Friedreich's ataxia–associated GAA repeats induce replication-fork reversal and unusual molecular junctions

Friedreich's ataxia is one of several hereditary neurodegenerative disorders caused expansion of trinucleotide repeats, but the mechanism of their genomic propagation is unknown. A new plasmid-based system to probe human replicative intermediates reveals that GAA/TTC repeats interfere with repl...

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Published in:	Nature structural & molecular biology Vol. 20; no. 4; pp. 486 - 494
Main Authors:	Follonier, Cindy, Oehler, Judith, Herrador, Raquel, Lopes, Massimo
Format:	Journal Article
Language:	English
Published:	New York Nature Publishing Group US 01.04.2013 Nature Publishing Group
Subjects:	631/337/151 631/378/1689/2014 631/45/535 Ataxia Biochemistry Biological Microscopy Care and treatment Crystal structure DNA Replication Electrophoresis Friedreich Ataxia - genetics Genetic aspects Genetic disorders Humans Life Sciences Membrane Biology Molecular biology Neurodegeneration Plasmids Protein Structure Repetitive Sequences, Nucleic Acid Signal transduction Switzerland
ISSN:	1545-9993, 1545-9985, 1545-9985
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Abstract	Friedreich's ataxia is one of several hereditary neurodegenerative disorders caused expansion of trinucleotide repeats, but the mechanism of their genomic propagation is unknown. A new plasmid-based system to probe human replicative intermediates reveals that GAA/TTC repeats interfere with replication, thus suggesting that repeat expansion occurs by postreplicative mechanisms. Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the mechanisms of replication interference and expansion in human cells remained elusive. To study in vivo replication structures at GAA repeats, we designed a new plasmid-based system that permits the analysis of human replication intermediates by two-dimensional gel electrophoresis and EM. We found that replication forks transiently pause and reverse at long GAA/TTC tracts in both orientations. Furthermore, we identified replication-associated intramolecular junctions, located between GAA/TTC repeats and other homopurine-homopyrimidine tracts, that were associated with breakage of the plasmid fork not traversing the repeats. Finally, we detected postreplicative, sister-chromatid hemicatenanes on control plasmids, which were replaced by persistent homology-driven junctions at GAA/TTC repeats. These data prove that GAA/TTC tracts interfere with replication in humans and implicate postreplicative mechanisms in trinucleotide repeat expansion.
AbstractList	Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the mechanisms of replication interference and expansion in human cells remained elusive. To study in vivo replication structures at GAA repeats, we designed a new plasmid-based system that permits the analysis of human replication intermediates by two-dimensional gel electrophoresis and EM. We found that replication forks transiently pause and reverse at long GAA/TTC tracts in both orientations. Furthermore, we identified replication-associated intramolecular junctions, located between GAA/TTC repeats and other homopurine-homopyrimidine tracts, that were associated with breakage of the plasmid fork not traversing the repeats. Finally, we detected postreplicative, sister-chromatid hemicatenanes on control plasmids, which were replaced by persistent homology- driven junctions at GAA/TTC repeats. These data prove that GAA/TTC tracts interfere with replication in humans and implicate postreplicative mechanisms in trinucleotide repeat expansion. Friedreich's ataxia is one of several hereditary neurodegenerative disorders caused expansion of trinucleotide repeats, but the mechanism of their genomic propagation is unknown. A new plasmid-based system to probe human replicative intermediates reveals that GAA/TTC repeats interfere with replication, thus suggesting that repeat expansion occurs by postreplicative mechanisms. Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the mechanisms of replication interference and expansion in human cells remained elusive. To study in vivo replication structures at GAA repeats, we designed a new plasmid-based system that permits the analysis of human replication intermediates by two-dimensional gel electrophoresis and EM. We found that replication forks transiently pause and reverse at long GAA/TTC tracts in both orientations. Furthermore, we identified replication-associated intramolecular junctions, located between GAA/TTC repeats and other homopurine-homopyrimidine tracts, that were associated with breakage of the plasmid fork not traversing the repeats. Finally, we detected postreplicative, sister-chromatid hemicatenanes on control plasmids, which were replaced by persistent homology-driven junctions at GAA/TTC repeats. These data prove that GAA/TTC tracts interfere with replication in humans and implicate postreplicative mechanisms in trinucleotide repeat expansion. Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the mechanisms of replication interference and expansion in human cells remained elusive. To study in vivo replication structures at GAA repeats, we designed a new plasmid-based system that permits the analysis of human replication intermediates by two-dimensional gel electrophoresis and EM. We found that replication forks transiently pause and reverse at long GAA/TTC tracts in both orientations. Furthermore, we identified replication-associated intramolecular junctions, located between GAA/TTC repeats and other homopurine-homopyrimidine tracts, that were associated with breakage of the plasmid fork not traversing the repeats. Finally, we detected postreplicative, sister-chromatid hemicatenanes on control plasmids, which were replaced by persistent homology-driven junctions at GAA/TTC repeats. These data prove that GAA/TTC tracts interfere with replication in humans and implicate postreplicative mechanisms in trinucleotide repeat expansion. [PUBLICATION ABSTRACT] Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the mechanisms of replication interference and expansion in human cells remained elusive. To study in vivo replication structures at GAA repeats, we designed a new plasmid-based system that permits the analysis of human replication intermediates by two-dimensional gel electrophoresis and EM. We found that replication forks transiently pause and reverse at long GAA/TTC tracts in both orientations. Furthermore, we identified replication-associated intramolecular junctions, located between GAA/TTC repeats and other homopurine-homopyrimidine tracts, that were associated with breakage of the plasmid fork not traversing the repeats. Finally, we detected postreplicative, sister-chromatid hemicatenanes on control plasmids, which were replaced by persistent homology-driven junctions at GAA/TTC repeats. These data prove that GAA/TTC tracts interfere with replication in humans and implicate postreplicative mechanisms in trinucleotide repeat expansion.Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the mechanisms of replication interference and expansion in human cells remained elusive. To study in vivo replication structures at GAA repeats, we designed a new plasmid-based system that permits the analysis of human replication intermediates by two-dimensional gel electrophoresis and EM. We found that replication forks transiently pause and reverse at long GAA/TTC tracts in both orientations. Furthermore, we identified replication-associated intramolecular junctions, located between GAA/TTC repeats and other homopurine-homopyrimidine tracts, that were associated with breakage of the plasmid fork not traversing the repeats. Finally, we detected postreplicative, sister-chromatid hemicatenanes on control plasmids, which were replaced by persistent homology-driven junctions at GAA/TTC repeats. These data prove that GAA/TTC tracts interfere with replication in humans and implicate postreplicative mechanisms in trinucleotide repeat expansion.
Audience	Academic
Author	Lopes, Massimo Oehler, Judith Follonier, Cindy Herrador, Raquel
Author_xml	– sequence: 1 givenname: Cindy surname: Follonier fullname: Follonier, Cindy organization: Institute of Molecular Cancer Research, University of Zürich – sequence: 2 givenname: Judith surname: Oehler fullname: Oehler, Judith organization: Institute of Molecular Cancer Research, University of Zürich, Present address: Institute of Pharmacology and Toxicology, University of Zürich, Zürich, Switzerland – sequence: 3 givenname: Raquel surname: Herrador fullname: Herrador, Raquel organization: Institute of Molecular Cancer Research, University of Zürich – sequence: 4 givenname: Massimo surname: Lopes fullname: Lopes, Massimo email: lopes@imcr.uzh.ch organization: Institute of Molecular Cancer Research, University of Zürich
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Snippet	Friedreich's ataxia is one of several hereditary neurodegenerative disorders caused expansion of trinucleotide repeats, but the mechanism of their genomic... Expansion of GAA/TTC repeats is the causative event in Friedreich's ataxia. GAA repeats have been shown to hinder replication in model systems, but the...
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SubjectTerms	631/337/151 631/378/1689/2014 631/45/535 Ataxia Biochemistry Biological Microscopy Care and treatment Crystal structure DNA Replication Electrophoresis Friedreich Ataxia - genetics Genetic aspects Genetic disorders Humans Life Sciences Membrane Biology Molecular biology Neurodegeneration Plasmids Protein Structure Repetitive Sequences, Nucleic Acid Signal transduction
Title	Friedreich's ataxia–associated GAA repeats induce replication-fork reversal and unusual molecular junctions
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