Multiple Rad52-Mediated Homology-Directed Repair Mechanisms Are Required to Prevent Telomere Attrition-Induced Senescence in Saccharomyces cerevisiae

PLoS Genetics

Volumn 12, Issue 7, 2016, Pages

  Claussin, Clémence ^a   Chang, Michael ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; LYSINE; RAD52 PROTEIN; HISTONE; RAD52 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; TELOMERASE;

ARTICLE; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; FUNGAL GENE; GENE MUTATION; GENETIC RECOMBINATION; HISTONE ACETYLATION; HOMOLOGY DIRECTED REPAIR; NONHUMAN; PROTEIN FUNCTION; RAD52 GENE; SACCHAROMYCES CEREVISIAE; SENESCENCE; SEPARATION OF FUNCTION MUTATION; SISTER CHROMATID; TELOMERE ATTRITION INDUCED SENESCENCE; TELOMERE HOMEOSTASIS; CHEMISTRY; CHROMATID; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MUTATION; PLASMID; POLYMERASE CHAIN REACTION; SISTER CHROMATID EXCHANGE; TELOMERE; ULTRASTRUCTURE;

CHROMATIDS; DNA REPAIR; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; LYSINE; MICROSCOPY, FLUORESCENCE; MUTATION; PLASMIDS; POLYMERASE CHAIN REACTION; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SISTER CHROMATID EXCHANGE; TELOMERASE; TELOMERE;

EID: 84982802688     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1006176     Document Type: Article

References (79)

1. Jain D, Cooper JP, Telomeric strategies: means to an end. Annu Rev Genet. 2010;44:243–69. Epub 2010/11/05. doi: 10.1146/annurev-genet-102108-13484121047259
2. Greider CW, Blackburn EH, A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis. Nature. 1989;337(6205):331–7. doi: 10.1038/337331a02463488
3. Lingner J, Hughes TR, Shevchenko A, Mann M, Lundblad V, Cech TR, Reverse transcriptase motifs in the catalytic subunit of telomerase. Science. 1997;276(5312):561–7. doi: 10.1126/science.276.5312.5619110970
4. Yu GL, Bradley JD, Attardi LD, Blackburn EH, In vivo alteration of telomere sequences and senescence caused by mutated Tetrahymena telomerase RNAs. Nature. 1990;344(6262):126–32. doi: 10.1038/344126a01689810
5. Singer MS, Gottschling DE, TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science. 1994;266(5184):404–9. doi: 10.1126/science.75459557545955
6. Artandi SE, DePinho RA, Telomeres and telomerase in cancer. Carcinogenesis. 2010;31(1):9–18. Epub 2009/11/06. doi: 10.1093/carcin/bgp26819887512
7. Shay JW, Bacchetti S, A survey of telomerase activity in human cancer. Eur J Cancer. 1997;33(5):787–91. doi: 10.1016/S0959-8049(97)00062-29282118
8. Bryan TM, Englezou A, Dalla-Pozza L, Dunham MA, Reddel RR, Evidence for an alternative mechanism for maintaining telomere length in human tumors and tumor-derived cell lines. Nat Med. 1997;3(11):1271–4. Epub 1997/11/14. doi: 10.1038/nm1197-12719359704
9. Lundblad V, Blackburn EH, An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell. 1993;73(2):347–60. Epub 1993/04/23. doi: 10.1016/0092-8674(93)90234-H8477448
10. Lydeard JR, Jain S, Yamaguchi M, Haber JE, Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature. 2007;448(7155):820–3. Epub 2007/08/03. doi: 10.1038/nature0604717671506
11. Symington LS, Rothstein R, Lisby M, Mechanisms and Regulation of Mitotic Recombination in Saccharomyces cerevisiae. Genetics. 2014;198(3):795–835. doi: 10.1534/genetics.114.16614025381364
12. Chen Q, Ijpma A, Greider CW, Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol Cell Biol. 2001;21(5):1819–27. doi: 10.1128/MCB.21.5.1819–1827.200111238918
13. Teng SC, Chang J, McCowan B, Zakian VA, Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol Cell. 2000;6(4):947–52. doi: 10.1016/s1097-2765(05)00094-811090632
14. Huang P, Pryde FE, Lester D, Maddison RL, Borts RH, Hickson ID, et al. SGS1 is required for telomere elongation in the absence of telomerase. Curr Biol. 2001;11(2):125–9. doi: 10.1016/s0960-9822(01)00021-511231130
15. Johnson FB, Marciniak RA, McVey M, Stewart SA, Hahn WC, Guarente L, The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J. 2001;20(4):905–13. doi: 10.1093/emboj/20.4.90511179234
16. Davis AP, Symington LS, RAD51-dependent break-induced replication in yeast. Mol Cell Biol. 2004;24(6):2344–51. doi: 10.1128/mcb.24.6.2344–2351.200414993274
17. Signon L, Malkova A, Naylor ML, Klein H, Haber JE, Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol Cell Biol. 2001;21(6):2048–56. doi: 10.1128/MCB.21.6.2048–2056.200111238940
18. Claussin C, Chang M, The many facets of homologous recombination at telomeres. Microbial Cell. 2015;2(9):308–21. doi: 10.15698/mic2015.09.224
19. Khadaroo B, Teixeira MT, Luciano P, Eckert-Boulet N, Germann SM, Simon MN, et al. The DNA damage response at eroded telomeres and tethering to the nuclear pore complex. Nat Cell Biol. 2009;11(8):980–7. doi: 10.1038/ncb191019597487
20. 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(1):143–52. 10224249
21. Churikov D, Charifi F, Simon MN, Geli V, Rad59-facilitated acquisition of Y' elements by short telomeres delays the onset of senescence. PLoS Genet. 2014;10(11):e1004736. doi: 10.1371/journal.pgen.100473625375789
22. 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(6):3648–65. doi: 10.1093/nar/gkt132824393774
23. 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/ncomms868026158780
24. Lee JY, Kozak M, Martin JD, Pennock E, Johnson FB, Evidence that a RecQ helicase slows senescence by resolving recombining telomeres. PLoS Biol. 2007;5(6):e160. doi: 10.1371/journal.pbio.005016017550308
25. Sung P, Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J Biol Chem. 1997;272(45):28194–7. 9353267
26. New JH, Sugiyama T, Zaitseva E, Kowalczykowski SC, Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature. 1998;391(6665):407–10. doi: 10.1038/349509450760
27. Petukhova G, Stratton SA, Sung P, Single strand DNA binding and annealing activities in the yeast recombination factor Rad59. J Biol Chem. 1999;274(48):33839–42. 10567339
28. Davis AP, Symington LS, The yeast recombinational repair protein Rad59 interacts with Rad52 and stimulates single-strand annealing. Genetics. 2001;159(2):515–25. 11606529
29. Wu Y, Sugiyama T, Kowalczykowski SC, DNA annealing mediated by Rad52 and Rad59 proteins. J Biol Chem. 2006;281(22):15441–9. doi: 10.1074/jbc.M60182720016565518
30. Mortensen UH, Erdeniz N, Feng Q, Rothstein R, A molecular genetic dissection of the evolutionarily conserved N terminus of yeast Rad52. Genetics. 2002;161(2):549–62. 12072453
31. Shi I, Hallwyl SC, Seong C, Mortensen U, Rothstein R, Sung P, Role of the Rad52 amino-terminal DNA binding activity in DNA strand capture in homologous recombination. J Biol Chem. 2009;284(48):33275–84. doi: 10.1074/jbc.M109.05775219812039
32. Lettier G, Feng Q, de Mayolo AA, Erdeniz N, Reid RJ, Lisby M, et al. The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet. 2006;2(11):e194. doi: 10.1371/journal.pgen.002019417096599
33. Munoz-Galvan S, Jimeno S, Rothstein R, Aguilera A, Histone H3K56 acetylation, Rad52, and non-DNA repair factors control double-strand break repair choice with the sister chromatid. PLoS Genet. 2013;9(1):e1003237. doi: 10.1371/journal.pgen.100323723357952
34. Teixeira MT, Arneric M, Sperisen P, Lingner J, Telomere length homeostasis is achieved via a switch between telomerase- extendible and -nonextendible states. Cell. 2004;117(3):323–35. doi: 10.1016/S0092-8674(04)00334-415109493
35. 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. Nat Cell Biol. 2009;11(8):988–93. doi: 10.1038/ncb191119597486
36. Kozak ML, Chavez A, Dang W, Berger SL, Ashok A, Guo X, et al. Inactivation of the Sas2 histone acetyltransferase delays senescence driven by telomere dysfunction. EMBO J. 2010;29(1):158–70. doi: 10.1038/emboj.2009.31419875981
37. Chang M, Dittmar JC, Rothstein R, Long telomeres are preferentially extended during recombination-mediated telomere maintenance. Nat Struct Mol Biol. 2011;18(4):451–6. doi: 10.1038/nsmb.203421441915
38. Pfeiffer V, Crittin J, Grolimund L, Lingner J, The THO complex component Thp2 counteracts telomeric R-loops and telomere shortening. EMBO J. 2013;32(21):2861–71. doi: 10.1038/emboj.2013.21724084588
39. Balk B, Maicher A, Dees M, Klermund J, Luke-Glaser S, Bender K, et al. Telomeric RNA-DNA hybrids affect telomere-length dynamics and senescence. Nat Struct Mol Biol. 2013;20(10):1199–205. doi: 10.1038/nsmb.266224013207
40. Balk B, Dees M, Bender K, Luke B, The differential processing of telomeres in response to increased telomeric transcription and RNA-DNA hybrid accumulation. RNA Biol. 2014;11(2):95–100. doi: 10.4161/rna.2779824525824
41. Fu XH, Duan YM, Liu YT, Cai C, Meng FL, Zhou JQ, Telomere recombination preferentially occurs at short telomeres in telomerase-null type II survivors. PLoS One. 2014;9(3):e90644. doi: 10.1371/journal.pone.009064424594632
42. Peng J, He MH, Duan YM, Liu YT, Zhou JQ, Inhibition of telomere recombination by inactivation of KEOPS subunit Cgi121 promotes cell longevity. PLoS Genet. 2015;11(3):e1005071. doi: 10.1371/journal.pgen.100507125822194
43. Förstemann K, Lingner J, Molecular basis for telomere repeat divergence in budding yeast. Mol Cell Biol. 2001;21(21):7277–86. doi: 10.1128/MCB.21.21.7277–7286.200111585910
44. Wang SS, Zakian VA, Sequencing of Saccharomyces telomeres cloned using T4 DNA polymerase reveals two domains. Mol Cell Biol. 1990;10(8):4415–9. doi: 10.1128/MCB.10.8.44152196453
45. Förstemann K, Hoss M, Lingner J, Telomerase-dependent repeat divergence at the 3' ends of yeast telomeres. Nucleic Acids Res. 2000;28(14):2690–4. doi: 10.1093/nar/28.14.269010908324
46. Tong AH, Lesage G, Bader GD, Ding H, Xu H, Xin X, et al. Global mapping of the yeast genetic interaction network. Science. 2004;303(5659):808–13. doi: 10.1126/science.109131714764870
47. Hanna M, Ball LG, Tong AH, Boone C, Xiao W, Pol32 is required for Pol zeta-dependent translesion synthesis and prevents double-strand breaks at the replication fork. Mutat Res. 2007;625(1–2):164–76. doi: 10.1016/j.mrfmmm.2007.06.00817681555
48. Huang ME, Rio AG, Nicolas A, Kolodner RD, A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations. Proc Natl Acad Sci U S A. 2003;100(20):11529–34. doi: 10.1073/pnas.203501810012972632
49. Chang M, Arneric M, Lingner J, Telomerase repeat addition processivity is increased at critically short telomeres in a Tel1-dependent manner in Saccharomyces cerevisiae. Genes Dev. 2007;21(19):2485–94. doi: 10.1101/gad.158880717908934
50. Xu Z, Duc KD, Holcman D, Teixeira MT, The length of the shortest telomere as the major determinant of the onset of replicative senescence. Genetics. 2013;194(4):847–57. doi: 10.1534/genetics.113.15232223733785
51. Marcand S, Brevet V, Gilson E, Progressive cis-inhibition of telomerase upon telomere elongation. EMBO J. 1999;18(12):3509–19. 10369690
52. Teng SC, Zakian VA, Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol. 1999;19(12):8083–93. 10567534
53. Coïc E, Feldman T, Landman AS, Haber JE, Mechanisms of Rad52-independent spontaneous and UV-induced mitotic recombination in Saccharomyces cerevisiae. Genetics. 2008;179(1):199–211. Epub 2008/05/07. doi: 10.1534/genetics.108.08718918458103
54. Pannunzio NR, Manthey GM, Bailis AM, RAD59 is required for efficient repair of simultaneous double-strand breaks resulting in translocations in Saccharomyces cerevisiae. DNA Repair (Amst). 2008;7(5):788–800. doi: 10.1016/j.dnarep.2008.02.003
55. Pannunzio NR, Manthey GM, Liddell LC, Fu BX, Roberts CM, Bailis AM, Rad59 regulates association of Rad52 with DNA double-strand breaks. Microbiologyopen. 2012;1(3):285–97. doi: 10.1002/mbo3.3123170228
56. Xu X, Blackwell S, Lin A, Li F, Qin Z, Xiao W, Error-free DNA-damage tolerance in Saccharomyces cerevisiae. Mutat Res Rev Mutat Res. 2015;764:43–50. doi: 10.1016/j.mrrev.2015.02.00126041265
57. Ball LG, Zhang K, Cobb JA, Boone C, Xiao W, The yeast Shu complex couples error-free post-replication repair to homologous recombination. Mol Microbiol. 2009;73(1):89–102. doi: 10.1111/j.1365-2958.2009.06748.x19496932
58. Gangavarapu V, Prakash S, Prakash L, Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol Cell Biol. 2007;27(21):7758–64. doi: 10.1128/MCB.01331-0717785441
59. Schneider J, Bajwa P, Johnson FC, Bhaumik SR, Shilatifard A, Rtt109 is required for proper H3K56 acetylation: a chromatin mark associated with the elongating RNA polymerase II. J Biol Chem. 2006;281(49):37270–4. doi: 10.1074/jbc.C60026520017046836
60. Driscoll R, Hudson A, Jackson SP, Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science. 2007;315(5812):649–52. doi: 10.1126/science.113586217272722
61. Han J, Zhou H, Horazdovsky B, Zhang K, Xu RM, Zhang Z, Rtt109 acetylates histone H3 lysine 56 and functions in DNA replication. Science. 2007;315(5812):653–5. doi: 10.1126/science.113323417272723
62. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, Boeke JD, et al. The sirtuins Hst3 and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr Biol. 2006;16(13):1280–9. doi: 10.1016/j.cub.2006.06.02316815704
63. Maas NL, Miller KM, DeFazio LG, Toczyski DP, Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell. 2006;23(1):109–19. doi: 10.1016/j.molcel.2006.06.00616818235
64. Celic I, Verreault A, Boeke JD, Histone H3 K56 hyperacetylation perturbs replisomes and causes DNA damage. Genetics. 2008;179(4):1769–84. doi: 10.1534/genetics.108.08891418579506
65. Pan X, Ye P, Yuan DS, Wang X, Bader JS, Boeke JD, A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell. 2006;124(5):1069–81. doi: 10.1016/j.cell.2005.12.03616487579
66. Lee JY KM, Martin JD, Pennock E, Johnson FB, Evidence that a RecQ helicase slows senescence by resolving recombining telomeres. PLoS Biol. 2007.
67. 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(8):3198–212. 15060144
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. 15082794
69. van Mourik PM, de Jong J, Agpalo D, Claussin C, Rothstein R, Chang M, Recombination-Mediated Telomere Maintenance in Saccharomyces cerevisiae Is Not Dependent on the Shu Complex. PLoS One. 2016. doi: 10.1371/journal.pone.0151314
70. Cusanelli E, Romero CA, Chartrand P, Telomeric noncoding RNA TERRA is induced by telomere shortening to nucleate telomerase molecules at short telomeres. Mol Cell. 2013;51(6):780–91. doi: 10.1016/j.molcel.2013.08.02924074956
71. Liu J, Heyer WD, Who's who in human recombination: BRCA2 and RAD52. Proc Natl Acad Sci U S A. 2011;108(2):441–2. doi: 10.1073/pnas.101661410821189297
72. Badie S, Escandell JM, Bouwman P, Carlos AR, Thanasoula M, Gallardo MM, et al. BRCA2 acts as a RAD51 loader to facilitate telomere replication and capping. Nat Struct Mol Biol. 2010;17(12):1461–9. doi: 10.1038/nsmb.194321076401
73. Zimmer J, Tacconi EM, Folio C, Badie S, Porru M, Klare K, et al. Targeting BRCA1 and BRCA2 Deficiencies with G-Quadruplex-Interacting Compounds. Mol Cell. 2015. doi: 10.1016/j.molcel.2015.12.004
74. Treco DA, Lundblad V, Preparation of yeast media. Curr Protoc Mol Biol. 2001;Chapter 13:Unit13 1. doi: 10.1002/0471142727.mb1301s23
75. Sherman F, Getting started with yeast. Methods Enzymol. 2002;350:3–41. 12073320
76. Thomas BJ, Rothstein R, Elevated recombination rates in transcriptionally active DNA. Cell. 1989;56(4):619–30. 2645056
77. Zhao X, Muller EG, Rothstein R, A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell. 1998;2(3):329–40. 9774971
78. Gupta A, Sharma S, Reichenbach P, Marjavaara L, Nilsson AK, Lingner J, et al. Telomere length homeostasis responds to changes in intracellular dNTP pools. Genetics. 2013;193(4):1095–105. doi: 10.1534/genetics.112.14912023335335
79. Chang M, Rothstein R, Rif1/2 and Tel1 function in separate pathways during replicative senescence. Cell Cycle. 2011;10(21):3798–9. Epub 2011/10/29. doi: 10.4161/cc.10.21.1809522033189