The saccharomyces cerevisiae telomerase subunit Est3 binds telomeres in a cell cycle- and Est1-dependent manner and interacts directly with Est1 in vitro

PLoS Genetics

Volumn 7, Issue 5, 2011, Pages

  Tuzon, Creighton T ^a   Wu, Yun ^a   Chan, Angela ^a   Zakian, Virginia A ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EST1 PROTEIN; EST3 PROTEIN; FUNGAL PROTEIN; RECOMBINANT PROTEIN; TELOMERASE; UNCLASSIFIED DRUG; EST1 PROTEIN, S CEREVISIAE; EST2 PROTEIN, S CEREVISIAE; EST3 PROTEIN, S CEREVISIAE; GLYCINE; MYC PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; FUNGAL STRAIN; IN VITRO STUDY; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TELOMERE; CELL CYCLE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

CELL CYCLE; GLYCINE; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS C-MYC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE;

EID: 79957991359     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002060     Document Type: Article

References (64)

1. Gerton JL, Hawley RS, (2005) Homologous chromosome interactions in meiosis: diversity amidst conservation. Nat Rev Genet 6: 477-487.
2. Vega L, Mateyak M, Zakian V, (2003) Getting to the end: telomerase access in yeast and humans. Nat Rev Mol Cell Biol 4: 948-959.
3. de Lange T, (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
4. Larrivee M, LeBel C, Wellinger RJ, (2004) The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev 18: 1391-1396.
5. Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, et al. (1997) Reverse transcriptase motifs in the catalytic subunit of telomerase. Science 276: 561-567.
6. Singer MS, Gottschling DE, (1994) TLC1, the template RNA component of the Saccharomyces cerevisiae telomerase. Science 266: 404-409.
7. Lundblad V, Szostak JW, (1989) A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57: 633-643.
8. Lendvay TS, Morris DK, Sah J, Balasubramanian B, Lundblad V, (1996) Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics 144: 1399-1412.
9. Hughes TR, Evans SK, Weilbaecher RG, Lundblad V, (2000) The Est3 protein is a subunit of yeast telomerase. Curr Biol 10: 809-812.
10. Bourns BD, Alexander MK, Smith AM, Zakian VA, (1998) Sir proteins, Rif proteins and Cdc13p bind Saccharomyces telomeres in vivo. Mol Cell Biol 18: 5600-5608.
11. Tsukamoto Y, Taggart AKP, Zakian VA, (2001) The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr Biol 11: 1328-1335.
12. Nugent CI, Hughes TR, Lue NF, Lundblad V, (1996) Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274: 249-252.
13. Garvik B, Carson M, 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.
14. Evans SK, Lundblad V, (1999) Est1 and Cdc13 as comediators of telomerase access. Science 286: 117-120.
15. Bianchi A, Negrini S, Shore D, (2004) Delivery of yeast telomerase to a DNA break depends on the recruitment functions of Cdc13 and Est1. Mol Cell 16: 139-146.
16. McCarroll RM, Fangman WL, (1988) Time of replication of yeast centromeres and telomeres. Cell 54: 505-513.
17. Wellinger RJ, Wolf AJ, Zakian VA, (1993) Origin activation and formation of single-strand TG1-3 tails occur sequentially in late S phase on a yeast linear plasmid. Mol Cell Biol 13: 4057-4065.
18. Wellinger RJ, Wolf AJ, Zakian VA, (1993) Saccharomyces telomeres acquire single-strand TG1-3 tails late in S phase. Cell 72: 51-60.
19. Bonetti D, Martina M, Clerici M, Lucchini G, Longhese MP, (2009) Multiple pathways regulate 3′ overhang generation at S. cerevisiae telomeres. Mol Cell 35: 70-81.
20. Diede SJ, Gottschling DE, (1999) Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99: 723-733.
21. Marcand S, Brevet V, Mann C, Gilson E, (2000) Cell cycle restriction of telomere elongation. Curr Biol 10: 487-490.
22. Taggart AKP, Teng S-C, Zakian VA, (2002) Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297: 1023-1026.
23. Fisher T, Taggart A, Zakian V, (2004) Cell cycle-dependent regulation of yeast telomerase by Ku. Nat Struct Mol Biol 11: 1198-1205.
24. Chan A, Boule JB, Zakian VA, (2008) Two pathways recruit telomerase to Saccharomyces cerevisiae telomeres. PLoS Genet 4: e1000236 doi:10.1371/journal.pgen.1000236.
25. Osterhage JL, Talley JM, Friedman KL, (2006) Proteasome-dependent degradation of Est1p regulates the cell cycle-restricted assembly of telomerase in Saccharomyces cerevisiae. Nat Struct Mol Biol 13: 720-728.
26. Qi H, Zakian VA, (2000) The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase α and the telomerase-associated Est1 protein. Genes Dev 14: 1777-1788.
27. Pennock E, Buckley K, Lundblad V, (2001) Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104: 387-396.
28. Lin J-J, Zakian VA, (1995) An in vitro assay for Saccharomyces telomerase requires EST1. Cell 81: 1127-1135.
29. DeZwaan DC, Freeman BC, (2009) The conserved Est1 protein stimulates telomerase DNA extension activity. Proc Natl Acad Sci 106: 17337-17342.
30. Hsu M, Yu EY, Singh SM, Lue NF, (2007) Mutual dependence of Candida albicans Est1p and Est3p in telomerase assembly and activation. Eukaryot Cell 6: 1330-1338.
31. Lee J, Mandell EK, Rao T, Wuttke DS, Lundblad V, (2010) Investigating the role of the Est3 protein in yeast telomere replication. Nucleic Acids Res 38: 2279-2290.
32. Lee J, Mandell EK, Tucey TM, Morris DK, Lundblad V, (2008) The Est3 protein associates with yeast telomerase through an OB-fold domain. Nat Struct Mol Biol 15: 990-997.
33. Yu EY, Wang F, Lei M, Lue NF, (2008) A proposed OB-fold with a protein-interaction surface in Candida albicans telomerase protein Est3. Nat Struct Mol Biol 15: 985-989.
34. Hockemeyer D, Palm W, Else T, Daniels JP, Takai KK, et al. (2007) Telomere protection by mammalian Pot1 requires interaction with Tpp1. Nat Struct Mol Biol 14: 754-761.
35. Wang F, Podell ER, Zaug AJ, Yang Y, Baciu P, et al. (2007) The POT1-TPP1 telomere complex is a telomerase processivity factor. Nature 445: 506-510.
36. Xin H, Liu D, Wan M, Safari A, Kim H, et al. (2007) TPP1 is a homologue of ciliate TEBP-beta and interacts with POT1 to recruit telomerase. Nature 445: 559-562.
37. Sabourin M, Tuzon C, Fisher T, Zakian V, (2007) A flexible protein linker improves the function of epitope-tagged proteins in Saccharomyces cerevisiae. Yeast 24: 39-45.
38. Maier T, Drapal N, Thanbichler M, Bock A, (1998) Strep-tag II affinity purification: an approach to study intermediates of metalloenzyme biosynthesis. Anal Biochem 259: 68-73.
39. Goudsouzian L, Tuzon C, Zakian VA, (2006) S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol Cell 24: 603-610.
40. Sabourin M, Tuzon C, VA Z, (2007) Telomerase and Tel1p preferentially associate with short telomeres in S. cerevisiae. Mol Cell 27: 550-561.
41. Vodenicharov M, Wellinger RJ, (2006) DNA degradation at unprotected telomeres in yeast is regulated by the CDK1 (Cdc28/Clb) cell-cycle kinase. Mol Cell 24: 127-137.
42. Frank CJ, Hyde M, Greider CW, (2006) Regulation of telomere elongation by the cyclin-dependent kinase CDK1. Mol Cell 24: 423-432.
43. Li S, Makovets S, Matsuguchi T, Blethrow JD, Shokat KM, et al. (2009) Cdk1-dependent phosphorylation of Cdc13 coordinates telomere elongation during cell-cycle progression. Cell 136: 50-61.
44. Tseng SF, Shen ZJ, Tsai HJ, Lin YH, Teng SC, (2009) Rapid Cdc13 turnover and telomere length homeostasis are controlled by Cdk1-mediated phosphorylation of Cdc13. Nucleic Acids Res 37: 3602-3611.
45. Kinoshita E, Takahashi M, Takeda H, Shiro M, Koike T, (2004) Recognition of phosphate monoester dianion by an alkoxide-bridged dinuclear zinc(II) complex. Dalton Trans pp. 1189-1193.
46. Bianchi A, Shore D, (2007) Increased association of telomerase with short telomeres in yeast. Genes Dev 21: 1726-1730.
47. Arneric M, Lingner J, (2007) Tel1 kinase and subtelomere-bound Tbf1 mediate preferential elongation of short telomeres by telomerase in yeast. EMBO Rep 8: 1080-1085.
48. Hector R, Shtofman R, Ray A, Chen B, Nyun T, et al. (2007) Tel1p preferentially associates with short telomeres to stimulate their elongation. Mol Cell 27: 851-858.
49. Lue NF, (2010) Plasticity of telomere maintenance mechanisms in yeast. Trends Biochem Sci 35: 8-17.
50. Kelleher C, Kurth I, Lingner J, (2005) Human protection of telomeres 1 (POT1) is a negative regulator of telomerase activity in vitro. Mol Cell Biol 25: 808-818.
51. Zappulla DC, Roberts JN, Goodrich KJ, Cech TR, Wuttke DS, (2009) Inhibition of yeast telomerase action by the telomeric ssDNA-binding protein, Cdc13p. Nucleic Acids Res 37: 354-367.
52. Friedman KL, Heit JJ, Long DM, Cech TR, (2003) N-terminal domain of yeast telomerase reverse transcriptase: recruitment of Est3p to the telomerase complex. Mol Biol Cell 14: 1-13.
53. Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, et al. (2003) Global analysis of protein expression in yeast. Nature 425: 737-741.
54. Mozdy AD, Cech TR, (2006) Low abundance of telomerase in yeast: implications for telomerase haploinsufficiency. RNA 12: 1721-1737.
55. Yang CP, Chen YB, Meng FL, Zhou JQ, (2006) Saccharomyces cerevisiae Est3p dimerizes in vitro and dimerization contributes to efficient telomere replication in vivo. Nucl Acids Res 34: 407-416.
56. Zhang ML, Tong XJ, Fu XH, Zhou BO, Wang J, et al. (2010) Yeast telomerase subunit Est1p has guanine quadruplex-promoting activity that is required for telomere elongation. Nat Struct Mol Biol 17: 202-209.
57. Zhou J, Hidaka K, Futcher B, (2000) The Est1 subunit of yeast telomerase binds the Tlc1 telomerase RNA. Mol Cell Biol 20: 1947-1955.
58. Sikorski RS, Hieter P, (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
59. Morris DK, Lundblad V, (1997) Programmed translational frameshifting in a gene required for yeast telomere replication. Curr Biol 7: 969-976.
60. Foiani M, Marini F, Gamba D, Lucchini G, Plevani P, (1994) The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol Cell Biol 14: 923-933.
61. Kushnirov VV, (2000) Rapid and reliable protein extraction from yeast. Yeast 16: 857-860.
62. Wan S, Capasso H, Walworth NC, (1999) The topoisomerase I poison camptothecin generates a Chk1-dependent DNA damage checkpoint signal in fission yeast. Yeast 15: 821-828.
63. Runge KW, Zakian VA, (1989) Introduction of extra telomeric DNA sequences into Saccharomyces cerevisiae results in telomere elongation. Mol Cell Biol 9: 1488-1497.
64. McGee J, Phillips J, Chan A, Sabourin M, Paeschke K, et al. (2010) Reduced Rif2 and lack of Mec1 target short telomeres for elongation rather than double-strand break repair. Nature Struct Molec Biol 17: 1438-1445.