Short telomeres induce a DNA damage response in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 14, Issue 3, 2003, Pages 987-1001

  IJpma, Arne S ^a   Greider, Carol W ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN; PROTEIN MEC1; PROTEIN RAD24; PROTEIN RAD53P; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CULTURE; CELL CYCLE G2 PHASE; CELL GROWTH; CELL KINETICS; CELL VIABILITY; CHROMOSOME LOSS; CONTROLLED STUDY; CULTURE MEDIUM; DNA DAMAGE; ENZYME INACTIVATION; GROWTH RATE; HOMOLOGOUS RECOMBINATION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE; TELOMERE; WESTERN BLOTTING;

CELL CYCLE; CELL CYCLE PROTEINS; CELL DIVISION; DNA DAMAGE; DNA-BINDING PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE;

PROKARYOTA; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0037341611     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.02-04-0057     Document Type: Article

References (98)

1. Allen, J.B., Zhou, Z., Siede, W., Friedberg, E.C., and Elledge, S.J. (1994). The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev. 8, 2401-2415.
2. Blasco, M.A., Lee, H.-W., Hande, P.M., Samper, E., Lansdorp, P.M., DePinho, R.A., and Greider, C.W. (1997). Telomere shortening and tumor formation by mouse cells lacking telomerase RNA. Cell 91, 25-34.
3. Brachmann, C.B., Davies, A., Cost, G.J., Caputo, E., Li, J., Hieter, P., and Boeke, J.D. (1998). Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132.
4. Chan, S.W., Chang, J., Prescott, J., and Blackburn, E.H. (2001). Altering telomere structure allows telomerase to act in yeast lacking ATM kinases. Curr. Biol. 11, 1240-1250.
5. Charles, J.F., Jaspersen, S.L., Tinker-Kulberg, R.L., Hwang, L., Szidon, A., and Morgan, D.O. (1998). The Polo-related kinase Cdc5 activates and is destroyed by the mitotic cyclin destruction machinery in S. cerevisiae. Curr. Biol. 8, 497-507.
6. Chen, Q., IJpma, A., and Greider, C.W. (2001). Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol. Cell. Biol. 21, 1819-1827.
7. Cheng, L., Hunke, L., and Hardy, C.F. (1998). Cell cycle regulation of the Saccharomyces cerevisiae polo-like kinase cdc5p. Mol. Cell. Biol. 18, 7360-7370.
8. Chin, L., Artandi, S., Shen, Q., Tam, S., Lee, S.-L., Gottlieb, G., Greider, C.W., and DePinho, R.A. (1999). p53 deficiency rescues the adverse effects of telomere loss in vivo and cooperates with telomere dysfunction to accelerate carcinogenesis. Cell 97, 527-538.
9. Collart, M.A., and Oliviero, S. (1993). Preparation of yeast RNA. John Wiley & Sons, Inc., New York
10. Connelly, C., and Hieter, P. (1996). Budding yeast SKP1 encodes an evolutionarily conserved kinetochore protein required for cell cycle progression. Cell 86, 275-285.
11. D'Amours, D., and Jackson, S.P. (2001). The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15, 2238-2249.
12. de la Torre-Ruiz, M.A., Green, C.M., and Lowndes, N.F. (1998). RAD9 and RAD24 define two additive, interacting branches of the DNA damage checkpoint pathway in budding yeast normally required for Rad53 modification and activation. EMBO J. 17, 2687-2698.
13. de Lange, T. (2002). Protection of mammalian telomeres. Oncogene 21, 532-540.
14. Diede, S.J., and Gottschling, D.E. (1999). Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99, 723-733.
15. Eckardt-Schupp, F., Siede, W., and Game, J.C. (1987). The RAD24 (= Rs1) gene product of Saccharomyces cerevisiae participates in two different pathways of DNA repair. Genetics 115, 83-90.
16. Elledge, S.J., and Davis, R.W. (1990). Two genes differentially regulated in the cell cycle and by DNA-damaging agents encode alternative regulatory subunits of ribonucleotide reductase. Genes Dev. 4, 740-751.
17. Emili, A. (1998). MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol. Cell 2, 183-189.
18. Enomoto, S., Glowczewski, L., and Berman, J. (2002). 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, 2626-2638.
19. Evans, S.K., and Lundblad, V. (1999). Est1 and Cdc13 as comediators of telomerase access. Science 286, 117-120.
20. Feinberg, A.P., and Vogelstein, B. (1983). A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132, 6-13.
21. Gardner, R., Putnam, C.W., and Weinert, T. (1999). RAD53, DUN1 and PDS1 define two parallel G2/M checkpoint pathways in budding yeast. EMBO J. 18, 3173-3185.
22. Garvik, B., Carson, M., and Hartwell, L. (1995). Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol. Cell. Biol. 15, 6128-6138.
23. Goldstein, A.L., and McCusker, J.H. (1999). Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15, 1541-1553.
24. Goytisolo, F.A., Samper, E., Martin-Caballero, J., Finnon, P., Herrera, E., Flores, J.M., Bouffler, S.D., and Blasco, M.A. (2000). Short telomeres result in organismal hypersensitivity to ionizing radiation in mammals. J. Exp. Med. 192, 1625-1636.
25. Grandin, N., Damon, C., and Charbonneau, M. (2001). Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J. 20, 1173-1183.
26. Grandin, N., Reed, S.I., and Charbonneau, M. (1997). Stn1, a new Saccharomyces cerevisiae protein, is implicated in telomere size regulation in association with Cdc13. Genes Dev. 11, 512-527.
27. Green, C.M., Erdjument-Bromage, H., Tempst, P., and Lowndes, N.F. (2000). A novel Rad24 checkpoint protein complex closely related to replication factor C. Curr. Biol. 10, 39-42.
28. Greider, C.W. (1996). Telomere length regulation. Annu. Rev. Biochem. 65, 337-365.
29. Greider, C.W., and Blackburn, E.H. (1985). Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43, 405-413.
30. Grenon, M., Gilbert, C., and Lowndes, N.F. (2001). Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat. Cell Biol. 3, 844-847.
31. Hackett, J.A., Feldser, D.M., and Greider, C.W. (2001). Telomere dysfunction increases mutation rate and genomic instability. Cell 106, 275-286.
32. Hartwell, L.H. (1974). Saccharomyces cerevisiae cell cycle. Bacteriol. Rev. 38, 164-198.
33. Hathcock, K.S., Hemann, M.T., Opperman, K.K., Strong, M.A., Greider, C.W., and Hodes, R.J. (2002). Haploinsufficiency of mTR results in defects in telomere elongation. Proc. Natl. Acad. Sci. USA 99, 3591-3596.
34. Hegemann, J.H., Shero, J.H., Cottarel, G., Philippsen, P., and Hieter, P. (1988). Mutational analysis of centromere DNA from chromosome VI of Saccharomyces cerevisiae. Mol. Cell. Biol. 8, 2523-2535.
35. Hemann, M.T., Hackett, J., IJpma, A., and Greider, C.W. (2000). Telomere length, telomere binding proteins and DNA damage signaling. Cold Spring Harbor Laboratory Symp. Quant. Biol. LXV, 275-279.
36. Hemann, M.T., Rudolph, K.L., Strong, M.A., DePinho, R.A., Chin, L., and Greider, C.W. (2001a). Telomere dysfunction triggers developmentally regulated germ cell apoptosis. Mol. Biol. Cell 12, 2023-2030.
37. Hemann, M.T., Strong, M.A., Hao, L.Y., and Greider, C.W. (2001b). The shortest telomere, not average telomere length, is critical for cell viability and chromosome stability. Cell 107, 67-77.
38. Hieter, P., Mann, C., Snyder, M., and Davis, R.W. (1985). Mitotic stability of yeast chromosomes: a colony color assay that measures nondisjunction and chromosome loss. Cell 40, 381-392.
39. Hughes, T.R., Weilbaecher, R.G., Walterscheid, M., and Lundblad, V. (2000). Identification of the single-strand telomeric DNA binding domain of the Saccharomyces cerevisiae Cdc13 protein. Proc. Natl. Acad. Sci. USA 97, 6457-6462.
40. Hyland, K.M., Kingsbury, J., Koshland, D., and Hieter, P. (1999). Ctf19p: a novel kinetochore protein in Saccharomyces cerevisiae and a potential link between the kinetochore and mitotic spindle. J. Cell Biol. 145, 15-28.
41. Johnson, F.B., Marciniak, R.A., McVey, M., Stewart, S.A., Hahn, W.C., and Guarente, L. (2001). The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 20, 905-913.
42. Karlseder, J., Broccoli, D., Dai, Y., Hardy, S., and de Lange, T. (1999). p53- and ATM-dependent apoptosis induced by telomeres lacking TRF2. Science 283, 1321-1325.
43. Kirk, K.E., Harmon, B.P., Reichardt, I.K., Sedat, J.W., and Blackburn, E.H. (1997). Block in anaphase chromosome separation caused by a telomerase template mutation. Science 275, 1478-1481.
44. Kohli, J., Hottinger, H., Munz, P., Strauss, A., and Thuriaux, P. (1977). Genetic mapping in Schizosaccharomyces pombe by mitotic and meiotic analysis and induced haploidization. Genetics 87, 471-489.
45. Kondo, T., Matsumoto, K., and Sugimoto, K. (1999). Role of a complex containing Rad17, Mec3, and Ddc1 in the yeast DNA damage checkpoint pathway. Mol. Cell. Biol. 19, 1136-1143.
46. Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K., and Sugimoto, K. (2001). Recruitment of mec1 and ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 294, 867-870.
47. Le, S., Moore, J.K., Haber, J.E., and Greider, C.W. (1999). RAD51 and RAD50 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152, 143-152.
48. Lee, H.-W., Blasco, M.A., Gottlieb, G.J., Horner, J.W., Greider, C.W., and DePinho, R.A. (1998a). Essential role of mouse telomerase in highly proliferative organs. Nature 392, 569-574.
49. Lee, S.E., Moore, J.K., Holmes, A., Umezu, K., Kolodner, R.D., and Haber, J.E. (1998b). Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94, 399-409.
50. Lendvay, T.S., Morris, D.K., Sah, J., Balasubramanian, B., and Lundblad, V. (1996). Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics 144, 1399-1412.
51. Lin, J.J., and Zakian, V.A. (1996). The Saccharomyces CDC13 protein is a single-strand TG1-3 telomeric DNA-binding protein in vitro that affects telomere behavior in vivo. Proc. Natl. Acad. Sci. USA 93, 13760-13765.
52. Lingner, J., Cech, T.R., Hughes, T.R., and Lundblad, V. (1997a). Three ever shorter telomere (EST) genes are dispensable for in vitro yeast telomerase activity. Proc. Natl. Acad. Sci. USA 94, 11190-11195.
53. Lingner, J., Hughes, T.R., Shevchenko, A., Mann, M., Lundblad, V., and Cech, T.R. (1997b). Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276, 561-567.
54. Lundblad, V. (2002). Telomere maintenance without telomerase. Oncogene 21, 522-531.
55. Lundblad, V., and Blackburn, E.H. (1993). An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell 73, 347-360.
56. Lundblad, V., and Szostak, J.W. (1989). A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57, 633-643.
57. Lydall, D., and Weinert, T. (1995). Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270, 1488-1491.
58. Lydall, D., and Weinert, T. (1997). G2/M checkpoint genes of Saccharomyces cerevisiae: further evidence for roles in DNA replication and/or repair. Mol. Gen. Genet. 256, 638-651.
59. Marcand, S., Brevet, V., and Gilson, E. (1999). Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J. 18, 3509-3519.
60. McEachern, M.J., and Iyer, S. (2001). Short telomeres in yeast are highly recombinogenic. Mol. Cell 7, 695-704.
61. Melo, J., and Toczyski, D. (2002). A unified view of the DNA-damage checkpoint. Curr. Opin. Cell Biol. 14, 237-245.
62. Melo, J.A., Cohen, J., and Toczyski, D.P. (2001). Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15, 2809-2821.
63. Mortimer, R.K., Contopoulou, R., and Schild, D. (1981). Mitotic chromosome loss in a radiation-sensitive strain of the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 78, 5778-5782.
64. Naito, T., Matsuura, A., and Ishikawa, F. (1998). Circular chromosome formation in a fission yeast mutant defective in two ATM homologues. Nat. Genet. 20, 203-206.
65. Nakamura, T.M., Cooper, J.P., and Cech, T.R. (1998). Two modes of survival of fission yeast without telomerase. Science 282, 493-496.
66. Nugent, C.I., Hughes, T.R., Lue, N.F., and Lundblad, V. (1996). Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274, 249-252.
67. Pellicioli, A., Lee, S.E., Lucca, C., Foiani, M., and Haber, J.E. (2001). Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell 7, 293-300.
68. Pellicioli, A., Lucca, C., Liberi, G., Marini, F., Lopes, M., Plevani, P., Romano, A., Di Fiore, P.P., and Foiani, M. (1999). Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J. 18, 6561-6572.
69. Pennock, E., Buckley, K., and Lundblad, V. (2001). Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104, 387-396.
70. Qi, H., and Zakian, V.A. (2000). The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase alpha and the telomerase-associated est1 protein. Genes Dev. 14, 1777-1788.
71. Ritchie, K.B., Mallory, J.C., and Petes, T.D. (1999). Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 6065-6075.
72. Ritchie, K.B., and Petes, T.D. (2000). The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics 155, 475-479.
73. Rose, M.D., Winston, F., and Hieter, P. (1990). Methods in yeast genetics. A laboratory course manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
74. Rouse, J., and Jackson, S.P. (2002). Interfaces between the detection, signaling, and repair of DNA damage. Science 297, 547-551.
75. Sanchez, Y., Bachant, J., Wang, H., Hu, F., Liu, D., Tetzlaff, M., and Elledge, S.J. (1999). Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286, 1166-1171.
76. Sanchez, Y., Desany, B.A., Jones, W.J., Liu, Q., Wang, B., and Elledge, S.J. (1996). Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271, 357-360.
77. Sandell, L.L., and Zakian, V.A. (1993). Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75, 729-739.
78. Schiestl, R.H., and Gietz, R.D. (1989). High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16, 339-346.
79. Schupbach, M. (1971). The isolation and genetic classification of UV-sensitive mutants of Schizosaccharomyces pombe. Mutat. Res. 11, 361-371.
80. Schwartz, M.F., Duong, J.K., Sun, Z., Morrow, J.S., Pradhan, D., and Stern, D.F. (2002). Rad9 phosphorylation sites couple Rad53 to the Saccharomyces cerevisiae DNA damage checkpoint. Mol. Cell 9, 1055-1065.
81. Shimomura, T., Ando, S., Matsumoto, K., and Sugimoto, K. (1998). Functional and physical interaction between Rad24 and Rfc5 in the yeast checkpoint pathways. Mol. Cell. Biol. 18, 5485-5491.
82. Singer, M.S., and Gottschling, D.E. (1994). TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science 266, 404-409.
83. Soulier, J., and Lowndes, N.F. (1999). The BRCT domain of the S. cerevisiae checkpoint protein Rad9 mediates a Rad9-Rad9 interaction after DNA damage. Curr. Biol. 9, 551-554.
84. Spencer, F., Gerring, S.L., Connelly, C., and Hieter, P. (1990). Mitotic chromosome transmission fidelity mutants in Saccharomyces cerevisiae. Genetics 124, 237-249.
85. Sun, Z., Fay, D.S., Marini, F., Foiani, M., and Stern, D.F. (1996). Spk1/Rad53 is regulated by Mec1-dependent protein phosphorylation in DNA replication and damage checkpoint pathways. Genes Dev. 10, 395-406.
86. Sun, Z., Hsiao, J., Fay, D.S., and Stern, D.F. (1998). Rad53 FHA domain associated with phosphorylated Rad9 in the DNA damage checkpoint. Science 281, 272-274.
87. Teng, S., Chang, J., McCowan, B., and Zakian, V.A. (2000). Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol. Cell 6, 947-952.
88. Teng, S.C., and Zakian, V.A. (1999). Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 8083-8093.
89. Toczyski, D.P., Galgoczy, D.J., and Hartwell, L.H. (1997). CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90, 1097-1106.
90. Tsai, Y.L., Tseng, S.F., Chang, S.H., Lin, C.C., and Teng, S.C. (2002). Involvement of replicative polymerases, tel1p, mec1p, cdc13p, and the ku complex in telomere-telomere recombination. Mol. Cell. Biol. 22, 5679-5687.
91. Usui, T., Ogawa, H., and Petrini, J.H. (2001). A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 7, 1255-1266.
92. van Steensel, B., Smogorzewska, A., and de Lange, T. (1998). TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413.
93. Venclovas, C., and Thelen, M.P. (2000). Structure-based predictions of Rad1, Rad9, Hus1 and Rad17 participation in sliding clamp and clamp-loading complexes. Nucleic Acids Res. 28, 2481-2493.
94. Weinert, T.A., and Hartwell, L.H. (1988). The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241, 317-322.
95. Winzeler, E.A. et al. (1999). Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906.
96. Wong, K.K. et al. (2000). Telomere dysfunction impairs DNA repair and enhances sensitivity to ionizing radiation. Nat. Genet. 26, 85-88.
97. Zakian, V.A. (1989). Structure and function of telomeres. Annu. Rev. Genet. 23, 579-604.
98. Zhou, B.B., and Elledge, S.J. (2000). The DNA damage response: putting checkpoints in perspective. Nature 408, 433-439.