ERCC1/XPF Removes the 3′ Overhang from Uncapped Telomeres and Represses Formation of Telomeric DNA-Containing Double Minute Chromosomes

Molecular Cell

Volumn 12, Issue 6, 2003, Pages 1489-1498

  Zhu, Xu Dong ^a,d   Niedernhofer, Laura ^b,e   Kuster, Bernhard ^c,f   Mann, Matthias ^c   Hoeijmakers, Jan H J ^b   De Lange, Titia ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY OF PITTSBURGH   (United States)

^f GLAXOSMITHKLINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; ENDONUCLEASE; EXCISION REPAIR CROSS COMPLEMENTING PROTEIN 1; PROTEIN; PROTEIN XPF; TELOMERE BINDING PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA DETERMINATION; DOUBLE MINUTE CHROMOSOME; EXCISION REPAIR; FEMALE; HUMAN; HUMAN CELL; MITOTIC RECOMBINATION; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN FUNCTION; REGULATORY MECHANISM; TELOMERE;

ANIMALIA;

EID: 0347416975     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00478-7     Document Type: Article

References (51)

1. Aboussekhra A., Biggerstaff M., Shivji M.K., Vilpo J.A., Moncollin V., Podust V.N., Protic M., Hubscher U., Egly J.M., 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., Nairn R.S. Role of ERCC1 in removal of long non-homologous tails during targeted homologous recombination. EMBO J. 19:2000;5552-5561.
3. Azzalin C.M., Mucciolo E., Bertoni L., Giulotto E. Fluorescence in situ hybridization with a synthetic (T2AG3)n polynucleotide detects several intrachromosomal telomere-like repeats on human chromosomes. Cytogenet. Cell Genet. 78:1997;112-115.
4. Bailey S.M., Cornforth M.N., Kurimasa A., Chen D.J., Goodwin E.H. Strand-specific postreplicative processing of mammalian telomeres. Science. 293:2001;2462-2465.
5. Baird D.M., Rowson J., Wynford-Thomas D., Kipling D. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat. Genet. 33:2003;203-207.
6. Biggerstaff M., Szymkowski D.E., 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.
7. Bilaud T., Brun C., Ancelin K., Koering C.E., Laroche T., Gilson E. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17:1997;236-239.
8. Broccoli D., Smogorzewska A., Chong L., de Lange T. Human telomeres contain two distinct Myb-related proteins, TRF1 and TRF2. Nat. Genet. 17:1997;231-235.
9. 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., Thompson L.H. ERCC4 (XPF) encodes a human nucleotide excision repair protein with eukaryotic recombination homologs. Mol. Cell. Biol. 16:1996;6553-6562.
10. Chong L., van Steensel B., Broccoli D., Erdjument-Bromage H., Hanish J., Tempst P., de Lange T. A human telomeric protein. Science. 270:1995;1663-1667.
11. de Laat W.L., Appeldoorn E., Jaspers N.G., Hoeijmakers J.H. DNA structural elements required for ERCC1-XPF endonuclease activity. J. Biol. Chem. 273:1998;7835-7842. a.
12. de Laat W.L., Appeldoorn E., Sugasawa K., Weterings E., Jaspers N.G., Hoeijmakers J.H. DNA-binding polarity of human replication protein A positions nucleases in nucleotide excision repair. Genes Dev. 12:1998;2598-2609. b.
13. de Laat W.L., Jaspers N.G., Hoeijmakers J.H. Molecular mechanism of nucleotide excision repair. Genes Dev. 13:1999;768-785.
14. de Lange T. Protection of mammalian telomeres. Oncogene. 21:2002;532-540.
15. de Vries A., van Oostrom C.T., Hofhuis F.M., Dortant P.M., Berg R.J., de Gruijl F.R., Wester P.W., van Kreijl C.F., Capel P.J., van Steeg H.et al. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature. 377:1995;169-173.
16. Fanning T.G. Origin and evolution of a major feline satellite DNA. J. Mol. Biol. 197:1987;627-634.
17. Fishman-Lobell J., Haber J.E. Removal of nonhomologous DNA ends in double-strand break recombination. the role of the yeast ultraviolet repair gene RAD1 Science. 258:1992;480-484.
18. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., de Lange T. Mammalian telomeres end in a large duplex loop. Cell. 97:1999;503-514.
19. Hahn P.J. Molecular biology of double-minute chromosomes. Bioessays. 15:1993;477-484.
20. Hemann M.T., Greider C.W. G-strand overhangs on telomeres in telomerase-deficient mouse cells. Nucleic Acids Res. 27:1999;3964-3969.
21. Hoeijmakers J.H. Genome maintenance mechanisms for preventing cancer. Nature. 411:2001;366-374.
22. Houtsmuller A.B., Rademakers S., Nigg A.L., Hoogstraten D., Hoeijmakers J.H., Vermeulen W. Action of DNA repair endonuclease ERCC1/XPF in living cells. Science. 284:1999;958-961.
23. Ivanov E.L., Haber J.E. RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:1995;2245-2251.
24. Karlseder J., Broccoli D., Dai Y., Hardy S., de Lange T. p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science. 283:1999;1321-1325.
25. Karlseder J., Smogorzewska A., de Lange T. Senescence induced by altered telomere state, not telomere loss. Science. 295:2002;2446-2449.
26. Kondo S., Mamada A., Miyamoto C., Keong C.H., Satoh Y., 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. Photodermatol. 6:1989;89-95.
27. Lansdorp P.M., Verwoerd N.P., van de Rijke F.M., Dragowska V., Little M.T., Dirks R.W., Raap A.K., Tanke H.J. Heterogeneity in telomere length of human chromosomes. Hum. Mol. Genet. 5:1996;685-691.
28. Lin C.C., Meyne J., Sasi R., Moyzis R.K. Apparent lack of telomere sequences on double minute chromosomes. Cancer Genet. Cytogenet. 48:1990;271-274.
29. Makarov V.L., Hirose Y., Langmore J.P. Long G tails at both ends of human chromosomes suggest a C strand degradation mechanism for telomere shortening. Cell. 88:1997;657-666.
30. McWhir J., Selfridge J., Harrison D.J., Squires S., 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. Meyne J., Baker R.J., Hobart H.H., Hsu T.C., Ryder O.A., Ward O.G., Wiley J.E., Wurster-Hill D.H., Yates T.L., Moyzis R.K. Distribution of non-telomeric sites of the (TTAGGG)n telomeric sequence in vertebrate chromosomes. Chromosoma. 99:1990;3-10.
32. Nakane H., Takeuchi S., Yuba S., Saijo M., Nakatsu Y., Murai H., Nakatsuru Y., Ishikawa T., Hirota S., Kitamura Y.et al. High incidence of ultraviolet-B-or chemical-carcinogen-induced skin tumours in mice lacking the xeroderma pigmentosum group A gene. Nature. 377:1995;165-168.
33. Niedernhofer L.J., Essers J., Weeda G., Beverloo B., de Wit J., Muijtjens M., Odijk H., Hoeijmakers J.H., Kanaar R. The structure-specific endonuclease Ercc1-Xpf is required for targeted gene replacement in embryonic stem cells. EMBO J. 20:2001;6540-6549.
34. Park C.H., Sancar A. Formation of a ternary complex by human XPA, ERCC1, and ERCC4(XPF) excision repair proteins. Proc. Natl. Acad. Sci. USA. 91:1994;5017-5021.
35. Sands A.T., Abuin A., Sanchez A., Conti C.J., Bradley A. High susceptibility to ultraviolet-induced carcinogenesis in mice lacking XPC. Nature. 377:1995;162-165.
36. Sargent R.G., Meservy J.L., Perkins B.D., Kilburn A.E., Intody Z., Adair G.M., Nairn R.S., Wilson J.H. Role of the nucleotide excision repair gene ERCC1 in formation of recombination-dependent rearrangements in mammalian cells. Nucleic Acids Res. 28:2000;3771-3778.
37. Schiestl R.H., Prakash S. RAD1, an excision repair gene of Saccharomyces cerevisiae, is also involved in recombination. Mol. Cell. Biol. 8:1988;3619-3626.
38. 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.et al. Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell. 86:1996;811-822.
39. Smogorzewska A., de Lange T. Different telomere damage signaling pathways in human and mouse cells. EMBO J. 21:2002;4338-4348.
40. Smogorzewska A., Karlseder J., Holtgreve-Grez H., Jauch A., de Lange T. DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr. Biol. 12:2002;1635-1644.
41. Southern E.M. Base sequence and evolution of guinea-pig alpha-satellite DNA. Nature. 227:1970;794-798.
42. Stansel R.M., de Lange T., Griffith J.D. T-loop assembly in vitro involves binding of TRF2 near the 3′ telomeric overhang. EMBO J. 20:2001;E5532-E5540.
43. Stewart S.A., Ben-Porath I., Carey V.J., O'Connor B.F., Hahn W.C., Weinberg R.A. Erosion of the telomeric single-strand overhang at replicative senescence. Nat. Genet. 33:2003;492-496.
44. Takai H., Smogorzewska A., d Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:2003;1540-1556.
45. van Steensel B., de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature. 385:1997;740-743.
46. van Steensel B., Smogorzewska A., 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., 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., 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. Wilm M., Shevchenko A., Houthaeve T., Breit S., Schweigerer L., Fotsis T., Mann M. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature. 379:1996;466-469.
50. Yagi T., Wood R.D., 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.
51. Zhu X.D., Kuster B., Mann M., Petrini J.H., de Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25:2000;347-352.