Telomeres and the DNA damage response: Why the fox is guarding the henhouse

DNA Repair

Volumn 3, Issue 8-9, 2004, Pages 979-988

  Maser, Richard S ^a   DePinho, Ronald A ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

Checkpoints; DNA damage; DNA repair; Telomeres

Indexed keywords

DOUBLE STRANDED DNA; NUCLEOPROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; TELOMERE BINDING PROTEIN;

CATALYSIS; CATALYST; CELL DAMAGE; CELL PROLIFERATION; CHROMOSOME; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; ENZYME SUBSTRATE; GENETIC RECOMBINATION; GENOME; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; TELOMERE;

DNA DAMAGE; DNA REPAIR; ENDODEOXYRIBONUCLEASES; EXODEOXYRIBONUCLEASES; FUNGAL PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTATION; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE;

CANIDAE;

EID: 3242886697     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2004.05.009     Document Type: Review

References (100)

1. H.J. Muller, The remaking of chromosomes, Collecting Net 8 (1938) 182-195, 198.
2. J.G. Gall, Beginning of the end: origins of the telomere concept, in: E.H. Blackburn, C.W. Greider (Eds.), Telomeres, Cold Spring Harbor Laboratory Press, Plainville, NY, 1995, pp. 1-10.
3. McClintock B. The stability of broken ends of chromosomes in Zea mays. Genetics. 26:1941;234-282
4. 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
5. Henderson E.R., Blackburn E.H. An overhanging 3′ terminus is a conserved feature of telomeres. Mol. Cell. Biol. 9:1989;345-348
6. McElligott R., Wellinger R.J. The terminal DNA structure of mammalian chromosomes. EMBO J. 16:1997;3705-3714
7. Wright W.E., Tesmer V.M., Huffman K.E., Levene S.D., Shay J.W. Normal human chromosomes have long G-rich telomeric overhangs at one end. Genes Dev. 11:1997;2801-2809
8. 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
9. Lingner J., Cech T.R. Purification of telomerase from Euplotes aediculatus: requirement of a primer 3′ overhang. Proc. Natl. Acad. Sci. U.S.A. 93:1996;10712-10717
10. Wang H., Blackburn E.H. De novo telomere addition by Tetrahymenatelomerase in vitro. EMBO J. 16:1997;866-879
11. Vega L.R., Mateyak M.K., Zakian V.A. Getting to the end: telomerase access in yeast and humans. Nat. Rev. Mol. Cell. Biol. 4:2003;948-959
12. Ben-Porath I., Weinberg R.A. When cells get stressed: an integrative view of cellular senescence. J. Clin. Invest. 113:2004;8-13
13. Maser R.S., DePinho R.A. Connecting chromosomes, crisis, and cancer. Science. 297:2002;565-569
14. Lundblad V., Szostak J.W. A mutant with a defect in telomere elongation leads to senescence in yeast. Cell. 57:1989;633-643
15. Chin L., Artandi S.E., Shen Q., Tam A., Lee S.L., Gottlieb G.J., Greider C.W., DePinho R.A. p53 deficiency rescues the adverse effects of telomere loss and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell. 97:1999;527-538
16. Singer M.S., Gottschling D.E. TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science. 266:1994;404-409
17. Lendvay T.S., Morris D.K., Sah J., Balasubramanian B., Lundblad V. Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics. 144:1996;1399-1412
18. Bodnar A.G., Ouellette M., Frolkis M., Holt S.E., Chiu C.P., Morin G.B., Harley C.B., Shay J.W., Lichtsteiner S., Wright W.E. Extension of life-span by introduction of telomerase into normal human cells. Science. 279:1998;349-352
19. Vaziri H., Benchimol S. Reconstitution of telomerase activity in normal human cells leads to elongation of telomeres and extended replicative life span. Curr. Biol. 8:1998;279-282
20. Counter C.M., Hahn W.C., Wei W., Caddle S.D., Beijersbergen R.L., Lansdorp P.M., Sedivy J.M., Weinberg R.A. Dissociation among in vitro telomerase activity, telomere maintenance, and cellular immortalization. Proc. Natl. Acad. Sci. U.S.A. 95:1998;14723-14728
21. Sandell L.L., Zakian V.A. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell. 75:1993;729-739
22. Garvik B., Carson M., 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
23. Enomoto S., Glowczewski L., Berman J. MEC3, MEC1, and DDC2 are essential components of a telomere checkpoint pathway required for cell cycle arrest during senescence in Saccharomyces cerevisiae. Mol. Biol. Cell. 13:2002;2626-2638
24. Ijpma A.S., Greider C.W. Short telomeres induce a DNA damage response in Saccharomyces cerevisiae. Mol. Biol. Cell. 14:2003;987-1001
25. Nautiyal S., DeRisi J.L., Blackburn E.H. The genome-wide expression response to telomerase deletion in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 99:2002;9316-9321
26. van Steensel B., Smogorzewska A., de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell. 92:1998;401-413
27. 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
28. Karlseder J., Smogorzewska A., de Lange T. Senescence induced by altered telomere state, not telomere loss. Science. 295:2002;2446-2449
29. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer. 3:2003;155-168
30. Wahl G.M., Carr A.M. The evolution of diverse biological responses to DNA damage: insights from yeast and p53. Nat. Cell Biol. 3:2001;E277-E286
31. Hemann M.T., Rudolph K.L., Strong M.A., DePinho R.A., Chin L., Greider C.W. Telomere dysfunction triggers developmentally regulated germ cell apoptosis. Mol. Biol. Cell. 12:2001;2023-2030
32. Artandi S.E., Chang S., Lee S.L., Alson S., Gottlieb G.J., Chin L., DePinho R.A. Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature. 406:2000;641-645
33. Wong K.K., Maser R.S., Bachoo R.M., Menon J., Carrasco D.R., Gu Y., Alt F.W., DePinho R.A. Telomere dysfunction and Atm deficiency compromises organ homeostasis and accelerates ageing. Nature. 421:2003;643-648
34. d'Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature. 426:2003;194-198
35. Sedelnikova O.A., Horikawa I., Zimonjic D.B., Popescu N.C., Bonner W.M., Barrett J.C. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol. 6:2004;168-170
36. Takai H., Smogorzewska A., de Lange T. DNA damage foci at dysfunctional telomeres. Curr. Biol. 13:2003;1549-1556
37. Webley K., Bond J.A., Jones C.J., Blaydes J.P., Craig A., Hupp T., Wuynford-Thomas D. Posttranslational modifications of p53 in replicative senenscence overlapping but distinct from those induced by DNA damage. Mol. Cell. Biol. 20:2000;2803-2808
38. Lee S.E., Moore J.K., Holmes A., Umezu K., Kolodner R.D., Haber J.E. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell. 94:1998;399-409
39. Valerie K., Povirk L.F. Regulation and mechanisms of mammalian double-strand break repair. Oncogene. 22:2003;5792-5812
40. Martin S.G., Laroche T., Suka N., Grunstein M., Gasser S.M. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell. 97:1999;621-633
41. Mills K.D., Sinclair D.A., Guarente L. MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell. 97:1999;609-620
42. Porter S.E., Greenwell P.W., Ritchie K.B., Petes T.D. The DNA-binding protein Hdf1p (a putative Ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res. 24:1996;582-585
43. Boulton S.J., Jackson S.P. Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 24:1996;4639-4648
44. Boulton S.J., Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1998;1819-1828
45. Gravel S., Larrivee M., Labrecque P., Wellinger R.J. Yeast Ku as a regulator of chromosomal DNA end structure. Science. 280:1998;741-744
46. Polotnianka R.M., Li J., Lustig A.J. The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8:1998;831-834
47. Nugent C.I., Bosco G., Ross L.O., Evans S.K., Salinger A.P., Moore J.K., Haber J.E., Lundblad V. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8:1998;657-660
48. Maringele L., Lydall D. EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Delta mutants. Genes Dev. 16:2002;1919-1933
49. Mishra K., Shore D. Yeast Ku protein plays a direct role in telomeric silencing and counteracts inhibition by rif proteins. Curr. Biol. 9:1999;1123-1126
50. Laroche T., Martin S.G., Gotta M., Gorham H.C., Pryde F.E., Louis E.J., Gasser S.M. Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Curr. Biol. 8:1998;653-656
51. Stellwagen A.E., Haimberger Z.W., Veatch J.R., Gottschling D.E. Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev. 17:2003;2384-2395
52. Peterson S.E., Stellwagen A.E., Diede S.J., Singer M.S., Haimberger Z.W., Johnson C.O., Tzoneva M., Gottschling D.E. The function of a stem-loop in telomerase RNA is linked to the DNA repair protein Ku. Nat. Genet. 27:2001;64-67
53. Teo S.H., Jackson S.P. Telomerase subunit overexpression suppresses telomere-specific checkpoint activation in the yeast yku80 mutant. EMBO Rep. 2:2001;197-202
54. Hande P., Slijepcevic P., Silver A., Bouffler S., van Buul P., Bryant P., Lansdorp P. Elongated telomeres in scid mice. Genomics. 56:1999;221-223
55. Goytisolo F.A., Samper E., Edmonson S., Taccioli G.E., Blasco M.A. The absence of the dna-dependent protein kinase catalytic subunit in mice results in anaphase bridges and in increased telomeric fusions with normal telomere length and G-strand overhang. Mol. Cell. Biol. 21:2001;3642-3651
56. Gilley D., Tanaka H., Hande M.P., Kurimasa A., Li G.C., Oshimura M., Chen D.J. DNA-PKcs is critical for telomere capping. Proc. Natl. Acad. Sci. U.S.A. 98:2001;15084-15088
57. d'Adda di Fagagna F., Hande M.P., Tong W.M., Roth D., Lansdorp P.M., Wang Z.Q., Jackson S.P. Effects of DNA nonhomologous end-joining factors on telomere length and chromosomal stability in mammalian cells. Curr. Biol. 11:2001;1192-1196
58. Samper E., Goytisolo F.A., Slijepcevic P., van Buul P.P., Blasco M.A. Mammalian Ku86 protein prevents telomeric fusions independently of the length of TTAGGG repeats and the G-strand overhang. EMBO Rep. 1:2000;244-252
59. Bianchi A., de Lange T. Ku binds telomeric DNA in vitro. J. Biol. Chem. 274:1999;21223-21227
60. Hsu H.L., Gilley D., Blackburn E.H., Chen D.J. Ku is associated with the telomere in mammals. Proc. Natl. Acad. Sci. U.S.A. 96:1999;12454-12458
61. Hsu H.L., Gilley D., Galande S.A., Hande M.P., Allen B., Kim S.H., Li G.C., Campisi J., Kohwi-Shigematsu T., Chen D.J. Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev. 14:2000;2807-2812
62. Song K., Jung D., Jung Y., Lee S.G., Lee I. Interaction of human Ku70 with TRF2. FEBS Lett. 481:2000;81-85
63. Bailey S.M., Meyne J., Chen D.J., Kurimasa A., Li G.C., Lehnert B.E., Goodwin E.H. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc. Natl. Acad. Sci. U.S.A. 96:1999;14899-14904
64. Rooney S., Alt F.W., Lombard D., Whitlow S., Eckersdorff M., Fleming J., Fugmann S., Ferguson D.O., Schatz D.G., Sekiguchi J. Defective DNA repair and increased genomic instability in Artemis-deficient murine cells. J. Exp. Med. 197:2003;553-565
65. Jeggo P., O'Neill P. The Greek Goddess, Artemis, reveals the secrets of her cleavage. DNA Repair (Amst.). 1:2002;771-777
66. Karlseder J., Kachatrian L., Takai H., Mercer K., Hingorani S., Jacks T., de Lange T. Targeted deletion reveals an essential function for the telomere length regulator Trf1. Mol. Cell. Biol. 23:2003;6533-6541
67. Iwano T., Tachibana M., Reth M., Shinkai Y. Importance of TRF1 for functional telomere structure. J. Biol. Chem. 14:2003;14
68. 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
69. Masutomi K., Yu E.Y., Khurts S., Ben-Porath I., Currier J.L., Metz G.B., Brooks M.W., Kaneko S., Murakami S., DeCaprio J.A., Weinberg R.A., Stewart S.A., Hahn W.C. Telomerase maintains telomere structure in normal human cells. Cell. 114:2003;241-253
70. D'Amours D., Jackson S.P. The Mre11 complex: at the crossroads of DNA repair and checkpoint signalling. Nat. Rev. Mol. Cell. Biol. 3:2002;317-327
71. Kironmai K.M., Muniyappa K. Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells. 2:1997;443-455
72. Gallego M.E., White C.I. RAD50 function is essential for telomere maintenance in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 98:2001;1711-1716
73. Wilson S., Warr N., Taylor D.L., Watts F.Z. The role of Schizosaccharomyces pombe Rad32, the Mre11 homologue, and other DNA damage response proteins in non-homologous end joining and telomere length maintenance. Nucleic Acids Res. 27:1999;2655-2661
74. Ueno M., Nakazaki T., Akamatsu Y., Watanabe K., Tomita K., Lindsay H.D., Shinagawa H., Iwasaki H. Molecular characterization of the Schizosaccharomyces pombe nbs1+ gene involved in DNA repair and telomere maintenance. Mol. Cell. Biol. 23:2003;6553-6563
75. Ritchie K.B., Petes T.D. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics. 155:2000;475-479
76. Chan S.W., Blackburn E.H. Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining. Mol. Cell. 11:2003;1379-1387
77. Usui T., Ogawa H., Petrini J.H. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol. Cell. 7:2001;1255-1266
78. Moreau S., Ferguson J.R., Symington L.S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19:1999;556-566
79. Lee S.E., Bressan D.A., Petrini J.H., Haber J.E. Complementation between N-terminal Saccharomyces cerevisiae mre11 alleles in DNA repair and telomere length maintenance. DNA Repair (Amst.). 1:2002;27-40
80. 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
81. Paull T.T., Gellert M. The 3′ to 5′ exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell. 1:1998;969-979
82. Bender C.F., Sikes M.L., Sullivan R., Huye L.E., Le Beau M.M., Roth D.B., Mirzoeva O.K., Oltz E.M., Petrini J.H. Cancer predisposition and hematopoietic failure in Rad50(S/S) mice. Genes Dev. 16:2002;2237-2251
83. Wood L.D., Halvorsen T.L., Dhar S., Baur J.A., Pandita R.K., Wright W.E., Hande M.P., Calaf G., Hei T.K., Levine F., Shay J.W., Wang J.J., Pandita T.K. Characterization of ataxia telangiectasia fibroblasts with extended life-span through telomerase expression. Oncogene. 20:2001;278-288
84. Metcalfe J.A., Parkhill J., Campbell L., Stacey M., Biggs P., Byrd P.J., Taylor A.M. Accelerated telomere shortening in ataxia telangiectasia. Nat. Genet. 13:1996;350-353
85. S.J. Xia, M.A. Shammas, R.J. Shmookler Reis, Reduced telomere length in ataxia-telangiectasia fibroblasts, Mutat. Res. 364 (1996) 1-11.
86. Hande M.P., Balajee A.S., Tchirkov A., Wynshaw-Boris A., Lansdorp P.M. Extra-chromosomal telomeric DNA in cells from Atm(-/-) mice and patients with ataxia-telangiectasia. Hum. Mol. Genet. 10:2001;519-528
87. Pandita T.K., Dhar S. Influence of ATM function on interactions between telomeres and nuclear matrix. Radiat. Res. 154:2000;133-139
88. 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
89. Ferreira M.G., Miller K.M., Cooper J.P. Indecent exposure: when telomeres become uncapped. Mol. Cell. 13:2004;7-18
90. Hemann M.T., Strong M.A., Hao L.Y., Greider C.W. The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell. 107:2001;67-77
91. Chen C., Kolodner R.D. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23:1999;81-85
92. Espejel S., Franco S., Rodriguez-Perales S., Bouffler S.D., Cigudosa J.C., Blasco M.A. Mammalian Ku86 mediates chromosomal fusions and apoptosis caused by critically short telomeres. EMBO J. 21:2002;2207-2219
93. Espejel S., Franco S., Sgura A., Gae D., Bailey S.M., Taccioli G.E., Blasco M.A. Functional interaction between DNA-PKcs and telomerase in telomere length maintenance. EMBO J. 21:2002;6275-6287
94. Riha K., Shippen D.E. Ku is required for telomeric C-rich strand maintenance but not for end-to-end chromosome fusions in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 100:2003;611-615
95. Lundblad V., Blackburn E.H. An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell. 73:1993;347-360
96. Teng S.C., Zakian V.A. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:1999;8083-8093
97. Bryan T.M., Englezou A., Dalla-Pozza L., Dunham M.A., Reddel R.R. Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat. Med. 3:1997;1271-1274
98. Yeager T.R., Neumann A.A., Englezou A., Huschtscha L.I., Noble J.R., Reddel R.R. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59:1999;4175-4179
99. Dunham M.A., Neumann A.A., Fasching C.L., Reddel R.R. Telomere maintenance by recombination in human cells. Nat. Genet. 26:2000;447-450
100. Tarsounas M., Munoz P., Claas A., Smiraldo P.G., Pittman D.L., Blasco M.A., West S.C. Telomere maintenance requires the RAD51D recombination/repair protein. Cell. 117:2004;337-347