A Chromatin-Dependent Role of the Fragile X Mental Retardation Protein FMRP in the DNA Damage Response

Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm, where it regulates translation of proteins that are important for synaptic function. We identify FMRP as a chrom...

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Published in	Cell Vol. 157; no. 4; pp. 869 - 881
Main Authors	Alpatov, Roman, Lesch, Bluma J., Nakamoto-Kinoshita, Mika, Blanco, Andres, Chen, Shuzhen, Stützer, Alexandra, Armache, Karim J., Simon, Matthew D., Xu, Chao, Ali, Muzaffar, Murn, Jernej, Prisic, Sladjana, Kutateladze, Tatiana G., Vakoc, Christopher R., Min, Jinrong, Kingston, Robert E., Fischle, Wolfgang, Warren, Stephen T., Page, David C., Shi, Yang
Format	Journal Article
Language	English
Published	United States Elsevier Inc 08.05.2014
Subjects	Animals chromatin Chromatin - metabolism Chromosome Pairing cytoplasm DNA Damage Embryo, Mammalian - cytology Fibroblasts Fragile X Mental Retardation Protein - genetics Fragile X Mental Retardation Protein - metabolism Hippocampus - cytology Histones - metabolism Humans Male Meiosis Mice Mice, Knockout Mutation Neurons - metabolism Prophase Receptors, AMPA - metabolism Spermatogenesis
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Abstract	Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm, where it regulates translation of proteins that are important for synaptic function. We identify FMRP as a chromatin-binding protein that functions in the DNA damage response (DDR). Specifically, we show that FMRP binds chromatin through its tandem Tudor (Agenet) domain in vitro and associates with chromatin in vivo. We also demonstrate that FMRP participates in the DDR in a chromatin-binding-dependent manner. The DDR machinery is known to play important roles in developmental processes such as gametogenesis. We show that FMRP occupies meiotic chromosomes and regulates the dynamics of the DDR machinery during mouse spermatogenesis. These findings suggest that nuclear FMRP regulates genomic stability at the chromatin interface and may impact gametogenesis and some developmental aspects of fragile X syndrome. [Display omitted] •Fragile X mental retardation protein FMRP binds chromatin via its Agenet domain•FMRP participates in the DNA damage response in a chromatin-dependent manner•FMRP occupies chromosomes and regulates DNA damage machinery in male mouse meiosis•Lack of FMRP results in meiotic defects such as incomplete chromosome pairing In addition to its classical role as a translational regulator at neuronal synapses, the fragile X mental retardation protein has a role in the nucleus, where it targets chromatin and regulates the DNA damage response and mammalian gametogenesis.
AbstractList	Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm, where it regulates translation of proteins that are important for synaptic function. We identify FMRP as a chromatin-binding protein that functions in the DNA damage response (DDR). Specifically, we show that FMRP binds chromatin through its tandem Tudor (Agenet) domain in vitro and associates with chromatin in vivo. We also demonstrate that FMRP participates in the DDR in a chromatin-binding-dependent manner. The DDR machinery is known to play important roles in developmental processes such as gametogenesis. We show that FMRP occupies meiotic chromosomes and regulates the dynamics of the DDR machinery during mouse spermatogenesis. These findings suggest that nuclear FMRP regulates genomic stability at the chromatin interface and may impact gametogenesis and some developmental aspects of fragile X syndrome. [Display omitted] •Fragile X mental retardation protein FMRP binds chromatin via its Agenet domain•FMRP participates in the DNA damage response in a chromatin-dependent manner•FMRP occupies chromosomes and regulates DNA damage machinery in male mouse meiosis•Lack of FMRP results in meiotic defects such as incomplete chromosome pairing In addition to its classical role as a translational regulator at neuronal synapses, the fragile X mental retardation protein has a role in the nucleus, where it targets chromatin and regulates the DNA damage response and mammalian gametogenesis. Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm, where it regulates translation of proteins that are important for synaptic function. We identify FMRP as a chromatin-binding protein that functions in the DNA damage response (DDR). Specifically, we show that FMRP binds chromatin through its tandem Tudor (Agenet) domain in vitro and associates with chromatin in vivo. We also demonstrate that FMRP participates in the DDR in a chromatin-binding-dependent manner. The DDR machinery is known to play important roles in developmental processes such as gametogenesis. We show that FMRP occupies meiotic chromosomes and regulates the dynamics of the DDR machinery during mouse spermatogenesis. These findings suggest that nuclear FMRP regulates genomic stability at the chromatin interface and may impact gametogenesis and some developmental aspects of fragile X syndrome. The fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm where it regulates translation of proteins important for synaptic function. We identify FMRP as a chromatin binding protein that functions in the DNA damage response (DDR). Specifically, we show that FMRP binds chromatin through its tandem Tudor (Agenet) domain in vitro , and associates with chromatin in vivo . We also demonstrate that FMRP participates in the DDR in a chromatin binding-dependent manner. The DDR machinery is known to play important roles in developmental processes such as gametogenesis. We show that FMRP occupies meiotic chromosomes and regulates the dynamics of DDR machinery during mouse spermatogenesis. These findings suggest that nuclear FMRP regulates genomic stability at the chromatin interface, and may impact gametogenesis and some developmental aspects of the fragile X syndrome. Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm, where it regulates translation of proteins that are important for synaptic function. We identify FMRP as a chromatin-binding protein that functions in the DNA damage response (DDR). Specifically, we show that FMRP binds chromatin through its tandem Tudor (Agenet) domain in vitro and associates with chromatin in vivo. We also demonstrate that FMRP participates in the DDR in a chromatin-binding-dependent manner. The DDR machinery is known to play important roles in developmental processes such as gametogenesis. We show that FMRP occupies meiotic chromosomes and regulates the dynamics of the DDR machinery during mouse spermatogenesis. These findings suggest that nuclear FMRP regulates genomic stability at the chromatin interface and may impact gametogenesis and some developmental aspects of fragile X syndrome.Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present predominantly in the cytoplasm, where it regulates translation of proteins that are important for synaptic function. We identify FMRP as a chromatin-binding protein that functions in the DNA damage response (DDR). Specifically, we show that FMRP binds chromatin through its tandem Tudor (Agenet) domain in vitro and associates with chromatin in vivo. We also demonstrate that FMRP participates in the DDR in a chromatin-binding-dependent manner. The DDR machinery is known to play important roles in developmental processes such as gametogenesis. We show that FMRP occupies meiotic chromosomes and regulates the dynamics of the DDR machinery during mouse spermatogenesis. These findings suggest that nuclear FMRP regulates genomic stability at the chromatin interface and may impact gametogenesis and some developmental aspects of fragile X syndrome.
Author	Murn, Jernej Nakamoto-Kinoshita, Mika Fischle, Wolfgang Simon, Matthew D. Ali, Muzaffar Kutateladze, Tatiana G. Vakoc, Christopher R. Stützer, Alexandra Min, Jinrong Page, David C. Armache, Karim J. Alpatov, Roman Shi, Yang Lesch, Bluma J. Prisic, Sladjana Warren, Stephen T. Chen, Shuzhen Kingston, Robert E. Xu, Chao Blanco, Andres
AuthorAffiliation	5 Laboratory of Chromatin Biochemistry, Max Plank Institute for Biophysical Chemistry, 37077 Göttingen, Germany 1 Division of Newborn Medicine, Boston Children’s Hospital, Boston, MA 02115, USA 4 Departments of Human Genetics, Biochemistry, and Pediatrics, Emory University School of Medicine, Atlanta, GA 30322, USA 9 Division of Infectious Diseases, Boston Children’s Hospital and Harvard Medical School, Boston, MA, 02115, USA 2 Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA 7 Structural Genomics Consortium and Department of Physiology, University of Toronto, Toronto, ON M5G 1L7, Canada 10 Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA 6 Massachusetts General Hospital, Department of Molecular Biology and Department of Genetics, Harvard Medical School, Boston, MA 02114, USA 8 Department of Pharmacology, University of Colorado School of Medicine, Aurora, CO 80045, USA 3 Howard Hughes Medical Institute, Whitehead Institute, Department of Biology, Massach
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Snippet	Fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present... The fragile X syndrome, a common form of inherited intellectual disability, is caused by loss of the fragile X mental retardation protein FMRP. FMRP is present...
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SubjectTerms	Animals chromatin Chromatin - metabolism Chromosome Pairing cytoplasm DNA Damage Embryo, Mammalian - cytology Fibroblasts Fragile X Mental Retardation Protein - genetics Fragile X Mental Retardation Protein - metabolism Hippocampus - cytology Histones - metabolism Humans Male Meiosis Mice Mice, Knockout Mutation Neurons - metabolism Prophase Receptors, AMPA - metabolism Spermatogenesis
Title	A Chromatin-Dependent Role of the Fragile X Mental Retardation Protein FMRP in the DNA Damage Response
URI	https://dx.doi.org/10.1016/j.cell.2014.03.040 https://www.ncbi.nlm.nih.gov/pubmed/24813610 https://www.proquest.com/docview/1524176805 https://www.proquest.com/docview/1543999929 https://www.proquest.com/docview/2000200362 https://pubmed.ncbi.nlm.nih.gov/PMC4038154
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