A genomewide suppressor and enhancer analysis of cdc13-1 reveals varied cellular processes influencing telomere capping in Saccharomyces cerevisiae

Genetics

Volumn 180, Issue 4, 2008, Pages 2251-2266

  Addinall, S G ^a   Downey, M ^b,c   Yu, M ^a   Zubko, M K ^a,e   Dewar, J ^a   Leake, A ^a   Hallinan, J ^a,d   Shaw, O ^a,d   James, K ^a,d   Wilkinson, D J ^a,d   Wipat, A ^a,d   Durocher, D ^b,c   Lydall, D ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b MOUNT SINAI HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

^e MANCHESTER METROPOLITAN UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CASEIN KINASE II; CELL CYCLE PROTEIN; CELL CYCLE PROTEIN 13; TELOMERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE PROGRESSION; CELL POLARITY; CONTROLLED STUDY; DNA DAMAGE; DNA DEGRADATION; FUNGUS GROWTH; GENE DELETION; GENE INTERACTION; GENE MUTATION; IRON TRANSPORT; NONHUMAN; PHENOTYPE; PHOSPHATE TRANSPORT; PRIORITY JOURNAL; PROTEIN DEGRADATION; RNA DEGRADATION; SACCHAROMYCES CEREVISIAE; TELOMERE;

DNA REPAIR; DNA, FUNGAL; GENE DELETION; GENES, SUPPRESSOR; GENOME, FUNGAL; MUTATION; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TELOMERE; TELOMERE-BINDING PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES;

EID: 54949084810     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.092577     Document Type: Article

References (69)

1. ALIC, N., V. J. HIGGINS and I. W. DAWES, 2001 Identification of a Saccharomyces cerevisiae gene that is required for G1 arrest in response to the lipid oxidation product linoleic acid hydroperoxide. Mol. Biol. Cell 12: 1801-1810.
2. ALVARO, D., M. LISBY and R. ROTHSTEIN, 2007 Genomewide analysis of Rad52 foci reveals diverse mechanisms impacting recombination. PLoS Genet. 3: e228.
3. ASKREE, S. H., T. YEHUDA, S. SMOLIKOV, R. GUREVICH, J. HAWK et al., 2004 A genome-wide screen for Saccharomyces cerevisiae deletion mutants that affect telomere length. Proc. Natl. Acad. Sci. USA 101: 8658-8663.
4. BAETZ, K., V. MEASDAY and B. ANDREWS, 2006 Revealing hidden relationships among yeast genes involved in chromosome segregation using systematic synthetic lethal and synthetic dosage lethal screens. Cell Cycle 5: 592-595.
5. BENNETT, C. B., L. K. LEWIS, G. KARTHIKEYAN, K. S. LOBACHEV, Y. H. JIN et al., 2001 Genes required for ionizing radiation resistance in yeast. Nat. Genet. 29: 426-434.
6. BHATTACHARYA, A., and J. R. WARNER, 2008 Tbf1 or not Tbf1? Mol. Cell 29: 537-538.
7. BIRRELL, G. W., G. GIAEVER, A. M. CHU, R. W. DAVIS and J. M. BROWN, 2001 A genome-wide screen in Saccharomyces cerevisiae for genes affecting UV radiation sensitivity. Proc. Natl. Acad. Sci. USA 98: 12608-12613.
8. BLASCO, M. A., 2007 Telomere length, stem cells and aging. Nat. Chem. Biol. 3: 640-649.
9. BOLES, E., P. DE JONG-GUBBELS and J. T. PRONK, 1998 Identification and characterization of MAE1, the Saccharomyces cerevisiae structural gene encoding mitochondrial malic enzyme. J. Bacteriol. 180: 2875-2882.
10. BREITKREUTZ, B. J., C. STARK and M. TYERS, 2003 Osprey: a network visualization system. Genome Biol. 4: R22.
11. BREITKREUTZ, B. J., C. STARK, T. REGULY, L. BOUCHER, A. BREITKREUTZ et al., 2008 The BioGRID Interaction Database: 2008 update. Nucleic Acids Res. 36: D637-D640.
12. BRETON, A. M., J. SCHAEFFER and M. AIGLE, 2001 The yeast Rvs161 and Rvs167 proteins are involved in secretory vesicles targeting the plasma membrane and in cell integrity. Yeast 18: 1053-1068.
13. CARE, A., K. A. VOUSDEN, K. M. BINLEY, P. RADCLIFFE, J. TREVETHICK et al., 2004 A synthetic lethal screen identifies a role for the cortical actin patch/endocytosis complex in the response to nutrient deprivation in Saccharomyces cerevisiae. Genetics 166: 707-719.
14. CHANG, M., M. BELLAOUI, C. BOONE and G. W. BROWN, 2002 A genomewide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. USA 99: 16934-16939.
15. CHEUNG, A. L., and W. DENG, 2008 Telomere dysfunction, genome instability and cancer. Front. Biosci. 13: 2075-2090.
16. CHOUDHURY, A. R., Z. JU, M. W. DJOJOSUBROTO, A. SCHIENKE, A. LECHEL et al., 2007 Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation. Nat. Genet. 39: 99-105.
17. DAHLSEID, J. N., J. LEW-SMITH, M. J. LELIVELT, S. ENOMOTO, A. FORD et al., 2003 mRNAs encoding telomerase components and regulators are controlled by UPF genes in Saccharomyces cerevisiae. Eukaryot. Cell 2: 134-142.
18. DOWNEY, M., R. HOULSWORTH, L. MARINGELE, A. ROLLIE, M. BREHME et al., 2006 A genome-wide screen identifies the evolutionarily conserved KEOPS complex as a telomere regulator. Cell 124: 1155-1168.
19. EISEN, M. B., P. T. SPELLMAN, P. O. BROWN and D. BOTSTEIN, 1998 Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95: 14863-14868.
20. ENOMOTO, S., L. GLOWCZEWSKI, J. LEW- SMITH and J. G. BERMAN, 2004 Telomere cap components influence the rate of senescence in telomerase-deficient yeast cells. Mol. Cell. Biol. 24: 837-845.
21. FALCON, S., and R. GENTLEMAN, 2007 Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258.
22. FOUREL, G., E. REVARDEL, C. E. KOERING and E. GILSON, 1999 Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J. 18: 2522-2537.
23. GALLARDO, F., C. OLIVIER, A. T. DANDJINOU, R. J. WELLINGER and P. CHARTRAND, 2008 TLC1 RNA nucleo-cytoplasmic trafficking links telomerase biogenesis to its recruitment to telomeres. EMBO J. 27: 748-757.
24. GARDNER, R. G., Z. W. NELSON and D. E. GOTTSCHLING, 2005 Degradation-mediated protein quality control in the nucleus. Cell 120: 803-815.
25. GARVIK, B., M. CARSON and L. HARTWELL, 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.
26. GATBONTON, T., M. IMBESI, M. NELSON, J. M. AKEY, D. M. RUDERFER et al., 2006 Telomere length as a quantitative trait: genome-wide survey and genetic mapping of telomere length-control genes in yeast. PLoS Genet. 2: e35.
27. GREIDER, C. W., and E. H. BLACKBURN, 1985 Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43: 405-413.
28. HE, F., X. LI, P. SPATRICK, R. CASILLO, S. DONG et al., 2003 Genome-wide analysis of mRNAs regulated by the nonsense-mediated and 5′ to 3′ mRNA decay pathways in yeast. Mol. Cell 12: 1439-1452.
29. HOGUES, H., H. LAVOIE, A. SELLAM, M. MANGOS, T. ROEMER et al., 2008 Transcription factor substitution during the evolution of fungal ribosome regulation. Mol. Cell 29: 552-562.
30. JELINSKY, S. A., and L. D. SAMSON, 1999 Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Natl. Acad. Sci. USA 96: 1486-1491.
31. JIA, X., T. WEINERT and D. LYDALL, 2004 Mec1 and Rad53 inhibit formation of single-stranded DNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 166: 753-764.
32. KIM, M. K., M. R. KANG, H. W. NAM, Y. S. BAE, Y. S. KIM et al., 2008 Regulation of telomeric-repeat binding factor 1 binding to telomeres by casein kinase 2-mediated phosphorylation. J. Biol. Chem. 283: 14144-14152.
33. KOERING, C. E., G. FOUREL, E. BINET- BRASSELET, T. LAROCHE, F. KLEIN et al., 2000 Identification of high affinity Tbf1p-binding sites within the budding yeast genome. Nucleic Acids Res. 28: 2519-2526.
34. KOSTELANSKY, M. S., C. SCHLUTER, Y. Y. TAM, S. LEE, R. GHIRLANDO et al., 2007 Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer. Cell 129: 485-498.
35. KUSHNER, D. B., B. D. LINDENBACH, V. Z. GRDZELISHVILI, A. O. NOUEIRY, S. M. PAUL et al., 2003 Systematic, genome-wide identification of host genes affecting replication of a positive-strand RNA virus. Proc. Natl. Acad. Sci. USA 100: 15764-15769.
36. LAZZARO, F., V. SAPOUNTZI, M. GRANATA, A. PELLICIOLI, M. VAZE et al., 2008 Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 27: 1502-1512.
37. LOMBARDI, R., and H. RIEZMAN, 2001 Rvs161p and Rvs167p, the two yeast amphiphysin homologs, function together in vivo. J. Biol. Chem. 276: 6016-6022.
38. LONGHESE, M. P., 2008 DNA damage response at functional and dysfunctional telomeres. Genes Dev. 22: 125-140.
39. LOTTERSBERGER, F., F. RUBERT, V. BALDO, G. LUCCHINI and M. P. LONGHESE, 2003 Functions of Saccharomyces cerevisiae 14-3-3 proteins in response to DNA damage and to DNA replication stress. Genetics 165: 1717-1732.
40. LOTTERSBERGER, F., A. PANZA, G. LUCCHINI, S. PIATTI and M. P. LONGHESE, 2006 The Saccharomyces cerevisiae 14-3-3 proteins are required for the G1/S transition, actin cytoskeleton organization and cell wall integrity. Genetics 173: 661-675.
41. LOTTERSBERGER, F., A. PANZA, G. LUCCHINI and M. P. LONGHESE, 2007 Functional and physical interactions between yeast 14-3-3 proteins, acetyltransferases, and deacetylases in response to DNA replication perturbations. Mol. Cell. Biol. 27: 3266-3281.
42. LYDALL, D., 2003 Hiding at the ends of yeast chromosomes: telomeres, nucleases and checkpoint pathways. J. Cell Sci. 116: 4057-4065.
43. 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 yku70Delta mutants. Genes Dev. 16: 1919-1933.
44. MEASDAY, V., K. BAETZ, J. GUZZO, K. YUEN, T. KWOK et al., 2005 Systematic yeast synthetic lethal and synthetic dosage lethal screens identify genes required for chromosome segregation. Proc. Natl. Acad. Sci. USA 102: 13956-13961.
45. NAUTIYAL, S., J. L. DERISI and E. H. BLACKBURN, 2002 The genome-wide expression response to telomerase deletion in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99: 9316-9321.
46. NUGENT, C. I., T. R. HUGHES, N. F. LUE and V. LUNDBLAD, 1996 Cdc13p: a single-strand telomeric DNA-binding protein with a dual role in yeast telomere maintenance. Science 274: 249-252.
47. OLOVNIKOV, A. M., 1973 A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41: 181-190.
48. PASSOS, J. F., G. SARETZKI, S. AHMED, G. NELSON, T. RICHTER et al., 2007 Mitochondrial dysfunction accounts for the stochastic heterogeneity in telomere-dependent senescence. PLoS Biol. 5: e110.
49. POLOTNIANKA, R. M., J. LI and A. J. LUSTIG, 1998 The yeast Ku heterodimer is essential for protection of the telomere against nucleolytic and recombinational activities. Curr. Biol. 8: 831-834.
50. REAPER, P. M., F. DI FAGAGNA and S. P. JACKSON, 2004 Activation of the DNA damage response by telomere attrition: a passage to cellular senescence. Cell Cycle 3: 543-546.
51. ROG, O., S. SMOLIKOV, A. KRAUSKOPF and M. KUPIEC, 2005 The yeast VPS genes affect telomere length regulation. Curr. Genet. 47: 18-28.
52. ROGUEV, A., M. WIREN, J. S. WEISSMAN and N. J. KROGAN, 2007 High-throughput genetic interaction mapping in the fission yeast Schizosaccharomyces pombe. Nat. Methods 4: 861-866.
53. SALDANHA, A. J., 2004 Java Treeview: extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
54. SANDELL, L. L., and V. A. ZAKIAN, 1993 Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75: 729-739.
55. SCHAETZLEIN, S., N. R. KODANDARAMIREDDY, Z. JU, A. LECHEL, A. STEPCZYNSKA et al., 2007 Exonuclease-1 deletion impairs DNA damage signaling and prolongs lifespan of telomere-dysfunctional mice. Cell 130: 863-877.
56. SACCHAROMYCES GENOME DATABASE, 2008 Saccharomyces Genome Database. http://www.yeastgenome.org.
57. SHACHAR, R., L. UNGAR, M. KUPIEC, E. RUPPIN and R. SHARAN, 2008 A systems-level approach to mapping the telomere length maintenance gene circuitry. Mol. Syst. Biol. 4: 172.
58. STARK, C., B. J. BREITKREUTZ, T. REGULY, L. BOUCHER, A. BREITKREUTZ et al., 2006 BioGRID: a general repository for interaction datasets. Nucleic Acids Res. 34: D535-D539.
59. TEIXEIRA, M. T., K. FORSTEMANN, S. M. GASSER and J. LINGNER, 2002 Intracellular trafficking of yeast telomerase components. EMBO Rep. 3: 652-659.
60. THORSNESS, P. E., K. H. WHITE and T. D. FOX, 1993 Inactivation of YME1, a member of the ftsH-SEC18-PAS1-CDC48 family of putative ATPase-encoding genes, causes increased escape of DNA from mitochondria in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 5418-5426.
61. TOCZYSKI, D. P., D. J. GALGOCZY and L. H. HARTWELL, 1997 CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90: 1097-1106.
62. TONG, A. H., and C. BOONE, 2006 Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 313: 171-192.
63. TONG, A. H., M. EVANGELISTA, A. B. PARSONS, H. XU, G. D. BADER et al., 2001 Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
64. VAN HEUSDEN, G. P., and H. Y. STEENSMA, 2006 Yeast 14-3-3 proteins. Yeast 23: 159-171.
65. WEINERT, T. A., G. L. KISER and L. H. HARTWELL, 1994 Mitotic checkpoint genes in budding yeast and the dependence of mitosis on DNA replication and repair. Genes Dev. 8: 652-665.
66. 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.
67. YU, E. Y., O. STEINBERG-NEIFACH, A. T. DANDJINOU, F. KANG, A. J. MORRISON et al., 2007 Regulation of telomere structure and functions by subunits of the INO80 chromatin remodeling complex. Mol. Cell. Biol. 27: 5639-5649.
68. ZELLER, C. E., S. C. PARNELL and H. G. DOHLMAN, 2007 The RACK1 ortholog Asc1 functions as a G-protein beta subunit coupled to glucose responsiveness in yeast. J. Biol. Chem. 282: 25168-25176.
69. ZUBKO, M. K., S. GUILLARD and D. LYDALL, 2004 Exo1 and Rad24 differentially regulate generation of ssDNA at telomeres of Saccharomyces cerevisiae cdc13-1 mutants. Genetics 168: 103-115.