A Genome-Wide Screen Identifies the Evolutionarily Conserved KEOPS Complex as a Telomere Regulator

Cell

Volumn 124, Issue 6, 2006, Pages 1155-1168

  Downey, Michael ^a,b   Houlsworth, Rebecca ^d   Maringele, Laura ^d,g   Rollie, Adrienne ^b   Brehme, Marc ^d,e   Galicia, Sarah ^a   Guillard, Sandrine ^d,f   Partington, Melanie ^a   Zubko, Mikhajlo K ^d,g   Krogan, Nevan J ^b   Emili, Andrew ^b   Greenblatt, Jack F ^b   Harrington, Lea ^c   Lydall, David ^d,g,h   Durocher, Daniel ^a,b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^g NEWCASTLE UNIVERSITY   (United Kingdom)

^h NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CGI 121 PROTEIN; CYCLIN DEPENDENT KINASE; CYCLIN DEPENDENT KINASE 13; ENZYME; FUNGAL PROTEIN; KINASE PUTATIVE ENDOPEPTIDASE AND OTHER PROTEIN OF SMALL SIZE; PEPTIDASE; PROTEIN KINASE; UNCLASSIFIED DRUG; BUD32 PROTEIN, S CEREVISIAE; CDC13 PROTEIN, S CEREVISIAE; KEOPS COMPLEX, S CEREVISIAE; MULTIPROTEIN COMPLEX; PROTEIN SERINE THREONINE KINASE; SACCHAROMYCES CEREVISIAE PROTEIN; TELOMERASE; TELOMERE BINDING PROTEIN;

ARTICLE; CELL FUNCTION; DNA STRAND BREAKAGE; GENE DELETION; GENE IDENTIFICATION; GENE REPRESSION; GENETIC CONSERVATION; GENOME ANALYSIS; MOLECULAR EVOLUTION; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; SCREENING TEST; TELOMERE; TELOMERE CAPPING; CHEMISTRY; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

SACCHAROMYCES CEREVISIAE;

EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOMIC LIBRARY; MULTIPROTEIN COMPLEXES; MUTATION; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERASE; TELOMERE; TELOMERE-BINDING PROTEINS;

EID: 33646178457     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2005.12.044     Document Type: Article

References (60)

1. Bertuch A.A., and Lundblad V. EXO1 contributes to telomere maintenance in both telomerase-proficient and telomerase-deficient Saccharomyces cerevisiae. Genetics 166 (2004) 1651-1659
2. Bianchi A., Negrini S., and Shore D. Delivery of yeast telomerase to a DNA break depends on the recruitment functions of Cdc13 and Est1. Mol. Cell 16 (2004) 139-146
3. Booth C., Griffith E., Brady G., and Lydall D. Quantitative amplification of single-stranded DNA (QAOS) demonstrates that cdc13-1 mutants generate ssDNA in a telomere to centromere direction. Nucleic Acids Res. 29 (2001) 4414-4422
4. Boule J.B., Vega L.R., and Zakian V.A. The yeast Pif1p helicase removes telomerase from telomeric DNA. Nature 438 (2005) 57-61
5. Cervantes R.B., and Lundblad V. Mechanisms of chromosome-end protection. Curr. Opin. Cell Biol. 14 (2002) 351-356
6. Chan S.W., and Blackburn E.H. Telomerase and ATM/Tel1p protect telomeres from nonhomologous end joining. Mol. Cell 11 (2003) 1379-1387
7. Chen C., and Kolodner R.D. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat. Genet. 23 (1999) 81-85
8. Chen Q., Ijpma A., and Greider C.W. Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol. Cell. Biol. 21 (2001) 1819-1827
9. Chiu S.Y., Serin G., Ohara O., and Maquat L.E. Characterization of human Smg5/7a: a protein with similarities to Caenorhabditis elegans SMG5 and SMG7 that functions in the dephosphorylation of Upf1. RNA 9 (2003) 77-87
10. Cohn M., and Blackburn E.H. Telomerase in yeast. Science 269 (1995) 396-400
11. Craven R.J., and Petes T.D. Dependence of the regulation of telomere length on the type of subtelomeric repeat in the yeast Saccharomyces cerevisiae. Genetics 152 (1999) 1531-1541
12. 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
13. d'Adda di Fagagna F., Teo S.H., and Jackson S.P. Functional links between telomeres and proteins of the DNA-damage response. Genes Dev. 18 (2004) 1781-1799
14. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 19 (2005) 2100-2110
15. Diede S.J., and Gottschling D.E. Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99 (1999) 723-733
16. Diede S.J., and Gottschling D.E. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 11 (2001) 1336-1340
17. DuBois M.L., Haimberger Z.W., McIntosh M.W., and Gottschling D.E. A quantitative assay for telomere protection in Saccharomyces cerevisiae. Genetics 161 (2002) 995-1013
18. Enomoto S., Glowczewski L., Lew-Smith J., and Berman J.G. Telomere cap components influence the rate of senescence in telomerase-deficient yeast cells. Mol. Cell. Biol. 24 (2004) 837-845
19. Evans S.K., and Lundblad V. Est1 and Cdc13 as comediators of telomerase access. Science 286 (1999) 117-120
20. Facchin S., Lopreiato R., Stocchetto S., Arrigoni G., Cesaro L., Marin O., Carignani G., and Pinna L.A. Structure-function analysis of yeast piD261/Bud32, an atypical protein kinase essential for normal cell life. Biochem. J. 364 (2002) 457-463
21. Facchin S., Lopreiato R., Ruzzene M., Marin O., Sartori G., Gotz C., Montenarh M., Carignani G., and Pinna L.A. Functional homology between yeast piD261/Bud32 and human PRPK: both phosphorylate p53 and PRPK partially complements piD261/Bud32 deficiency. FEBS Lett. 549 (2003) 63-66
22. Fukuhara N., Ebert J., Unterholzner L., Lindner D., Izaurralde E., and Conti E. SMG7 is a 14-3-3-like adaptor in the nonsense-mediated mRNA decay pathway. Mol. Cell 17 (2005) 537-547
23. Gardner R.G., Nelson Z.W., and Gottschling D.E. Degradation-mediated protein quality control in the nucleus. Cell 120 (2005) 803-815
24. 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
25. Grandin N., Reed S.I., and Charbonneau M. Stn1, a new Saccharomyces cerevisiae protein, is implicated in telomere size regulation in association with Cdc13. Genes Dev. 11 (1997) 512-527
26. Grandin N., Damon C., and Charbonneau M. Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. EMBO J. 20 (2001) 6127-6139
27. 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
28. Hackett J.A., and Greider C.W. End resection initiates genomic instability in the absence of telomerase. Mol. Cell. Biol. 23 (2003) 8450-8461
29. Hackett J.A., Feldser D.M., and Greider C.W. Telomere dysfunction increases mutation rate and genomic instability. Cell 106 (2001) 275-286
30. - mutant. Proc. Natl. Acad. Sci. USA 90 (1993) 7034-7038
31. Ho Y., Gruhler A., Heilbut A., Bader G.D., Moore L., Adams S.L., Millar A., Taylor P., Bennett K., Boutilier K., et al. Systematic identification of protein complexes in Saccharomyces cerevisiae by mass spectrometry. Nature 415 (2002) 180-183
32. Hughes T.R., Weilbaecher R.G., Walterscheid M., and Lundblad V. Identification of the single-strand telomeric DNA binding domain of the Saccharomyces cerevisiae Cdc13 protein. Proc. Natl. Acad. Sci. USA 97 (2000) 6457-6462
33. Kanellis P., Agyei R., and Durocher D. Elg1 forms an alternative PCNA-interacting RFC complex required to maintain genome stability. Curr. Biol. 13 (2003) 1583-1595
34. Larrivee M., LeBel C., and Wellinger R.J. The generation of proper constitutive G-tails on yeast telomeres is dependent on the MRX complex. Genes Dev. 18 (2004) 1391-1396
35. Lin J.J., and Zakian V.A. 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 (1996) 13760-13765
36. Lopreiato R., Facchin S., Sartori G., Arrigoni G., Casonato S., Ruzzene M., Pinna L.A., and Carignani G. Analysis of the interaction between piD261/Bud32, an evolutionarily conserved protein kinase of Saccharomyces cerevisiae, and the Grx4 glutaredoxin. Biochem. J. 377 (2004) 395-405
37. Lottersberger F., Rubert F., Baldo V., Lucchini G., and Longhese M.P. Functions of Saccharomyces cerevisiae 14-3-3 proteins in response to DNA damage and to DNA replication stress. Genetics 165 (2003) 1717-1732
38. - senescence. Cell 73 (1993) 347-360
39. Lydall D. Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways. J. Cell Sci. 116 (2003) 4057-4065
40. Lydall D., and Weinert T. Yeast checkpoint genes in DNA damage processing: implications for repair and arrest. Science 270 (1995) 1488-1491
41. Mangahas J.L., Alexander M.K., Sandell L.L., and Zakian V.A. Repair of chromosome ends after telomere loss in Saccharomyces. Mol. Biol. Cell 12 (2001) 4078-4089
42. Maringele L., and 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
43. Miyoshi A., Kito K., Aramoto T., Abe Y., Kobayashi N., and Ueda N. Identification of CGI-121, a novel PRPK (p53-related protein kinase)-binding protein. Biochem. Biophys. Res. Commun. 303 (2003) 399-405
44. Myung K., Chen C., and Kolodner R.D. Multiple pathways cooperate in the suppression of genome instability in Saccharomyces cerevisiae. Nature 411 (2001) 1073-1076
45. Ni L., and Snyder M. A genomic study of the bipolar bud site selection pattern in Saccharomyces cerevisiae. Mol. Biol. Cell 12 (2001) 2147-2170
46. Nugent C.I., Hughes T.R., Lue N.F., and Lundblad V. Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274 (1996) 249-252
47. Nugent C.I., Bosco G., Ross L.O., Evans S.K., Salinger A.P., Moore J.K., Haber J.E., and Lundblad V. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8 (1998) 657-660
48. Pennock E., Buckley K., and Lundblad V. Cdc13 delivers separate complexes to the telomere for end protection and replication. Cell 104 (2001) 387-396
49. Reichenbach P., Hoss M., Azzalin C.M., Nabholz M., Bucher P., and Lingner J. A human homolog of yeast Est1 associates with telomerase and uncaps chromosome ends when overexpressed. Curr. Biol. 13 (2003) 568-574
50. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., and Seraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat. Biotechnol. 17 (1999) 1030-1032
51. Schulz V.P., and Zakian V.A. The saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell 76 (1994) 145-155
52. Seki Y., Ikeda S., Kiyohara H., Ayabe H., Seki T., and Matsui H. Sequencing analysis of a putative human O-sialoglycoprotein endopeptidase gene (OSGEP) and analysis of a bidirectional promoter between the OSGEP and APEX genes. Gene 285 (2002) 101-108
53. Snow B.E., Erdmann N., Cruickshank J., Goldman H., Gill R.M., Robinson M.O., and Harrington L. Functional conservation of the telomerase protein Est1p in humans. Curr. Biol. 13 (2003) 698-704
54. Stellwagen A.E., Haimberger Z.W., Veatch J.R., and Gottschling D.E. Ku interacts with telomerase RNA to promote telomere addition at native and broken chromosome ends. Genes Dev. 17 (2003) 2384-2395
55. Taggart A.K., and Zakian V.A. Telomerase: what are the Est proteins doing?. Curr. Opin. Cell Biol. 15 (2003) 275-280
56. Taggart A.K., Teng S.C., and Zakian V.A. Est1p as a cell cycle-regulated activator of telomere-bound telomerase. Science 297 (2002) 1023-1026
57. Teo S.H., and Jackson S.P. Telomerase subunit overexpression suppresses telomere-specific checkpoint activation in the yeast yku80 mutant. EMBO Rep. 2 (2001) 197-202
58. Tong A.H., Evangelista M., Parsons A.B., Xu H., Bader G.D., Page N., Robinson M., Raghibizadeh S., Hogue C.W., Bussey H., et al. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294 (2001) 2364-2368
59. Zhou J., Hidaka K., and Futcher B. The Est1 subunit of yeast telomerase binds the Tlc1 telomerase RNA. Mol. Cell. Biol. 20 (2000) 1947-1955
60. Zubko M.K., Guillard S., and Lydall D. Exo1 and Rad24 differentially regulate generation of ssDNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 168 (2004) 103-115