JWA regulates XRCC1 and functions as a novel base excision repair protein in oxidative-stress-induced DNA single-strand breaks

Nucleic Acids Research

Volumn 37, Issue 6, 2009, Pages 1936-1950

  Wang, Shouyu ^a   Gong, Zhenghua ^a   Chen, Rui ^a   Liu, Yunru ^a   Li, Aiping ^a   Li, Gang ^b   Zhou, Jianwei ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; HYDROGEN PEROXIDE; JWA PROTEIN; MESYLIC ACID; MITOGEN ACTIVATED PROTEIN KINASE; PROTEASOME; TRANSCRIPTION FACTOR E2F1; UNCLASSIFIED DRUG; XRCC1 PROTEIN; ARL6IP5 PROTEIN, HUMAN; HEAT SHOCK PROTEIN; SIGNAL PEPTIDE; X-RAY REPAIR CROSS COMPLEMENTING PROTEIN 1;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXCISION REPAIR; GENE FUNCTION; GENE INTERACTION; GENE LOCATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DNA INTERACTION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SINGLE STRANDED DNA BREAK; TRANSCRIPTION REGULATION; UBIQUITINATION; ANIMAL; BIOSYNTHESIS; CELL LINE; DNA REPAIR; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN STABILITY;

ANIMALS; CELL LINE; CELL NUCLEUS; DNA BREAKS, SINGLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; E2F1 TRANSCRIPTION FACTOR; HEAT-SHOCK PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; OXIDATIVE STRESS; PROTEIN STABILITY; PROTEIN TRANSPORT; TRANSCRIPTION, GENETIC;

EID: 64549145363     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkp054     Document Type: Article

References (65)

1. Lindahl,T. (1993) Instability and decay of the primary structure of DNA. Nature, 362, 709-715.
2. Caldecott,K.W. (2001) Mammalian DNA single-strand break repair: An X-ra(y)ted affair. Bioessays, 23, 447-455.
3. Xu,Y.J., Kim,E.Y. and Demple,B. (1998) Excision of C-4'-oxidized deoxyribose lesions from double-stranded DNA by human apurinic/ apyrimidinic endonuclease (Ape1 protein) and DNA polymerase beta. J. Biol. Chem., 273, 28837-28844.
4. Carrano,A.V., Minkler,J.L., Dillehay,L.E. and Thompson,L.H. (1986) Incorporated bromodeoxyuridine enhances the sisterchromatid exchange and chromosomal aberration frequencies in an EMS-sensitive Chinese hamster cell line. Mutat. Res., 162, 233-239.
5. Dominguez,I., Daza,P., Natarajan,A.T. and Cortes,F. (1998) A high yield of translocations parallels the high yield of sister chromatid exchanges in the CHO mutant EM9. Mutat. Res., 398, 67-73.
6. Kuzminov,A. (2001) Single-strand interruptions in replicating chromosomes cause double-strand breaks. Proc. Natl Acad. Sci. USA, 98, 8241-8246.
7. Hanahan,D. and Weinberg,R.A. (2000) The hallmarks of cancer. Cell, 100, 57-70.
8. Caldecott,K.W. (2008) Single-strand break repair and genetic disease. Nat. Rev. Genet., 9, 619-631.
9. Caldecott,K.W. (2007) Mammalian single-strand break repair: Mechanisms and links with chromatin. DNA Repair (Amst), 6, 443-453.
10. Benjamin,R.C. and Gill,D.M. (1980) Poly(ADP-ribose) synthesis in vitro programmed by damaged DNA. A comparison of DNA molecules containing different types of strand breaks. J. Biol. Chem., 255, 10502-10508.
11. D'Amours,D., Desnoyers,S., D'Silva,I. and Poirier,G.G. (1999) Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. Biochem. J., 342 (Pt 2), 249-268.
12. Ohgushi,H., Yoshihara,K. and Kamiya,T. (1980) Bovine thymus poly(adenosine diphosphate ribose) polymerase. Physical properties and binding to DNA. J. Biol. Chem., 255, 6205-6211.
13. Ogata,N., Ueda,K., Kawaichi,M. and Hayaishi,O. (1981) Poly(ADP-ribose) synthetase, a main acceptor of poly(ADP-ribose) in isolated nuclei. J. Biol. Chem., 256, 4135-4137.
14. El-Khamisy,S.F., Masutani,M., Suzuki,H. and Caldecott,K.W. (2003) A requirement for PARP-1 for the assembly or stability of XRCC1 nuclear foci at sites of oxidative DNA damage. Nucleic Acids Res., 31 5526-5533.
15. Mortusewicz,O., Ame,J.C., Schreiber,V. and Leonhardt,H. (2007) Feedback-regulated poly(ADP-ribosyl)ation by PARP-1 is required for rapid response to DNA damage in living cells. Nucleic Acids Res., 35, 7665-7675.
16. Vidal,A.E., Boiteux,S., Hickson,I.D. and Radicella,J.P. (2001) XRCC1 coordinates the initial and late stages of DNA abasic site repair through protein-protein interactions. EMBO J., 20, 6530-6539.
17. Kubota,Y., Nash,R.A., Klungland,A., Schar,P., Barnes,D.E. and Lindahl,T. (1996) Reconstitution of DNA base excision-repair with purified human proteins: Interaction between DNA polymerase beta and the XRCC1 protein. EMBO J., 15, 6662-6670.
18. Whitehouse,C.J., Taylor,R.M., Thistlethwaite,A., Zhang,H., Karimi-Busheri,F., Lasko,D.D., Weinfeld,M. and Caldecott,K.W. (2001) XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell, 104, 107-117.
19. Fan,J., Otterlei,M., Wong,H.K., Tomkinson,A.E. and Wilson,D.M. III (2004) XRCC1 co-localizes and physically interacts with PCNA. Nucleic Acids Res., 32, 2193-2201.
20. Taylor,R.M., Wickstead,B., Cronin,S. and Caldecott,K.W. (1998) Role of a BRCT domain in the interaction of DNA ligase III-alpha with the DNA repair protein XRCC1. Curr. Biol., 8, 877-880.
21. Petermann,E., Keil,C. and Oei,S.L. (2006) Roles of DNA ligase III and XRCC1 in regulating the switch between short patch and long patch BER. DNA Repair (Amst), 5, 544-555.
22. Mortusewicz,O., Rothbauer,U., Cardoso,M.C. and Leonhardt,H. (2006) Differential recruitment of DNA ligase I and III to DNA repair sites. Nucleic Acids Res., 34, 3523-3532.
23. Zdzienicka,M.Z., van der Schans,G.P., Natarajan,A.T., Thompson,L.H., Neuteboom,I. and Simons,J.W. (1992) A Chinese hamster ovary cell mutant (EM-C11) with sensitivity to simple alkylating agents and a very high level of sister chromatid exchanges. Mutagenesis, 7, 265-269.
24. 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.
25. Green,A., Prager,A., Stoudt,P.M. and Murray,D. (1992) Relationships between DNA damage and the survival of radiosensitive mutant Chinese hamster cell lines exposed to gamma-radiation. Part 1: Intrinsic radiosensitivity. Int. J. Radiat. Biol, 61, 465-472.
26. Brem,R. and Hall,J. (2005) XRCC1 is required for DNA single-strand break repair in human cells. Nucleic Acids Res., 33, 2512-2520.
27. Puebla-Osorio,N., Lacey,D.B., Alt,F.W. and Zhu,C. (2006) Early embryonic lethality due to targeted inactivation of DNA ligase III. Mol. Cell Biol., 26, 3935-3941.
28. Tebbs,R.S., Thompson,L.H. and Cleaver,J.E. (2003) Rescue of Xrcc1 knockout mouse embryo lethality by transgenecomplementation. DNA Repair (Amst), 2, 1405-1417.
29. Tebbs,R.S., Flannery,M.L., Meneses,J.J., Hartmann,A., Tucker,J.D., Thompson,L.H., Cleaver,J.E. and Pedersen,R.A. (1999) Requirement for the Xrcc1 DNA base excision repair gene during early mouse development. Dev. Biol., 208, 513-529.
30. Yacoub,A., McKinstry,R., Hinman,D., Chung,T., Dent,P. and Hagan,M.P. (2003) Epidermal growth factor and ionizing radiation up-regulate the DNA repair genes XRCC1 and ERCC1 in DU145 and LNCaP prostate carcinoma through MAPK signaling. Radiat. Res., 159, 439-452.
31. Berkovich,E. and Ginsberg,D. (2001) Ras induces elevation of E2F-1 mRNA levels. J. Biol. Chem., 276, 42851-42856.
32. Pintus,G., Tadolini,B., Posadino,A.M., Sanna,B., Debidda,M., Carru,C., Deiana,L. and Ventura,C. (2003) PKC/Raf/MEK/ERK signaling pathway modulates native-LDL-induced E2F-1 gene expression and endothelial cell proliferation. Cardiovasc. Res., 59, 934-944.
33. Chen,D., Yu,Z., Zhu,Z. and Lopez,C.D. (2008) E2F1 regulates the base excision repair gene XRCC1 and promotes DNA repair. J. Biol. Chem. 283, 15381-15389.
34. Parsons,J.L., Tait,P.S., Finch,D., Dianova,II, Allinson,S.L. and Dianov,G.L. (2008) CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol. Cell, 29, 477-487.
35. Sobol,R.W. (2008) CHIPping away at base excision repair. Mol. Cell 29, 413-415.
36. Zhou,J.W., Di,Y.P., Zhao,Y.H. and Wu,R. (1999) In Ye,X.S., Shen,B.F. and Tang, (eds), Investigation on Cell Modulation: Signal Transduction, Apoptosis and Gene Expression, Military Medical Sciences Press, Beijing, pp. 110-119.
37. Chen,H., Bai,J., Ye,J., Liu,Z., Chen,R., Mao,W., Li,A. and Zhou,J. (2007) JWA as a functional molecule to regulate cancer cells migration via MAPK cascades and F-actin cytoskeleton. Cell Signal, 19, 1315-1327.
38. Huang,S., Shen,Q., Mao,W.G., Li,A.P., Ye,J., Liu,Q.Z., Zou,C.P. and Zhou,J.W. (2006) JWA, a novel signaling molecule, involved in all-trans retinoic acid induced differentiation of HL-60 cells. J. Biomed. Sci. 13, 357-371.
39. Huang,S., Shen,Q., Mao,W.G., Li,A.P., Ye,J., Liu,Q.Z., Zou,C.P. and Zhou,J.W. (2006) JWA, a novel signaling molecule, involved in the induction of differentiation of human myeloid leukemia cells. Biochem. Biophys. Res. Commun., 341, 440-450.
40. Zhu,T., Chen,R., Li,A., Liu,J., Gu,D., Liu,Q., H,C.C. and Zhou,J. (2006) JWA as a novel molecule involved in oxidative stress-associated signal pathway in myelogenous leukemia cells. J. Toxicol. Environ. Health A 69, 1399-1411.
41. Zhu,T., Chen,R., Li,A.P., Liu,J., Liu,Q.Z., Chang,H.C. and Zhou,J.W. (2005) Regulation of a novel cell differentiation-associated gene, JWA during oxidative damage in K562 and MCF-7 cells. J. Biomed. Sci., 12, 219-227.
42. Chen,R., Qiu,W., Liu,Z., Cao,X., Zhu,T., Li,A., Wei,Q. and Zhou,J. (2007) Identification of JWA as a novel functional gene responsive to environmental oxidative stress induced by benzo[a]-pyrene and hydrogen peroxide. Free Radic. Biol. Med., 42, 1704-1714.
43. Qiao,Y., Spitz,M.R., Guo,Z., Hadeyati,M., Grossman,L., Kraemer,K.H. and Wei,Q. (2002) Rapid assessment of repair of ultraviolet DNA damage with a modified host-cell reactivation assay using a luciferase reporter gene and correlation with polymorphisms of DNA repair genes in normal human lymphocytes. Mutat. Res., 509, 165-174.
44. Philpott,S.M. and Buehring,G.C. (1999) Defective DNA repair in cells with human T-cell leukemia/bovine leukemia viruses: Role of tax gene. J. Natl. Cancer Inst., 91, 933-942.
45. Nakamura,J., Asakura,S., Hester,S.D., de Murcia,G., Caldecott,K.W. and Swenberg,J.A. (2003) Quantitation of intracellular NAD(P)H can monitor an imbalance of DNA single strand break repair in base excision repair deficient cells in real time. Nucleic Acids Res., 31, e104.
46. Miyamae,Y., Iwasaki,K., Kinae,N., Tsuda,S., Murakami,M., Tanaka,M. and Sasaki,Y.F. (1997) Detection of DNA lesions induced by chemical mutagens using the single-cell gel electrophoresis (comet) assay. 2. Relationship between DNA migration and alkaline condition. Mutat. Res., 393 107-113.
47. Izumi,T., Wiederhold,L.R., Roy,G., Roy,R., Jaiswal,A., Bhakat,K.K., Mitra,S. and Hazra,T.K. (2003) Mammalian DNA base excision repair proteins: Their interactions and role in repair of oxidative DNA damage. Toxicology, 193, 43-65.
48. Watabe,M., Aoyama,K. and Nakaki,T. (2008) A dominant role of GTRAP3-18 in neuronal glutathione synthesis. J. Neurosci., 28, 9404-9413.
49. Fan,J., Wilson,P.F., Wong,H.K., Urbin,S.S., Thompson,L.H. and Wilson,D.M. III (2007) XRCC1 down-regulation in human cells leads to DNA-damaging agent hypersensitivity, elevated sister chromatid exchange, and reduced survival of BRCA2 mutant cells. Environ. Mol. Mutagen. 48, 491-500.
50. Okano,S., Lan,L., Caldecott,K.W., Mori,T. and Yasui,A. (2003) Spatial and temporal cellular responses to single-strand breaks in human cells. Mol. Cell Biol., 23, 3974-3981.
51. Au,W.W. and Henderson,B.R. (2007) Identification of sequences that target BRCA1 to nuclear foci following alkylative DNA damage. Cell Signal, 19, 1879-1892.
52. Petrini,J.H. and Stracker,T.H. (2003) The cellular response to DNA double-strand breaks: Defining the sensors and mediators. Trends Cell Biol., 13, 458-462.
53. Dellaire,G. and Bazett-Jones,D.P. (2007) Beyond repair foci: Subnuclear domains and the cellular response to DNA damage. Cell Cycle, 6 1864-1872.
54. Masson,M., Niedergang,C., Schreiber,V., Muller,S., Menissier-de Murcia,J. and de Murcia,G. (1998) XRCC1 is specifically associated with poly(ADP-ribose) polymerase and negatively regulates its activity following DNA damage. Mol. Cell Biol., 18, 3563-3571.
55. Yoon,S.O., Shin,S., Liu,Y., Ballif,B.A., Woo,M.S., Gygi,S.P. and Blenis,J. (2008) Ran-binding protein 3 phosphorylation links the Ras and PI3-kinase pathways to nucleocytoplasmic transport. Mol. Cell, 29, 362-375.
56. van der Horst,A., de Vries-Smits,A.M., Brenkman,A.B., van Triest,M.H., van den Broek,N., Colland,F., Maurice,M.M. and Burgering,B.M. (2006) FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP. Nat. Cell Biol., 8, 1064-1073.
57. Holbrook,N.J., Liu,Y. and Fornace,A.J. Jr. (1996) Signaling events controlling the molecular response to genotoxic stress. EXS, 77, 273-288.
58. Kharbanda,S., Pandey,P., Yamauchi,T., Kumar,S., Kaneki,M., Kumar,V., Bharti,A., Yuan,Z.M., Ghanem,L., Rana,A. et al. (2000) Activation of MEK kinase 1 by the c-Abl protein tyrosine kinase in response to DNA damage. Mol. Cell Biol., 20, 4979-4989.
59. Sundaresan,M., Yu,Z.X., Ferrans,V.J., Irani,K. and Finkel,T. (1995) Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science, 270, 296-299.
60. Lin,W.C., Lin,F.T. and Nevins,J.R. (2001) Selective induction of E2F1 in response to DNA damage, mediated by ATM-dependent phosphorylation. Genes Dev, 15, 1833-1844.
61. Stevens,C., Smith,L. and La Thangue,N.B. (2003) Chk2 activates E2F-1 in response to DNA damage. Nat. Cell Biol, 5, 401-409.
62. Dimova,D.K. and Dyson,N.J. (2005) The E2F transcriptional network: Old acquaintances with new faces. Oncogene, 24, 2810-2826.
63. Harris,S.L. and Levine,A.J. (2005) The p53 pathway: Positive and negative feedback loops. Oncogene, 24, 2899-2908.
64. Levy,N., Martz,A., Bresson,A., Spenlehauer,C., de Murcia,G. and Menissier-de Murcia,J. (2006) XRCC1 is phosphorylated by DNA-dependent protein kinase in response to DNA damage. Nucleic Acids Res., 34, 32-41.
65. Loizou,J.I., El-Khamisy,S.F., Zlatanou,A., Moore,D.J., Chan,D.W., Qin,J., Sarno,S., Meggio,F., Pinna,L.A. and Caldecott,K.W. (2004) The protein kinase CK2 facilitates repair of chromosomal DNA single-strand breaks. Cell, 117, 17-28.