Non-homologous end joining shapes the genomic rearrangement landscape of chromothripsis from mitotic errors

Non-homologous end joining shapes the genomic rearrangement landscape of chromothripsis from mitotic errors

Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with...

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Published in:Nature communications Vol. 15; no. 1; pp. 5611 - 13
Main Authors: Hu, Qing, Espejo Valle-Inclán, Jose, Dahiya, Rashmi, Guyer, Alison, Mazzagatti, Alice, Maurais, Elizabeth G., Engel, Justin L., Lu, Huiming, Davis, Anthony J., Cortés-Ciriano, Isidro, Ly, Peter
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 04-07-2024
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Subjects:
13
13/106
14
14/32
14/63
45/23
631/208/1405
631/208/211
631/67/68
631/80/103
631/80/641/2002
Cell cycle
Chromosome deletion
Chromosomes
Chromothripsis
CRISPR
CRISPR-Cas Systems
DNA Breaks, Double-Stranded
DNA damage
DNA End-Joining Repair
DNA fragmentation
DNA repair
Double-strand break repair
Errors
Fragmentation
Gene Rearrangement
Genomics
Humanities and Social Sciences
Humans
Kinetics
Micronuclei
Micronuclei, Chromosome-Defective
Mitosis - genetics
multidisciplinary
Non-homologous end joining
Science
Science (multidisciplinary)
Tumor Suppressor p53-Binding Protein 1 - genetics
Tumor Suppressor p53-Binding Protein 1 - metabolism
Yeast
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Abstract Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors. Mitotic errors promote chromosome fragmentation and rearrangements through chromothripsis. Here, the authors identify NHEJ as the primary DSB repair pathway underlying chromothripsis and investigate the kinetics of fragment reassembly across the cell cycle.
AbstractList Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors. Mitotic errors promote chromosome fragmentation and rearrangements through chromothripsis. Here, the authors identify NHEJ as the primary DSB repair pathway underlying chromothripsis and investigate the kinetics of fragment reassembly across the cell cycle.
Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors.Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors.
Abstract Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors.
Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors.
Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The reassembly of fragmented chromosomes by error-prone DNA double-strand break (DSB) repair generates diverse genomic rearrangements associated with human diseases. How specific repair pathways recognize and process these lesions remains poorly understood. Here we use CRISPR/Cas9 to systematically inactivate distinct DSB repair pathways and interrogate the rearrangement landscape of fragmented chromosomes. Deletion of canonical non-homologous end joining (NHEJ) components substantially reduces complex rearrangements and shifts the rearrangement landscape toward simple alterations without the characteristic patterns of chromothripsis. Following reincorporation into the nucleus, fragmented chromosomes localize within sub-nuclear micronuclei bodies (MN bodies) and undergo ligation by NHEJ within a single cell cycle. In the absence of NHEJ, chromosome fragments are rarely engaged by alternative end-joining or recombination-based mechanisms, resulting in delayed repair kinetics, persistent 53BP1-labeled MN bodies, and cell cycle arrest. Thus, we provide evidence supporting NHEJ as the exclusive DSB repair pathway generating complex rearrangements from mitotic errors.Mitotic errors promote chromosome fragmentation and rearrangements through chromothripsis. Here, the authors identify NHEJ as the primary DSB repair pathway underlying chromothripsis and investigate the kinetics of fragment reassembly across the cell cycle.
ArticleNumber 5611
Author Espejo Valle-Inclán, Jose
Maurais, Elizabeth G.
Lu, Huiming
Davis, Anthony J.
Mazzagatti, Alice
Cortés-Ciriano, Isidro
Engel, Justin L.
Ly, Peter
Dahiya, Rashmi
Guyer, Alison
Hu, Qing
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/38965240$$D View this record in MEDLINE/PubMed
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PublicationDate 2024-07-04
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PublicationTitle Nature communications
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Nature Publishing Group
Nature Portfolio
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Snippet Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis. The...
Abstract Mitotic errors generate micronuclei entrapping mis-segregated chromosomes, which are susceptible to catastrophic fragmentation through chromothripsis....
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SubjectTerms 13
13/106
14
14/32
14/63
45/23
631/208/1405
631/208/211
631/67/68
631/80/103
631/80/641/2002
Cell cycle
Chromosome deletion
Chromosomes
Chromothripsis
CRISPR
CRISPR-Cas Systems
DNA Breaks, Double-Stranded
DNA damage
DNA End-Joining Repair
DNA fragmentation
DNA repair
Double-strand break repair
Errors
Fragmentation
Gene Rearrangement
Genomics
Humanities and Social Sciences
Humans
Kinetics
Micronuclei
Micronuclei, Chromosome-Defective
Mitosis - genetics
multidisciplinary
Non-homologous end joining
Science
Science (multidisciplinary)
Tumor Suppressor p53-Binding Protein 1 - genetics
Tumor Suppressor p53-Binding Protein 1 - metabolism
Yeast
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Title Non-homologous end joining shapes the genomic rearrangement landscape of chromothripsis from mitotic errors
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