The DNA damage response pathway contributes to the stability of chromosome III derivatives lacking efficient replicators

PLoS Genetics

Volumn 6, Issue 12, 2010, Pages 1-14

  Theis, James F ^a   Irene, Carmela ^a   Dershowitz, Ann ^a   Brost, Renee L ^b   Tobin, Michael L ^a   di Sanzo, Fabiana M ^a   Wang, Jian Ying ^a   Boone, Charles ^b   Newlon, Carol S ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; DNA; DNA FRAGMENT; HYDROXYUREA; PROTEIN KINASE; PROTEIN RAD9; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CELLULAR STRESS SIGNAL; CHROMOSOMAL INSTABILITY; CHROMOSOME; CHROMOSOME 3; CONTROLLED STUDY; DNA DAMAGE; DNA MICROARRAY; DNA REPAIR; DNA REPLICATION; DNA REPLICATION ORIGIN; DNA TEMPLATE; ENZYMOLOGY; GENE DELETION; GENE IDENTIFICATION; GENETIC SCREENING; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; NONHUMAN; PROTEIN DEPLETION; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION; WILD TYPE;

CHROMOSOMAL INSTABILITY; CHROMOSOMES, FUNGAL; DNA DAMAGE; DNA REPLICATION; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN KINASES; REPLICATION ORIGIN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 78650693977     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001227     Document Type: Article

References (94)

1. Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71: 333-374.
2. Newlon CS, Burke WG (1980) Replication of small chromosomal DNAs in yeast. In: Alberts B, Fox CF, eds. Mechanistic Studies of DNA Replication and Recombination. NY: Academic Press. pp 339-409.
3. Feng W, Collingwood D, Boeck ME, Fox LA, Alvino GM, et al. (2006) Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat Cell Biol 8: 148-155.
4. Raghuraman MK, Winzeler EA, Collingwood D, Hunt S, Wodicka L, et al. (2001) Replication dynamics of the yeast genome. Science 294: 115-121.
5. Patel PK, Arcangioli B, Baker SP, Bensimon A, Rhind N (2006) DNA replication origins fire stochastically in fission yeast. Mol Biol Cell 17: 308-316.
6. Donaldson AD, Raghuraman MK, Friedman KL, Cross FR, Brewer BJ, et al. (1998) CLB5-dependent activation of late replication origins in S. cerevisiae. Mol Cell 2: 173-182.
7. Ferguson BM, Brewer BJ, Fangman WL (1991) Temporal control of DNA replication in yeast. Cold Spring Harbor Symp Quant Biol 56: 293-302.
8. Friedman KL, Brewer BJ, Fangman WL (1997) Replication profile of Saccharomyces cerevisiae chromosome VI. Genes Cells 2: 667-678.
9. McCarroll RM, Fangman WL (1988) Time of replication of yeast centromeres and telomeres. Cell 54: 505-513.
10. Reynolds AE, McCarroll RM, Newlon CS, Fangman WL (1989) Time of replication of ARS elements along yeast chromosome III. Mol Cell Biol 9: 4488-4494.
11. McCune HJ, Danielson LS, Alvino GM, Collingwood D, Delrow JJ, et al. (2008) The temporal program of chromosome replication: genomewide replication in clb5D Saccharomyces cerevisiae. Genetics 180: 1833-1847.
12. Yabuki N, Terashima H, Kitada K (2002) Mapping of early firing origins on a replication profile of budding yeast. Genes Cells 7: 781-789.
13. Czajkowsky DM, Liu J, Hamlin JL, Shao Z (2008) DNA combing reveals intrinsic temporal disorder in the replication of yeast chromosome VI. J Mol Biol 375: 12-19.
14. Pasero P, Bensimon A, Schwob E (2002) Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev 16: 2479-2484.
15. Segurado M, de Luis A, Antequera F (2003) Genome-wide distribution of DNA replication origins at A+T-rich islands in Schizosaccharomyces pombe. EMBO Rep 4: 1048-1053.
16. Heichinger C, Penkett CJ, Bahler J, Nurse P (2006) Genome-wide characterization of fission yeast DNA replication origins. EMBO Journal 25: 5171-5179.
17. Hayashi M, Katou Y, Itoh T, Tazumi A, Yamada Y, et al. (2007) Genome-wide localization of pre-RC sites and identification of replication origins in fission yeast. EMBO Journal 26: 1327-1339.
18. Dai J, Chuang RY, Kelly TJ (2005) DNA replication origins in the Schizosaccharomyces pombe genome. Proc Natl Acad Sci U S A 102: 337-342.
19. Hyrien O, Marheineke K, Goldar A (2003) Paradoxes of eukaryotic DNA replication: MCM proteins and the random completion problem. Bioessays 25: 116-125.
20. Lygeros J, Koutroumpas K, Dimopoulos S, Legouras I, Kouretas P, et al. (2008) Stochastic hybrid modeling of DNA replication across a complete genome. Proc Natl Acad Sci U S A 105: 12295-12300.
21. Branzei D, Foiani M (2005) The DNA damage response during DNA replication. Curr Opin Cell Biol 17: 568-575.
22. Branzei D, Foiani M (2009) The checkpoint response to replication stress. DNA Repair (Amst) 8: 1038-1046.
23. Gibson DG, Aparicio JG, Hu F, Aparicio OM (2004) Diminished S-phase cyclin-dependent kinase function elicits vital Rad53-dependent checkpoint responses in Saccharomyces cerevisiae. Mol Cell Biol 24: 10208-10222.
24. Gibson DG, Bell SP, Aparicio OM (2006) Cell cycle execution point analysis of ORC function and characterization of the checkpoint response to ORC inactivation in Saccharomyces cerevisiae. Genes Cells 11: 557-573.
25. van Brabant AJ, Buchanan CD, Charboneau E, Fangman WL, Brewer BJ (2001) An origin-deficient yeast artificial chromosome triggers a cell cycle checkpoint. Mol Cell 7: 705-713.
26. Piatti S, Lengauer C, Nasmyth K (1995) Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J 14: 3788-3799.
27. Kelly TJ, Martin GS, Forsburg SL, Stephen RJ, Russo A, et al. (1993) The fission yeast cdc18+ gene product couples S phase to START and mitosis. Cell 74: 371-382.
28. Pasero P, Duncker BP, Schwob E, Gasser SM (1999) A role for the Cdc7 kinase regulatory subunit Dbf4p in the formation of initiation-competent origins of replication. Genes Dev 13: 2159-2176.
29. Lengronne A, Schwob E (2002) The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Molecular Cell 9: 1067-1078.
30. Torres-Rosell J, De Piccoli G, Cordon-Preciado V, Farmer S, Jarmuz A, et al. (2007) Anaphase onset before complete DNA replication with intact checkpoint responses. Science 315: 1411-1415.
31. Dershowitz A, Snyder M, Sbia M, Skurnick JH, Ong LY, et al. (2007) Linear derivatives of Saccharomyces cerevisiae chromosome III can be maintained in the absence of autonomously replicating sequence elements. Mol Cell Biol 27: 4652-4663.
32. Theis JF, Dershowitz A, Irene C, Maciariello C, Tobin ML, et al. (2007) Identification of mutations that decrease the stability of a fragment of Saccharomyces cerevisiae chromosome III lacking efficient replicators. Genetics 177: 1445-1458.
33. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, et al. (2001) Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294: 2364-2368.
34. Tong AH, Boone C (2006) Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313: 171-192.
35. Ji H, Moore DP, Blomberg MA, Braiterman LT, Voytas DF, et al. (1993) Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell 73: 1007-1018.
36. Garber PM, Rine J (2002) Overlapping roles of the spindle assembly and DNA damage checkpoints in the cell-cycle response to altered chromosomes in Saccharomyces cerevisiae. Genetics 161: 521-534.
37. Kim EM, Burke DJ (2008) DNA damage activates the SAC in an ATM/ATRdependent manner, independently of the kinetochore. PLoS Genet 4: e1000015.
38. Maringele L, Lydall D (2002) EXO1-dependent single-stranded DNA at telomeres activates subsets of DNA damage and spindle checkpoint pathways in budding yeast yku70D mutants. Genes Dev 16: 1919-1933.
39. Wang Y, Hu F, Elledge SJ (2000) The Bfa1/Bub2 GAP complex comprises a universal checkpoint required to prevent mitotic exit. Curr Biol 10: 1379-1382.
40. Beckwith WH, Sun Q, Bosso R, Gerik KJ, Burgers PM, et al. (1998) Destabilized PCNA trimers suppress defective Rfc1 proteins in vivo and in vitro. Biochemistry 37: 3711-3722.
41. Emili A (1998) MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol Cell 2: 183-189.
42. Feijoo C, Hall-Jackson C, Wu R, Jenkins D, Leitch J, et al. (2001) Activation of mammalian Chk1 during DNA replication arrest: a role for Chk1 in the intra-S phase checkpoint monitoring replication origin firing. J Cell Biol 154: 913-923.
43. Schwartz MF, Duong JK, Sun Z, Morrow JS, Pradhan D, et al. (2002) Rad9 phosphorylation sites couple Rad53 to the Saccharomyces cerevisiae DNA damage checkpoint. Mol Cell 9: 1055-1065.
44. Vialard JE, Gilbert CS, Green CM, Lowndes NF (1998) The budding yeast Rad9 checkpoint protein is subjected to Mec1/Tel1-dependent hyperphosphorylation and interacts with Rad53 after DNA damage. EMBO J 17: 5679-5688.
45. Alcasabas AA, Osborn AJ, Bachant J, Hu F, Werler PJ, et al. (2001) Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat Cell Biol 3: 958-965.
46. 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: 1078-1083.
47. 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.
48. Tourriere H, Versini G, Cordon-Preciado V, Alabert C, Pasero P (2005) Mrc1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol Cell 19: 699-706.
49. Szyjka SJ, Viggiani CJ, Aparicio OM (2005) Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol Cell 19: 691-697.
50. 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.
51. Vujcic M, Miller CA, Kowalski D (1999) Activation of silent replication origins at autonomously replicating sequence elements near the HML locus in budding yeast. Mol Cell Biol 19: 6098-6109.
52. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, et al. (1996) Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271: 357-360.
53. Zhao X, Muller EG, Rothstein R (1998) A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 2: 329-340.
54. Symington LS (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 66: 630-670, table of contents.
55. Poloumienko A, Dershowitz A, De J, Newlon CS (2001) Completion of replication map of Saccharomyces cerevisiae chromosome III. Mol Biol Cell 12: 3317-3327.
56. Cha RS, Kleckner N (2002) ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297: 602-606.
57. Santocanale C, Sharma K, Diffley JF (1999) Activation of dormant origins of DNA replication in budding yeast. Genes Dev 13: 2360-2364.
58. Llorente B, Smith CE, Symington LS (2008) Break-induced replication: what is it and what is it for? Cell Cycle 7: 859-864.
59. Yuen KW, Warren CD, Chen O, Kwok T, Hieter P, et al. (2007) Systematic genome instability screens in yeast and their potential relevance to cancer. Proc Natl Acad Sci U S A 104: 3925-3930.
60. Sanchez Y, Bachant J, Wang H, Hu F, Liu D, et al. (1999) Control of the DNA damage checkpoint by chk1 and rad53 protein kinases through distinct mechanisms. Science 286: 1166-1171.
61. Segurado M, Diffley JF (2008) Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev 22: 1816-1827.
62. Tercero JA, Longhese MP, Diffley JF (2003) A central role for DNA replication forks in checkpoint activation and response. Mol Cell 11: 1323-1336.
63. Lopes M, Cotta-Ramusino C, Liberi G, Foiani M (2003) Branch migrating sister chromatid junctions form at replication origins through Rad51/Rad52-independent mechanisms. Mol Cell 12: 1499-1510.
64. Caldwell JM, Chen Y, Schollaert KL, Theis JF, Babcock GF, et al. (2008) Orchestration of the S-phase and DNA damage checkpoint pathways by replication forks from early origins. J Cell Biol 180: 1073-1086.
65. Lopes M, Cotta-Ramusino C, Pellicioli A, Liberi G, Plevani P, et al. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412: 557-561.
66. Sogo JM, Lopes M, Foiani M (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297: 599-602.
67. Newlon CS (1988) Yeast chromosome replication and segregation. Microbiological Reviews 52: 568-601.
68. Pan X, Ye P, Yuan DS, Wang X, Bader JS, et al. (2006) A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124: 1069-1081.
69. Celic I, Masumoto H, Griffith WP, Meluh P, Cotter RJ, et al. (2006) The sirtuins Hst3p and Hst4p preserve genome integrity by controlling histone H3 lysine 56 deacetylation. Curr Biol 16: 1280-1289.
70. Maas NL, Miller KM, DeFazio LG, Toczyski DP (2006) Cell cycle and checkpoint regulation of histone H3 K56 acetylation by Hst3 and Hst4. Mol Cell 23: 109-119.
71. Thaminy S, Newcomb B, Kim J, Gatbonton T, Foss E, et al. (2007) Hst3 is regulated by Mec1-dependent proteolysis and controls the S phase checkpoint and sister chromatid cohesion by deacetylating histone H3 at lysine 56. J Biol Chem 282: 37805-37814.
72. Lydeard JR, Jain S, Yamaguchi M, Haber JE (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820-823.
73. Burgers PM, Gerik KJ (1998) Structure and processivity of two forms of Saccharomyces cerevisiae DNA polymerase delta. J Biol Chem 273: 19756-19762.
74. Smith CE, Lam AF, Symington LS (2009) Aberrant double-strand break repair resulting in half crossovers in mutants defective for Rad51 or the DNA polymerase delta complex. Mol Cell Biol 29: 1432-1441.
75. Formosa T, Nittis T (1999) Dna2 mutants reveal interactions with DNA polymerase a and Ctf4, a Pol a accessory factor, and show that full Dna2 helicase activity is not essential for growth. Genetics 151: 1459-1470.
76. Sikorski RS, Hieter P (1989) A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122: 19-27.
77. Brachmann CB, Davies A, Cost GJ, Caputo E, Li J, et al. (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.
78. Tong AHY, Boone C (2007) High-throughput strain construction and systematic synthetic lethal screening in Saccharomyces cerevisiae. Meth Microbiol 36: 369-383.
79. Goldstein AL, McCusker JH (1999) Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast 15: 1541-1553.
80. Wach A, Brachat A, Pohlmann R, Philippsen P (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10: 1793-1808.
81. Rothstein R (1991) Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol 194: 281-301.
82. Vallen EA, Hiller MA, Scherson TY, Rose MD (1992) Separate domains of KAR1 mediate distinct functions in mitosis and nuclear fusion. J Cell Biol 117: 1277-1287.
83. Dershowitz A, Newlon CS (1993) The effect on chromosome stability of deleting replication origins. Mol Cell Biol 13: 391-398.
84. Lea D, Coulson C (1949) The distribution of numbers of mutants in bacterial population. J Genetics 49: 264-285.
85. Brewer BJ, Lockshon D, Fangman WL (1992) The arrest of replication forks in the rDNA of yeast occurs independently of transcription. Cell 71: 267-276.
86. Theis JF, Newlon CS (2001) Two compound replication origins in Saccharomyces cerevisiae contain redundant origin recognition complex binding sites. Mol Cell Biol 21: 2790-2801.
87. Newlon CS, Lipchitz LR, Collins I, Deshpande A, Devenish RJ, et al. (1991) Analysis of a circular derivative of Saccharomyces cerevisiae chromosome III: a physical map and identification and location of ARS elements. Genetics 129: 343-357.
88. Zou L, Elledge SJ (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
89. 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 294: 867-870.
90. Majka J, Binz SK, Wold MS, Burgers PM (2006) Replication protein A directs loading of the DNA damage checkpoint clamp to 59-DNA junctions. J Biol Chem 281: 27855-27861.
91. Majka J, Burgers PM (2003) Yeast Rad17/Mec3/Ddc1: a sliding clamp for the DNA damage checkpoint. Proc Natl Acad Sci U S A 100: 2249-2254.
92. Melo JA, Cohen J, Toczyski DP (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev 15: 2809-2821.
93. Wang H, Elledge SJ (2002) Genetic and physical interactions between DPB11 and DDC1 in the yeast DNA damage response pathway. Genetics 160: 1295-1304.
94. Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R (1994) The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol Cell Biol 14: 8391-8398.