Antisense transcripts of the expanded C9ORF72 hexanucleotide repeat form nuclear RNA foci and undergo repeat-associated non-ATG translation in c9FTD/ALS

Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mecha...

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Bibliographic Details
Published inActa neuropathologica Vol. 126; no. 6; pp. 829 - 844
Main Authors Gendron, Tania F., Bieniek, Kevin F., Zhang, Yong-Jie, Jansen-West, Karen, Ash, Peter E. A., Caulfield, Thomas, Daughrity, Lillian, Dunmore, Judith H., Castanedes-Casey, Monica, Chew, Jeannie, Cosio, Danielle M., van Blitterswijk, Marka, Lee, Wing C., Rademakers, Rosa, Boylan, Kevin B., Dickson, Dennis W., Petrucelli, Leonard
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer Berlin Heidelberg 01.12.2013
Springer
Springer Nature B.V
Subjects
Aged
Aged, 80 and over
Amyotrophic lateral sclerosis
Amyotrophic Lateral Sclerosis - genetics
Amyotrophic Lateral Sclerosis - metabolism
Amyotrophic Lateral Sclerosis - pathology
Brain
C9orf72 Protein
Cerebellum - metabolism
Cerebellum - pathology
Dementia
DNA Repeat Expansion
Female
Frontal Lobe - metabolism
Frontal Lobe - pathology
Frontotemporal Dementia - genetics
Frontotemporal Dementia - metabolism
Frontotemporal Dementia - pathology
Genetic translation
Health aspects
HEK293 Cells
Humans
Male
Medicine
Medicine & Public Health
Middle Aged
Nervous system diseases
Neuropathology
Neurosciences
Neurotoxicity
Original Paper
Pathology
Physicians (General practice)
Protein Structure, Secondary
Proteins
Proteins - genetics
Proteins - metabolism
RNA
RNA, Nuclear - genetics
RNA, Nuclear - metabolism
Spinal Cord - metabolism
Spinal Cord - pathology
Toxicity
Florida
United States > US
Bidirectional transcription
Expanded repeat
Repeat-associated non-ATG translation
Amyotrophic lateral sclerosis
Frontotemporal dementia
C9ORF72
RNA foci
Online AccessGet full text

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Abstract Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes “c9FTD/ALS” are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG) 66 in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG) exp RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG) 66 is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.
AbstractList Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes "c9FTD/ALS" are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG) sub(66) in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG) sub(exp) RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG) sub(66) is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.
Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes "c9FTD/ALS" are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG)66 in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG)exp RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG)66 is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.
Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes "c9FTD/ALS" are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG)66 in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG)exp RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG)66 is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes "c9FTD/ALS" are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG)66 in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG)exp RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG)66 is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.
Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes “c9FTD/ALS” are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG) 66 in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG) exp RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG) 66 is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.
Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes "c9FTD/ALS" are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of (CCCCGG)^sub 66^ in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible (CCCCGG)^sub exp^ RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that (CCCCGG)^sub 66^ is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies.[PUBLICATION ABSTRACT]
Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological overlap. A hexanucleotide (GGGGCC) repeat expansion in a non-coding region of C9ORF72 is the major genetic cause of both diseases. The mechanisms by which this repeat expansion causes "c9FTD/ALS" are not definitively known, but RNA-mediated toxicity is a likely culprit. RNA transcripts of the expanded GGGGCC repeat form nuclear foci in c9FTD/ALS, and also undergo repeat-associated non-ATG (RAN) translation resulting in the production of three aggregation-prone proteins. The goal of this study was to examine whether antisense transcripts resulting from bidirectional transcription of the expanded repeat behave in a similar manner. We show that ectopic expression of [(CCCCGG).sub.66] in cultured cells results in foci formation. Using novel polyclonal antibodies for the detection of possible [(CCCCGG).sub.exp] RAN proteins [poly(PR), poly(GP) and poly(PA)], we validated that [(CCCCGG).sub.66] is also subject to RAN translation in transfected cells. Of importance, foci composed of antisense transcripts are observed in the frontal cortex, spinal cord and cerebellum of c9FTD/ALS cases, and neuronal inclusions of poly(PR), poly(GP) and poly(PA) are present in various brain tissues in c9FTD/ALS, but not in other neurodegenerative diseases, including CAG repeat disorders. Of note, RNA foci and poly(GP) inclusions infrequently co-occur in the same cell, suggesting these events represent two distinct ways in which the C9ORF72 repeat expansion may evoke neurotoxic effects. These findings provide mechanistic insight into the pathogenesis of c9FTD/ALS, and have significant implications for therapeutic strategies. Keywords Amyotrophic lateral sclerosis * Bidirectional transcription * C9ORF72 * Expanded repeat * Frontotemporal dementia * Repeat-associated non-ATG translation * RNA foci
Audience Academic
Author Rademakers, Rosa
Bieniek, Kevin F.
Lee, Wing C.
Dickson, Dennis W.
Caulfield, Thomas
Gendron, Tania F.
Dunmore, Judith H.
van Blitterswijk, Marka
Boylan, Kevin B.
Petrucelli, Leonard
Zhang, Yong-Jie
Jansen-West, Karen
Daughrity, Lillian
Chew, Jeannie
Ash, Peter E. A.
Castanedes-Casey, Monica
Cosio, Danielle M.
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  surname: Gendron
  fullname: Gendron, Tania F.
  organization: Department of Neuroscience, Mayo Clinic Florida
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  surname: Bieniek
  fullname: Bieniek, Kevin F.
  organization: Department of Neuroscience, Mayo Clinic Florida, Mayo Graduate School, Mayo Clinic College of Medicine
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  givenname: Yong-Jie
  surname: Zhang
  fullname: Zhang, Yong-Jie
  organization: Department of Neuroscience, Mayo Clinic Florida
– sequence: 4
  givenname: Karen
  surname: Jansen-West
  fullname: Jansen-West, Karen
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Peter E. A.
  surname: Ash
  fullname: Ash, Peter E. A.
  organization: Department of Pharmacology, Boston University School of Medicine
– sequence: 6
  givenname: Thomas
  surname: Caulfield
  fullname: Caulfield, Thomas
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Lillian
  surname: Daughrity
  fullname: Daughrity, Lillian
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Judith H.
  surname: Dunmore
  fullname: Dunmore, Judith H.
  organization: Department of Neuroscience, Mayo Clinic Florida
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  surname: Castanedes-Casey
  fullname: Castanedes-Casey, Monica
  organization: Department of Neuroscience, Mayo Clinic Florida
– sequence: 10
  givenname: Jeannie
  surname: Chew
  fullname: Chew, Jeannie
  organization: Department of Neuroscience, Mayo Clinic Florida, Mayo Graduate School, Mayo Clinic College of Medicine
– sequence: 11
  givenname: Danielle M.
  surname: Cosio
  fullname: Cosio, Danielle M.
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Marka
  surname: van Blitterswijk
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  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Wing C.
  surname: Lee
  fullname: Lee, Wing C.
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Rosa
  surname: Rademakers
  fullname: Rademakers, Rosa
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Kevin B.
  surname: Boylan
  fullname: Boylan, Kevin B.
  organization: Department of Neurology, Mayo Clinic Florida
– sequence: 16
  givenname: Dennis W.
  surname: Dickson
  fullname: Dickson, Dennis W.
  email: dickson.dennis@mayo.edu
  organization: Department of Neuroscience, Mayo Clinic Florida
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  givenname: Leonard
  surname: Petrucelli
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  email: petrucelli.leonard@mayo.edu
  organization: Department of Neuroscience, Mayo Clinic Florida
BackLink https://www.ncbi.nlm.nih.gov/pubmed/24129584$$D View this record in MEDLINE/PubMed
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Issue 6
Keywords Bidirectional transcription
Expanded repeat
Repeat-associated non-ATG translation
Amyotrophic lateral sclerosis
Frontotemporal dementia
C9ORF72
RNA foci
Language English
License http://creativecommons.org/licenses/by/2.0
Open AccessThis article is distributed under the terms of the Creative Commons Attribution License which permits any use, distribution, and reproduction in any medium, provided the original author(s) and the source are credited.
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PublicationSubtitle Pathology and Mechanisms of Neurological Disease
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Snippet Frontotemporal dementia (FTD) and amyotrophic lateral sclerosis (ALS) are devastating neurodegenerative disorders with clinical, genetic, and neuropathological...
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StartPage 829
SubjectTerms Aged
Aged, 80 and over
Amyotrophic lateral sclerosis
Amyotrophic Lateral Sclerosis - genetics
Amyotrophic Lateral Sclerosis - metabolism
Amyotrophic Lateral Sclerosis - pathology
Brain
C9orf72 Protein
Cerebellum - metabolism
Cerebellum - pathology
Dementia
DNA Repeat Expansion
Female
Frontal Lobe - metabolism
Frontal Lobe - pathology
Frontotemporal Dementia - genetics
Frontotemporal Dementia - metabolism
Frontotemporal Dementia - pathology
Genetic translation
Health aspects
HEK293 Cells
Humans
Male
Medicine
Medicine & Public Health
Middle Aged
Nervous system diseases
Neuropathology
Neurosciences
Neurotoxicity
Original Paper
Pathology
Physicians (General practice)
Protein Structure, Secondary
Proteins
Proteins - genetics
Proteins - metabolism
RNA
RNA, Nuclear - genetics
RNA, Nuclear - metabolism
Spinal Cord - metabolism
Spinal Cord - pathology
Toxicity
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  providerName: Springer Nature
Title Antisense transcripts of the expanded C9ORF72 hexanucleotide repeat form nuclear RNA foci and undergo repeat-associated non-ATG translation in c9FTD/ALS
URI https://link.springer.com/article/10.1007/s00401-013-1192-8
https://www.ncbi.nlm.nih.gov/pubmed/24129584
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https://www.proquest.com/docview/1468338600
https://pubmed.ncbi.nlm.nih.gov/PMC3830741
Volume 126
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