Abstract
The repair of DNA double-strand breaks (DSB) requires processing of the broken ends to complete the ligation process. Recently, it has been shown that DNA polymerase mu (polmu) and DNA polymerase lambda (pollambda) are both involved in such processing during non-homologous end joining in vitro. However, no phenotype was observed in animal models defective for either polmu and/or pollambda. Such observations could result from a functional redundancy shared by the X family of DNA polymerases. To avoid such redundancy and to clarify the role of polmu in the end joining process, we generated cells over-expressing the wild type as well as an inactive form of polmu (polmuD). We observed that cell sensitivity to ionizing radiation (IR) was increased when either polmu or polmuD was over-expressed. However, the genetic instability in response to IR increased only in cells expressing polmuD. Moreover, analysis of intrachromosomal repair of the I-SceI-induced DNA DSB, did not reveal any effect of either polmu or polmuD expression on the efficiency of ligation of both cohesive and partially complementary ends. Finally, the sequences of the repaired ends were specifically affected when polmu or polmuD was over-expressed, supporting the hypothesis that polmu could be involved in the repair of a DSB subset when resolution of junctions requires some gap filling.
MeSH Terms
Animals
Base Sequence
CHO Cells
Cell Line
Chromosome Aberrations
Cricetinae
Cricetulus
DNA/chemistry
DNA Breaks, Double-Stranded
DNA Repair
DNA-Directed DNA Polymerase/physiology
Deoxyribonucleases, Type II Site-Specific/metabolism
Humans
Molecular Sequence Data
Radiation, Ionizing
Saccharomyces cerevisiae Proteins
Chemicals
Saccharomyces cerevisiae Proteins
DNA
DNA polymerase mu
DNA-Directed DNA Polymerase
SCEI protein, S cerevisiae
Deoxyribonucleases, Type II Site-Specific
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Capp Jean-Pascal
Genetic instability and Cancer group, Institute of Pharmacology and Structural Biology, University Paul Sabatier, UMR CNRS 5089, 205 route de Narbonne, 31077 Toulouse cedex, France.
Boudsocq François
Besnard Anne-Gaelle
Lopez Bernard S
Cazaux Christophe
Hoffmann Jean-Sébastien
Canitrot Yvan
References (20)
20 references, click to expand
-
DNA polymerase mu (Pol mu), homologous to TdT, could act as a DNA mutator in eukaryotic cells.
EMBO J. 2000 Apr 3;19(7):1731-42
PMID: 10747040
-
Structural insight into the substrate specificity of DNA Polymerase mu.
Nat Struct Mol Biol. 2007 Jan;14(1):45-53
PMID: 17159995
-
Two novel human and mouse DNA polymerases of the polX family.
Nucleic Acids Res. 2000 Sep 15;28(18):3684-93
PMID: 10982892
-
Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): an archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic poleta.
Nucleic Acids Res. 2001 Nov 15;29(22):4607-16
PMID: 11713310
-
Hydrocephalus, situs inversus, chronic sinusitis, and male infertility in DNA polymerase lambda-deficient mice: possible implication for the pathogenesis of immotile cilia syndrome.
Mol Cell Biol. 2002 Apr;22(8):2769-76
PMID: 11909969
-
Deregulated DNA polymerase beta strengthens ionizing radiation-induced nucleotidic and chromosomal instabilities.
Oncogene. 2002 Apr 4;21(15):2320-7
PMID: 11948415
-
Deregulated DNA polymerase beta induces chromosome instability and tumorigenesis.
Cancer Res. 2002 Jun 15;62(12):3511-4
PMID: 12067997
-
Association of DNA polymerase mu (pol mu) with Ku and ligase IV: role for pol mu in end-joining double-strand break repair.
Mol Cell Biol. 2002 Jul;22(14):5194-202
PMID: 12077346
-
Immunoglobulin kappa light chain gene rearrangement is impaired in mice deficient for DNA polymerase mu.
Immunity. 2003 Aug;19(2):203-11
PMID: 12932354
-
The frameshift infidelity of human DNA polymerase lambda. Implications for function.
J Biol Chem. 2003 Sep 5;278(36):34685-90
PMID: 12829698
-
Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells.
Mol Cell. 2004 Jun 4;14(5):611-23
PMID: 15175156
-
The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination.
Cell. 1995 Dec 29;83(7):1079-89
PMID: 8548796
-
Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination.
Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8076-81
PMID: 9223317
-
Homology-directed repair is a major double-strand break repair pathway in mammalian cells.
Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5172-7
PMID: 9560248
-
Identification of a defect in DNA ligase IV in a radiosensitive leukaemia patient.
Curr Biol. 1999 Jul 1;9(13):699-702
PMID: 10395545
-
A biochemically defined system for mammalian nonhomologous DNA end joining.
Mol Cell. 2004 Dec 3;16(5):701-13
PMID: 15574326
-
A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining.
Mol Cell. 2005 Aug 5;19(3):357-66
PMID: 16061182
-
The DNA polymerase lambda is required for the repair of non-compatible DNA double strand breaks by NHEJ in mammalian cells.
Nucleic Acids Res. 2006;34(10):2998-3007
PMID: 16738138
-
Nonoverlapping functions of DNA polymerases mu, lambda, and terminal deoxynucleotidyltransferase during immunoglobulin V(D)J recombination in vivo.
Immunity. 2006 Jul;25(1):31-41
PMID: 16860755
-
DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis.
J Mol Biol. 2000 Aug 25;301(4):851-67
PMID: 10966791