Human XPF controls TRF2 and telomere length maintenance through distinctive mechanisms

Mechanisms of Ageing and Development

Volumn 129, Issue 10, 2008, Pages 602-610

  Wu, Yili ^a   Mitchell, Taylor R H ^a   Zhu, Xu Dong ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

ERCC1; Telomere length maintenance; TRF2; XPF

Indexed keywords

EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; TELOMERASE; TELOMERIC REPEAT BINDING FACTOR 2;

ARTICLE; CHROMOSOME SIZE; CONTROLLED STUDY; ENZYME ACTIVITY; EXCISION REPAIR; GENE MUTATION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; TELOMERE;

ALLELES; ANIMALS; BETA-GALACTOSIDASE; CELL AGING; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; ENDONUCLEASES; GENE EXPRESSION REGULATION; HUMANS; IMMUNOPRECIPITATION; MICE; MODELS, BIOLOGICAL; RECOMBINATION, GENETIC; TELOMERE; TELOMERIC REPEAT BINDING PROTEIN 2;

EID: 54249112218     PISSN: 00476374     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mad.2008.08.004     Document Type: Article

References (54)

1. Aboussekhra A., Biggerstaff M., Shivji M.K., Vilpo J.A., Moncollin V., Podust V.N., Protic M., Hubscher U., Egly J.M., and Wood R.D. Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80 (1995) 859-868
2. Adair G.M., Rolig R.L., Moore-Faver D., Zabelshansky M., Wilson J.H., and Nairn R.S. Role of ERCC1 in removal of long non-homologous tails during targeted homologous recombination. EMBO J. 19 (2000) 5552-5561
3. Ancelin K., Brunori M., Bauwens S., Koering C.E., Brun C., Ricoul M., Pommier J.P., Sabatier L., and Gilson E. Targeting assay to study the cis functions of human telomeric proteins: evidence for inhibition of telomerase by TRF1 and for activation of telomere degradation by TRF2. Mol. Cell. Biol. 22 (2002) 3474-3487
4. Biggerstaff M., Szymkowski D.E., and Wood R.D. Co-correction of the ERCC1, ERCC4 and xeroderma pigmentosum group F DNA repair defects in vitro. EMBO J. 12 (1993) 3685-3692
5. Blackburn E.H. Telomere states and cell fates. Nature 408 (2000) 53-56
6. Blanco R., Munoz P., Flores J.M., Klatt P., and Blasco M.A. Telomerase abrogation dramatically accelerates TRF2-induced epithelial carcinogenesis. Genes Dev. 21 (2007) 206-220
7. Brookman K.W., Lamerdin J.E., Thelen M.P., Hwang M., Reardon J.T., Sancar A., Zhou Z.Q., Walter C.A., Parris C.N., and Thompson L.H. ERCC4 (XPF) encodes a human nucleotide excision repair protein with eukaryotic recombination homologs. Mol. Cell. Biol. 16 (1996) 6553-6562
8. Celli G.B., and de Lange T. DNA processing is not required for ATM-mediated telomere damage response after TRF2 deletion. Nat. Cell. Biol. 7 (2005) 712-718
9. de Laat W.L., Appeldoorn E., Jaspers N.G., and Hoeijmakers J.H. DNA structural elements required for ERCC1-XPF endonuclease activity. J. Biol. Chem. 273 (1998) 7835-7842
10. de Lange T. Protection of mammalian telomeres. Oncogene 21 (2002) 532-540
11. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
12. Enzlin J.H., and Scharer O.D. The active site of the DNA repair endonuclease XPF-ERCC1 forms a highly conserved nuclease motif. EMBO J. 21 (2002) 2045-2053
13. Fouche N., Cesare A.J., Willcox S., Ozgur S., Compton S.A., and Griffith J.D. The basic domain of TRF2 directs binding to DNA junctions irrespective of the presence of TTAGGG repeats. J. Biol. Chem. 281 (2006) 37486-37495
14. Freibaum B.D., and Counter C.M. hSnm1B is a novel telomere-associated protein. J. Biol. Chem. 281 (2006) 15033-15036
15. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., and de Lange T. Mammalian telomeres end in a large duplex loop. Cell 97 (1999) 503-514
16. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature 411 (2001) 366-374
17. Houtsmuller A.B., Rademakers S., Nigg A.L., Hoogstraten D., Hoeijmakers J.H., and Vermeulen W. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science 284 (1999) 958-961
18. Jaspers N.G., Raams A., Silengo M.C., Wijgers N., Niedernhofer L.J., Robinson A.R., Giglia-Mari G., Hoogstraten D., Kleijer W.J., Hoeijmakers J.H., and Vermeulen W. First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am. J. Hum. Genet. 80 (2007) 457-466
19. Karlseder J., Broccoli D., Dai Y., Hardy S., and de Lange T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283 (1999) 1321-1325
20. Karlseder J., Hoke K., Mirzoeva O.K., Bakkenist C., Kastan M.B., Petrini J.H., and de Lange T. The telomeric protein TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol. 2 (2004) E240
21. Karlseder J., Smogorzewska A., and de Lange T. Senescence induced by altered telomere state, not telomere loss. Science 295 (2002) 2446-2449
22. Kondo S., Mamada A., Miyamoto C., Keong C.H., Satoh Y., and Fujiwara Y. Late onset of skin cancers in 2 xeroderma pigmentosum group F siblings and a review of 30 Japanese xeroderma pigmentosum patients in groups D, E and F. Photodermatology 6 (1989) 89-95
23. Kuraoka I., Kobertz W.R., Ariza R.R., Biggerstaff M., Essigmann J.M., and Wood R.D. Repair of an interstrand DNA cross-link initiated by ERCC1-XPF repair/recombination nuclease. J. Biol. Chem. 275 (2000) 26632-26636
24. Lenain C., Bauwens S., Amiard S., Brunori M., Giraud-Panis M.J., and Gilson E. The Apollo 5′ exonuclease functions together with TRF2 to protect telomeres from DNA repair. Curr. Biol. (2006)
25. Li B., and de Lange T. Rap1 affects the length and heterogeneity of human telomeres. Mol. Biol. Cell. 14 (2003) 5060-5068
26. Loayza D., and De Lange T. POT1 as a terminal transducer of TRF1 telomere length control. Nature 424 (2003) 1013-1018
27. Mao Z., Seluanov A., Jiang Y., and Gorbunova V. TRF2 is required for repair of nontelomeric DNA double-strand breaks by homologous recombination. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 13068-13073
28. Maser R.S., and DePinho R.A. Connecting chromosomes, crisis, and cancer. Science 297 (2002) 565-569
29. Matsunaga T., Mu D., Park C.H., Reardon J.T., and Sancar A. Human DNA repair excision nuclease. Analysis of the roles of the subunits involved in dual incisions by using anti-XPG and anti-ERCC1 antibodies. J. Biol. Chem. 270 (1995) 20862-20869
30. McWhir J., Selfridge J., Harrison D.J., Squires S., and Melton D.W. Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Genet. 5 (1993) 217-224
31. Munoz P., Blanco R., Flores J.M., and Blasco M.A. XPF nuclease-dependent telomere loss and increased DNA damage in mice overexpressing TRF2 result in premature aging and cancer. Nat. Genet. 37 (2005) 1063-1071
32. Niedernhofer L.J., Essers J., Weeda G., Beverloo B., de Wit J., Muijtjens M., Odijk H., Hoeijmakers J.H., and Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J. 20 (2001) 6540-6549
33. Niedernhofer L.J., Garinis G.A., Raams A., Lalai A.S., Robinson A.R., Appeldoorn E., Odijk H., Oostendorp R., Ahmad A., van Leeuwen W., Theil A.F., Vermeulen W., van der Horst G.T., Meinecke P., Kleijer W.J., Vijg J., Jaspers N.G., and Hoeijmakers J.H. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444 (2006) 1038-1043
34. Niedernhofer L.J., Odijk H., Budzowska M., van Drunen E., Maas A., Theil A.F., de Wit J., Jaspers N.G., Beverloo H.B., Hoeijmakers J.H., and Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required to resolve DNA interstrand cross-link-induced double-strand breaks. Mol. Cell. Biol. 24 (2004) 5776-5787
35. Nishino T., Komori K., Ishino Y., and Morikawa K. X-ray and biochemical anatomy of an archaeal XPF/Rad1/Mus81 family nuclease: similarity between its endonuclease domain and restriction enzymes. Structure (Camb) 11 (2003) 445-457
36. Opresko P.L., Von Kobbe C., Laine J.P., Harrigan J., Hickson I.D., and Bohr V.A. Telomere binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. (2002)
37. Park C.H., Bessho T., Matsunaga T., and Sancar A. Purification and characterization of the XPF-ERCC1 complex of human DNA repair excision nuclease. J. Biol. Chem. 270 (1995) 22657-22660
38. Park C.H., and Sancar A. Formation of a ternary complex by human XPA, ERCC1, and ERCC4(XPF) excision repair proteins. Proc. Natl. Acad. Sci. U.S.A. 91 (1994) 5017-5021
39. -/- mice. EMBO J. 24 (2005) 861-871
40. Sijbers A.M., de Laat W.L., Ariza R.R., Biggerstaff M., Wei Y.F., Moggs J.G., Carter K.C., Shell B.K., Evans E., de Jong M.C., Rademakers S., de Rooij J., Jaspers N.G., Hoeijmakers J.H., and Wood R.D. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell 86 (1996) 811-822
41. Smogorzewska A., van Steensel B., Bianchi A., Oelmann S., Schaefer M.R., Schnapp G., and de Lange T. Control of human telomere length by TRF1 and TRF2. Mol. Cell. Biol. 20 (2000) 1659-1668
42. Stansel R.M., de Lange T., and Griffith J.D. T-loop assembly in vitro involves binding of TRF2 near the 3′ telomeric overhang. EMBO J. 20 (2001) E5532-E5540
43. Tian M., Shinkura R., Shinkura N., and Alt F.W. Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol. Cell. Biol. 24 (2004) 1200-1205
44. van Overbeek M., and de Lange T. Apollo, an artemis-related nuclease interacts with TRF2 and protects human telomeres in S phase. Curr. Biol. (2006)
45. van Steensel B., and de Lange T. Control of telomere length by the human telomeric protein TRF1 [see comments]. Nature 385 (1997) 740-743
46. van Steensel B., Smogorzewska A., and de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 92 (1998) 401-413
47. van Vuuren A.J., Appeldoorn E., Odijk H., Yasui A., Jaspers N.G., Bootsma D., and Hoeijmakers J.H. Evidence for a repair enzyme complex involving ERCC1 and complementing activities of ERCC4, ERCC11 and xeroderma pigmentosum group F. EMBO J. 12 (1993) 3693-3701
48. Weeda G., Donker I., de Wit J., Morreau H., Janssens R., Vissers C.J., Nigg A., van Steeg H., Bootsma D., and Hoeijmakers J.H. Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr. Biol. 7 (1997) 427-439
49. Wu Y., Xiao S., and Zhu X.D. MRE11-RAD50-NBS1 and ATM function as co-mediators of TRF1 in telomere length control. Nat. Struct. Mol. Biol. 14 (2007) 832-840
50. Wu Y., Zacal N.J., Rainbow A.J., and Zhu X.D. XPF with mutations in its conserved nuclease domain is defective in DNA repair but functions in TRF2-mediated telomere shortening. DNA Repair (Amst.) 6 (2007) 157-166
51. Yagi T., Matsumura Y., Sato M., Nishigori C., Mori T., Sijbers A.M., and Takebe H. Complete restoration of normal DNA repair characteristics in group F xeroderma pigmentosum cells by over-expression of transfected XPF cDNA. Carcinogenesis 19 (1998) 55-60
52. Yagi T., Wood R.D., and Takebe H. A low content of ERCC1 and a 120 kDa protein is a frequent feature of group F xeroderma pigmentosum fibroblast cells. Mutagenesis 12 (1997) 41-44
53. Zhu X.D., Kuster B., Mann M., Petrini J.H., and Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25 (2000) 347-352
54. Zhu X.D., Niedernhofer L., Kuster B., Mann M., Hoeijmakers J.H., and de Lange T. ERCC1/XPF removes the 3′ overhang from uncapped telomeres and represses formation of telomeric DNA-containing double minute chromosomes. Mol. Cell 12 (2003) 1489-1498