Mutant telomeric repeats in yeast can disrupt the negative regulation of recombination-mediated telomere maintenance and create an alternative lengthening of telomeres-like phenotype

Molecular and Cellular Biology

Volumn 29, Issue 3, 2009, Pages 626-639

  Bechard, Laura H ^a   Butuner, Bilge D ^b   Peterson, George J ^a,c   McRae, Will ^a   Topcu, Zeki ^b   McEachern, Michael J ^a  

^a University of Georgia ^*  (United States)

^b EGE UNIVERSITY   (Turkey)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN ACC; PROTEIN SNAB; RAP1 PROTEIN; TELOMERASE; TELOMERE BINDING PROTEIN; UNCLASSIFIED DRUG; FUNGAL DNA;

ARTICLE; BINDING SITE; CONTROLLED STUDY; DNA STRAND; FUNGAL STRAIN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; TELOMERE; YEAST; GENE DELETION; GENETIC RECOMBINATION; GENETICS; HUMAN; KLUYVEROMYCES; METABOLISM; MICROBIAL VIABILITY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE;

KLUYVEROMYCES LACTIS;

BASE SEQUENCE; DNA, FUNGAL; GENE DELETION; HUMANS; KLUYVEROMYCES; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MUTATION; PHENOTYPE; RECOMBINATION, GENETIC; REPETITIVE SEQUENCES, NUCLEIC ACID; TELOMERASE; TELOMERE;

EID: 59249106535     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00423-08     Document Type: Article

References (91)

1. Autexier, C., and N. F. Lue. 2006. The structure and function of telomerase reverse transcriptase. Annu. Rev. Biochem. 75:493-517.
2. Baumann, P., and T. R. Cech. 2001. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292:1171-1175.
3. Beernink, H. T., K. Miller, A. Deshpande, P. Bucher, and J. P. Cooper. 2003. Telomere maintenance in fission yeast requires an Est1 ortholog. Curr. Biol. 13:575-580.
4. Bertuch, A. A., and V. Lundblad. 2006. The maintenance and masking of chromosome termini. Curr. Opin. Cell Biol. 18:247-253.
5. Boulton, S. J., and S. P. Jackson. 1998. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1819-1828.
6. Bryan, T. M., A. Englezou, J. Gupta, S. Bacchetti, and R. R. Reddel. 1995. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 14:4240-1248.
7. Carter, S. D., S. Iyer, J. Xu, M. J. McEachern, and S. U. Astrom. 2007. The role of nonhomologous end-joining components in telomere metabolism in Kluyveromyces lactis. Genetics 175:1035-1045.
8. Cervantes, R. B., and V. Lundblad. 2002. Mechanisms of chromosome-end protection. Curr. Opin. Cell Biol. 14:351-356.
9. Cesare, A. J., and J. D. Griffith. 2004. Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol. Cell. Biol. 24:9948-9957.
10. Chakhparonian, M., and R. J. Wellinger. 2003. Telomere maintenance and DNA replication: how closely are these two connected? Trends Genet. 19:439-446.
11. Chan, S. R., and E. H. Blackburn. 2004. Telomeres and telomerase. Philos. Trans. R. Soc. London B 359:109-121.
12. Chandra, A., T. R. Hughes, C. I. Nugent, and V. Lundblad. 2001. Cdc13both positively and negatively regulates telomere replication. Genes Dev. 15:404-414.
13. Chen, Q., A. Ijpma, and C. W. Greider. 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.
14. Church, G.M., and W. Gilbert.1984. Genomic sequencing. Proc. Natl. Acad. Sci. USA 81:1991-1995.
15. de Lange, T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19:2100-2110.
16. Dionne, I., and R. J. Wellinger. 1996. Cell cycle-regulated generation of single-stranded G-rich DNAin the absence oftelomerase. Proc. Natl. Acad. Sci. USA 93:13902-13907.
17. Dunham, M. A., A. A. Neumann, C. L. Fasching, and R. R. Reddel. 2000. Telomere maintenance by recombination in human cells. Nat. Genet. 26: 447-450.
18. Eldridge, A. M., W. A. Halsey, and D. S. Wuttke. 2006. Identification of the determinants for the specific recognition of single-strand telomeric DNA by Cdc13. Biochemistry 45:871-879.
19. Evans, S. K., and V. Lundblad. 1999. Est1 and Cdc13 as comediators of telomerase access. Science 286:117-120.
20. Evans, S. K., and V. Lundblad. 2002. The Est1 subunit of Saccharomyces cerevisiae telomerase makes multiple contributions to telomere length maintenance. Genetics 162:1101-1115.
21. Ferreira, M. G., K. M. Miller, and J. P. Cooper. 2004. Indecent exposure: when telomeres become uncapped. Mol. Cell 13:7-18.
22. Gilson, E., M. Roberge, R. Giraldo, D. Rhodes, and S. M. Gasser. 1993. Distortion of the DNA double helix by RAP1 at silencers and multiple telomeric binding sites. J. Mol. Biol. 231:293-310.
23. Grandin, N., and M. Charbonneau. 2003. The Rad51 pathway of telomerase independent maintenance of telomeres can amplify TG1-3 sequences in yku and cdc13 mutants of Saccharomyces cerevisiae. Mol. Cell. Biol. 23:3721-3734.
24. Grandin, N., C. Damon, and M. Charbonneau. 2000. Cdc13 cooperates with the yeast Ku proteins and Stn1 to regulate telomerase recruitment. Mol. Cell. Biol. 20:8397-8408.
25. Grandin, N., C. Damon, and M. Charbonneau. 2001. Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. EMBO J. 20:6127-6139.
26. Grandin, N., C. Damon, and M. Charbonneau. 2001. Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. EMBO J. 20:1173-1183.
27. Grandin, N., S. I. Reed, and M. Charbonneau. 1997. Stn1, a new Saccharomyces cerevisiae protein, is implicated in telomere size regulation in association with Cdc13. Genes Dev. 11:512-527.
28. Griffith, J. D., L. Comeau, S. Rosenfield, R. M. Stansel, A. Bianchi, H. Moss, and T. de Lange. 1999. Mammalian telomeres end in a large duplex loop. Cell 97:503-514.
29. Groff-Vindman, C., A. J. Cesare, S. Natarajan, J. D. Griffith, and M. J. McEachern. 2005. Recombination at long mutant telomeres produces tiny single-and double-stranded telomeric circles. Mol. Cell. Biol. 25:4406-4412.
30. Grossi, S., A. Bianchi, P. Damay, and D. Shore. 2001. Telomere formation by Rap1p binding site arrays reveals end-specific length regulation requirements and active telomeric recombination. Mol. Cell. Biol. 21:8117-8128.
31. Hardy, C. F., L. Sussel, and D. Shore. 1992. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev. 6:801-814.
32. Hug, N., and J. Lingner. 2006. Telomere length homeostasis. Chromosoma 115:413-425.
33. Iyer, S., A. D. Chadha, and M. J. McEachern. 2005. A mutation in the STN1 gene triggers an alternative lengthening of telomere-like runaway recombinational telomere elongation and rapid deletion in yeast. Mol. Cell. Biol. 25:8064-8073.
34. Kim, N. W., M. A. Piatyszek, K. R. Prowse, C. B. Harley, M. D. West, P. L. Ho, G. M. Coviello, W. E. Wright, S. L. Weinrich, and J. W. Shay. 1994. Specific association of human telomerase activity with immortal cells and cancer. Science 266:2011-2015.
35. Kironmai, K. M., and K. Muniyappa. 1997. Alteration of telomeric sequences and senescence caused by mutations in RAD50 of Saccharomyces cerevisiae. Genes Cells 2:443-455.
36. Kooistra, R., P. J. Hooykaas, and H. Y. Steensma. 2004. Efficient gene targeting in Kluuyveromyces lactis. Yeast 21:781-792.
37. Krauskopf, A., and E. H. Blackburn. 1996. Control of telomere growth by interactions of RAP1 with the most distal telomeric repeats. Nature 383: 354-357.
38. Lansdorp, P. M., S. Poon, E. Chavez, V. Dragowska, M. Zijlmans, T. Bryan, R. Reddel, M. Egholm, S. Bacchetti, and U. Martens. 1997. Telomeres inthe haemopoietic system. Ciba Found. Symp. 211:209-218. (Discussion, 211: 219-222.)
39. Le, S., J. K. Moore, J. E. Haber, and C. W. Greider. 1999. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152:143-152.
40. Legassie, J. D., and M. B. Jarstfer. 2006. The unmasking of telomerase. Structure 14:1603-1609.
41. Lin, C. Y., H. H. Chang, K. J. Wu, S. F. Tseng, C. C. Lin, C. P. Lin, and S. C. Teng. 2005. Extrachromosomal telomeric circles contribute to Rad52-, Rad50-, and polymerase delta-mediated telomere-telomere recombination in Saccharomyces cerevisiae. Eukaryot. Cell 4:327-336.
42. Lundblad, V., and E. H. Blackburn. 1993. An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell 73:347-360.
43. Lustig, A. J., and T. D. Petes. 1986. Identification of yeast mutants with altered telomere structure. Proc. Natl. Acad. Sci. USA 83:1398-1402.
44. Marcand, S., E. Gilson, and D. Shore. 1997. Aprotein-counting mechanism for telomere length regulation in yeast. Science 275:986-990.
45. Maringele, L., and D. Lydall. 2002. EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70Δ mutants. Genes Dev. 16:1919-1933.
46. Maringele, L., and D. Lydall. 2004. EXO1 plays a role in generating type I and type II survivors in budding yeast. Genetics 166:1641-1649.
47. McEachern, M. J., and E. H. Blackburn. 1996. Cap-prevented recombination between terminal telomeric repeat arrays (telomere CPR) maintains telomeres in Kluyveromyces lactis lacking telomerase. Genes Dev. 10:1822-1834.
48. McEachern, M. J., and E. H. Blackburn. 1995. Runaway telomere elongation caused by telomerase RNA gene mutations. Nature 376:403-409.
49. McEachern, M. J., and J. E. Haber. 2006. Breakinduced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75:111-135.
50. McEachern, M. J., and S. Iyer. 2001. Short telomeres in yeast are highly recombinogenic. Mol. Cell 7:695-704.
51. McEachern, M. J., S. Iyer, T. B. Fulton, and E. H. Blackburn. 2000. Telo mere fusions caused by mutating the terminal region of telomeric DNA. Proc. Natl. Acad. Sci. USA 97:11409-11414.
52. McEachern, M. J., A. Krauskopf, and E. H. Blackburn. 2000. Telomeres and their control. Annu. Rev. Genet. 34:331-358.
53. McEachern, M. J., D. H. Underwood, and E. H. Blackburn. 2002. Dynamics of telomeric DNA turnover in yeast. Genetics 160:63-73.
54. Muller, T., E. Gilson, R. Schmidt, R. Giraldo, J. Sogo, H. Gross, and S. M. Gasser. 1994. Imaging the asymmetrical DNA bend induced by repressor activator protein 1 with scanning tunneling microscopy. J. Struct. Biol. 113: 1-12.
55. Muntoni, A., and R. R. Reddel. 2005. The first molecular details of ALT in human tumor cells. Hum. Mol. Genet. 14(Spec. No. 2):R191-R196.
56. Murnane, J. P., L. Sabatier, B. A. Marder, and W. F. Morgan. 1994. Telomere dynamics in an immortal human cell line. EMBO J. 13:4953-4962.
57. Nakamura, T. M., J. P. Cooper, and T. R. Cech. 1998. Two modes of survival of fission yeast without telomerase. Science 282:493-496.
58. Natarajan, S., C. Groff-Vindman, and M. J. McEachern. 2003. Factors influencing the recombinational expansion and spread of telomeric tandem arrays in Kluyveromyces lactis. Eukaryot. Cell 2:1115-1127.
59. Natarajan, S., and M. J. McEachern. 2002. Recombinational telomere elongation promoted by DNA circles. Mol. Cell. Biol. 22:4512-4521.
60. Negrini, S., V. Ribaud, A. Bianchi, and D. Shore. 2007. DNA breaks are masked by multiple Rap1 binding in yeast: implications for telomere capping and telomerase regulation. Genes Dev. 21:292-302.
61. Nugent, C. I., G. Bosco, L. O. Ross, S. K. Evans, A. P. Salinger, J. K. Moore, J. E. Haber, and V. Lundblad. 1998. Telomere maintenance is dependent on activities required for end repair of doublestrand breaks. Curr. Biol. 8:657-660.
62. Ogino, H., K. Nakabayashi, M. Suzuki, E. Takahashi, M. Fujii, T. Suzuki, and D. Ayusawa. 1998. Release of telomeric DNA from chromosomes in immortal human cells lacking telomerase activity. Biochem. Biophys. Res. Commun. 248:223-227.
63. Pardo, B., and S. Marcand. 2005. Rap1 prevents telomere fusions by nonhomologous end joining. EMBO J. 24:3117-3127.
64. Pennock, E., K. Buckley, and V. Lundblad. 2001. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104:387-396.
65. Perrem, K., L. M. Colgin, A. A. Neumann, T. R. Yeager, and R. R. Reddel. 2001. Coexistence of alternative lengthening of telomeres and telomerase in hTERT-transfected GM847 cells. Mol. Cell. Biol. 21:3862-3875.
66. Petreaca, R. C., H. C. Chiu, and C. I. Nugent. 2007. The role of Stn1p in Saccharomyces cerevisiae telomere capping can be separated from its interaction with Cdc13p. Genetics 177:1459-1474.
67. Ritchie, K. B., and T. D. Petes. 2000. The Mre11p/Rad50p/Xrs2p complex and the Tel1p function in a single pathway for telomere maintenance in yeast. Genetics 155:475-479.
68. Roy, J., T. B. Fulton, and E. H. Blackburn. 1998. Specific telomerase RNA residues distant from the template are essential for telomerase function. Genes Dev. 12:3286-3300.
69. Shay, J. W., and W. E. Wright. 2005. Senescence and immortalization: role of telomeres and telomerase. Carcinogenesis 26:867-874.
70. Shay, J. W., and W. E. Wright. 2001. Telomeres and telomerase: implications for cancer and aging. Radiat. Res. 155:188-193.
71. Smogorzewska, A., and T. de Lange. 2004. Regulation of telomerase by telomeric proteins. Annu. Rev. Biochem. 73:177-208.
72. Taggart, A. K., S. C. Teng, and V. A. Zakian. 2002. Est1p as a cell cycleregulated activator of telomere-bound telomerase. Science 297:1023-1026.
73. Teixeira, M. T., M. Arneric, P. Sperisen, and J. Lingner. 2004. Telomere length homeostasis is achieved via a switch between telomerase-extendible and -nonextendible states. Cell 117:323-335.
74. Teng, S. C., J. Chang, B. McCowan, and V. A. Zakian. 2000. Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p- dependent, Rif-inhibited recombinational process. Mol. Cell 6:947-952.
75. Teng, S. C., and V. A. Zakian. 1999. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:8083-8093.
76. Tomita, K., A. Matsuura, T. Caspari, A. M. Carr, Y. Akamatsu, H. Iwasaki, K. Mizuno, K. Ohta, M. Uritani, T. Ushimaru, K. Yoshinaga, and M. Ueno. 2003. Competition between the Rad50 complex and the Ku heterodimer reveals a role for Exo1 in processing double-strand breaks but not telomeres. Mol. Cell. Biol. 23:5186-5197.
77. Topcu, Z., K. Nickles, C. Davis, and M. J. McEachern. 2005. Abrupt disruption of capping and a single source for recombinationally elongated telomeres in Kluyveromyces lactis. Proc. Natl. Acad. Sci. USA 102:3348-3353.
78. Tsai, Y. L., S. F. Tseng, S. H. Chang, C. C. Lin, and S. C. Teng. 2002. Involvement of replicative polymerases, Tel1p, Mec1p, Cdc13p, and the Ku complex in telomere-telomere recombination. Mol. Cell. Biol. 22:5679-5687.
79. Tsukamoto, Y., A. K. Taggart, and V. A. Zakian. 2001. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr. Biol. 11:1328-1335.
80. Underwood, D. H., C. Carroll, and M. J. McEachern. 2004. Genetic dissection of the Kluyveromyces lactis telomere and evidence for telomere capping defects in TER1 mutants with long telomeres. Eukaryot. Cell 3:369-384.
81. Underwood, D. H., and M. J. McEachern. 2001. Totally mutant telomeres: single-step mutagenesis of tandem repeat DNA sequences. BioTechniques 30:934-935, 938.
82. Underwood, D. H., R. P. Zinzen, and M. J. McEachern. 2004. Template requirements for telomerase translocation in Kluyveromyces lactis. Mol. Cell. Biol. 24:912-923.
83. Verdun, R. E., and J. Karlseder. 2007. Replication and protection of telomeres. Nature 447:924-931.
84. Vignais, M. L., and A. Sentenac. 1989. Asymmetric DNA bending induced by the yeast multifunctional factor TUF. J. Biol. Chem. 264:8463-8466.
85. Wang, R. C., A. Smogorzewska, and T. de Lange. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119:355-368.
86. White, C. I., and J. E. Haber. 1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9:663-673.
87. Wotton, D., and D. Shore. 1997. A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev. 11:748-760.
88. Wray, L. V., Jr., M. M. Witte, R. C. Dickson, and M. I. Riley. 1987. Characterization of a positive regulatory gene, LAC9, that controls induction of the lactose-galactose regulon of Kluyveromyces lactis: structural and functional relationships to GAL4 of Saccharomyces cerevisiae. Mol. Cell. Biol. 7:1111-1121.
89. Wu, G., W. H. Lee, and P. L. Chen. 2000. NBS1 and TRF1 colocalize at promyelocytic leukemia bodies during late S/G2 phases in immortalized telomerase-negative cells. Implication of NBS1 in alternative lengthening of telomeres. J. Biol. Chem. 275:30618-30622.
90. Yeager, T. R., A. A. Neumann, A. Englezou, L. I. Huschtscha, J. R. Noble, and R. R. Reddel. 1999. Telomerase-negative immortalized human cells contain a novel type of promyelocytic leukemia (PML) body. Cancer Res. 59:4175-4179.
91. Zhu, X. D., B. Kuster, M. Mann, J. H. Petrini, and T. de Lange. 2000. Cell-cycle-regulated association of RAD50/MRE11/NBS1 with TRF2 and human telomeres. Nat. Genet. 25:347-352.