Abstract
Shelterin is an essential telomeric protein complex that prevents DNA damage signaling and DNA repair at mammalian chromosome ends. Here we report on the role of the TRF2-interacting factor Rap1, a conserved shelterin subunit of unknown function. We removed Rap1 from mouse telomeres either through gene deletion or by replacing TRF2 with a mutant that does not bind Rap1. Rap1 was dispensable for the essential functions of TRF2--repression of ATM kinase signaling and nonhomologous end joining (NHEJ)--and mice lacking telomeric Rap1 were viable and fertile. However, Rap1 was critical for the repression of homology-directed repair (HDR), which can alter telomere length. The data reveal that HDR at telomeres can take place in the absence of DNA damage foci and underscore the functional compartmentalization within shelterin.
MeSH Terms
Amino Acid Sequence
Animals
Ataxia Telangiectasia Mutated Proteins
Cell Cycle Proteins/metabolism
Cell Proliferation
Cells, Cultured
Checkpoint Kinase 2
DNA Damage
DNA Repair
DNA-Binding Proteins/metabolism
Gene Deletion
Mice
Mice, Inbred C57BL
Mice, Knockout
Molecular Sequence Data
Protein Serine-Threonine Kinases/metabolism
Recombination, Genetic
Shelterin Complex
Signal Transduction
Sister Chromatid Exchange
Telomere/genetics,metabolism
Telomere-Binding Proteins/chemistry,genetics,metabolism
Telomeric Repeat Binding Protein 2/genetics,metabolism
Tumor Suppressor Proteins/metabolism
Chemicals
Cell Cycle Proteins
DNA-Binding Proteins
Shelterin Complex
TERF2IP protein, mouse
TRF2 protein, mouse
Telomere-Binding Proteins
Telomeric Repeat Binding Protein 2
Tumor Suppressor Proteins
Checkpoint Kinase 2
Ataxia Telangiectasia Mutated Proteins
Atm protein, mouse
Chek2 protein, mouse
Protein Serine-Threonine Kinases
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Sfeir Agnel
The Rockefeller University, 1230 York Avenue, New York, NY 10065, USA.
Kabir Shaheen
van Overbeek Megan
Celli Giulia B
de Lange Titia
References (20)
20 references, click to expand
-
Telomere protection by TPP1 is mediated by POT1a and POT1b.
Mol Cell Biol. 2010 Feb;30(4):1059-66
PMID: 19995905
-
Telomere loops and homologous recombination-dependent telomeric circles in a Kluyveromyces lactis telomere mutant strain.
Mol Cell Biol. 2008 Jan;28(1):20-9
PMID: 17967889
-
Protection of telomeres through independent control of ATM and ATR by TRF2 and POT1.
Nature. 2007 Aug 30;448(7157):1068-71
PMID: 17687332
-
Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication.
Cell. 2009 Jul 10;138(1):90-103
PMID: 19596237
-
Human RAP1 inhibits non-homologous end joining at telomeres.
EMBO J. 2009 Nov 4;28(21):3390-9
PMID: 19763083
-
How telomeres solve the end-protection problem.
Science. 2009 Nov 13;326(5955):948-52
PMID: 19965504
-
NMR structure of the hRap1 Myb motif reveals a canonical three-helix bundle lacking the positive surface charge typical of Myb DNA-binding domains.
J Mol Biol. 2001 Sep 7;312(1):167-75
PMID: 11545594
-
Taz1, Rap1 and Rif1 act both interdependently and independently to maintain telomeres.
EMBO J. 2005 Sep 7;24(17):3128-35
PMID: 16096639
-
A critical role for TPP1 and TIN2 interaction in high-order telomeric complex assembly.
Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):11874-9
PMID: 16880378
-
Involvement of replicative polymerases, Tel1p, Mec1p, Cdc13p, and the Ku complex in telomere-telomere recombination.
Mol Cell Biol. 2002 Aug;22(16):5679-87
PMID: 12138180
-
DNA damage foci at dysfunctional telomeres.
Curr Biol. 2003 Sep 2;13(17):1549-56
PMID: 12956959
-
Rap1 prevents telomere fusions by nonhomologous end joining.
EMBO J. 2005 Sep 7;24(17):3117-27
PMID: 16096640
-
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
-
Functional dissection of human and mouse POT1 proteins.
Mol Cell Biol. 2009 Jan;29(2):471-82
PMID: 18955498
-
Rap1 affects the length and heterogeneity of human telomeres.
Mol Biol Cell. 2003 Dec;14(12):5060-8
PMID: 14565979
-
Multiple pathways inhibit NHEJ at telomeres.
Genes Dev. 2008 May 1;22(9):1153-8
PMID: 18451106
-
Ku70 stimulates fusion of dysfunctional telomeres yet protects chromosome ends from homologous recombination.
Nat Cell Biol. 2006 Aug;8(8):885-90
PMID: 16845382
-
Identification of human Rap1: implications for telomere evolution.
Cell. 2000 May 26;101(5):471-83
PMID: 10850490
-
Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends.
Science. 2007 Nov 2;318(5851):798-801
PMID: 17916692
-
Pot1 deficiency initiates DNA damage checkpoint activation and aberrant homologous recombination at telomeres.
Cell. 2006 Jul 14;126(1):49-62
PMID: 16839876