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Saccharomyces cerevisiae Mus81-Mms4 prevents accelerated senescence in telomerase-deficient cells


Autoři: Erin K. Schwartz aff001;  Shih-Hsun Hung aff001;  Damon Meyer aff001;  Aurèle Piazza aff001;  Kevin Yan aff001;  Becky Xu Hua Fu aff001;  Wolf-Dietrich Heyer aff001
Působiště autorů: Department of Microbiology and Molecular Genetics, University of California, Davis, Davis, California, United States of America aff001;  Department of Molecular and Cellular Biology, University of California, Davis, Davis, California, United States of America aff002
Vyšlo v časopise: Saccharomyces cerevisiae Mus81-Mms4 prevents accelerated senescence in telomerase-deficient cells. PLoS Genet 16(5): e32767. doi:10.1371/journal.pgen.1008816
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008816

Souhrn

Alternative lengthening of telomeres (ALT) in human cells is a conserved process that is often activated in telomerase-deficient human cancers. This process exploits components of the recombination machinery to extend telomere ends, thus allowing for increased proliferative potential. Human MUS81 (Mus81 in Saccharomyces cerevisiae) is the catalytic subunit of structure-selective endonucleases involved in recombination and has been implicated in the ALT mechanism. However, it is unclear whether MUS81 activity at the telomere is specific to ALT cells or if it is required for more general aspects of telomere stability. In this study, we use S. cerevisiae to evaluate the contribution of the conserved Mus81-Mms4 endonuclease in telomerase-deficient yeast cells that maintain their telomeres by mechanisms akin to human ALT. Similar to human cells, we find that yeast Mus81 readily localizes to telomeres and its activity is important for viability after initial loss of telomerase. Interestingly, our analysis reveals that yeast Mus81 is not required for the survival of cells undergoing recombination-mediated telomere lengthening, i.e. for ALT itself. Rather we infer from genetic analysis that Mus81-Mms4 facilitates telomere replication during times of telomere instability. Furthermore, combining mus81 mutants with mutants of a yeast telomere replication factor, Rrm3, reveals that the two proteins function in parallel to promote normal growth during times of telomere stress. Combined with previous reports, our data can be interpreted in a consistent model in which both yeast and human MUS81-dependent nucleases participate in the recovery of stalled replication forks within telomeric DNA. Furthermore, this process becomes crucial under conditions of additional replication stress, such as telomere replication in telomerase-deficient cells.

Klíčová slova:

Cell growth – DNA recombination – DNA replication – Polymerase chain reaction – Recombinant proteins – Saccharomyces cerevisiae – Telomeres – Yeast


Zdroje

1. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. 2005;19:2100–10.

2. Greider CW, Blackburn EH. The telomere terminal transferase of Tetrahymena is a ribonucleoprotein enzyme with two kinds of primer specificity. Cell. 1987;51:887–98. doi: 10.1016/0092-8674(87)90576-9 3319189

3. Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J. 1995;14:4240–8. 7556065

4. Schwartz EK, Heyer WD. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma. 2011;120:109–27. doi: 10.1007/s00412-010-0304-7 21369956

5. Wan BB, Yin JH, Horvath K, Sarkar J, Chen Y, Wu J, et al. SLX4 Assembles a Telomere Maintenance Toolkit by Bridging Multiple Endonucleases with Telomeres. Cell Reports. 2013;4:861–9. doi: 10.1016/j.celrep.2013.08.017 24012755

6. Svendsen JM, Smogorzewska A, Sowa ME, O'Connell BC, Gygi SP, Elledge SJ, et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell. 2009;138:63–77. doi: 10.1016/j.cell.2009.06.030 19596235

7. Sarkar J, Wan B, Yin J, Vallabhaneni H, Horvath K, Kulikowicz T, et al. SLX4 contributes to telomere preservation and regulated processing of telomeric joint molecule intermediates. Nucleic Acids Res. 2015;43:5912–23. doi: 10.1093/nar/gkv522 25990736

8. Verma P, Dilley RL, Zhang T, Gyparaki MT, Li Y, Greenberg RA. RAD52 and SLX4 act nonepistatically to ensure telomere stability during alternative telomere lengthening. Genes Dev. 2019;33:221–35. doi: 10.1101/gad.319723.118 30692206

9. Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A, Coulon S, et al. Human SLX4 Is a Holliday Junction Resolvase Subunit that Binds Multiple DNA Repair/Recombination Endonucleases. Cell. 2009;138:78–89. doi: 10.1016/j.cell.2009.06.029 19596236

10. Munoz IM, Hain K, Declais AC, Gardiner M, Toh GW, Sanchez-Pulido L, et al. Coordination of Structure-Specific Nucleases by Human SLX4/BTBD12 Is Required for DNA Repair. Mol Cell. 2009;35(1):116–27. doi: 10.1016/j.molcel.2009.06.020 ISI:000268003300011. 19595721

11. Castor D, Nair N, Declais AC, Lachaud C, Toth R, Macartney TJ, et al. Cooperative Control of Holliday Junction Resolution and DNA Repair by the SLX1 and MUS81-EME1 Nucleases. Mol Cell. 2013;52:221–33. doi: 10.1016/j.molcel.2013.08.036 24076219

12. Garner E, Kim Y, Lach FP, Kottemann MC, Smogorzewska A. Human GEN1 and the SLX4-Associated Nucleases MUS81 and SLX1 Are Essential for the Resolution of Replication-Induced Holliday Junctions. Cell Reports. 2013;5:207–15. doi: 10.1016/j.celrep.2013.08.041 24080495

13. Wyatt HDM, Sarbajna S, Matos J, West SC. Coordinated Actions of SLX1-SLX4 and MUS81-EME1 for Holliday Junction Resolution in Human Cells. Mol Cell. 2013;52:234–47. doi: 10.1016/j.molcel.2013.08.035 24076221

14. Zeng SC, Xiang T, Pandita TK, Gonzalez-Suarez I, Gonzalo S, Harris CC, et al. Telomere recombination requires the MUS81 endonuclease. Nature Cell Biology. 2009;11:616–23. doi: 10.1038/ncb1867 19363487

15. Yin J, Wan B, Sarkar J, Horvath K, Wu J, Chen Y, et al. Dimerization of SLX4 contributes to functioning of the SLX4-nuclease complex. Nucleic Acids Res. 2016;44:4871–80. doi: 10.1093/nar/gkw354 27131364

16. Ciccia A, McDonald N, West SC. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem. 2008;77:259–87. doi: 10.1146/annurev.biochem.77.070306.102408 18518821

17. Pepe A, West SC. Substrate specificity of the MUS81-EME2 structure selective endonuclease. Nucleic Acids Res. 2014;42:3833–45. doi: 10.1093/nar/gkt1333 24371268

18. Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics. 2001;157:103–18. 11139495

19. Boddy MN, Lopez-Girona A, Shanahan P, Interthal H, Heyer WD, Russell P. Damage tolerance protein Mus81 associates with the FHA1 domain of checkpoint kinase Cds1. Mol Cell Biol. 2000;20:8758–66. doi: 10.1128/mcb.20.23.8758-8766.2000 11073977

20. Osman F, Whitby MC. Exploring the roles of Mus81-Eme1/Mms4 at perturbed replication forks. DNA Repair (Amst). 2007;6:1004–17. doi: 10.1016/j.dnarep.2007.02.019 17409028

21. Pepe A, West SC. MUS81-EME2 Promotes Replication Fork Restart. Cell Reports. 2014;7:1048–55. doi: 10.1016/j.celrep.2014.04.007 24813886

22. Interthal H, Heyer WD. MUS81 encodes a novel Helix-hairpin-Helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol Gen Genet. 2000;263:812–27. doi: 10.1007/s004380000241 10905349

23. de los Santos T, Hunter N, Lee C, Larkin B, Loidl J, Hollingsworth NM. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics. 2003;164:81–94. 12750322

24. Dendouga N, Gao H, Moechars D, Janicot M, Vialard J, McGowan CH. Disruption of murine Mus81 increases genomic instability and DNA damage sensitivity but does not promote tumorigenesis. Mol Cell Biol. 2005;25:7569–79. doi: 10.1128/MCB.25.17.7569-7579.2005 16107704

25. Berchowitz LE, Francis KE, Bey AL, Copenhaver GP. The role of AtMUS81 in interference-insensitive crossovers in A. thaliana. PLoS Genet. 2007;3:e132. doi: 10.1371/journal.pgen.0030132 17696612

26. Holloway JK, Booth J, Edelmann W, McGowan CH, Cohen PE. MUS81 generates a subset of MLH1-MLH3-independent crossovers in mammalian meiosis. PLoS Genet. 2008;4:e1000186. doi: 10.1371/journal.pgen.1000186 18787696

27. Jessop L, Lichten M. Mus81/Mms4 endonuclease and sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol Cell. 2008;31:313–23. doi: 10.1016/j.molcel.2008.05.021 18691964

28. Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N. RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol Cell. 2008;31:324–36. doi: 10.1016/j.molcel.2008.07.006 18691965

29. Ho CK, Mazón G, Lam AF, Symington LS. Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol Cell. 2010;40:988–1000. doi: 10.1016/j.molcel.2010.11.016 21172663

30. De Muyt A, Jessop L, Kolar E, Sourirajan A, Chen JH, Dayani Y, et al. BLM Helicase Ortholog Sgs1 Is a Central Regulator of Meiotic Recombination Intermediate Metabolism. Mol Cell. 2012;46:43–53. doi: 10.1016/j.molcel.2012.02.020 22500736

31. Zakharyevich K, Tang SM, Ma YM, Hunter N. Delineation of Joint Molecule Resolution Pathways in Meiosis Identifies a Crossover-Specific Resolvase. Cell. 2012;149:334–47. doi: 10.1016/j.cell.2012.03.023 22500800

32. Kaliraman V, Mullen JR, Fricke WM, Bastin-Shanower, Brill SJ. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 2001;15:2730–40. doi: 10.1101/gad.932201 11641278

33. Fabre F, Chan A, Heyer WD, Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc Natl Acad Sci USA. 2002;99:16887–92. doi: 10.1073/pnas.252652399 12475932

34. Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol Cell Biol. 2003;23:3487–96. doi: 10.1128/mcb.23.10.3487-3496.2003 12724407

35. Minocherhomji S, Ying S, Bjerregaard VA, Bursomanno S, Aleliunaite A, Wu W, et al. Replication stress activates DNA repair synthesis in mitosis. Nature. 2015;528:286–90. doi: 10.1038/nature16139 26633632

36. Bhowmick R, Minocherhomji S, Hickson ID. RAD52 Facilitates Mitotic DNA Synthesis Following Replication Stress. Mol Cell. 2016;64:1117–26. doi: 10.1016/j.molcel.2016.10.037 27984745

37. Di Marco S, Hasanova Z, Kanagaraj R, Chappidi N, Altmannova V, Menon S, et al. RECQ5 Helicase Cooperates with MUS81 Endonuclease in Processing Stalled Replication Forks at Common Fragile Sites during Mitosis. Mol Cell. 2017;66:658–71. doi: 10.1016/j.molcel.2017.05.006 28575661

38. Spardy N, Duensing A, Hoskins EE, Wells SI, Duensing S. HPV-16 E7 reveals a link between DNA replication stress, fanconi anemia D2 protein, and alternative lengthening of telomere-associated promyelocytic leukemia bodies. Cancer Res. 2008;68:9954–63. doi: 10.1158/0008-5472.CAN-08-0224 19047177

39. Saint-Leger A, Koelblen M, Civitelli L, Bah A, Djerbi N, Giraud-Panis MJ, et al. The basic N-terminal domain of TRF2 limits recombination endonuclease action at human telomeres. Cell Cycle. 2014;13:2469–79. doi: 10.4161/cc.29422 25483196

40. Mosig G. Recombination and recombination-dependent DNA replication in bacteriophage T4. Annu Rev Genet. 1998;32:379–413. doi: 10.1146/annurev.genet.32.1.379 9928485

41. Formosa T, Alberts BM. DNA synthesis dependent on genetic recombination: Characterization of a reaction catalyzed by purified bacteriophage T4 proteins. Cell. 1986;47:793–806. doi: 10.1016/0092-8674(86)90522-2 3022939

42. Asai T, Sommer S, Bailone A, Kogoma T. Homologous Recombination-Dependent Initiation of DNA Replication from DNA Damage-Inducible Origins in Escherichia-Coli. EMBO J. 1993;12:3287–95. 8344265

43. Malkova A, Ivanov EL, Haber JE. Double-strand break repair in the absence of RAD51 in yeast: A possible role for break-induced DNA replication. Proc Natl Acad Sci USA. 1996;93:7131–6. doi: 10.1073/pnas.93.14.7131 8692957

44. Pâques F, Haber JE. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1999;63:349–404. 10357855

45. McEachern MJ, Haber JE. Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem. 2006;75:111–35. doi: 10.1146/annurev.biochem.74.082803.133234 16756487

46. Anand RP, Lovett ST, Haber JE. Break-Induced DNA Replication. Cold Spring Harbor Perspectives in Biology. 2013;5:a010397. doi: 10.1101/cshperspect.a010397 23881940

47. Dunham MA, Neumann AA, Fasching CL, Reddel RR. Telomere maintenance by recombination in human cells. Nat Genet. 2000;26(4):447–50. doi: 10.1038/82586 11101843

48. Wang RC, Smogorzewska A, de Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell. 2004;119:355–68. doi: 10.1016/j.cell.2004.10.011 15507207

49. Lundblad V, Blackburn EH. An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell. 1993;73:347–60. doi: 10.1016/0092-8674(93)90234-h 8477448

50. Teng SC, Zakian VA. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol. 1999;19:8083–93. doi: 10.1128/mcb.19.12.8083 10567534

51. Le S, Moore JK, Haber JE, Greider CW. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics. 1999;152:143–52. 10224249

52. Chen Q, Ijpma A, Greider CW. Two survivor pathways that allow growth in the absence of telomerase are geenrated by distinct telomere recombination events. Mol Cell Biol. 2001;21:1819–27. doi: 10.1128/MCB.21.5.1819-1827.2001 11238918

53. Stafa A, Donnianni RA, Timashev LA, Lam AF, Symington LS. Template switching during break-induced replication is promoted by the Mph1 helicase in Saccharomyces cerevisiae. Genetics. 2014;196:1017–28. doi: 10.1534/genetics.114.162297 24496010

54. Misino S, Bonetti D, Luke-Glaser S, Luke B. Increased TERRA levels and RNase H sensitivity are conserved hallmarks of post-senescent survivors in budding yeast. Differentiation. 2018;100:37–45. doi: 10.1016/j.diff.2018.02.002 29494831

55. Lundblad V, Szostak JW. A mutant with a defect in telomere elongation leads to senescence in yeast Cell. 1989;57:633–43. doi: 10.1016/0092-8674(89)90132-3 2655926

56. Lendvay TS, Morris DK, Sah J, Balasubramanian B, Lundblad V. Senescence mutants of Saccharomyces cerevisiae with a defect in telomere replication identify three additional EST genes. Genetics. 1996;144:1399–412. 8978029

57. Singer MS, Gottschling DE. TLC1: Template RNA component of Saccharomyces cerevisiae telomerase. Science. 1994;266:404–9. doi: 10.1126/science.7545955 7545955

58. Ehmsen KT, Heyer WD. Saccharomyces cerevisiae Mus81-Mms4 is a catalytic structure-selective endonuclease. Nucleic Acids Res. 2008;36:2182–95. doi: 10.1093/nar/gkm1152 18281703

59. Wilson JSJ, Tejera AM, Castor D, Toth R, Blasco MA, Rouse J. Localization-Dependent and -Independent Roles of SLX4 in Regulating Telomeres. Cell Reports. 2013;4:853–60. doi: 10.1016/j.celrep.2013.07.033 23994477

60. Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, et al. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol. 2007;14:1096–104. doi: 10.1038/nsmb1313 17934473

61. Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes Dev. 1994;8:2401–15. doi: 10.1101/gad.8.20.2401 7958905

62. Bianchi A, Negrini S, Shore D. Delivery of yeast telomerase to a DNA break depends on the recruitment functions of Cdc13 and Est1. Mol Cell. 2004;16:139–46. doi: 10.1016/j.molcel.2004.09.009 15469829

63. Qi H, Zakian VA. The Saccharomyces telomere-binding protein Cdc13p interacts with both the catalytic subunit of DNA polymerase alpha and the telomerase-associated est1 protein. Genes Dev. 2000;14:1777–88. 10898792

64. Chandra A, Hughes TR, Nugent CI, Lundblad V. Cdc13 both positively and negatively regulates telomere replication. Genes Dev. 2001;15:404–14. doi: 10.1101/gad.861001 11230149

65. Paschini M, Toro TB, Lubin JW, Braunstein-Ballew B, Morris DK, Lundblad V. A naturally thermolabile activity compromises genetic analysis of telomere function in Saccharomyces cerevisiae. Genetics. 2012;191:79–93. PMC3338272. doi: 10.1534/genetics.111.137869 22377634

66. Ivessa AS, Zhou JQ, Schulz VP, Monson EK, Zakian VA. Saccharomyces Rrm3p, a 5' to 3' DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 2002;16:1383–96. doi: 10.1101/gad.982902 12050116

67. Azam M, Lee JY, Abraham V, Chanoux R, Schoenly KA, Johnson FB. Evidence that the S.cerevisiae Sgs1 protein facilitates recombinational repair of telomeres during senescence. Nucleic Acids Res. 2006;34:506–16. doi: 10.1093/nar/gkj452 16428246

68. Makovets S, Herskowitz I, Blackburn EH. Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol Cell Biol. 2004;24(9):4019–31. Epub 2004/04/15. PubMed Central PMCID: PMC387773. doi: 10.1128/mcb.24.9.4019-4031.2004 15082794

69. Fallet E, Jolivet P, Soudet J, Lisby M, Gilson E, Teixeira MT. Length-dependent processing of telomeres in the absence of telomerase. Nucleic Acids Res. 2014;42:3648–65. doi: 10.1093/nar/gkt1328 24393774

70. Greider CW, Blackburn EH. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989;337:331–7. doi: 10.1038/337331a0 2463488

71. Blastyak A, Pinter L, Unk I, Prakash L, Prakash S, Haracska L. Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol Cell. 2007;28:167–75. doi: 10.1016/j.molcel.2007.07.030 17936713

72. Ii M, Brill SJ. Roles of SGS1, MUS81, and RAD51 in the repair of lagging-strand replication defects in Saccharomyces cerevisiae. Curr Genet. 2005;48:213–25. doi: 10.1007/s00294-005-0014-5 16193328

73. Olivier M, Da Ines O, Amiard S, Serra H, Goubely C, White CI, et al. The Structure-Specific Endonucleases MUS81 and SEND1 Are Essential for Telomere Stability in Arabidopsis. Plant Cell. 2016;28:74–86. doi: 10.1105/tpc.15.00898 26704385

74. Gilson E, Geli V. How telomeres are replicated. Nature Rev Mol Cell Biol. 2007;8:825–38.

75. Ozer O, Bhowmick R, Liu Y, Hickson ID. Human cancer cells utilize mitotic DNA synthesis to resist replication stress at telomeres regardless of their telomere maintenance mechanism. Oncotarget. 2018;9:15836–46. doi: 10.18632/oncotarget.24745 29662610

76. Ohki R, Ishikawa F. Telomere-bound TRF1 and TRF2 stall the replication fork at telomeric repeats. Nucleic Acids Res. 2004;32:1627–37. doi: 10.1093/nar/gkh309 15007108

77. Fouche N, Ozgur S, Roy D, Griffith JD. Replication fork regression in repetitive DNAs. Nucleic Acids Res. 2006;34:6044–50. doi: 10.1093/nar/gkl757 17071963

78. Verdun RE, Karlseder J. The DNA damage machinery and homologous recombination pathway act consecutively to protect human telomeres. Cell. 2006;127:709–20. doi: 10.1016/j.cell.2006.09.034 17110331

79. Tacconi EM, Tarsounas M. How homologous recombination maintains telomere integrity. Chromosoma. 2015;124:119–30. doi: 10.1007/s00412-014-0497-2 25430998

80. Kai M, Boddy MN, Russell P, Wang TSF. Replication checkpoint kinase Cds1 regulates Mus81 to reserve genome integrity during replication stress. Genes Dev. 2005;19:919–32. doi: 10.1101/gad.1304305 15805465

81. Roseaulin L, Yamada Y, Tsutsui Y, Russell P, Iwasaki H, Arcangioli B. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J. 2008;27:1378–87. doi: 10.1038/emboj.2008.65 18388861

82. Simon MN, Churikov D, Geli V. Replication stress as a source of telomere recombination during replicative senescence in Saccharomyces cerevisiae. FEMS Yeast Res. 2016;16:10.1093.

83. Grandin N, Charbonneau M. 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. 2007;277:685–99. doi: 10.1007/s00438-007-0218-0 17323081

84. Hackett JA, Feldser DM, Greider CW. Telomere dysfunction increases mutation rate and genomic instability. Cell. 2001;106:275–86. doi: 10.1016/s0092-8674(01)00457-3 11509177

85. Hackett JA, Greider CW. End resection initiates genomic instability in the absence of telomerase. Mol Cell Biol. 2003;23\:8450–61. doi: 10.1128/mcb.23.23.8450-8461.2003 14612391

86. Garvik B, Carson M, Hartwell L. Single-stranded DNA arising at telomeres in cdc13 mutants may constitute a specific signal for the RAD9 checkpoint. Mol Cell Biol. 1995;15:6128–38. doi: 10.1128/mcb.15.11.6128 7565765

87. Grandin N, Damon C, Charbonneau M. Cdc13 prevents telomere uncapping and Rad50-dependent homologous recombination. Embo J. 2001;20:6127–39. doi: 10.1093/emboj/20.21.6127 11689452

88. Xu Z, Fallet E, Paoletti C, Fehrmann S, Charvin G, Teixeira MT. Two routes to senescence revealed by real-time analysis of telomerase-negative single lineages. Nat Commun. 2015;6:7680. doi: 10.1038/ncomms8680 26158780

89. Coutelier H, Xu Z, Morisse MC, Lhuillier-Akakpo M, Pelet S, Charvin G, et al. Adaptation to DNA damage checkpoint in senescent telomerase-negative cells promotes genome instability. Genes Dev. 2018;32:1499–513. doi: 10.1101/gad.318485.118 30463903

90. Abdallah P, Luciano P, Runge KW, Lisby M, Geli V, Gilson E, et al. A two-step model for senescence triggered by a single critically short telomere. Nature Cell Biol. 2009;11:988–93. doi: 10.1038/ncb1911 19597486

91. Crabbe L, Verdun RE, Haggblom CI, Karlseder J. Defective telomere lagging strand synthesis in cells lacking WRN helicase activity. 2004;306:1951–3.

92. Gao H, Chen XB, McGowan CH. Mus81 endonuclease localizes to nucleoli and to regions of DNA damage in human S-phase cells. Mol Biol Cell. 2003;14:4826–34. doi: 10.1091/mbc.e03-05-0276 14638871

93. Franchitto A, Pirzio LM, Prosperi E, Sapora O, Bignami M, Pichierri P. Replication fork stalling in WRN-deficient cells is overcome by prompt activation of a MUS81-dependent pathway. J Cell Biol. 2008; 183:241–52. doi: 10.1083/jcb.200803173 18852298

94. Schwartz EK, Wright WD, Ehmsen KT, Evans JE, Stahlberg H, Heyer WD. Mus81-Mms4 Functions as a Single Heterodimer To Cleave Nicked Intermediates in Recombinational DNA Repair. Mol Cell Biol. 2012;32:3065–80. doi: 10.1128/MCB.00547-12 22645308

95. Ii M, Ii T, Brill SJ. Mus81 functions in the quality control of replication forks at the rDNA and is involved in the maintenance of rDNA repeat number in Saccharomyces cerevisiae. Mutation Research. 2007;625(1–2):1–19. doi: 10.1016/j.mrfmmm.2007.04.007 17555773

96. Coulon S, Gaillard PHL, Chahwan C, McDonald WH, Yates JR, Russell P. Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol Biol Cell. 2004;15:71–80. doi: 10.1091/mbc.e03-08-0586 14528010

97. Ying SM, Minocherhomji S, Chan KL, Palmai-Pallag T, Chu WK, Wass T, et al. MUS81 promotes common fragile site expression. Nature Cell Biol. 2013;15:1001–7. doi: 10.1038/ncb2773 23811685

98. Naim V, Wilhelm T, Debatisse M, Rosselli F. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nature Cell Biology. 2013;15:1008–15. doi: 10.1038/ncb2793 23811686

99. Pellicioli A, Muzi-Falconi M. A blooming resolvase at chromosomal fragile sites. Nature Cell Biology. 2013;15:883–5. doi: 10.1038/ncb2812 23907189

100. Minocherhomji S, Hickson ID. Structure-specific endonucleases: guardians of fragile site stability. Trends Cell Biol. 2014;24:321–7. doi: 10.1016/j.tcb.2013.11.007 24361091

101. Chan KL, Palmai-Pallag T, Ying SM, Hickson ID. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nature Cell Biology. 2009;11:753–60. doi: 10.1038/ncb1882 19465922

102. Arlt MF, Casper AM, Glover TM. Common fagile sites. Cytogenet Genome Res. 2003;100:92–100. doi: 10.1159/000072843 14526169

103. Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet. 2007;41:169–92. doi: 10.1146/annurev.genet.41.042007.165900 17608616

104. Zeng SC, Yang Q. The MUS81 endonuclease is essential for telomerase negative cell proliferation. Cell Cycle. 2009;8:2157–60. P doi: 10.4161/cc.8.14.9149 19617716

105. Meyer DH, Bailis AM. Telomerase Deficiency Affects the Formation of Chromosomal Translocations by Homologous Recombination in Saccharomyces cerevisiae. Plos One. 2008;3:e3318. doi: 10.1371/journal.pone.0003318 18830407

106. Singer MS, Kahana A, Wolf AJ, Meisinger LL, Peterson SE, Goggin C, et al. Identification of high-copy disrupters of telomeric silencing in Saccharomyces cerevisiae. Genetics. 1998;150:613–32. 9755194

107. Herzberg K, Bashkirov VI, Rolfsmeier M, Haghnazari E, McDonald WH, Anderson S, et al. Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Mol Cell Biol. 2006;26:8396–409. doi: 10.1128/MCB.01317-06 16966380

108. Tsukamoto Y, Taggart AKP, Zakian VA. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr Biol. 2001;11:1328–35. doi: 10.1016/s0960-9822(01)00372-4 11553325

109. Torres JZ, Schnakenberg SL, Zakian VA. Saccharomyces cerevisiae rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: Viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol Cell Biol. 2004;24:3198–212. doi: 10.1128/mcb.24.8.3198-3212.2004 15060144

110. Pasero P, Vindigni A. Nucleases Acting at Stalled Forks: How to Reboot the Replication Program with a Few Shortcuts. Annu Rev Genet. 2017;51:477–99. doi: 10.1146/annurev-genet-120116-024745 29178820


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