Mec1ATR is needed for extensive telomere elongation in response to ethanol in yeast

Current Genetics

Volumn 64, Issue 1, 2018, Pages 223-234

  Harari, Yaniv ^a   Kupiec, Martin ^a  

^a TEL AVIV UNIVERSITY   (Israel)

Author keywords

Ethanol; Rif1; Rif2; Stress; Telomeres; Yeast

Indexed keywords

ALCOHOL; ATR PROTEIN; MATING HORMONE ALPHA FACTOR; MEC1 PROTEIN; MESSENGER RNA; PROTEIN KINASE; RAP1 PROTEIN; RIF1 PROTEIN; TEL1 PROTEIN; TELOMERASE; UNCLASSIFIED DRUG; MEC1 PROTEIN, S CEREVISIAE; PROTEIN SERINE THREONINE KINASE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL PEPTIDE;

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL INTERACTION; CLINICAL ASSESSMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; TELOMERE ELONGATION; TELOMERE HOMEOSTASIS; TELOMERE LENGTH; TELOMERE SHORTENING; TRANSCRIPTION ELONGATION; VEGETATIVE GROWTH; YEAST CELL; BIOLOGICAL MODEL; CELL CYCLE; CHROMATIN IMMUNOPRECIPITATION; DRUG EFFECT; GENETICS; METABOLISM; MUTATION; PHENOTYPE; PHYSIOLOGICAL STRESS; TELOMERE;

CELL CYCLE; CHROMATIN IMMUNOPRECIPITATION; ETHANOL; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, BIOLOGICAL; MUTATION; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRESS, PHYSIOLOGICAL; TELOMERE; TELOMERE HOMEOSTASIS;

EID: 85026815019     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-017-0728-1     Document Type: Article

References (56)

1. Abdallah P, Luciano P, Runge KW, Lisby M, Geli V, Gilson E, Teixeira MT (2009) A two-step model for senescence triggered by a single critically short telomere. Nat Cell Biol 11:988–993. doi:10.1038/ncb1911
2. Adamczyk J, Deregowska A, Panek A, Golec E, Lewinska A, Wnuk M (2016) Affected chromosome homeostasis and genomic instability of clonal yeast cultures. Curr Genet 62:405–418. doi:10.1007/s00294-015-0537-3
3. 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. doi:10.1038/sj.embor.7401082
4. Blackburn EH (2000) Telomeres and telomerase. Keio J Med 49:59–65
5. Blackburn EH (2001) Switching and signaling at the telomere. Cell 106:661–673
6. Blasco MA (2005) Telomeres and human disease: ageing, cancer and beyond. Nat Rev Genet 6:611–622. doi:10.1038/nrg1656
7. Bodnar AG, Ouellette M, Frolkis M, Holt SE, Chiu CP, Morin GB, Harley CB, Shay JW, Lichtsteiner S, Wright WE (1998) Extension of life-span by introduction of telomerase into normal human cells. Science 279:349–352
8. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, Hieter P, Boeke JD (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. doi:10.1002/(SICI)1097-0061(19980130)14:2<115:AID-YEA204>3.0.CO;2-2
9. Chakhparonian M, Faucher D, Wellinger RJ (2005) A mutation in yeast Tel1p that causes differential effects on the DNA damage checkpoint and telomere maintenance. Curr Genet 48:310–322. doi:10.1007/s00294-005-0020-7
10. Chan SW, Blackburn EH (2002) New ways not to make ends meet: telomerase, DNA damage proteins and heterochromatin. Oncogene 21:553–563
11. Chang M, Arneric M, Lingner J (2007) Telomerase repeat addition processivity is increased at critically short telomeres in a Tel1-dependent manner in Saccharomyces cerevisiae. Genes Dev 21:2485–2494. doi:10.1101/gad.1588807
12. Chidi BS, Rossouw D, Bauer FF (2016) Identifying and assessing the impact of wine acid-related genes in yeast. Curr Genet 62:149–164. doi:10.1007/s00294-015-0498-6
13. Chymkowitch P, Nguea AP, Aanes H, Koehler CJ, Thiede B, Lorenz S, Meza-Zepeda LA, Klungland A, Enserink JM (2015) Sumoylation of Rap1 mediates the recruitment of TFIID to promote transcription of ribosomal protein genes. Genome Res 25:897–906. doi:10.1101/gr.185793.114
14. Collins K, Mitchell JR (2002) Telomerase in the human organism. Oncogene 21:564–579
15. Cubillos FA (2016) Exploiting budding yeast natural variation for industrial processes. Curr Genet 62:745–751. doi:10.1007/s00294-016-0602-6
16. de Lange T (2009) How telomeres solve the end-protection problem. Science 326:948–952
17. Eleutherio E, Panek A, De Mesquita JF, Trevisol E, Magalhaes R (2015) Revisiting yeast trehalose metabolism. Curr Genet 61:263–274. doi:10.1007/s00294-014-0450-1
18. Gadaleta MC, Gonzalez-Medina A, Noguchi E (2016) Timeless protection of telomeres. Curr Genet 62:725–730. doi:10.1007/s00294-016-0599-x
19. Gallardo F, Laterreur N, Cusanelli E, Ouenzar F, Querido E, Wellinger RJ, Chartrand P (2011) Live cell imaging of telomerase RNA dynamics reveals cell cycle-dependent clustering of telomerase at elongating telomeres. Mol Cell 44:819–827. doi:10.1016/j.molcel.2011.09.020
20. Garbett KA, Tripathi MK, Cencki B, Layer JH, Weil PA (2007) Yeast TFIID serves as a coactivator for Rap1p by direct protein–protein interaction. Mol Cell Biol 27:297–311. doi:10.1128/MCB.01558-06
21. Girish V, Vijayalakshmi A (2004) Affordable image analysis using NIH Image/ImageJ. Indian J Cancer 41:47
22. Greider CW (2016) Regulating telomere length from the inside out: the replication fork model. Genes Dev 30:1483–1491. doi:10.1101/gad.280578.116
23. Hahn WC, Stewart SA, Brooks MW, York SG, Eaton E, Kurachi A, Beijersbergen RL, Knoll JH, Meyerson M, Weinberg RA (1999) Inhibition of telomerase limits the growth of human cancer cells. Nat Med 5:1164–1170. doi:10.1038/13495
24. Harari Y, Kupiec M (2014) Genome-wide studies of telomere biology in budding yeast. Microbial cell 1:70–80. doi:10.15698/mic2014.01.132
25. Harley CB, Kim NW, Prowse KR, Weinrich SL, Hirsch KS, West MD, Bacchetti S, Hirte HW, Counter CM, Greider CW et al (1994) Telomerase, cell immortality, and cancer. Cold Spring Harb Symp Quant Biol 59:307–315
26. Harrington L (2003) Biochemical aspects of telomerase function. Cancer Lett 194:139–154
27. Hayflick L (1965) The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 37:614–636
28. Hector RE, Ray A, Chen BR, Shtofman R, Berkner KL, Runge KW (2012) Mec1p associates with functionally compromised telomeres. Chromosoma 121:277–290. doi:10.1007/s00412-011-0359-0
29. Ho YH, Gasch AP (2015) Exploiting the yeast stress-activated signaling network to inform on stress biology and disease signaling. Curr Genet 61:503–511. doi:10.1007/s00294-015-0491-0
30. Holt SE, Shay JW, Wright WE (1996) Refining the telomere-telomerase hypothesis of aging and cancer. Nat Biotechnol 14:836–839. doi:10.1038/nbt0796-836
31. Kupiec M (2014) Biology of telomeres: lessons from budding yeast. FEMS Microbiol Rev 38:144–171. doi:10.1111/1574-6976.12054
32. Levy MZ, Allsopp RC, Futcher AB, Greider CW, Harley CB (1992) Telomere end-replication problem and cell aging. J Mol Biol 225:951–960
33. Luo K, Vega-Palas MA, Grunstein M (2002) Rap1-Sir4 binding independent of other Sir, yKu, or histone interactions initiates the assembly of telomeric heterochromatin in yeast. Genes Dev 16:1528–1539. doi:10.1101/gad.988802
34. Marcand S, Brevet V, Gilson E (1999) Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J 18:3509–3519. doi:10.1093/emboj/18.12.3509
35. McGee JS, Phillips JA, Chan A, Sabourin M, Paeschke K, Zakian VA (2010) Reduced Rif2 and lack of Mec1 target short telomeres for elongation rather than double-strand break repair. Nat Struct Mol Biol 17:1438–1445. doi:10.1038/nsmb.1947
36. Millet C, Makovets S (2016) Aneuploidy as a mechanism of adaptation to telomerase insufficiency. Curr Genet 62:557–564. doi:10.1007/s00294-015-0559-x
37. Nishida N, Jing D, Kuroda K, Ueda M (2014) Activation of signaling pathways related to cell wall integrity and multidrug resistance by organic solvent in Saccharomyces cerevisiae. Curr Genet 60:149–162. doi:10.1007/s00294-013-0419-5
38. Nishida-Aoki N, Mori H, Kuroda K, Ueda M (2015) Activation of the mitochondrial signaling pathway in response to organic solvent stress in yeast. Curr Genet 61:153–164. doi:10.1007/s00294-014-0463-9
39. Paciotti V, Clerici M, Scotti M, Lucchini G, Longhese MP (2001) Characterization of mec1 kinase-deficient mutants and of new hypomorphic mec1 alleles impairing subsets of the DNA damage response pathway. Mol Cell Biol 21:3913–3925. doi:10.1128/MCB.21.12.3913-3925.2001
40. Piccirillo S, Kapros T, Honigberg SM (2016) Phenotypic plasticity within yeast colonies: differential partitioning of cell fates. Curr Genet 62:467–473. doi:10.1007/s00294-015-0558-y
41. Ritchie KB, Mallory JC, Petes TD (1999) Interactions of TLC1 (which encodes the RNA subunit of telomerase), TEL1, and MEC1 in regulating telomere length in the yeast Saccharomyces cerevisiae. Mole Cell Biol 19:6065–6075
42. Romano GH, Harari Y, Yehuda T, Podhorzer A, Rubinstein L, Shamir R, Gottlieb A, Silberberg Y, Pe’er D, Ruppin E, Sharan R, Kupiec M (2013) Environmental stresses disrupt telomere length homeostasis. PLoS Genet 9:e1003721. doi:10.1371/journal.pgen.1003721
43. Rubinstein L, Ungar L, Harari Y, Babin V, Ben-Aroya S, Merenyi G, Marjavaara L, Chabes A, Kupiec M (2014) Telomere length kinetics assay (TELKA) sorts the telomere length maintenance (tlm) mutants into functional groups. Nucleic Acids Res 42:6314–6325. doi:10.1093/nar/gku267
44. Sabourin M, Tuzon CT, Zakian VA (2007) Telomerase and Tel1p preferentially associate with short telomeres in S. cerevisiae. Mol Cell 27:550–561. doi:10.1016/j.molcel.2007.07.016
45. Schawalder SB, Kabani M, Howald I, Choudhury U, Werner M, Shore D (2004) Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1. Nature 432:1058–1061. doi:10.1038/nature03200
46. Shay JW, Wright WE (2011) Role of telomeres and telomerase in cancer. Semin Cancer Biol 21:349–353. doi:10.1016/j.semcancer.2011.10.001
47. Shore D, Bianchi A (2009) Telomere length regulation: coupling DNA end processing to feedback regulation of telomerase. EMBO J 28:2309–2322. doi:10.1038/emboj.2009.195
48. Simon MN, Churikov D, Geli V (2016) Replication stress as a source of telomere recombination during replicative senescence in Saccharomyces cerevisiae. FEMS Yeast Res 16:fow85. doi:10.1093/femsyr/fow085
49. Simonicova L, Dudekova H, Ferenc J, Prochazkova K, Nebohacova M, Dusinsky R, Nosek J, Tomaska L (2015) Saccharomyces cerevisiae as a model for the study of extranuclear functions of mammalian telomerase. Curr Genet 61:517–527. doi:10.1007/s00294-014-0472-8
50. Smogorzewska A, de Lange T (2004) Regulation of telomerase by telomeric proteins. Annu Rev Biochem 73:177–208
51. Teixeira MT, Arneric M, Sperisen P, Lingner J (2004) Telomere length homeostasis is achieved via a switch between telomerase-extendible and -nonextendible states. Cell 117:323–335
52. Tercero JA, Longhese MP, Diffley JF (2003) A central role for DNA replication forks in checkpoint activation and response. Mol Cell 11:1323–1336
53. Tsukamoto Y, Taggart AK, Zakian VA (2001) The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr Biol 11:1328–1335
54. Wade JT, Hall DB, Struhl K (2004) The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes. Nature 432:1054–1058. doi:10.1038/nature03175
55. Wotton D, Shore D (1997) A novel Rap1p-interacting factor, Rif2p, cooperates with Rif1p to regulate telomere length in Saccharomyces cerevisiae. Genes Dev 11:748–760
56. Yadav KK, Singh N, Rajasekharan R (2016) Responses to phosphate deprivation in yeast cells. Curr Genet 62:301–307. doi:10.1007/s00294-015-0544-4