Binding of Multiple Rap1 Proteins Stimulates Chromosome Breakage Induction during DNA Replication

1. Smogorzewska A, de Lange T (2004) Regulation of telomerase by telomeric proteins. Annu Rev Biochem 73: 177–208. 15189140

2. Wellinger RJ, Zakian VA (2012) Everything you ever wanted to know about Saccharomyces cerevisiae telomeres: beginning to end. Genetics 191: 1073–1105. doi: 10.1534/genetics.111.137851 22879408

3. de Lange T (2005) Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100–2110. 16166375

4. Nandakumar J, Cech TR (2013) Finding the end: recruitment of telomerase to telomeres. Nat Rev Mol Cell Biol 14: 69–82. doi: 10.1038/nrm3505 23299958

5. Soudet J, Jolivet P, Teixeira MT (2014) Elucidation of the DNA end-replication problem in Saccharomyces cerevisiae. Mol Cell 53: 954–964. doi: 10.1016/j.molcel.2014.02.030 24656131

6. Lundblad V, Szostak JW (1989) A mutant with a defect in telomere elongation leads to senescence in yeast. Cell 57: 633–643. 2655926

7. Harley CB, Futcher AB, Greider CW (1990) Telomeres shorten during ageing of human fibroblasts. Nature 345: 458–460. 2342578

8. Huffman KE, Levene SD, Tesmer VM, Shay JW, Wright WE (2000) Telomere shortening is proportional to the size of the G-rich telomeric 3'-overhang. J Biol Chem 275: 19719–19722. 10787419

9. Marcand S, Brevet V, Gilson E (1999) Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J 18: 3509–3519. 10369690

10. Li B, Lustig AJ (1996) A novel mechanism for telomere size control in Saccharomyces cerevisiae. Genes Dev 10: 1310–1326. 8647430

11. Wang RC, Smogorzewska A, de Lange T (2004) Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119: 355–368. 15507207

12. Pickett HA, Cesare AJ, Johnston RL, Neumann AA, Reddel RR (2009) Control of telomere length by a trimming mechanism that involves generation of t-circles. EMBO J 28: 799–809. doi: 10.1038/emboj.2009.42 19214183

13. Pickett HA, Henson JD, Au AY, Neumann AA, Reddel RR (2011) Normal mammalian cells negatively regulate telomere length by telomere trimming. Hum Mol Genet 20: 4684–4692. doi: 10.1093/hmg/ddr402 21903669

14. Lin JJ, Zakian VA (1996) 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 U S A 93: 13760–13765. 8943008

15. 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. 8824190

16. Grandin N, Damon C, Charbonneau M (2001) Ten1 functions in telomere end protection and length regulation in association with Stn1 and Cdc13. Embo J 20: 1173–1183. 11230140

17. Shore D (1994) RAP1: a protean regulator in yeast. Trends Genet 10: 408–412. 7809947

18. Lieb JD, Liu X, Botstein D, Brown PO (2001) Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association. Nat Genet 28: 327–334. 11455386

19. Muller T, Gilson E, Schmidt R, Giraldo R, Sogo J, et al. (1994) Imaging the asymmetrical DNA bend induced by repressor activator protein 1 with scanning tunneling microscopy. J Struct Biol 113: 1–12. 7880649

20. Moretti P, Freeman K, Coodly L, Shore D (1994) Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes Dev 8: 2257–2269. 7958893

21. Conrad MN, Wright JH, Wolf AJ, Zakian VA (1990) RAP1 protein interacts with yeast telomeres in vivo: overproduction alters telomere structure and decreases chromosome stability. Cell 63: 739–750. 2225074

22. Lustig AJ, Kurtz S, Shore D (1990) Involvement of the silencer and UAS binding protein RAP1 in regulation of telomere length. Science 250: 549–553. 2237406

23. Hardy CF, Sussel L, Shore D (1992) A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev 6: 801–814. 1577274

24. 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. 9087429

25. Marcand S, Gilson E, Shore D (1997) A protein-counting mechanism for telomere length regulation in yeast. Science 275: 986–990. 9020083

26. Levy DL, Blackburn EH (2004) Counting of Rif1p and Rif2p on Saccharomyces cerevisiae telomeres regulates telomere length. Mol Cell Biol 24: 10857–10867. 15572688

27. Symington LS, Gautier J (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247–271. doi: 10.1146/annurev-genet-110410-132435 21910633

28. Greenwell PW, Kronmal SL, Porter SE, Gassenhuber J, Obermaier B, et al. (1995) TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82: 823–829. 7671310

29. Nakada D, Matsumoto K, Sugimoto K (2003) ATM-related Tel1 associates with double-strand breaks through an Xrs2-dependent mechanism. Genes & Dev 17: 1957–1962.

30. Bianchi A, Shore D (2007) Increased association of telomerase with short telomeres in yeast. Genes Dev 21: 1726–1730. 17639079

31. Hector RE, Shtofman RL, Ray A, Chen BR, Nyun T, et al. (2007) Tel1p preferentially associates with short telomeres to stimulate their elongation. Mol Cell 27: 851–858. 17803948

32. Sabourin M, Tuzon CT, Zakian VA (2007) Telomerase and Tel1p preferentially associate with short telomeres in S. cerevisiae. Mol Cell 27: 550–561. 17656141

33. Goudsouzian LK, Tuzon CT, Zakian VA (2006) S. cerevisiae Tel1p and Mre11p are required for normal levels of Est1p and Est2p telomere association. Mol Cell 24: 603–610. 17188035

34. 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. 17908934

35. Hirano Y, Fukunaga K, Sugimoto K (2009) Rif1 and Rif2 inhibit localization of Tel1 to DNA ends. Mol Cell 33: 312–322. doi: 10.1016/j.molcel.2008.12.027 19217405

36. Negrini S, Ribaud V, Bianchi A, Shore D (2007) DNA breaks are masked by multiple Rap1 binding in yeast: implications for telomere capping and telomerase regulation. Genes Dev 21: 292–302. 17289918

37. Bochman ML, Paeschke K, Zakian VA (2012) DNA secondary structures: stability and function of G-quadruplex structures. Nat Rev Genet 13: 770–780. doi: 10.1038/nrg3296 23032257

38. Gottschling DE, Aparicio OM, Billington BL, Zakian VA (1990) Position effect at S. cerevisiae telomeres: reversible repression of Pol II transcription. Cell 63: 751–762. 2225075

39. Giraldo R, Rhodes D (1994) The yeast telomere-binding protein RAP1 binds to and promotes the formation of DNA quadruplexes in telomeric DNA. EMBO J 13: 2411–2420. 8194531

40. Diede SJ, Gottschling DE (1999) Telomerase-mediated telomere addition in vivo requires DNA primase and DNA polymerases alpha and delta. Cell 99: 723–733. 10619426

41. Boeke JD, Trueheart J, Natsoulis G, Fink GR (1987) 5-Fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol 154: 164–175. 3323810

42. Branzei D, Foiani M (2010) Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 11: 208–219. doi: 10.1038/nrm2852 20177396

43. Ivessa AS, Zhou JQ, Schulz VP, Monson EK, Zakian VA (2002) Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev 16: 1383–1396. 12050116

44. Pardo B, Marcand S (2005) Rap1 prevents telomere fusions by nonhomologous end joining. EMBO J 24: 3117–3127. 16096640

45. Kyrion G, Boakye KA, Lustig AJ (1992) C-terminal truncation of RAP1 results in the deregulation of telomere size, stability, and function in Saccharomyces cerevisiae. Mol Cell Biol 12: 5159–5173. 1406688

46. Kirkpatrick DT, Fan Q, Petes TD (1999) Maximal stimulation of meiotic recombination by a yeast transcription factor requires the transcription activation domain and a DNA-binding domain. Genetics 152: 101–115. 10224246

47. Kikin O, D'Antonio L, Bagga PS (2006) QGRS Mapper: a web-based server for predicting G-quadruplexes in nucleotide sequences. Nucleic Acids Res 34: W676–682. 16845096

48. Lewis M (2005) The lac repressor. C R Biol 328: 521–548. 15950160

49. Konig P, Giraldo R, Chapman L, Rhodes D (1996) The crystal structure of the DNA-binding domain of yeast RAP1 in complex with telomeric DNA. Cell 85: 125–136. 8620531

50. Falcon CM, Matthews KS (1999) Glycine insertion in the hinge region of lactose repressor protein alters DNA binding. J Biol Chem 274: 30849–30857. 10521477

51. Dubarry M, Loiodice I, Chen CL, Thermes C, Taddei A (2011) Tight protein-DNA interactions favor gene silencing. Genes Dev 25: 1365–1370. doi: 10.1101/gad.611011 21724830

52. Leduc F, Faucher D, Bikond Nkoma G, Gregoire MC, Arguin M, et al. (2011) Genome-wide mapping of DNA strand breaks. PLoS One 6: e17353. doi: 10.1371/journal.pone.0017353 21364894

53. Zeman MK, Cimprich KA (2014) Causes and consequences of replication stress. Nat Cell Biol 16: 2–9. doi: 10.1038/ncb2897 24366029

54. Foss EJ (2001) Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157: 567–577. 11156979

55. Osborn AJ, Elledge SJ (2003) Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev 17: 1755–1767. 12865299

56. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, et al. (2003) S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424: 1073–1083.

57. Hodgson B, Calzada A, Labib K (2007) Mrc1 and Tof1 regulate DNA replication forks in different ways during normal S phase. Mol Biol Cell 18: 3894–3902. 17652453

58. Grandin N, Charbonneau M (2007) Mrc1, a non-essential DNA replication protein, is required for telomere end protection following loss of capping by Cdc13, Yku or telomerase. Mol Genet Genomics 277: 685–699. 17323081

59. Tsolou A, Lydall D (2007) Mrc1 protects uncapped budding yeast telomeres from exonuclease EXO1. DNA Repair (Amst) 6: 1607–1617.

60. Bairwa NK, Mohanty BK, Stamenova R, Curcio MJ, Bastia D (2011) The intra-S phase checkpoint protein Tof1 collaborates with the helicase Rrm3 and the F-box protein Dia2 to maintain genome stability in Saccharomyces cerevisiae. J Biol Chem 286: 2445–2454. doi: 10.1074/jbc.M110.189456 21087929

61. Vaze MB, Pellicioli A, Lee SE, Ira G, Liberi G, et al. (2002) Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol Cell 10: 373–385. 12191482

62. Ray A, Runge KW (1998) The C terminus of the major yeast telomere binding protein Rap1p enhances telomere formation. Mol Cell Biol 18: 1284–1295. 9488443

63. Hirano Y, Sugimoto K (2007) Cdc13 telomere capping decreases Mec1 association but does not affect Tel1 association with DNA ends. Mol Biol Cell 18: 2026–2036. 17377065

64. 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 19629031

65. 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. 15109493

66. Makovets S, Herskowitz I, Blackburn EH (2004) Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol Cell Biol 24: 4019–4031. 15082794

67. Miller KM, Rog O, Cooper JP (2006) Semi-conservative DNA replication through telomeres requires Taz1. Nature 440: 824–828. 16598261

68. Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, et al. (2009) Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 138: 90–103. doi: 10.1016/j.cell.2009.06.021 19596237

69. Labib K, Hodgson B (2007) Replication fork barriers: pausing for a break or stalling for time? EMBO Rep 8: 346–353. 17401409

70. Marcand S, Pardo B, Gratias A, Cahun S, Callebaut I (2008) Multiple pathways inhibit NHEJ at telomeres. Genes Dev 22: 1153–1158. doi: 10.1101/gad.455108 18451106

71. Pan J, Sasaki M, Kniewel R, Murakami H, Blitzblau HG, et al. (2011) A hierarchical combination of factors shapes the genome-wide topography of yeast meiotic recombination initiation. Cell 144: 719–731. doi: 10.1016/j.cell.2011.02.009 21376234

72. Smith CD, Smith DL, DeRisi JL, Blackburn EH (2003) Telomeric protein distributions and remodeling through the cell cycle in Saccharomyces cerevisiae. Mol Biol Cell 14: 556–570. 12589054

73. Li B, Oestreich S, de Lange T (2000) Identification of human Rap1: implications for telomere evolution. Cell 101: 471–483. 10850490

74. Kanoh J, Ishikawa F (2001) spRap1 and spRif1, recruited to telomeres by Taz1, are essential for telomere function in fission yeast. Curr Biol 11: 1624–1630. 11676925

75. Yu EY, Yen WF, Steinberg-Neifach O, Lue NF (2010) Rap1 in Candida albicans: an unusual structural organization and a critical function in suppressing telomere recombination. Mol Cell Biol 30: 1254–1268. doi: 10.1128/MCB.00986-09 20008550

76. Reid RJ, Lisby M, Rothstein R (2002) Cloning-free genome alterations in Saccharomyces cerevisiae using adaptamer-mediated PCR. Methods Enzymol 350: 258–277. 12073317

77. Kondo T, Wakayama T, Naiki T, Matsumoto K, Sugimoto K (2001) Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science 5543: 867–870.

78. Fukunaga K, Hirano Y, Sugimoto K (2012) Subtelomere-binding protein Tbf1 and telomere-binding protein Rap1 collaborate to inhibit localization of the Mre11 complex to DNA ends in budding yeast. Mol Biol Cell 23: 347–359. doi: 10.1091/mbc.E11-06-0568 22130795

79. Goldstein AL, McCusker JH (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541–1553. 10514571

80. Moqtaderi Z, Bai Y, Poon D, Weil PA, Struhl K (1996) TBP-associated factors are not generally required for transcriptional activation in yeast. Nature 383: 188–191. 8774887

81. Hall BM, Ma CX, Liang P, Singh KK (2009) Fluctuation analysis CalculatOR: a web tool for the determination of mutation rate using Luria-Delbruck fluctuation analysis. Bioinformatics 25: 1564–1565. doi: 10.1093/bioinformatics/btp253 19369502

82. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, et al. (2001) Replication dynamics of the yeast genome. Science 294: 115–121. 11588253