, Nippon Medical School, Tokyo 113-8602, Japan.
Kristen JepsenInstitute for Genomic Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Juro SakaiDivision of Metabolic Medicine, Research Center for Advanced Science and Technology, The University of Tokyo, Tokyo 153-8904, Japan; Division of Molecular Physiology and Metabolism, Tohoku University Graduate School of Medicine, Sendai 980-8575, Japan.
Michael DownesGene Expression Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
Ronald M EvansGene Expression Laboratory, Salk Institute for Biological Studies, La Jolla, CA 92037, USA.
Gene W YeoDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA; Stem Cell Program, University of California San Diego, La Jolla, CA 92093, USA; Institute for Genomic Medicine, University of California San Diego, La Jolla, CA 92093, USA.
James T KadonagaDepartment of Molecular Biology, University of California San Diego, La Jolla, CA 92093, USA.
Stavros C ManolagasDivision of Endocrinology and Metabolism, Center for Osteoporosis and Metabolic Bone Diseases, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA; Department of Orthopedic Surgery, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USA; Central Arkansas Veterans Healthcare System, Little Rock, AR 72205, USA.
Michael G RosenfeldDepartment of Medicine, University of California San Diego, La Jolla, CA 92093, USA.
Christopher K GlassDepartment of Cellular and Molecular Medicine, University of California San Diego, La Jolla, CA 92093, USA; Department of Medicine, University of California San Diego, La Jolla, CA 92093, USA. Electronic address: ckg@ucsd.edu.
University of California San Diego · USSalk Institute for Biological Studies · USCentral Arkansas Veterans Healthcare System · USUniversity of Arkansas for Medical Sciences · USNippon Medical School · JPTohoku University · JP
Funding
Transgenic & Knock-out MouseP30DK063491 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI Andrea L Hevener · 2003 to 2026
$40.4MTranscriptional GenomicsP01HL088093 · NHLBI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI WITZTUM, JOSEPH L. · 2008 to 2018
$26.4MSYNTHETIC SYSTEMSP50GM085764 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI WINZELER, ELIZABETH A · 2010 to 2018
$23.3MUnderstanding the Negative Prognostic Impact of Intraosseous Focal Lesions in Multiple MyelomaP20GM125503 · NIGMS · UNIV OF ARKANSAS FOR MED SCIS · PI CHARLES A O'BRIEN · 2018 to 2026
$23.0MHORMONAL AND DEVELOPMENTAL REGULATION OF GENE EXPRESSIONR01DK018477 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI ROSENFELD, MICHAEL G · 1986 to 2025
$12.7MTissue-specific roles of FXR in CVD and NASHP01HL147835 · NHLBI · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI EVANS, RONALD M · 2020 to 2024
$12.2MTranscriptional co-regulators and macrophage gene expressionR01DK091183 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI GLASS, CHRISTOPHER K · 2011 to 2025
$9.9MMechanisms of Eukaryotic Gene RegulationR35GM118060 · NIGMS · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI James T. Kadonaga · 2016 to 2026
$7.5MREGULATION OF NEUROENDOCRINE SWITCHING EVENTSR01DK039949 · NIDDK · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI ROSENFELD, MICHAEL G · 1996 to 2024
$2.4MDifferent consequences of cellular aging in cortical versus cancellous bone- ResubmissionR01AG068449 · NIA · UNIV OF ARKANSAS FOR MED SCIS · PI ALMEIDA, MARIA JOSE, O'BRIEN, CHARLES A · 2021 to 2025
$1.9MIllumina NovaSeq 6000 Sequencing SystemS10OD026929 · OD · UNIVERSITY OF CALIFORNIA, SAN DIEGO · PI JEPSEN, KRISTEN LYNN · 2019 to 2019
$600kInterleukin 18 and Atherosclerosis during StressR21HL088083 · NHLBI · SCRIPPS RESEARCH INSTITUTE, THE · PI CONTI, BRUNO · 2008 to 2009
$520kNHLBI NIH HHS P01 HL088093NHLBI NIH HHS P01 HL147835NHLBI NIH HHS R21 HL088083NIA NIH HHS R01 AG068449NIDDK NIH HHS P30 DK063491NIDDK NIH HHS R01 DK018477NIDDK NIH HHS R01 DK039949NIDDK NIH HHS R01 DK091183NIGMS NIH HHS P20 GM125503NIGMS NIH HHS P50 GM085764NIGMS NIH HHS R35 GM118060NIH HHS S10 OD026929
Abstract
The nuclear receptor co-repressor (NCoR) complex mediates transcriptional repression dependent on histone deacetylation by histone deacetylase 3 (HDAC3) as a component of the complex. Unexpectedly, we found that signaling by the receptor activator of nuclear factor κB (RANK) converts the NCoR/HDAC3 co-repressor complex to a co-activator of AP-1 and NF-κB target genes that are required for mouse osteoclast differentiation. Accordingly, the dominant function of NCoR/HDAC3 complexes in response to RANK signaling is to activate, rather than repress, gene expression. Mechanistically, RANK signaling promotes RNA-dependent interaction of the transcriptional co-activator PGC1β with the NCoR/HDAC3 complex, resulting in the activation of PGC1β and inhibition of HDAC3 activity for acetylated histone H3. Non-coding RNAs Dancr and Rnu12, which are associated with altered human bone homeostasis, promote NCoR/HDAC3 complex assembly and are necessary for RANKL-induced osteoclast differentiation in vitro. These findings may be prototypic for signal-dependent functions of NCoR in other biological contexts.
Indexed as
OsteoclastsRNAAnimalsCo-Repressor ProteinsGene ExpressionHistone Deacetylase 3HumansMiceNuclear Receptor Co-Repressor 1RANK LigandCo-Repressor ProteinsHistone Deacetylase 3Nuclear Receptor Co-Repressor 1RANK LigandRNAAP-1co-activatordeacetylationgene expressionH3K27acHDAC3NCoRNF-κBnon-coding RNAosteoclastPGC1βRANK
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