L1 retrotransposition in neurons is modulated by MeCP2

Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes. Active L1 retrotransposons can impact the genome in a variety of ways, creating insertions, deletions, new splice sites or gene expression fine-tuning. We have sho...

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Published in	Nature (London) Vol. 468; no. 7322; pp. 443 - 446
Main Authors	Muotri, Alysson R, Gage, Fred H, Marchetto, Maria C. N, Coufal, Nicole G, Oefner, Ruth, Yeo, Gene, Nakashima, Kinichi
Format	Journal Article
Language	English
Published	London Nature Publishing Group UK 18.11.2010 Nature Publishing Group
Subjects	5' Untranslated Regions - genetics 631/208/2489/144 631/208/726/2001/1428 692/420 692/699/375/366 Animals Brain - cytology Brain - metabolism DNA Methylation Gene expression Gene Silencing Genetic aspects Genetic transcription Humanities and Social Sciences Humans Induced Pluripotent Stem Cells - metabolism letter Long Interspersed Nucleotide Elements - genetics Male Methyl-CpG-Binding Protein 2 - deficiency Methyl-CpG-Binding Protein 2 - genetics Methyl-CpG-Binding Protein 2 - metabolism Methylation Mice multidisciplinary Mutation Nervous system diseases Neuroepithelial Cells - metabolism Neurons - metabolism Organ Specificity Promoter Regions, Genetic - genetics Rats Recombination, Genetic - genetics Retrotransposons Rett Syndrome - genetics Rett Syndrome - pathology Rodents Science Science (multidisciplinary) Stem cells Transcription, Genetic - genetics United States
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Abstract	Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes. Active L1 retrotransposons can impact the genome in a variety of ways, creating insertions, deletions, new splice sites or gene expression fine-tuning. We have shown previously that L1 retrotransposons are capable of mobilization in neuronal progenitor cells from rodents and humans and evidence of massive L1 insertions was observed in adult brain tissues but not in other somatic tissues. In addition, L1 mobility in the adult hippocampus can be influenced by the environment. The neuronal specificity of somatic L1 retrotransposition in neural progenitors is partially due to the transition of a Sox2/HDAC1 repressor complex to a Wnt-mediated T-cell factor/lymphoid enhancer factor (TCF/LEF) transcriptional activator. The transcriptional switch accompanies chromatin remodelling during neuronal differentiation, allowing a transient stimulation of L1 transcription. The activity of L1 retrotransposons during brain development can have an impact on gene expression and neuronal function, thereby increasing brain-specific genetic mosaicism. Further understanding of the molecular mechanisms that regulate L1 expression should provide new insights into the role of L1 retrotransposition during brain development. Here we show that L1 neuronal transcription and retrotransposition in rodents are increased in the absence of methyl-CpG-binding protein 2 (MeCP2), a protein involved in global DNA methylation and human neurodevelopmental diseases. Using neuronal progenitor cells derived from human induced pluripotent stem cells and human tissues, we revealed that patients with Rett syndrome (RTT), carrying MeCP2 mutations, have increased susceptibility for L1 retrotransposition. Our data demonstrate that L1 retrotransposition can be controlled in a tissue-specific manner and that disease-related genetic mutations can influence the frequency of neuronal L1 retrotransposition. Our findings add a new level of complexity to the molecular events that can lead to neurological disorders.
AbstractList	Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes. Active L1 retrotransposons can impact the genome in a variety of ways, creating insertions, deletions, new splice sites or gene expression fine-tuning. We have shown previously that L1 retrotransposons are capable of mobilization in neuronal progenitor cells from rodents and humans and evidence of massive L1 insertions was observed in adult brain tissues but not in other somatic tissues. In addition, L1 mobility in the adult hippocampus can be influenced by the environment. The neuronal specificity of somatic L1 retrotransposition in neural progenitors is partially due to the transition of a Sox2/HDAC1 repressor complex to a Wnt-mediated T-cell factor/lymphoid enhancer factor (TCF/LEF) transcriptional activator. The transcriptional switch accompanies chromatin remodelling during neuronal differentiation, allowing a transient stimulation of L1 transcription. The activity of L1 retrotransposons during brain development can have an impact on gene expression and neuronal function, thereby increasing brain-specific genetic mosaicism. Further understanding of the molecular mechanisms that regulate L1 expression should provide new insights into the role of L1 retrotransposition during brain development. Here we show that L1 neuronal transcription and retrotransposition in rodents are increased in the absence of methyl-CpG-binding protein 2 (MeCP2), a protein involved in global DNA methylation and human neurodevelopmental diseases. Using neuronal progenitor cells derived from human induced pluripotent stem cells and human tissues, we revealed that patients with Rett syndrome (RTT), carrying MeCP2 mutations, have increased susceptibility for L1 retrotransposition. Our data demonstrate that L1 retrotransposition can be controlled in a tissue-specific manner and that disease-related genetic mutations can influence the frequency of neuronal L1 retrotransposition. Our findings add a new level of complexity to the molecular events that can lead to neurological disorders. Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes. Active L1 retrotransposons can impact the genome in a variety of ways, creating insertions, deletions, new splice sites or gene expression fine-tuning. We have shown previously that L1 retrotransposons are capable of mobilization in neuronal progenitor cells from rodents and humans and evidence of massive L1 insertions was observed in adult brain tissues but not in other somatic tissues. In addition, L1 mobility in the adult hippocampus can be influenced by the environment. The neuronal specificity of somatic L1 retrotransposition in neural progenitors is partially due to the transition of a Sox2/HDAC1 repressor complex to a Wnt-mediated T-cell factor/lymphoid enhancer factor (TCF/LEF) transcriptional activator. The transcriptional switch accompanies chromatin remodelling during neuronal differentiation, allowing a transient stimulation of L1 transcription. The activity of L1 retrotransposons during brain development can have an impact on gene expression and neuronal function, thereby increasing brain-specific genetic mosaicism. Further understanding of the molecular mechanisms that regulate L1 expression should provide new insights into the role of L1 retrotransposition during brain development. Here we show that L1 neuronal transcription and retrotransposition in rodents are increased in the absence of methyl-CpG-binding protein 2 (MeCP2), a protein involved in global DNA methylation and human neurodevelopmental diseases. Using neuronal progenitor cells derived from human induced pluripotent stem cells and human tissues, we revealed that patients with Rett syndrome (RTT), carrying MeCP2 mutations, have increased susceptibility for L1 retrotransposition. Our data demonstrate that L1 retrotransposition can be controlled in a tissue-specific manner and that disease-related genetic mutations can influence the frequency of neuronal L1 retrotransposition. Our findings add a new level of complexity to the molecular events that can lead to neurological disorders. [PUBLICATION ABSTRACT] Retrotransposition in neurons L1 retrotransposons are dynamically regulated and active genomic elements that affect gene expression and neuronal function throughout brain development. According to a new study by Alysson Muotri and colleagues, the absence of MeCP2, a modulator of DNA methylation implicated in several neurodevelopmental disorders, increases L1 retrotransposon activity in rodent models. This increase in susceptibility to L1 retrotransposition is duplicated in iPS cells derived from patients with Rett syndrome. These data correlations suggest that disease-related genetic mutations may influence L1 retrotransposon activity, adding another layer of complexity to our understanding of molecular neurological disorders. Long interspersed nuclear elements-1 (L1) retrotransposons affect gene expression and neuronal function throughout brain development. These authors show that the absence of methyl-CpG-binding protein 2, a modulator of DNA methylation implicated in several neurodevelopmental disorders, increases L1 retrotransposon activity in rodent models, with this increase in susceptibility duplicated in patients with Rett syndrome. These correlations suggest that disease-related genetic mutations may influence L1 retrotransposon activity. Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes 1 , 2 , 3 . Active L1 retrotransposons can impact the genome in a variety of ways, creating insertions, deletions, new splice sites or gene expression fine-tuning 4 , 5 , 6 . We have shown previously that L1 retrotransposons are capable of mobilization in neuronal progenitor cells from rodents and humans and evidence of massive L1 insertions was observed in adult brain tissues but not in other somatic tissues 7 , 8 . In addition, L1 mobility in the adult hippocampus can be influenced by the environment 9 . The neuronal specificity of somatic L1 retrotransposition in neural progenitors is partially due to the transition of a Sox2/HDAC1 repressor complex to a Wnt-mediated T-cell factor/lymphoid enhancer factor (TCF/LEF) transcriptional activator 7 , 10 . The transcriptional switch accompanies chromatin remodelling during neuronal differentiation, allowing a transient stimulation of L1 transcription 7 . The activity of L1 retrotransposons during brain development can have an impact on gene expression and neuronal function, thereby increasing brain-specific genetic mosaicism 11 , 12 . Further understanding of the molecular mechanisms that regulate L1 expression should provide new insights into the role of L1 retrotransposition during brain development. Here we show that L1 neuronal transcription and retrotransposition in rodents are increased in the absence of methyl-CpG-binding protein 2 (MeCP2), a protein involved in global DNA methylation and human neurodevelopmental diseases. Using neuronal progenitor cells derived from human induced pluripotent stem cells and human tissues, we revealed that patients with Rett syndrome (RTT), carrying MeCP2 mutations, have increased susceptibility for L1 retrotransposition. Our data demonstrate that L1 retrotransposition can be controlled in a tissue-specific manner and that disease-related genetic mutations can influence the frequency of neuronal L1 retrotransposition. Our findings add a new level of complexity to the molecular events that can lead to neurological disorders. Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes (1-3). Active Li retrotransposons can impact the genome in a variety of ways, creating insertions, deletions, new splice sites or gene expression fine-tuning (4-6). We have shown previously that Li retrotransposons are capable of mobilization in neuronal progenitor cells from rodents and humans and evidence of massive L1 insertions was observed in adult brain tissues but not in other somatic tissues (7,8). In addition, Li mobility in the adult hippocampus can be influenced by the environment (9). The neuronal specificity of somatic Li retrotransposition in neural progenitors is partially due to the transition of a Sox2/HDACi repressor complex to a W nt-mediated T-cell factor/lymphoid enhancer factor (TCF/LEF) transcriptional activator (7,10). The transcriptional switch accompanies chromatin remodelling during neuronal differentiation, allowing a transient stimulation of Li transcription (7). The activity of Li retrotransposons during brain development can have an impact on gene expression and neuronal function, thereby increasing brain-specific genetic mosaicism (11,12). Further understanding of the molecular mechanisms that regulate Li expression should provide new insights into the role of Li retrotransposition during brain development. Here we show that Li neuronal transcription and retrotransposition in rodents are increased in the absence of methyl-CpG-binding protein 2 (MeCP2), a protein involved in global DNA methylation and human neurodevelopmental diseases. Using neuronal progenitor cells derived from human induced pluripotent stem cells and human tissues, we revealed that patients with Rett syndrome (RTT), carrying MeCP2 mutations, have increased susceptibility for Li retrotransposition. Our data demonstrate that Li retrotransposition can be controlled in a tissue-specific manner and that disease-related genetic mutations can influence the frequency of neuronal Li retrotransposition. Our findings add a new level of complexity to the molecular events that can lead to neurological disorders.
Audience	Academic
Author	Coufal, Nicole G Gage, Fred H Yeo, Gene Oefner, Ruth Nakashima, Kinichi Muotri, Alysson R Marchetto, Maria C. N
AuthorAffiliation	4 Laboratory of Molecular Neuroscience, Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma 630-0101, Japan 2 Laboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA 1 University of California San Diego, School of Medicine, Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program, 9500 Gilman Dr, La Jolla, CA 92093, MC 0695, USA 3 University of California San Diego, School of Medicine, Department of Cellular & Molecular Medicine, Stem Cell Program, 9500 Gilman Dr, La Jolla, CA 92093-0695, USA
AuthorAffiliation_xml	– name: 3 University of California San Diego, School of Medicine, Department of Cellular & Molecular Medicine, Stem Cell Program, 9500 Gilman Dr, La Jolla, CA 92093-0695, USA – name: 4 Laboratory of Molecular Neuroscience, Graduate School of Biological Sciences, Nara Institute of Science and Technology, 8916-5 Takayama, Ikoma 630-0101, Japan – name: 2 Laboratory of Genetics, The Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA – name: 1 University of California San Diego, School of Medicine, Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program, 9500 Gilman Dr, La Jolla, CA 92093, MC 0695, USA
Author_xml	– sequence: 1 givenname: Alysson R surname: Muotri fullname: Muotri, Alysson R organization: University of California San Diego, School of Medicine, Department of Pediatrics/Rady Children's Hospital San Diego, Department of Cellular & Molecular Medicine, Stem Cell Program – sequence: 2 givenname: Fred H surname: Gage fullname: Gage, Fred H organization: Laboratory of Genetics, The Salk Institute for Biological Studies – sequence: 3 givenname: Maria C. N surname: Marchetto fullname: Marchetto, Maria C. N organization: Laboratory of Genetics, The Salk Institute for Biological Studies – sequence: 4 givenname: Nicole G surname: Coufal fullname: Coufal, Nicole G organization: Laboratory of Genetics, The Salk Institute for Biological Studies – sequence: 5 givenname: Ruth surname: Oefner fullname: Oefner, Ruth organization: Laboratory of Genetics, The Salk Institute for Biological Studies – sequence: 6 givenname: Gene surname: Yeo fullname: Yeo, Gene organization: University of California San Diego, School of Medicine, Department of Cellular & Molecular Medicine, Stem Cell Program – sequence: 7 givenname: Kinichi surname: Nakashima fullname: Nakashima, Kinichi organization: Laboratory of Molecular Neuroscience, Graduate School of Biological Sciences, Nara Institute of Science and Technology
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/21085180$$D View this record in MEDLINE/PubMed
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Publisher_xml	– name: Nature Publishing Group UK – name: Nature Publishing Group
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Snippet	Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes. Active L1... Retrotransposition in neurons L1 retrotransposons are dynamically regulated and active genomic elements that affect gene expression and neuronal function... Long interspersed nuclear elements-1 (LINE-1 or L1s) are abundant retrotransposons that comprise approximately 20% of mammalian genomes (1-3). Active Li...
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SubjectTerms	5' Untranslated Regions - genetics 631/208/2489/144 631/208/726/2001/1428 692/420 692/699/375/366 Animals Brain - cytology Brain - metabolism DNA Methylation Gene expression Gene Silencing Genetic aspects Genetic transcription Humanities and Social Sciences Humans Induced Pluripotent Stem Cells - metabolism letter Long Interspersed Nucleotide Elements - genetics Male Methyl-CpG-Binding Protein 2 - deficiency Methyl-CpG-Binding Protein 2 - genetics Methyl-CpG-Binding Protein 2 - metabolism Methylation Mice multidisciplinary Mutation Nervous system diseases Neuroepithelial Cells - metabolism Neurons - metabolism Organ Specificity Promoter Regions, Genetic - genetics Rats Recombination, Genetic - genetics Retrotransposons Rett Syndrome - genetics Rett Syndrome - pathology Rodents Science Science (multidisciplinary) Stem cells Transcription, Genetic - genetics
Title	L1 retrotransposition in neurons is modulated by MeCP2
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