DNA ligase III as a candidate component of backup pathways of nonhomologous end joining

Cancer Research

Volumn 65, Issue 10, 2005, Pages 4020-4030

  Wang, Huichen ^a,c   Rosidi, Bustanur ^b   Perrault, Ronel ^a,d   Wang, Minli ^b   Zhang, Lihua ^b   Windhofer, Frank ^b   Iliakis, George ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

^c Temple University   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA NONHOMOLOGOUS END JOINING; DNA REPAIR; DNA STRAND BREAKAGE; EMBRYO; FIBROBLAST; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; WESTERN BLOTTING;

ANIMALS; CELL NUCLEUS; DNA DAMAGE; DNA LIGASES; DNA REPAIR; DNA, NEOPLASM; FIBROBLASTS; HELA CELLS; HUMANS; MICE; MICE, KNOCKOUT; RNA INTERFERENCE;

EID: 20144363082     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-04-3055     Document Type: Article

References (62)

1. Valerie K, Povirk LF. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 2003; 22:5792-812.
2. Thompson LH, Limoli CL. Origin, recognition, signaling, and repair of DNA double-strand breaks in mammalian cells. In: Caldecott K, editor. Eukaryotic DNA damage surveillance and repair. Landes Press. Chapter 6, p. 107-45. Available from: http://www.landesbioscience.com.
3. Jackson SP. Sensing and repairing DNA double-strand breaks. Carcinogenesis 2002;23:687-96.
4. Dynan WS, Yoo S. Interaction of ku protein and DNA-dependent protein kinase catalytic subunit with nucleic acids. Nucleic Acids Res 1998;26:1551-9.
5. Wang H, Perrault AR, Takeda Y, Qin W, Wang H, Iliakis G. Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res 2003;31:5377-88.
6. Iliakis G, Wang H, Perrault AR, et al. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet Genome Res 2004;104: 14-20.
7. Perrault R, Wang H, Wang M, Rosidi B, Iliakis G. Backup pathways of NHEJ are suppressed by DNA-PK. J Cell Biochem 2004;92:781-94.
8. Zhu C, Mills KD, Ferguson DO, et al. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002; 109:811-21.
9. Gao Y, Ferguson DO, Xie W, et al. Interplay of p53 and DNA-repair protein XRCC4 in tumorigenesis, genomic stability and development. Nature 2000;404: 897-900.
10. Difilippantonio MJ, Zhu J, Chen HT, et al. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature 2000;404:510-4.
11. Lee GS, Neiditch MB, Salus SS, Roth DB. RAG proteins shepherd double-strand breaks to a specific pathway, suppressing error-prone repair, but RAG nicking initiates homologous recombination. Cell 2004;117:171-84.
12. Verkaik NS, Esveldt-van Lange REE, van Heemst D, et al. Different types of V(D)J recombination and end-joining defects in DNA double-strand break repair mutant mammalian ceils. Eur J Immunol 2002; 32:701-9.
13. Plowman PN, Bridges BA, Arlett CF, Hinney A, Kingston JE. An instance of clinical radiation morbidity and cellular radiosensitivity, not associated with ataxiatelagiectasia. Br J Radiol 1990;63:624-8.
14. Riballo E, Critchlow SE, Teo S-H, et al. Identification of a defect in DNA ligase IV in a radiosensitive leukaemia patient. Curr Biol 1999;9:699-702.
15. Riballo E, Doherty AJ, Dai Y, et al. Cellular and biochemical impact of a mutation in DNA ligase IV conferring clinical radiosensitivity. J Biol Chem 2001; 276:31124-32.
16. Badie C, Iliakis G, Foray N, et al. Induction and rejoining of DNA double-strand breaks and interphase chromosome breaks after exposure to X rays in one normal and two hypersensitive human fibroblast cell lines. Radiat Res 1995;144:26-35.
17. Frank KM, Sharpless NE, Gao Y, et al. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol Cell 2000; 5:993-1002.
18. Labhart P. Ku-dependent nonhomologous DNA end joining in Xenopus egg extracts. Mol Cell Biol 1999;19: 2585-93.
19. Tomkinson AE, Roberts E, Daly G, Totty NF, Lindahl T. Three distinct DNA ligases in mammalian cells. J Biol Chem 1991;266:21728-35.
20. Mackey ZB, Niedergang C, Menissier-de Murcia J, et al. DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly (ADP-ribose) polymerase. J Biol Chem 1999;274:21679-87.
21. Seluanov A, Mittelman D, Pereira-Smith OM, Wilson JH, Gorbunova V. DNA end joining becomes less efficient and more error-prone during cellular senescence. Proc Natl Acad Sci U S A 2004;101:7624-9.
22. Baumann P, West SC. DNA end-joining catalyzed by human cell-free extracts. Proc Natl Acad Sci U S A 1998; 95:14066-70.
23. Udayakumar D, Bladen CL, Hudson FZ, Dynan WS. Distinct pathways of nonhomologous end joining that are differentially regulated by DNA-dependent protein kinase-mediated phosphorylation. J Biol Chem 2003; 278:41631-5.
24. Lee K-J, Jovanovic M, Udayakumar D, Bladen CL, Dynan WS. Identification of DNA-PKcs phosphorylation sites in XRCC4 and effects of mutations at these sites on DNA end joining in a cell-free system. DNA Repair 2004;3:267-76.
25. Wang H, Zhao-Chong Z, Perrault AR, Cheng X Qin W, Iliakis G. Genetic evidence for the involvement of DNA ligase IV in the DNA-PK-dependent pathway of non-homologous end joining in mammalian cells. Nucleic Acids Res 2001;29:1653-60.
26. Levin DS, Bai W, Yao N, O'Donnell M, Tomkinson AE. An interaction between DNA ligase I and proliferating cell nuclear antigen: implications for Okazaki fragment synthesis and joining. Proc Natl Acad Sci U S A 1997; 94:12863-8.
27. Taylor AM, Whitehouse CJ, Cappelli E, Frosina G, Caldecott KW. Role of DNA ligase III zinc finger in polynucleotide binding and ligation. Nucleic Acids Res 1998;26:4804-10.
28. Timson DJ, Singleton MR, Wigley DB. DNA ligases in the repair and replication of DNA. Mutat Res 2000;460: 301-18.
29. Tomkinson AE, Mackey ZB. Structure and function of mammalian DNA ligases. Mutat Res 1998;407:1-9.
30. Tomkinson A, Levin DS. Mammalian DNA ligases. BioEssays 1997;19:893-901.
31. Caldecott KW, McKeown CK, Tucker JD, Ljungquist S, Thompson LH. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol Cell Biol 1994;14:68-76.
32. Caldecott K, Tucker JD, Stanker LH, Thompson LH. Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res 1995;23:4836-43.
33. Caldecott KW, Aoufouchi S, Johnson P, Shall S. XRCC1 polypeptide interacts with DNA polymerase β and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular "nick-sensor" in vitro. Nucleic Acids Res 1996;24:4387-94.
34. Cappelli E, Taylor R, Cevasco M, Abbondandolo A, Caldecott K, Frosina G. Involvement of XRCC1 and DNA ligase III gene products in DNA base excision repair. J Biol Chem 1997;272:23970-5.
35. Taylor AM, Whitehouse CJ, Caldecott KW. The DNA ligase III zinc finger stimulates binding to DNA secondary structure and promotes endjoining. Nucleic Acids Res 2000;28:3558-63.
36. Chen L, Trujillo K, Sung P, Tomkinson AE. Interactions of the DNA ligase IV-XRCC4 complex with DNA ends and the DNA-dependent protein kinase. J Biol Chem 2000;275:26196-205.
37. Lakshmipathy U, Campbell C. Double strand break rejoining by mammalian mitochondrial extracts. Nucleic Acids Res 1999;27:1198-204.
38. Audebert M, Salles B, Calsou P. Involvement of poly(ADP-ribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 2004;279:55117-26.
39. McVey M, LaRocque JR, Adams MD, Sekelsky JJ. Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc Natl Acad Sci U S A 2004;101:15694-9.
40. Cheong N, Perrault AR, Wang H, et al. DNA-PK-independent rejoining of DNA double-strand breaks in human cell extracts in vitro. Int J Radiat Biol 1999;75: 67-81.
41. DiBiase SJ, Zeng Z-C, Chen R, Hyslop T, Curran WJ Jr, Iliakis G. DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res 2000;60:1245-53.
42. Wang H, Zeng Z-C, Bui T-A, et al. Efficient rejoining of radiation-induced DNA double-strand breaks in vertebrate cells deficient in genes of the RAD52 epistasis group. Oncogene 2001;20:2212-24.
43. Goettlich B, Reichenberger S, Feldmann E, Pfeiffer P. Rejoining of DNA double-strand breaks in vitro by single-strand annealing. Eur J Biochem 1998;258:387-95.
44. Lakshmipathy U, Campbell C. The human DNA ligase III gene encodes nuclear and mitochondrial proteins. Mol Cell Biol 1999;19:3869-76.
45. Perez-Jannotti RM, Klein SM, Bogenhagen DF. Two forms of mitochondrial DNA ligase III are produced in Xenopus laevis oocytes. J Biol Chem 2001;276:48978-87.
46. Lakshmipathy U, Campbell C. Mitochondrial DNA ligase III function is independent of Xrcc1. Nucleic Acids Res 2000;28:3880-6.
47. Lakshmipathy U, Campbell C. Antisense-mediated decrease in DNA ligase III expression results in reduced mitochondrial DNA integrity. Nucleic Acids Res 2001;29: 668-76.
48. Thompson LH, Brookman KVV, Jones NJ, Allen SA, Carrano AV. Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol Cell Biol 1990;10: 6160-71.
49. van Ankeren SC, Murray D, Stafford PM, Meyn RE. Cell survival and recovery processes in Chinese hamster AA8 cell and in two radiosensitive clones. Radiat Res 1988;115:223-37.
50. Adachi N, Ishino T, Ishii Y, Takeda S, Koyama H. DNA ligase IV-deficient cells are more resistant to ionizing radiation in the absence of Ku70: implications for DNA double-strand break repair. Proc Natl Acad Sci U S A 2001;98:12109-13.
51. Süsse S, Scholz C-J, Bürkle A, Wiesmüller L. Poly(ADP-ribose) polymerase (PARP-1) and p53 independently function in regulating double-strand break repair in primate cells. Nucleic Acids Res 2004;32:669-80.
52. Rudat V, Bachmann N, Küpper J-H, Weber K-J. Overexpression of the DNA-binding domain of poly(ADP-ribose) polymerase inhibits rejoining of ionizing radiation-induced DNA double-strand breaks. Int J Radiat Biol 2001;77:303-7.
53. Noel G, Giocanti N, Fernet M, Megnin-Chanet F, Favaudon V. Poly(ADP-ribose) polymerase (PARP-1) is not involved in DNA double-strand break recovery. BMC Cell Biol 2003;4:7-16.
54. D'Amours D, Desnoyers S, D'Silva I, Poirier GG. Poly(ADP-rihosyl)ation reactions in the regulation of nuclear functions. Biochem J 1999;342:249-68.
55. Yang Y-G, Cortes U, Patnaik S, Jasin M, Wang Z-Q. Ablation of PARP-1 does not interfere with the repair of DNA double-strand breaks, but compromises the reactivation of stalled replication forks. Oncogene 2004;23:3872-82.
56. Roth DB, Porter TM, Wilson JH. Mechanisms of nonhomologous recombination in mammalian cells. Mol Cell Biol 19855;2599-607.
57. Roth DB, Wilson JH. Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol Cell Biol 1986; 6:4295-304.
58. Chang C, Biedermann KA, Mezzina M, Brown JM. Characterization of the DNA double strand break repair defect in seid mice. Cancer Res 1993;53:1244-8.
59. Harrington J, Hsieh CL, Gerton J, Bosma G, Lieber MR Analysis of the defect in DNA end joining in the murine scid mutation. Mol Cell Biol 1992;12:4758-68.
60. Kabotyanski EB, Gomelsky L, Han J-O, Stamato TD, Roth DB. Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res 1998;26: 5333-42.
61. Feldmann E, Schmiemann V, Goedecke W Reichenberger S, Pfeiffer P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res 2000;28:2585-96.
62. Chen S, Inamdar KV Pfeiffer P, et al. Accurate in vitro end joining of a DNA double strand break with partially cohesive 3′-overhangs and 3′-phosphoglycolate termini. Effect of Ku on repair fidelity. J Biol Chem 2001;276: 24323-30.