An epigenetic blockade of cognitive functions in the neurodegenerating brain
Histone deacetylase 2 is shown to suppress genes involved in cognitive function epigenetically, potentially opening the door to treatments for Alzheimer’s and other neurodegenerative diseases by developing HDAC2-selective inhibitors. Blocking cognitive decline What causes the cognitive decline assoc...
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| Published in | Nature (London) Vol. 483; no. 7388; pp. 222 - 226 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
08.03.2012
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0028-0836 1476-4687 1476-4687 |
| DOI | 10.1038/nature10849 |
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| Abstract | Histone deacetylase 2 is shown to suppress genes involved in cognitive function epigenetically, potentially opening the door to treatments for Alzheimer’s and other neurodegenerative diseases by developing HDAC2-selective inhibitors.
Blocking cognitive decline
What causes the cognitive decline associated with neurodegenerative diseases is not fully understood. This study reveals a novel epigenetic mechanism by which Alzheimer's-disease-related neurotoxicity reduces the expression of genes necessary for neural plasticity. In two mouse models of Alzheimer's disease — and in post-mortem samples from human subjects — expression of the epigenetic regulator histone deacetylase 2 (HDAC2) is elevated. Reversing the upregulation of HDAC2 by short-hairpin-RNA-mediated knockdown in mice restores the expression of HDAC2 target genes and abolishes the neurodegeneration-associated memory impairment.
Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer’s disease
1
. The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge
2
. Here we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase 2, which is increased by Alzheimer’s-disease-related neurotoxic insults
in vitro
, in two mouse models of neurodegeneration and in patients with Alzheimer’s disease. Histone deacetylase 2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the build-up of histone deacetylase 2 by short-hairpin-RNA-mediated knockdown unlocks the repression of these genes, reinstates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of selective inhibitors of histone deacetylase 2 and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade. |
|---|---|
| AbstractList | Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer's disease (1). The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge (2). Here we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase 2, which is increased by Alzheimer's-disease-related neurotoxic insults in vitro, in two mouse models of neurodegeneration and in patients with Alzheimer's disease. Histone deacetylase 2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the build-up of histone deacetylase 2 by short-hairpin-RNA-mediated knockdown unlocks the repression of these genes, reinstates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of selective inhibitors of histone deacetylase 2 and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade. [...] pharmacological treatments aimed at increasing histone acetylation have shown promising results in reversing cognitive deficits in some of these models, predominantly by the use of nonselective histone deacetylase (HDAC) inhibitors6.However, the causative agent of such memory-impairing histone acetylation changes, and, hence, the best targets for pharmacological strategies, remain unknown. [...] our finding that HDAC2 inhibition probably reinstates transcriptional, morphological and synaptic plasticity in the surviving neurons of the neurodegenerating brain raises hope that such plasticity is not irrevocably lost, but merely constrained by the epigenetic blockade. Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer's disease. The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge. Here we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase 2, which is increased by Alzheimer's-disease-related neurotoxic insults in vitro, in two mouse models of neurodegeneration and in patients with Alzheimer's disease. Histone deacetylase 2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the build-up of histone deacetylase 2 by short-hairpin-RNA-mediated knockdown unlocks the repression of these genes, reinstates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of selective inhibitors of histone deacetylase 2 and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade. Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer's disease. The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge. Here we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase 2, which is increased by Alzheimer's-disease-related neurotoxic insults in vitro, in two mouse models of neurodegeneration and in patients with Alzheimer's disease. Histone deacetylase 2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the build-up of histone deacetylase 2 by short-hairpin-RNA-mediated knockdown unlocks the repression of these genes, reinstates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of selective inhibitors of histone deacetylase 2 and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade.Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer's disease. The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge. Here we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase 2, which is increased by Alzheimer's-disease-related neurotoxic insults in vitro, in two mouse models of neurodegeneration and in patients with Alzheimer's disease. Histone deacetylase 2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the build-up of histone deacetylase 2 by short-hairpin-RNA-mediated knockdown unlocks the repression of these genes, reinstates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of selective inhibitors of histone deacetylase 2 and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade. Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer’s disease (AD)1. The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge2. Here, we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase (HDAC) 2, which is increased by AD-related neurotoxic insults in vitro, in two mouse models of neurodegeneration, and in AD patients. HDAC2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the buildup of HDAC2 by shRNA-mediated knockdown unlocks the repression of these genes, re-instates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of HDAC2-selective inhibitors, and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade. Histone deacetylase 2 is shown to suppress genes involved in cognitive function epigenetically, potentially opening the door to treatments for Alzheimer’s and other neurodegenerative diseases by developing HDAC2-selective inhibitors. Blocking cognitive decline What causes the cognitive decline associated with neurodegenerative diseases is not fully understood. This study reveals a novel epigenetic mechanism by which Alzheimer's-disease-related neurotoxicity reduces the expression of genes necessary for neural plasticity. In two mouse models of Alzheimer's disease — and in post-mortem samples from human subjects — expression of the epigenetic regulator histone deacetylase 2 (HDAC2) is elevated. Reversing the upregulation of HDAC2 by short-hairpin-RNA-mediated knockdown in mice restores the expression of HDAC2 target genes and abolishes the neurodegeneration-associated memory impairment. Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer’s disease 1 . The causes leading to such impairment are only poorly understood and effective treatments are slow to emerge 2 . Here we show that cognitive capacities in the neurodegenerating brain are constrained by an epigenetic blockade of gene transcription that is potentially reversible. This blockade is mediated by histone deacetylase 2, which is increased by Alzheimer’s-disease-related neurotoxic insults in vitro , in two mouse models of neurodegeneration and in patients with Alzheimer’s disease. Histone deacetylase 2 associates with and reduces the histone acetylation of genes important for learning and memory, which show a concomitant decrease in expression. Importantly, reversing the build-up of histone deacetylase 2 by short-hairpin-RNA-mediated knockdown unlocks the repression of these genes, reinstates structural and synaptic plasticity, and abolishes neurodegeneration-associated memory impairments. These findings advocate for the development of selective inhibitors of histone deacetylase 2 and suggest that cognitive capacities following neurodegeneration are not entirely lost, but merely impaired by this epigenetic blockade. |
| Audience | Academic |
| Author | Haggarty, Stephen J. Samiei, Alireza Gräff, Johannes Delalle, Ivana Wang, Wen-Yuan Su, Susan C. Joseph, Nadine Kao, Patricia F. Guan, Ji-Song Kahn, Martin Rei, Damien Tsai, Li-Huei Fass, Daniel M. Hennig, Krista M. Seo, Jinsoo Nieland, Thomas J. F. |
| AuthorAffiliation | 5 Department of Pathology and Laboratory Medicine, Boston University School of Medicine, Boston, MA, 02118, USA 4 Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA 3 Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology, Cambridge, MA, 02142, USA 2 Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA 1 Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA |
| AuthorAffiliation_xml | – name: 5 Department of Pathology and Laboratory Medicine, Boston University School of Medicine, Boston, MA, 02118, USA – name: 4 Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School, Boston, MA 02114, USA – name: 1 Picower Institute for Learning and Memory, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA – name: 2 Howard Hughes Medical Institute, Massachusetts Institute of Technology, Cambridge, MA, 02139, USA – name: 3 Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology, Cambridge, MA, 02142, USA |
| Author_xml | – sequence: 1 givenname: Johannes surname: Gräff fullname: Gräff, Johannes organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology – sequence: 2 givenname: Damien surname: Rei fullname: Rei, Damien organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology – sequence: 3 givenname: Ji-Song surname: Guan fullname: Guan, Ji-Song organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology – sequence: 4 givenname: Wen-Yuan surname: Wang fullname: Wang, Wen-Yuan organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology – sequence: 5 givenname: Jinsoo surname: Seo fullname: Seo, Jinsoo organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology – sequence: 6 givenname: Krista M. surname: Hennig fullname: Hennig, Krista M. organization: Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology, Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School – sequence: 7 givenname: Thomas J. F. surname: Nieland fullname: Nieland, Thomas J. F. organization: Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology – sequence: 8 givenname: Daniel M. surname: Fass fullname: Fass, Daniel M. organization: Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology, Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School – sequence: 9 givenname: Patricia F. surname: Kao fullname: Kao, Patricia F. organization: Department of Pathology and Laboratory Medicine, Boston University School of Medicine – sequence: 10 givenname: Martin surname: Kahn fullname: Kahn, Martin organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology – sequence: 11 givenname: Susan C. surname: Su fullname: Su, Susan C. organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology – sequence: 12 givenname: Alireza surname: Samiei fullname: Samiei, Alireza organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology – sequence: 13 givenname: Nadine surname: Joseph fullname: Joseph, Nadine organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology – sequence: 14 givenname: Stephen J. surname: Haggarty fullname: Haggarty, Stephen J. organization: Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology, Center for Human Genetic Research, Massachusetts General Hospital, Harvard Medical School – sequence: 15 givenname: Ivana surname: Delalle fullname: Delalle, Ivana organization: Department of Pathology and Laboratory Medicine, Boston University School of Medicine – sequence: 16 givenname: Li-Huei surname: Tsai fullname: Tsai, Li-Huei email: lhtsai@mit.edu organization: Department of Brain and Cognitive Sciences, Picower Institute for Learning and Memory, Massachusetts Institute of Technology, Howard Hughes Medical Institute, Massachusetts Institute of Technology, Stanley Center for Psychiatric Research, Broad Institute of Harvard University and Massachusetts Institute of Technology |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25566945$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/22388814$$D View this record in MEDLINE/PubMed |
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| Snippet | Histone deacetylase 2 is shown to suppress genes involved in cognitive function epigenetically, potentially opening the door to treatments for Alzheimer’s and... Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer's disease. The causes leading... Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer's disease (1). The causes... [...] pharmacological treatments aimed at increasing histone acetylation have shown promising results in reversing cognitive deficits in some of these models,... Cognitive decline is a debilitating feature of most neurodegenerative diseases of the central nervous system, including Alzheimer’s disease (AD)1. The causes... |
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| SubjectTerms | 631/378/2584 631/378/2591 631/378/2649 692/699/375/365 Acetylation - drug effects Adult and adolescent clinical studies Alzheimer Disease - complications Alzheimer Disease - genetics Alzheimer Disease - physiopathology Amyloid beta-Peptides - toxicity Animals Biological and medical sciences Brain - drug effects Brain - metabolism Brain - physiopathology Causes of Cognition disorders Cognitive ability Cyclin-dependent kinases Degeneration Degenerative and inherited degenerative diseases of the nervous system. Leukodystrophies. Prion diseases Disease Models, Animal Epigenesis, Genetic - drug effects Epigenetic inheritance Epigenetics Gene Expression Regulation - drug effects Gene Knockdown Techniques Genetic aspects Genetics Health aspects Hippocampus - drug effects Hippocampus - metabolism Histone Deacetylase 2 - deficiency Histone Deacetylase 2 - genetics Histone Deacetylase 2 - metabolism Histones - metabolism Humanities and Social Sciences Humans Hydrogen Peroxide - toxicity Kinases letter Medical sciences Memory Disorders - complications Memory Disorders - genetics Memory Disorders - physiopathology Mice multidisciplinary Nervous system Neurodegeneration Neurodegenerative Diseases - complications Neurodegenerative Diseases - genetics Neurodegenerative Diseases - physiopathology Neurology Neuronal Plasticity - drug effects Neuronal Plasticity - genetics Organic mental disorders. Neuropsychology Peptide Fragments - toxicity Phosphorylation - drug effects Plasticity Promoter Regions, Genetic - drug effects Promoter Regions, Genetic - genetics Psychology. Psychoanalysis. Psychiatry Psychopathology. Psychiatry Receptors, Glucocorticoid - metabolism RNA polymerase RNA Polymerase II - metabolism Science Science (multidisciplinary) |
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| Title | An epigenetic blockade of cognitive functions in the neurodegenerating brain |
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