Repair Pathway Choices and Consequences at the Double-Strand Break

DNA double-strand breaks (DSBs) are cytotoxic lesions that threaten genomic integrity. Failure to repair a DSB has deleterious consequences, including genomic instability and cell death. Indeed, misrepair of DSBs can lead to inappropriate end-joining events, which commonly underlie oncogenic transfo...

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Veröffentlicht in:	Trends in cell biology Jg. 26; H. 1; S. 52 - 64
Hauptverfasser:	Ceccaldi, Raphael, Rondinelli, Beatrice, D’Andrea, Alan D.
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	England Elsevier Ltd 01.01.2016
Schlagworte:	alternative end joining Animals Cell Survival DNA Breaks, Double-Stranded DNA Repair Genomic Instability homologous recombination Humans Mutation Pathology Polθ synthetic lethality homologous recombination DNA repair Polθ alternative end joining synthetic lethality
ISSN:	0962-8924, 1879-3088
Online-Zugang:	Volltext
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Abstract	DNA double-strand breaks (DSBs) are cytotoxic lesions that threaten genomic integrity. Failure to repair a DSB has deleterious consequences, including genomic instability and cell death. Indeed, misrepair of DSBs can lead to inappropriate end-joining events, which commonly underlie oncogenic transformation due to chromosomal translocations. Typically, cells employ two main mechanisms to repair DSBs: homologous recombination (HR) and classical nonhomologous end joining (C-NHEJ). In addition, alternative error-prone DSB repair pathways, namely alternative end joining (alt-EJ) and single-strand annealing (SSA), have been recently shown to operate in many different conditions and to contribute to genome rearrangements and oncogenic transformation. Here, we review the mechanisms regulating DSB repair pathway choice, together with the potential interconnections between HR and the annealing-dependent error-prone DSB repair pathways. Of the four known pathways for repairing DNA DSBs, some evolved towards high-fidelity processes (HR and C-NHEJ), while others are intrinsically mutagenic (alt-EJ and SSA). Some repair pathways are end resection-independent (C-NHEJ), while others are end resection-dependent (HR, alt-EJ, and SSA). End resection likely plays a key role in dictating DNA repair pathway choice. Homology-based repair pathways (HR, alt-EJ, and SSA) are competitive and mutually regulated around the RAD51 presynaptic and postsynaptic steps of HR. Error-prone repair pathways can compensate for the loss of HR. Polθ (an alt-EJ polymerase) is upregulated in HR-deficient cancers: loss of the HR and Polθ-mediated alt-EJ pathways is synthetic lethal.
AbstractList	DNA double-strand breaks (DSBs) are cytotoxic lesions that threaten genomic integrity. Failure to repair a DSB has deleterious consequences, including genomic instability and cell death. Indeed, misrepair of DSBs can lead to inappropriate end-joining events, which commonly underlie oncogenic transformation due to chromosomal translocations. Typically, cells employ two main mechanisms to repair DSBs: homologous recombination (HR) and classical nonhomologous end joining (C-NHEJ). In addition, alternative error-prone DSB repair pathways, namely alternative end joining (alt-EJ) and single-strand annealing (SSA), have been recently shown to operate in many different conditions and to contribute to genome rearrangements and oncogenic transformation. Here, we review the mechanisms regulating DSB repair pathway choice, together with the potential interconnections between HR and the annealing-dependent error-prone DSB repair pathways. DNA double-strand breaks (DSBs) are cytotoxic lesions that threaten genomic integrity. Failure to repair a DSB has deleterious consequences, including genomic instability and cell death. Indeed, misrepair of DSBs can lead to inappropriate end-joining events, which commonly underlie oncogenic transformation due to chromosomal translocations. Typically, cells employ two main mechanisms to repair DSBs: homologous recombination (HR) and classical nonhomologous end joining (C-NHEJ). In addition, alternative error-prone DSB repair pathways, namely alternative end joining (alt-EJ) and single-strand annealing (SSA), have been recently shown to operate in many different conditions and to contribute to genome rearrangements and oncogenic transformation. Here, we review the mechanisms regulating DSB repair pathway choice, together with the potential interconnections between HR and the annealing-dependent error-prone DSB repair pathways. Of the four known pathways for repairing DNA DSBs, some evolved towards high-fidelity processes (HR and C-NHEJ), while others are intrinsically mutagenic (alt-EJ and SSA). Some repair pathways are end resection-independent (C-NHEJ), while others are end resection-dependent (HR, alt-EJ, and SSA). End resection likely plays a key role in dictating DNA repair pathway choice. Homology-based repair pathways (HR, alt-EJ, and SSA) are competitive and mutually regulated around the RAD51 presynaptic and postsynaptic steps of HR. Error-prone repair pathways can compensate for the loss of HR. Polθ (an alt-EJ polymerase) is upregulated in HR-deficient cancers: loss of the HR and Polθ-mediated alt-EJ pathways is synthetic lethal.
Author	D’Andrea, Alan D. Ceccaldi, Raphael Rondinelli, Beatrice
AuthorAffiliation	1 Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA
AuthorAffiliation_xml	– name: 1 Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA
Author_xml	– sequence: 1 givenname: Raphael surname: Ceccaldi fullname: Ceccaldi, Raphael organization: Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 2 givenname: Beatrice surname: Rondinelli fullname: Rondinelli, Beatrice organization: Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA – sequence: 3 givenname: Alan D. surname: D’Andrea fullname: D’Andrea, Alan D. email: alan_dandrea@dfci.harvard.edu organization: Department of Radiation Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA 02215, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/26437586$$D View this record in MEDLINE/PubMed
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Snippet	DNA double-strand breaks (DSBs) are cytotoxic lesions that threaten genomic integrity. Failure to repair a DSB has deleterious consequences, including genomic...
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SubjectTerms	alternative end joining Animals Cell Survival DNA Breaks, Double-Stranded DNA Repair Genomic Instability homologous recombination Humans Mutation Pathology Polθ synthetic lethality
Title	Repair Pathway Choices and Consequences at the Double-Strand Break
URI	https://www.clinicalkey.com/#!/content/1-s2.0-S0962892415001427 https://www.clinicalkey.es/playcontent/1-s2.0-S0962892415001427 https://dx.doi.org/10.1016/j.tcb.2015.07.009 https://www.ncbi.nlm.nih.gov/pubmed/26437586 https://www.proquest.com/docview/1753230558 https://pubmed.ncbi.nlm.nih.gov/PMC4862604
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