Pot1 Deficiency Initiates DNA Damage Checkpoint Activation and Aberrant Homologous Recombination at Telomeres

Cell

Volumn 126, Issue 1, 2006, Pages 49-62

  Wu, Ling ^a   Multani, Asha S ^a   He, Hua ^a   Cosme Blanco, Wilfredo ^a   Deng, Yu ^a   Deng, Jian Min ^a   Bachilo, Olga ^b   Pathak, Sen ^a   Tahara, Hedioshi ^c   Bailey, Susan M ^d   Deng, Yibin ^a   Behringer, Richard R ^a   Chang, Sandy ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b Rice University   (United States)

^c HIROSHIMA UNIVERSITY   (Japan)

^d Veterinary Dentistry and Oral Surgery   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; NIBRIN; PROTECTION OF TELOMERE PROTEIN; PROTEIN P53; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHROMATID; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CHROMOSOME SIZE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVATION; GENE DELETION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; TELOMERE;

MAMMALIA;

EID: 33745713451     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.05.037     Document Type: Article

References (63)

1. Arango N.A., Lovell-Badge R., and Behringer R.R. Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development. Cell 99 (1999) 409-419
2. Artandi S., Chang S., Lee S., Alson S., Gottlieb G., Chin L., and Depinho R.A. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 406 (2000) 641-645
3. Bailey S.M., Cornforth M.N., Kurimasa A., Chen D.J., and Goodwin E.H. Strand-specific postreplicative processing of mammalian telomeres. Science 293 (2001) 2462-2465
4. Bailey S.M., Brenneman M.A., and Goodwin E.H. Frequent recombination in telomeric DNA may extend the proliferative life of telomerase-negative cells. Nucleic Acids Res. 32 (2004) 3743-3751
5. Banin S., Moyal L., Shieh S., Taya Y., Anderson C.W., Chessa L., Smorodinsky N.I., Prives C., Reiss Y., Shiloh Y., and Ziv Y. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281 (1998) 1674-1677
6. Baumann P., and Cech T.R. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292 (2001) 1171-1175
7. Baumann P., Podell E., and Cech T.R. Human Pot1 (protection of telomeres) protein: cytolocalization, gene structure, and alternative splicing. Mol. Cell. Biol. 22 (2002) 8079-8087
8. Bechter O.E., Zou Y., Walker W., Wright W.E., and Shay J.W. Telomeric recombination in mismatch repair deficient human colon cancer cells after telomerase inhibition. Cancer Res. 64 (2004) 3444-3451
9. Blackburn E.H. Switching and signaling at the telomere. Cell 106 (2001) 661-673
10. Blasco M.A., Lee H.W., Hande M.P., Samper E., Lansdorp P.M., DePinho R.A., and Greider C.W. Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91 (1997) 25-34
11. Canman C.E., Lim D.S., Cimprich K.A., Taya Y., Tamai K., Sakaguchi K., Appella E., Kastan M.B., and Siliciano J.D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281 (1998) 1677-1679
12. 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
13. Cesare A.J., and Griffith J.D. Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol. Cell. Biol. 24 (2004) 9948-9957
14. Crabbe L., Verdun R.E., Haggblom C.I., and Karlseder J. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. Science 306 (2004) 1951-1953
15. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., and Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003) 194-198
16. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
17. Garvik B., Carson M., and Hartwell L. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 15 (1995) 6128-6138
18. 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
19. Hayashi S., and McMahon A.P. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev. Biol. 244 (2002) 305-318
20. Hemann M.T., and Greider C.W. G-strand overhangs on telomeres in telomerase-deficient mouse cells. Nucleic Acids Res. 27 (1999) 3964-3969
21. Hockemeyer D., Sfeir A.J., Shay J.W., Wright W.E., and de Lange T. POT1 protects telomeres from a transient DNA damage response and determines how human chromosomes end. EMBO J. 24 (2005) 2667-2678
22. Hockemeyer D., Daniels J.-P., Takai H., and de Lange T. Recent expansion of the telomeric complex in rodents: Two distinct POT1 proteins protect mouse telomeres. Cell 126 (2006) 63-77 this issue
23. Houghtaling B.R., Cuttonaro L., Chang W., and Smith S. A dynamic molecular link between the telomere length regulator TRF1 and the chromosome end protector TRF2. Curr. Biol. 14 (2004) 1621-1631
24. 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
25. Kelleher C., Kurth I., and Lingner J. Human protection of telomeres 1 (POT1) is a negative regulator of telomerase activity in vitro. Mol. Cell. Biol. 25 (2005) 808-818
26. Kim S.H., Beausejour C., Davalos A.R., Kaminker P., Heo S.J., and Campisi J. TIN2 mediates functions of TRF2 at human telomeres. J. Biol. Chem. 279 (2004) 43799-43804
27. Kondo T., Oue N., Yoshida K., Mitani Y., Naka K., Nakayama H., and Yasui W. Expression of POT1 is associated with tumor stage and telomere length in gastric carcinoma. Cancer Res. 64 (2004) 523-529
28. Laud P.R., Multani A.S., Bailey S.M., Wu L., Ma J., Kingsley C., Lebel M., Pathak S., DePinho R.A., and Chang S. Elevated telomere-telomere recombination in WRN-deficient, telomere dysfunctional cells promotes escape from senescence and engagement of the ALT pathway. Genes Dev. 19 (2005) 2560-2570
29. Lei M., Podell E.R., Baumann P., and Cech T.R. DNA self-recognition in the structure of Pot1 bound to telomeric single-stranded DNA. Nature 426 (2003) 198-203
30. Lei M., Podell E.R., and Cech T.R. Structure of human POT1 bound to telomeric single-stranded DNA provides a model for chromosome end-protection. Nat. Struct. Mol. Biol. 11 (2004) 1223-1229
31. Lei M., Zaug A.J., Podell E.R., and Cech T.R. Switching human telomerase on and off with hPOT1 protein in vitro. J. Biol. Chem. 280 (2005) 20449-20456
32. Li B., Oestreich S., and de Lange T. Identification of human Rap1: implications for telomere evolution. Cell 101 (2000) 471-483
33. Liu D., Safari A., O'Connor M.S., Chan D.W., Laegeler A., Qin J., and Songyang Z. PTOP interacts with POT1 and regulates its localization to telomeres. Nat. Cell Biol. 6 (2004) 673-680
34. Liu D., O'Connor M.S., Qin J., and Songyang Z. Telosome, a mammalian telomere-associated complex formed by multiple telomeric proteins. J. Biol. Chem. 279 (2004) 51338-51342
35. Loayza D., and de Lange T. POT1 as a terminal transducer of TRF1 telomere length control. Nature 423 (2003) 1013-1018
36. Londono-Vallejo J.A., Der-Sarkissian H., Cazes L., Bacchetti S., and Reddel R.R. Alternative lengthening of telomeres is characterized by high rates of telomeric exchange. Cancer Res. 64 (2004) 2324-2327
37. Lustig A.J. Clues to catastrophic telomere loss in mammals from yeast telomere rapid deletion. Nat. Rev. Genet. 4 (2003) 916-923
38. Maser R.S., and DePinho R.A. Telomeres and the DNA damage response: why the fox is guarding the henhouse. DNA Repair (Amst.) 3 (2004) 979-988
39. Mohaghegh P., Karow J.K., Brosh Jr. R.M., Bohr V.A., and Hickson I.D. The Bloom's and Werner's syndrome proteins are DNA structure-specific helicases. Nucleic Acids Res. 29 (2001) 2843-2849
40. Murti K.G., and Prescott D.M. Telomeres of polytene chromosomes in a ciliated protozoan terminate in duplex DNA loops. Proc. Natl. Acad. Sci. USA 96 (1999) 14436-14439
41. Nikitina T., and Woodcock C.L. Closed chromatin loops at the ends of chromosomes. J. Cell Biol. 166 (2004) 161-165
42. Opresko P.L., Otterlei M., Graakjaer J., Bruheim P., Dawut L., Kolvraa S., May A., Seidman M.M., and Bohr V.A. The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D Loops in a manner regulated by TRF1 and TRF2. Mol. Cell 14 (2004) 763-774
43. Opresko P.L., Mason P.A., Podell E.R., Lei M., Hickson I.D., Cech T.R., and Bohr V.A. POT1 stimulates recQ helicases WRN and BLM to unwind telomeric DNA substrates. J. Biol. Chem. 280 (2005) 32069-32080
44. Parrinello S., Samper E., Krtolica A., Goldstein J., Melov S., and Campisi J. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5 (2003) 741-747
45. Rudolph K.L., Chang S., Lee H.W., Blasco M., Gottlieb G.J., Greider C., and DePinho R.A. Longevity, stress response, and cancer in aging telomerase-deficient mice. Cell 96 (1999) 701-712
46. Shakirov E.V., Surovtseva Y.V., Osbun N., and Shippen D.E. The Arabidopsis Pot1 and Pot2 proteins function in telomere length homeostasis and chromosome end protection. Mol. Cell. Biol. 25 (2005) 7725-7733
47. Smogorzewska A., and de Lange T. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73 (2004) 177-208
48. Tahara H., Kusunoki M., Yamanaka Y., Matsumura S., and Ide T. G-tail telomere HPA: simple measurement of human single-stranded telomeric overhangs. Nat. Methods 2 (2005) 829-831
49. Takai H., Smogorzewska A., and de Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13 (2003) 1549-1556
50. Tarsounas M., Munoz P., Claas A., Smiraldo P.G., Pittman D.L., Blasco M.A., and West S.C. Telomere maintenance requires the RAD51D recombination/repair protein. Cell 117 (2004) 337-347
51. Teixeira M.T., Arneric M., Sperisen P., and Lingner J. Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell 117 (2004) 323-335
52. Tsukuda T., Fleming A.B., Nickoloff J.A., and Osley M.A. Chromatin remodelling at a DNA double-strand break site in Saccharomyces cerevisiae. Nature 438 (2005) 379-383
53. van Steensel B., and de Lange T. Control of telomere length by the human telomeric protein TRF1. Nature 385 (1997) 740-743
54. Veldman T., Etheridge K.T., and Counter C.M. Loss of hPot1 function leads to telomere instability and a cut-like phenotype. Curr. Biol. 14 (2004) 2264-2270
55. Verdun R.E., Crabbe L., Haggblom C., and Karlseder J. Functional human telomeres are recognized as DNA damage in G2 of the cell cycle. Mol. Cell 20 (2005) 551-561
56. Wang R.C., Smogorzewska A., and de Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119 (2004) 355-368
57. Wei C., and Price C.M. Cell cycle localization, dimerization, and binding domain architecture of the telomere protein cPot1. Mol. Cell. Biol. 24 (2004) 2091-2102
58. Yang Q., Zheng Y.L., and Harris C.C. POT1 and TRF2 cooperate to maintain telomeric integrity. Mol. Cell. Biol. 25 (2005) 1070-1080
59. Ye J.Z., Hockemeyer D., Krutchinsky A.N., Loayza D., Hooper S.M., Chait B.T., and de Lange T. POT1-interacting protein PIP1: a telomere length regulator that recruits POT1 to the TIN2/TRF1 complex. Genes Dev. 18 (2004) 1649-1654
60. Ye J.Z., Donigian J.R., van Overbeek M., Loayza D., Luo Y., Krutchinsky A.N., Chait B.T., and de Lange T. TIN2 binds TRF1 and TRF2 simultaneously and stabilizes the TRF2 complex on telomeres. J. Biol. Chem. 279 (2004) 47264-47271
61. Zaug A.J., Podell E.R., and Cech T.R. Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc. Natl. Acad. Sci. USA 102 (2005) 10864-10869
62. Zhu X.D., Kuster B., Mann M., Petrini J.H., and de Lange T. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25 (2000) 347-352
63. 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