Unligated Okazaki Fragments Induce PCNA Ubiquitination and a Requirement for Rad59-Dependent Replication Fork Progression

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Da Nguyen, Haing ^a   Becker, Jordan ^a   Thu, Yee Mon ^a   Costanzo, Michael ^b   Koch, Elizabeth N ^c   Smith, Stephanie ^d   Myung, Kyungjae ^d   Myers, Chad L ^c   Boone, Charles ^b   Bielinsky, Anja Katrin ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c University of Minnesota   (United States)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; FUNGAL DNA; OKAZAKI FRAGMENT; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN PCNA; PROTEIN RAD59; UNCLASSIFIED DRUG; ATP DEPENDENT DNA LIGASE; CDC9 PROTEIN, S CEREVISIAE; CYCLINE; DNA; OKAZAKI FRAGMENTS; RAD59 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOACCUMULATION; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA MODIFICATION; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; FUNGAL GENOME; GENE MUTATION; LETHALITY; NONHUMAN; PROTEIN DNA INTERACTION; PROTEIN PHOSPHORYLATION; UBIQUITINATION; GENETICS; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCETALES;

DNA; DNA LIGASE ATP; DNA REPLICATION; DNA-BINDING PROTEINS; MUTATION; PROLIFERATING CELL NUCLEAR ANTIGEN; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION;

EID: 84879134720     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066379     Document Type: Article

References (64)

1. Branzei D, Foiani M, (2007) Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 6: 994-1003.
2. Das-Bradoo S, Nguyen HD, Bielinsky AK, (2010) Damage-specific modification of PCNA. Cell Cycle 9: 3674-3679.
3. Barnes DE, Tomkinson AE, Lehmann AR, Webster AD, Lindahl T, (1992) Mutations in the DNA ligase I gene of an individual with immunodeficiencies and cellular hypersensitivity to DNA-damaging agents. Cell 69: 495-503.
4. Ellenberger T, Tomkinson AE, (2008) Eukaryotic DNA ligases: structural and functional insights. Annu Rev Biochem 77: 313-338.
5. Montelone BA, Prakash S, Prakash L, (1981) Spontaneous mitotic recombination in mms8-1, an allele of the CDC9 gene of Saccharomyces cerevisiae. J Bacteriol 147: 517-525.
6. Wilson TE, Grawunder U, Lieber MR, (1997) Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388: 495-498.
7. Wu X, Braithwaite E, Wang Z, (1999) DNA ligation during excision repair in yeast cell-free extracts is specifically catalyzed by the CDC9 gene product. Biochemistry 38: 2628-2635.
8. Vijayakumar S, Chapados BR, Schmidt KH, Kolodner RD, Tainer JA, et al. (2007) The C-terminal domain of yeast PCNA is required for physical and functional interactions with Cdc9 DNA ligase. Nucleic Acids Res 35: 1624-1637.
9. Sriskanda V, Schwer B, Ho CK, Shuman S, (1999) Mutational analysis of Escherichia coli DNA ligase identifies amino acids required for nick-ligation in vitro and for in vivo complementation of the growth of yeast cells deleted for CDC9 and LIG4. Nucleic Acids Res 27: 3953-3963.
10. Nair PA, Nandakumar J, Smith P, Odell M, Lima CD, et al. (2007) Structural basis for nick recognition by a minimal pluripotent DNA ligase. Nat Struct Mol Biol 14: 770-778.
11. Bielinsky AK, Gerbi SA, (1999) Chromosomal ARS1 has a single leading strand start site. Mol Cell 3: 477-486.
12. Weinert TA, Hartwell LH, (1993) Cell cycle arrest of cdc mutants and specificity of the RAD9 checkpoint. Genetics 134: 63-80.
13. Emili A, (1998) MEC1-dependent phosphorylation of Rad9p in response to DNA damage. Mol Cell 2: 183-189.
14. Naiki T, Wakayama T, Nakada D, Matsumoto K, Sugimoto K, (2004) Association of Rad9 with double-strand breaks through a Mec1-dependent mechanism. Mol Cell Biol 24: 3277-3285.
15. 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.
16. Das-Bradoo S, Nguyen HD, Wood JL, Ricke RM, Haworth JC, et al. (2010) Defects in DNA ligase I trigger PCNA ubiquitylation at Lys 107. Nat Cell Biol 12: 74-79.
17. Naylor ML, Li JM, Osborn AJ, Elledge SJ, (2009) Mrc1 phosphorylation in response to DNA replication stress is required for Mec1 accumulation at the stalled fork. Proc Natl Acad Sci USA 106: 12765-12770.
18. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S, (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419: 135-141.
19. Game JC, Johnston LH, von Borstel RC, (1979) Enhanced mitotic recombination in a ligase-defective mutant of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 76: 4589-4592.
20. Prigent C, Satoh MS, Daly G, Barnes DE, Lindahl T, (1994) Aberrant DNA repair and DNA replication due to an inherited enzymatic defect in human DNA ligase I. Mol Cell Biol. 14: 310-317.
21. Krogh BO, Symington LS, (2004) Recombination proteins in yeast. Annu Rev Genet 38: 233-271.
22. Krejci L, Song B, Bussen W, Rothstein R, Mortensen UH, et al. (2002) Interaction with Rad51 is indispensable for recombination mediator function of Rad52. J Biol Chem 277: 40132-40141.
23. Flott S, Alabert C, Toh GW, Toth R, Sugawara N, et al. (2007) Phosphorylation of Slx4 by Mec1 and Tel1 regulates the single-strand annealing mode of DNA repair in budding yeast. Mol Cell Biol 27: 6433-6445.
24. Toh GW, Sugawara N, Dong J, Toth R, Lee SE, et al. (2010) Mec1/Tel1-dependent phosphorylation of Slx4 stimulates Rad1-Rad10-dependent cleavage of non-homologous DNA tails. DNA Repair (Amst) 9: 718-726.
25. Tomkinson AE, Totty NF, Ginsburg M, Lindahl T, (1991) Location of the active site for enzyme-adenylate formation in DNA ligases. Proc Natl Acad Sci USA 88: 400-404.
26. Subramanian J, Vijayakumar S, Tomkinson AE, Arnheim N, (2005) Genetic instability induced by overexpression of DNA ligase I in budding yeast. Genetics 171: 427-441.
27. Ho CK, Van Etten JL, Shuman S, (1997) Characterization of an ATP-dependent DNA ligase encoded by Chlorella virus PBCV-1. J Virol 71: 1931-1937.
28. Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, et al. (1999) Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J 18: 6561-6572.
29. Szyjka SJ, Aparicio JG, Viggiani CJ, Knott S, Xu W, et al. (2008) Rad53 regulates replication fork restart after DNA damage in Saccharomyces cerevisiae. Genes Dev 22: 1906-1920.
30. Baryshnikova A, Costanzo M, Dixon S, Vizeacoumar FJ, Myers CL, et al. (2010) Synthetic genetic array (SGA) analysis in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Methods Enzymol 470: 145-179.
31. Baryshnikova A, Costanzo M, Kim Y, Ding H, Koh J, et al. (2010) Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nat Methods 7: 1017-1024.
32. Chen C, Merrill BJ, Lau PJ, Holm C, Kolodner RD, (1999) Saccharomyces cerevisiae pol30 (proliferating cell nuclear antigen) mutations impair replication fidelity and mismatch repair. Mol Cell Biol 19: 7801-7815.
33. Motegi A, Myung K, (2007) Measuring the rate of gross chromosomal rearrangements in Saccharomyces cerevisiae: A practical approach to study genomic rearrangements observed in cancer. Methods 41: 168-176.
34. Davierwala AP, Haynes J, Li Z, Brost RL, Robinson MD, et al. (2005) The synthetic genetic interaction spectrum of essential genes. Nat Genet 37: 1147-1152.
35. Bailly V, Sommers CH, Sung P, Prakash L, Prakash S, (1992) Specific complex formation between proteins encoded by the yeast DNA repair and recombination genes RAD1 and RAD10. Proc Natl Acad Sci USA 89: 8273-8277.
36. Guzder SN, Sommers CH, Prakash L, Prakash S, (2006) Complex formation with damage recognition protein Rad14 is essential for Saccharomyces cerevisiae Rad1-Rad10 nuclease to perform its function in nucleotide excision repair in vivo. Mol Cell Biol 26: 1135-1141.
37. Ivanov EL, Haber JE, (1995) RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol Cell Biol 15: 2245-2251.
38. Mott C, Symington LS, (2011) RAD51-independent inverted-repeat recombination by a strand-annealing mechanism. DNA Repair (Amst) 10: 408-415.
39. Harrington JJ, Lieber MR, (1994) Functional domains within FEN-1 and RAD2 define a family of structure-specific endonucleases: implications for nucleotide excision repair. Genes Dev 8: 1344-1355.
40. Mizuno K, Lambert S, Baldacci G, Murray JM, Carr AM, (2009) Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism. Genes Dev 23: 2876-2886.
41. Paek AL, Kaochar S, Jones H, Elezaby A, Shanks L, et al. (2009) Fusion of nearby inverted repeats by a replication-based mechanism leads to formation of dicentric and acentric chromosomes that cause genome instability in budding yeast. Genes Dev 23: 2861-2875.
42. Irmisch A, Ampatzidou E, Mizuno K, O'Connell MJ, Murray JM, (2009) Smc5/6 maintains stalled replication forks in a recombination-competent conformation. EMBO J 28: 144-155.
43. Smith DJ, Whitehouse I, (2012) Intrinsic coupling of lagging-strand synthesis to chromatin assembly. Nature 483: 434-438.
44. Chafin DR, Vitolo JM, Henricksen LA, Bambara RA, Hayes JJ, (2000) Human DNA ligase I efficiently seals nicks in nucleosomes. EMBO J 19: 5492-5501.
45. Collinge MA, Althaus FR, (1994) Expression of human poly(ADP-ribose) polymerase in Saccharomyces cerevisiae. Mol Gen Genet 245: 686-693.
46. Freudenthal BD, Ramaswamy S, Hingorani MM, Washington MT, (2008) Structure of a mutant form of proliferating cell nuclear antigen that blocks translesion synthesis. Biochemistry 47: 13354-13361.
47. Zou L, Elledge SJ, (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300: 1542-1548.
48. Nakada D, Hirano Y, Sugimoto K, (2004) Requirement of the Mre11 complex and exonuclease 1 for activation of the Mec1 signaling pathway. Mol Cell Biol 24: 10016-10025.
49. Budd ME, Antoshechkin IA, Reis C, Wold BJ, Campbell JL, (2011) Inviability of a DNA2 deletion mutant is due to the DNA damage checkpoint. Cell Cycle 10: 1690-1698.
50. Zhang Z, Zhang S, Lin SH, Wang X, Wu L, et al. (2012) Structure of monoubiquitinated PCNA: Implications for DNA polymerase switching and Okazaki fragment maturation. Cell Cycle 11: 2128-2136.
51. Wu Y, Sugiyama T, Kowalczykowski SC, (2006) DNA annealing mediated by Rad52 and Rad59 proteins. J Biol Chem 281: 15441-15449.
52. Alabert C, Bianco JN, Pasero P, (2009) Differential regulation of homologous recombination at DNA breaks and replication forks by the Mrc1 branch of the S-phase checkpoint. EMBO J 28: 1131-1141.
53. Barlow JH, Rothstein R, (2009) Rad52 recruitment is DNA replication independent and regulated by Cdc28 and the Mec1 kinase. EMBO J 28: 1121-1130.
54. Groth A, Corpet A, Cook AJ, Roche D, Bartek J, et al. (2007) Regulation of replication fork progression through histone supply and demand. Science 318: 1928-1931.
55. Kaufman PD, Kobayashi R, Stillman B, (1997) Ultraviolet radiation sensitivity and reduction of telomeric silencing in Saccharomyces cerevisiae cells lacking chromatin assembly factor-I. Genes Dev 11: 345-357.
56. Costanzo M, Baryshnikova A, Bellay J, Kim Y, Spear ED, et al. (2010) The genetic landscape of a cell. Science 327: 425-431.
57. Chanet R, Heude M, (2003) Characterization of mutations that are synthetic lethal with pol3-13, a mutated allele of DNA polymerase delta in Saccharomyces cerevisiae. Curr Genet 43: 337-350.
58. 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.
59. Symington LS, (1998) Homologous recombination is required for the viability of rad27 mutants. Nucleic Acids Res 26: 5589-5595.
60. 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.
61. Tong AH, Boone C, (2006) Synthetic genetic array analysis in Saccharomyces cerevisiae. Methods Mol Biol 313: 171-192.
62. Morin I, Ngo HP, Greenall A, Zubko MK, Morrice N, et al. (2008) Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J 27: 2400-2410.
63. Ben-Aroya S, Coombes C, Kwok T, O'Donnell KA, Boeke JD, et al. (2008) Toward a comprehensive temperature-sensitive mutant repository of the essential genes of Saccharomyces cerevisiae. Mol Cell 30: 248-258.
64. Ben-Aroya S, Pan X, Boeke JD, Hieter P, (2010) Making temperature-sensitive mutants. Methods Enzymol 470: 181-204.