Human DNA ligases I and III, but not ligase IV, are required for microhomology-mediated end joining of DNA double-strand breaks

Nucleic Acids Research

Volumn 36, Issue 10, 2008, Pages 3297-3310

  Liang, Li ^a   Deng, Li ^a   Nguyen, Son C ^a   Zhao, Xin ^a   Maulion, Christopher D ^a   Shao, Changshun ^a   Tischfield, Jay A ^a  

^a RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; KU ANTIGEN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; SMALL INTERFERING RNA; DNA LIGASE III; HELICASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE (ATP); XRCC5 PROTEIN, HUMAN;

ARTICLE; BIOCHEMISTRY; CELL FREE SYSTEM; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; DOWN REGULATION; FIBROBLAST; GENETIC ANALYSIS; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; MAMMAL CELL; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SEQUENCE HOMOLOGY; CELL LINE; DRUG ANTAGONISM; GENETIC RECOMBINATION; GENETICS; METABOLISM; PHYSIOLOGY;

MAMMALIA;

CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; DNA LIGASES; DNA REPAIR; HUMANS; RECOMBINATION, GENETIC; RNA INTERFERENCE;

EID: 45549094090     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn184     Document Type: Article

References (46)

1. Rich,T., Allen,R.L. and Wyllie,A.H. (2000) Defying death after DNA damage. Nature, 407, 777-783.
2. Jackson,S.P. (2002) Sensing and repairing DNA double-strand breaks. Carcinogenesis, 23, 687-696.
3. Lieber,M.R., Ma,Y., Pannicke,U. and Schwarz,K. (2003) Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell. Biol., 4, 712-720.
4. Chen,S., Inamdar,K.V., Pfeiffer,P., Feldmann,E., Hannah,M.F., Yu,Y., Lee,J.W., Zhou,T., Lees-Miller,S.P. and Povirk,L.F. (2001) 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., 276, 24323-24330.
5. DiBiase,S.J., Zeng,Z.C., Chen,R., Hyslop,T., Curran,W.J.,Jr and Iliakis,G. (2000) DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res., 60, 1245-1253.
6. Feldmann,E., Schmiemann,V., Goedecke,W., Reichenberger,S. and Pfeiffer,P. (2000) 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., 28, 2585-2596.
7. Kabotyanski,E.B., Gomelsky,L., Han,J.O., Stamato,T.D. and Roth,D.B. (1998) Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res., 26, 5333-5342.
8. Liang,F. and Jasin,M. (1996) Ku80-deficient cells exhibit excess degradation of extrachromosomal DNA. J. Biol. Chem., 271, 14405-14411.
9. Liang,L., Deng,L., Chen,Y., Li,G.C., Shao,C. and Tischfield,J.A. (2005) Modulation of DNA end joining by nuclear proteins. J. Biol. Chem., 280, 31442-31449.
10. Perrault,R., Wang,H., Wang,M., Rosidi,B. and Iliakis,G. (2004) Backup pathways of NHEJ are suppressed by DNA-PK. J. Cell. Biochem., 92, 781-794.
11. Smith,J., Riballo,E., Kysela,B., Baldeyron,C., Manolis,K., Musson,C., Lieber,M.R., Papadopoulo,D. and Jeggo,P. (2003) Impact of DNA ligase IV on the fidelity of end joining in human cells. Nucleic Acids Res., 31, 2157-2167.
12. Wang,H., Perrault,A.R., Takeda,Y., Qin,W., Wang,H. and Iliakis,G. (2003) Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res., 31, 5377-5388.
13. Wang,H.C., Zeng,Z.C., Perrault,A.R., Cheng,X.B., Qin,W. and Iliakis,G. (2001) 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., 29, 1653-1660.
14. Morris,T. and Thacker,J. (1993) Formation of large deletions by illegitimate recombination in the HPRT gene of primary human fibroblasts. Proc. Natl Acad. Sci. USA, 90, 1392-1396.
15. Miles,C. and Meuth,M. (1989) DNA sequence determination of gamma-radiation-induced mutations of the hamster aprt locus. Mutat. Res., 227, 97-102.
16. Zhu,C., Mills,K.D., Ferguson,D.O., Lee,C., Manis,J., Fleming,J., Gao,Y., Morton,C.C. and Alt,F.W. (2002) Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell, 109, 811-821.
17. Timson,D.J., Singleton,M.R. and Wigley,D.B. (2000) DNA ligases in the repair and replication of DNA. Mutat. Res., 460, 301-318.
18. Martin,I.V. and MacNeill,S.A. (2002) ATP-dependent DNA ligases. Genome Biol., 3, REVIEWS3005.
19. Levin,D.S., Bai,W., Yao,N., O'Donnell,M. and Tomkinson,A.E. (1997) An interaction between DNA ligase I and proliferating cell nuclear antigen: implications for Okazaki fragment synthesis and joining. Proc. Natl Acad. Sci. USA, 94, 12863-12868.
20. Montecucco,A., Rossi,R., Levin,D.S., Gary,R., ParkM.S., Motycka,T.A., Ciarrocchi,G., Villa,A., Biamonti,G. and Tomkinson,A.E. (1998) DNA ligase I is recruited to sites of DNA replication by an interaction with proliferating cell nuclear antigen: Identification of a common targeting mechanism for the assembly of replication factories. EMBO J., 17, 3786-3795.
21. Levin,D.S., McKenna,A.E., Motycka,T.A., Matsumoto,Y. and Tomkinson,A.E. (2000) Interaction between PCNA and DNA ligase I is critical for joining of Okazaki fragments and long-patch base-excision repair. Curr. Biol, 10, 919-922.
22. Mackey,Z.B., Ramos,W., Levin,D.S., Walter,C.A., McCarrey,J.R. and Tomkinson,A.E. (1997) An alternative splicing event which occurs in mouse pachytene spermatocytes generates a form of DNA ligase III with distinct biochemical properties that may function in meiotic recombination. Mol. Cell. Biol., 17, 989-998.
23. Caldecott,K.W., McKeown,C.K., Tucker,J.D., Ljungquist,S. and Thompson,L.H. (1994) An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell. Biol., 14, 68-76.
24. Bryans,M., Valmzano,M.C. and Stamato,T.D. (1999) Absence of DNA ligase IV protein in XR-1 cells: Evidence for stabilization by XRCC4. Mutat. Res., 433, 53-58.
25. Grawunder,U., Wihn,M., Wu,X., Kulesza,P., Wilson,T.E., Mann,M. and Lieber,M.R. (1997) Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature, 388 492-495.
26. Featherstone,C. and Jackson,S.P. (1999) DNA double-strand break repair. Curr. Biol., 9, R759-R761.
27. Liang,L., Chen,J., Vittal,R., Selvanayagam,Z.E., McAteer,J.A., Deng,L., Tischfield,J., Chin,K.V. and Sahota,A. (2006) Expression profiling of crystal-induced injury in human kidney epithelial cells. Nephron Physiol., 103, 53-62.
28. Jessberger,R. and Berg,P. (1991) Repair of deletions and double-strand gaps by homologous recombination in a mammalian in vitro system. Mol. Cell. Biol., 11, 445-457.
29. Bradford,M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
30. Barnes,D.E., Tomkinson,A.E., Lehmann,A.R., Webster,A.D. and 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.
31. Riballo,E., Doherty,A.J., Dai,Y., Stiff,T., Oettinger,M.A., Jeggo,P.A. and Kysela,B. (2001) Cellular and biochemical impact of a mutation in DNA ligase IV conferring clinical radiosensitivity. J. Biol. Chem. 276, 31124-31132.
32. Tomkinson,A.E., Vijayakumar,S., Pascal,J.M. and Ellenberger,T. (2006) DNA ligases: Structure, reaction mechanism, and function. Chem. Rev. 106, 687-699.
33. Caldecott,K.W. (2003) XRCC1 and DNA strand break repair. DNA Repair 2, 955-969.
34. Maga,G. and Hubscher,U. (2003) Proliferating cell nuclear antigen (PCNA): A dancer with many partners. J. Cell. Sci., 116, 3051-3060.
35. Gottlich,B., Reichenberger,S., Feldmann,E. and Pfeiffer,P. (1998) Rejoining of DNA double-strand breaks in vitro by single-strand annealing. Eur. J. Biochem., 258, 387-395.
36. Audebert,M., Salles,B. and Calsou,P. (2004) 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., 279, 55117-55126.
37. Wang,H., Rosidi,B., Perrault,R., Wang,M., Zhang,L., Windhofer,F. and Iliakis,G. (2005) DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res., 65, 4020-4030.
38. Thompson,L.H., Brookman,K.W., Dillehay,L.E., Carrano,A.V., Mazrimas,J.A., Mooney,C.L. and Minkler,J.L. (1982) A CHO-cell strain having hypersensitivity to mutagens, a defect in DNA strand-break repair, and an extraordinary baseline frequency of sister-chromatid exchange. Mutat. Res., 95, 427-440.
39. Thompson,L.H., Brookman,K.W., Jones,N.J., Allen,S.A. and Carrano,A.V. (1990) Molecular cloning of the human XRCC1 gene, which corrects defective DNA strand break repair and sister chromatid exchange. Mol. Cell. Biol., 10, 6160-6171.
40. Wei,Y.F., Robins,P., Carter,K., Caldecott,K., Pappin,D.J., Yu,G.L., Wang,R.P., Shell,B.K., Nash,R.A., Schar,P. et al. (1995) Molecular cloning and expression of human cDNAs encoding a novel DNA ligase IV and DNA ligase III, an enzyme active in DNA repair and recombination. Mol. Cell. Biol., 15, 3206-3216.
41. Mackey,Z.B., Niedergang,C., Murcia,J.M., Leppard,J., Au,K., Chen,J., de Murcia,G. and Tomkinson,A.E. (1999) DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly(ADP-ribose) polymerase. Identification of two functionally distinct DNA binding regions within DNA ligase III. J. Biol. Chem., 274 21679-21687.
42. Taylor, R.M., Whitehouse,C.J. and Caldecott,K.W. (2000) The DNA ligase III zinc finger stimulates binding to DNA secondary structure and promotes end joining. Nucleic Acids Res., 28, 3558-3563.
43. Critchlow,S.E., Bowater,R.P. and Jackson,S.P. (1997) Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol., 7, 588-598.
44. Ahnesorg,P., Smith,P. and Jackson,S.P. (2006) XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell, 124, 301-313.
45. Ma,Y., Lu,H., Tippin,B., Goodman,M.F., Shimazaki,N., Koiwai,O., Hsieh,C.L., Schwarz,K. and Lieber,M.R. (2004) A biochemically defined system for mammalian nonhomologous DNA end joining. Mol. Cell., 16, 701-713.
46. Tseng,H.M. and Tomkinson,A.E. (2004) Processing and joining of DNA ends coordinated by interactions among Dnl4/Lif1, Pol4, and FEN-1. J. Biol. Chem., 279, 47580-47588.