Abstract
TRF2 (telomeric repeat binding factor 2) is an essential component of the telomeric cap, where it forms and stabilizes the T-loop junctions. TRF2 forms the T-loops by stimulating strand invasion of the 3' overhang into duplex DNA. TRF2 also has been shown to localize to nontelomeric DNA double-strand breaks, but its functional role in DNA repair has not been examined. Here, we present evidence that TRF2 is involved in homologous recombination (HR) repair of nontelomeric double-strand breaks. Depletion of TRF2 strongly inhibited HR and delayed the formation of Rad51 foci after gamma-irradiation, whereas overexpression of TRF2 stimulated HR. Depletion of TRF2 had no effect on nonhomologous end-joining, and overexpression of TRF2 inhibited nonhomologous end-joining. We propose, based on our results and on the ability of TRF2 to mediate strand invasion, that TRF2 plays an essential role in HR by facilitating the formation of early recombination intermediates.
MeSH Terms
Cells, Cultured
DNA Breaks, Double-Stranded
DNA Repair
Humans
Nuclear Proteins/physiology
Rad51 Recombinase/analysis
Recombination, Genetic
TATA Box Binding Protein-Like Proteins/physiology
Telomeric Repeat Binding Protein 2
Chemicals
Nuclear Proteins
TATA Box Binding Protein-Like Proteins
TERF2 protein, human
Telomeric Repeat Binding Protein 2
RAD51 protein, human
Rad51 Recombinase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Mao Zhiyong
Department of Biology, University of Rochester, Rochester, NY 14627-0211, USA.
Seluanov Andrei
Jiang Ying
Gorbunova Vera
References (23)
23 references, click to expand
-
Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells.
EMBO J. 2000 Jul 3;19(13):3398-407
PMID: 10880452
-
A topological mechanism for TRF2-enhanced strand invasion.
Nat Struct Mol Biol. 2007 Feb;14(2):147-54
PMID: 17220898
-
Interaction of human Ku70 with TRF2.
FEBS Lett. 2000 Sep 8;481(1):81-5
PMID: 10984620
-
T-loop assembly in vitro involves binding of TRF2 near the 3' telomeric overhang.
EMBO J. 2001 Oct 1;20(19):5532-40
PMID: 11574485
-
Expression of human telomerase (hTERT) does not prevent stress-induced senescence in normal human fibroblasts but protects the cells from stress-induced apoptosis and necrosis.
J Biol Chem. 2002 Oct 11;277(41):38540-9
PMID: 12140282
-
Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases.
J Biol Chem. 2002 Oct 25;277(43):41110-9
PMID: 12181313
-
Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair.
Microbiol Mol Biol Rev. 2002 Dec;66(4):630-70, table of contents
PMID: 12456786
-
DNA end joining becomes less efficient and more error-prone during cellular senescence.
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7624-9
PMID: 15123826
-
The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response.
PLoS Biol. 2004 Aug;2(8):E240
PMID: 15314656
-
After double-strand break induction by UV-A, homologous recombination and nonhomologous end joining cooperate at the same DSB if both systems are available.
J Cell Sci. 2004 Oct 1;117(Pt 21):4935-45
PMID: 15367581
-
Homologous recombination generates T-loop-sized deletions at human telomeres.
Cell. 2004 Oct 29;119(3):355-68
PMID: 15507207
-
A human telomeric protein.
Science. 1995 Dec 8;270(5242):1663-7
PMID: 7502076
-
Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2.
Nat Genet. 1997 Oct;17(2):231-5
PMID: 9326950
-
Telomeric localization of TRF2, a novel human telobox protein.
Nat Genet. 1997 Oct;17(2):236-9
PMID: 9326951
-
Mammalian telomeres end in a large duplex loop.
Cell. 1999 May 14;97(4):503-14
PMID: 10338214
-
Human telomeric protein TRF2 associates with genomic double-strand breaks as an early response to DNA damage.
Nat Genet. 2005 Feb;37(2):193-7
PMID: 15665826
-
CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair.
Nature. 2005 Mar 31;434(7033):598-604
PMID: 15800615
-
DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion.
Nat Cell Biol. 2005 Jul;7(7):712-8
PMID: 15968270
-
Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells.
J Cell Biol. 2005 Aug 1;170(3):341-7
PMID: 16061690
-
DNA damage-induced phosphorylation of the human telomere-associated protein TRF2.
Proc Natl Acad Sci U S A. 2005 Oct 25;102(43):15539-44
PMID: 16223874
-
Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination.
Nat Cell Biol. 2006 Aug;8(8):885-90
PMID: 16845382
-
The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats.
J Biol Chem. 2006 Dec 8;281(49):37486-95
PMID: 17052985
-
Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres.
Nat Genet. 2000 Jul;25(3):347-52
PMID: 10888888