Single Cell Analysis of Human RAD18-Dependent DNA Post-Replication Repair by Alkaline Bromodeoxyuridine Comet Assay

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Mórocz, Mónika ^a   Gali, Himabindu ^a   Raskó, István ^a   Downes, C Stephen ^b   Haracska, Lajos ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF ULSTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BROXURIDINE; RAD18 PROTEIN;

ARTICLE; CELL LABELING; COMET ASSAY; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMAN; HUMAN CELL; INTERMETHOD COMPARISON; POSTREPLICATION REPAIR; SINGLE CELL ANALYSIS; ULTRAVIOLET RADIATION;

BROMODEOXYURIDINE; COMET ASSAY; DNA; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; DNA-BINDING PROTEINS; DOSE-RESPONSE RELATIONSHIP, RADIATION; GENE KNOCKOUT TECHNIQUES; HCT116 CELLS; HELA CELLS; HUMANS; KINETICS; S PHASE; SINGLE-CELL ANALYSIS; ULTRAVIOLET RAYS;

EID: 84881171891     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0070391     Document Type: Article

References (59)

1. Jansen JG, Tsaalbi-Shtylik A, de Wind N, (2009) Functional interactions between DNA damage signaling and mutagenic translesion synthesis at post-replicative gaps. Cell Cycle 8: 2857-2858.
2. Jansen JG, Tsaalbi-Shtylik A, Hendriks G, Gali H, Hendel A, et al. (2009) Separate domains of Rev1 mediate two modes of DNA damage bypass in mammalian cells. Mol Cell Biol 29: 3113-3123.
3. Smirnova M, Klein HL, (2003) Role of the error-free damage bypass postreplication repair pathway in the maintenance of genomic stability. Mutat Res 532: 117-135.
4. Karras GI, Jentsch S, (2010) The RAD6 DNA damage tolerance pathway operates uncoupled from the replication fork and is functional beyond S phase. Cell 141: 255-267.
5. Prakash L, (1981) Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol Gen Genet 184: 471-478.
6. Prakash S, Johnson RE, Prakash L, (2005) Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu Rev Biochem 74: 317-353.
7. Higgins NP, Kato K, Strauss B, (1976) A model for replication repair in mammalian cells. J Mol Biol 101: 417-425.
8. Blastyak A, Pinter L, Unk I, Prakash L, Prakash S, et al. (2007) Yeast Rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol Cell 28: 167-175.
9. Torres-Ramos CA, Prakash S, Prakash L, (2002) Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol Cell Biol 22: 2419-2426.
10. Torres-Ramos CA, Yoder BL, Burgers PM, Prakash S, Prakash L, (1996) Requirement of proliferating cell nuclear antigen in RAD6-dependent postreplicational DNA repair. Proc Natl Acad Sci U S A 93: 9676-9681.
11. Bailly V, Lauder S, Prakash S, Prakash L, (1997) Yeast DNA repair proteins Rad6 and Rad18 form a heterodimer that has ubiquitin conjugating, DNA binding, and ATP hydrolytic activities. J Biol Chem 272: 23360-23365.
12. Yamashita YM, Okada T, Matsusaka T, Sonoda E, Zhao GY, et al. (2002) RAD18 and RAD54 cooperatively contribute to maintenance of genomic stability in vertebrate cells. EMBO J 21: 5558-5566.
13. Tateishi S, Sakuraba Y, Masuyama S, Inoue H, Yamaizumi M, (2000) Dysfunction of human Rad18 results in defective postreplication repair and hypersensitivity to multiple mutagens. Proc Natl Acad Sci U S A 97: 7927-7932.
14. Tateishi S, Niwa H, Miyazaki J, Fujimoto S, Inoue H, et al. (2003) Enhanced genomic instability and defective postreplication repair in RAD18 knockout mouse embryonic stem cells. Mol Cell Biol 23: 474-481.
15. Yoon JH, Prakash S, Prakash L, (2012) Requirement of Rad18 protein for replication through DNA lesions in mouse and human cells. Proc Natl Acad Sci U S A 109: 7799-7804.
16. Bailly V, Lamb J, Sung P, Prakash S, Prakash L, (1994) Specific complex formation between yeast RAD6 and RAD18 proteins: a potential mechanism for targeting RAD6 ubiquitin-conjugating activity to DNA damage sites. Genes Dev 8: 811-820.
17. Gangavarapu V, Prakash S, Prakash L, (2007) Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol Cell Biol 27: 7758-7764.
18. San Filippo J, Sung P, Klein H, (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77: 229-257.
19. Sung P, Klein H, (2006) Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7: 739-750.
20. Ostling O, Johanson KJ, (1984) Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 123: 291-298.
21. Collins AR, (2002) The comet assay. Principles, applications, and limitations. Methods Mol Biol 203: 163-177.
22. Collins AR, (2004) The comet assay for DNA damage and repair: principles, applications, and limitations. Mol Biotechnol 26: 249-261.
23. Collins AR, (2009) Investigating oxidative DNA damage and its repair using the comet assay. Mutat Res 681: 24-32.
24. Collins AR, (2011) The use of bacterial repair endonucleases in the comet assay. Methods Mol Biol 691: 137-147.
25. Collins AR, Azqueta A (2011) DNA repair as a biomarker in human biomonitoring studies; further applications of the comet assay. Mutat Res.
26. Collins AR, Dobson VL, Dusinska M, Kennedy G, Stetina R, (1997) The comet assay: what can it really tell us? Mutat Res 375: 183-193.
27. Collins AR, Oscoz AA, Brunborg G, Gaivao I, Giovannelli L, et al. (2008) The comet assay: topical issues. Mutagenesis 23: 143-151.
28. Fairbairn DW, Olive PL, O'Neill KL, (1995) The comet assay: a comprehensive review. Mutat Res 339: 37-59.
29. Shaposhnikov SA, Salenko VB, Brunborg G, Nygren J, Collins AR, (2008) Single-cell gel electrophoresis (the comet assay): loops or fragments? Electrophoresis 29: 3005-3012.
30. Jackson DA, Pombo A, (1998) Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140: 1285-1295.
31. Magavi SS, Macklis JD, (2008) Identification of newborn cells by BrdU labeling and immunocytochemistry in vivo. Methods Mol Biol 438: 335-343.
32. Rothaeusler K, Baumgarth N, (2007) Assessment of cell proliferation by 5-bromodeoxyuridine (BrdU) labeling for multicolor flow cytometry. Curr Protoc Cytom Chapter 7: Unit731.
33. Varga A, Marcus AP, Himoto M, Iwai S, Szuts D, (2012) Analysis of CPD ultraviolet lesion bypass in chicken DT40 cells: polymerase eta and PCNA ubiquitylation play identical roles. PLoS One 7: e52472.
34. Dextraze ME, Wagner JR, Hunting DJ, (2007) 5-Bromodeoxyuridine radiosensitization: conformation-dependent DNA damage. Biochemistry 46: 9089-9097.
35. Hutchinson F, (1973) The lesions produced by ultraviolet light in DNA containing 5-bromouracil. Q Rev Biophys 6: 201-246.
36. Kohlmeier F, Maya-Mendoza A, Jackson DA, (2013) EdU induces DNA damage response and cell death in mESC in culture. Chromosome Res 21: 87-100.
37. McGlynn AP, Wasson GR, O'Reilly S, McKelvey-Martin VJ, McNulty H, et al. (2003) Detection of replicative integrity in small colonic biopsies using the BrdUrd comet assay. Br J Cancer 88: 895-901.
38. McGlynn AP, Wasson G, O'Connor J, McKerr G, McKelvey-Martin VJ, et al. (1999) The bromodeoxyuridine comet assay: detection of maturation of recently replicated DNA in individual cells. Cancer Res 59: 5912-5916.
39. Shiomi N, Mori M, Tsuji H, Imai T, Inoue H, et al. (2007) Human RAD18 is involved in S phase-specific single-strand break repair without PCNA monoubiquitination. Nucleic Acids Research 35: e9.
40. Mechali M, (2010) Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11: 728-738.
41. Ellenberger T, Tomkinson AE, (2008) Eukaryotic DNA ligases: structural and functional insights. Annu Rev Biochem 77: 313-338.
42. Leva V, Giuliano S, Bardoni A, Camerini S, Crescenzi M, et al. (2012) Phosphorylation of SRSF1 is modulated by replicational stress. Nucleic Acids Research 40: 1106-1117.
43. Edmunds CE, Simpson LJ, Sale JE, (2008) PCNA ubiquitination and REV1 define temporally distinct mechanisms for controlling translesion synthesis in the avian cell line DT40. Mol Cell 30: 519-529.
44. Karlsson KH, Radulescu I, Rydberg B, Stenerlow B, (2008) Repair of radiation-induced heat-labile sites is independent of DNA-PKcs, XRCC1 and PARP. Radiat Res 169: 506-512.
45. Lundin C, North M, Erixon K, Walters K, Jenssen D, et al. (2005) Methyl methanesulfonate (MMS) produces heat-labile DNA damage but no detectable in vivo DNA double-strand breaks. Nucleic Acids Research 33: 3799-3811.
46. Rydberg B, (2000) Radiation-induced heat-labile sites that convert into DNA double-strand breaks. Radiat Res 153: 805-812.
47. Ciccia A, Elledge SJ, (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40: 179-204.
48. Unk I, Hajdu I, Fatyol K, Hurwitz J, Yoon JH, et al. (2008) Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc Natl Acad Sci U S A 105: 3768-3773.
49. Unk I, Hajdu I, Fatyol K, Szakal B, Blastyak A, et al. (2006) Human SHPRH is a ubiquitin ligase for Mms2-Ubc13-dependent polyubiquitylation of proliferating cell nuclear antigen. Proc Natl Acad Sci U S A 103: 18107-18112.
50. Ciccia A, Nimonkar AV, Hu Y, Hajdu I, Achar YJ, et al. (2012) Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol Cell 47: 396-409.
51. Juhasz S, Balogh D, Hajdu I, Burkovics P, Villamil MA, et al. (2012) Characterization of human Spartan/C1orf124, an ubiquitin-PCNA interacting regulator of DNA damage tolerance. Nucleic Acids Research.
52. Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, et al. (2010) A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39: 36-47.
53. Yamada K, Kameyama Y, Inoue S, (1996) An improved method of alkaline sucrose density gradient sedimentation to detect less than one lesion per 1 Mb DNA. Mutat Res 364: 125-131.
54. Gangavarapu V, Haracska L, Unk I, Johnson RE, Prakash S, et al. (2006) Mms2-Ubc13-dependent and-independent roles of Rad5 ubiquitin ligase in postreplication repair and translesion DNA synthesis in Saccharomyces cerevisiae. Mol Cell Biol 26: 7783-7790.
55. Gangavarapu V, Santa MariaSR, Prakash S, Prakash L, (2011) Requirement of replication checkpoint protein kinases Mec1/Rad53 for postreplication repair in yeast. MBio 2: e00079-00011.
56. Johansson F, Lagerqvist A, Erixon K, Jenssen D, (2004) A method to monitor replication fork progression in mammalian cells: nucleotide excision repair enhances and homologous recombination delays elongation along damaged DNA. Nucleic Acids Research 32: e157.
57. Christie NT, Drake S, Meyn RE, Nelson JA, (1984) 6-Thioguanine-induced DNA damage as a determinant of cytotoxicity in cultured Chinese hamster ovary cells. Cancer Res 44: 3665-3671.
58. Clark JM, Hanawalt PC, (1984) Replicative intermediates in UV-irradiated simian virus 40. Mutat Res 132: 1-14.
59. Olive PL, Banath JP, (2006) The comet assay: a method to measure DNA damage in individual cells. Nat Protoc 1: 23-29.