Olig1 Acetylation and Nuclear Export Mediate Oligodendrocyte Development
The oligodendrocyte transcription factor Olig1 is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation of Olig1 protein occurs during brain development and in multiple sclerosis, but the detailed molecular mechanism of this translocation remai...
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Published in | The Journal of neuroscience Vol. 35; no. 48; pp. 15875 - 15893 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
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United States
Society for Neuroscience
02.12.2015
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Abstract | The oligodendrocyte transcription factor Olig1 is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation of Olig1 protein occurs during brain development and in multiple sclerosis, but the detailed molecular mechanism of this translocation remains elusive. Here, we report that Olig1 acetylation and deacetylation drive its active translocation between the nucleus and the cytoplasm in both mouse and rat oligodendrocytes. We identified three functional nuclear export sequences (NES) localized in the basic helix-loop-helix domain and one specific acetylation site at Lys 150 (human Olig1) in NES1. Olig1 acetylation and deacetylation are regulated by the acetyltransferase CREB-binding protein and the histone deacetylases HDAC1, HDAC3, and HDAC10. Acetylation of Olig1 decreased its chromatin association, increased its interaction with inhibitor of DNA binding 2 and facilitated its retention in the cytoplasm of mature oligodendrocytes. These studies establish that acetylation of Olig1 regulates its chromatin dissociation and subsequent translocation to the cytoplasm and is required for its function in oligodendrocyte maturation. |
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AbstractList | The oligodendrocyte transcription factor Oligl is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation of Oligl protein occurs during brain development and in multiple sclerosis, but the detailed molecular mechanism of this translocation remains elusive. Here, we report that Oligl acetylation and deacetylation drive its active translocation between the nucleus and the cytoplasm in both mouse and rat oligodendrocytes. We identified three functional nuclear export sequences (NES) localized in the basic helix-loop-helix domain and one specific acetylation site at Lys 150 (human Olig1) in NES1. Oligl acetylation and deacetylation are regulated by the acetyltransferase CREB-binding protein and the histone deacetylases HDAC1, HDAC3, and HDAC10. Acetylation of Oligl decreased its chromatin association, increased its interaction with inhibitor of DNA binding 2 and facilitated its retention in the cytoplasm of mature oligodendrocytes. These studies establish that acetylation of Oligl regulates its chromatin dissociation and subsequent translocation to the cytoplasm and is required for its function in oligodendrocyte maturation. The oligodendrocyte transcription factor Olig1 is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation of Olig1 protein occurs during brain development and in multiple sclerosis, but the detailed molecular mechanism of this translocation remains elusive. Here, we report that Olig1 acetylation and deacetylation drive its active translocation between the nucleus and the cytoplasm in both mouse and rat oligodendrocytes. We identified three functional nuclear export sequences (NES) localized in the basic helix-loop-helix domain and one specific acetylation site at Lys 150 (human Olig1) in NES1. Olig1 acetylation and deacetylation are regulated by the acetyltransferase CREB-binding protein and the histone deacetylases HDAC1, HDAC3, and HDAC10. Acetylation of Olig1 decreased its chromatin association, increased its interaction with inhibitor of DNA binding 2 and facilitated its retention in the cytoplasm of mature oligodendrocytes. These studies establish that acetylation of Olig1 regulates its chromatin dissociation and subsequent translocation to the cytoplasm and is required for its function in oligodendrocyte maturation. The oligodendrocyte transcription factor Olig1 is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation of Olig1 protein occurs during brain development and in multiple sclerosis, but the detailed molecular mechanism of this translocation remains elusive. Here, we report that Olig1 acetylation and deacetylation drive its active translocation between the nucleus and the cytoplasm in both mouse and rat oligodendrocytes. We identified three functional nuclear export sequences (NES) localized in the basic helix-loop-helix domain and one specific acetylation site at Lys 150 (human Olig1) in NES1. Olig1 acetylation and deacetylation are regulated by the acetyltransferase CREB-binding protein and the histone deacetylases HDAC1, HDAC3, and HDAC10. Acetylation of Olig1 decreased its chromatin association, increased its interaction with inhibitor of DNA binding 2 and facilitated its retention in the cytoplasm of mature oligodendrocytes. These studies establish that acetylation of Olig1 regulates its chromatin dissociation and subsequent translocation to the cytoplasm and is required for its function in oligodendrocyte maturation. SIGNIFICANCE STATEMENT The nuclear to cytoplasmic translocation of Olig1 protein has been observed during mouse and human brain development and in multiple sclerosis in several studies, but the detailed molecular mechanism of this translocation remains elusive. Here, we provide insight into the mechanism by which acetylation of Olig1 regulates its unique nuclear-cytoplasmic shuttling during oligodendrocyte development and how the acetylation status of Olig1 modulates its distinct function in the nucleus versus the cytoplasm. The current study provides a unique example of a lineage-specific transcription factor that is actively translocated from the nucleus to the cytoplasm as the cell differentiates. Importantly, we demonstrate that this process is tightly controlled by acetylation at a single lysine. |
Author | Macklin, Wendy B Dai, Jinxiang Jin, Weilin Bercury, Kathryn K |
Author_xml | – sequence: 1 givenname: Jinxiang surname: Dai fullname: Dai, Jinxiang organization: Department of Cell and Developmental Biology, University of Colorado School of Medicine, Aurora, Colorado 80045 – sequence: 2 givenname: Kathryn K surname: Bercury fullname: Bercury, Kathryn K organization: Department of Cell and Developmental Biology, University of Colorado School of Medicine, Aurora, Colorado 80045 – sequence: 3 givenname: Weilin surname: Jin fullname: Jin, Weilin organization: Institute of Bio-Nano-Science and Engineering, Department of Instrument Science and Engineering, School of Electronic Information and Electrical Engineering, and School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai 200240, China – sequence: 4 givenname: Wendy B surname: Macklin fullname: Macklin, Wendy B email: Wendy.Macklin@ucdenver.edu organization: Department of Cell and Developmental Biology, University of Colorado School of Medicine, Aurora, Colorado 80045, Wendy.Macklin@ucdenver.edu |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/26631469$$D View this record in MEDLINE/PubMed |
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Keywords | acetylation nuclear export Olig1 |
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Snippet | The oligodendrocyte transcription factor Olig1 is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation... The oligodendrocyte transcription factor Oligl is critical for both oligodendrocyte development and remyelination in mice. Nuclear to cytoplasmic translocation... |
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SubjectTerms | Active Transport, Cell Nucleus - drug effects Active Transport, Cell Nucleus - genetics Age Factors Animals Animals, Newborn Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Cells, Cultured CREB-Binding Protein - genetics CREB-Binding Protein - metabolism Embryo, Mammalian Female Gene Expression Regulation, Developmental - genetics Histone Acetyltransferases - metabolism Histone Deacetylases - genetics Histone Deacetylases - metabolism Humans Male Mice Mice, Inbred C57BL Mice, Transgenic Mutation - genetics Nestin - genetics Nestin - metabolism Oligodendroglia - physiology p300-CBP Transcription Factors - genetics p300-CBP Transcription Factors - metabolism Rats SOXE Transcription Factors - genetics SOXE Transcription Factors - metabolism Stem Cells - physiology |
Title | Olig1 Acetylation and Nuclear Export Mediate Oligodendrocyte Development |
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