Checkpoint protein Rad9 plays an important role in nucleotide excision repair

DNA Repair

Volumn 12, Issue 4, 2013, Pages 284-292

  Li, Tiepeng ^a,b   Wang, Zhixin ^c   Zhao, Yun ^a   He, Wei ^a,d   An, Lili ^a   Liu, Shengquan ^c   Liu, Yuheng ^a   Wang, Hailin ^c   Hang, Haiying ^a  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA damage checkpoint; Nucleotide excision repair; Rad9; Transcription regulation

Indexed keywords

BENZO[A]PYRENE 7,8 DIHYDRODIOL 9,10 OXIDE; DNA BINDING PROTEIN; PROTEIN DDB1; PROTEIN DDB2; PROTEIN RAD9; PYRIMIDINE DERIVATIVE; PYRIMIDINONE DERIVATIVE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; XERODERMA PIGMENTOSUM GROUP C PROTEIN; XERODERMA PIGMENTOSUM GROUP D PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; DNA DAMAGE CHECKPOINT; EXCISION REPAIR; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MAMMAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ULTRAVIOLET IRRADIATION;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; ANIMALS; CELL CYCLE PROTEINS; CHROMATIN; DNA ADDUCTS; DNA REPAIR; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; HEK293 CELLS; HELA CELLS; HUMANS; MICE; PROTEIN TRANSPORT; PYRIMIDINE DIMERS; RNA, SMALL INTERFERING; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

MAMMALIA;

EID: 84874982409     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.01.006     Document Type: Article

References (53)

1. Roos-Mattjus P., Hopkins K.M., Oestreich A.J., Vroman B.T., Johnson K.L., Naylor S., Lieberman H.B., Karnitz L.M. Phosphorylation of human Rad9 is required for genotoxin-activated checkpoint signaling. J. Biol. Chem. 2003, 278:24428-24437.
2. Hopkins K.M., Auerbach W., Wang X.Y., Hande M.P., Hang H., Wolgemuth D.J., Joyner A.L., Lieberman H.B. Deletion of mouse rad9 causes abnormal cellular responses to DNA damage, genomic instability, and embryonic lethality. Mol. Cell. Biol. 2004, 24:7235-7248.
3. Dang T., Bao S., Wang X.F. Human Rad9 is required for the activation of S-phase checkpoint and the maintenance of chromosomal stability. Genes Cells 2005, 10:287-295.
4. Pandita R.K., Sharma G.G., Laszlo A., Hopkins K.M., Davey S., Chakhparonian M., Gupta A., Wellinger R.J., Zhang J., Powell S.N., Roti Roti J.L., Lieberman H.B., Pandita T.K. Mammalian Rad9 plays a role in telomere stability, S- and G2-phase-specific cell survival, and homologous recombinational repair. Mol. Cell. Biol. 2006, 26:1850-1864.
5. Guan X., Bai H., Shi G., Theriot C.A., Hazra T.K., Mitra S., Lu A.L. The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates NEIL1 glycosylase. Nucleic Acids Res. 2007, 35:2463-2472.
6. Guan X., Madabushi A., Chang D.Y., Fitzgerald M.E., Shi G., Drohat A.C., Lu A.L. The human checkpoint sensor Rad9-Rad1-Hus1 interacts with and stimulates DNA repair enzyme TDG glycosylase. Nucleic Acids Res. 2007, 35:6207-6218.
7. He W., Zhao Y., Zhang C., An L., Hu Z., Liu Y., Han L., Bi L., Xie Z., Xue P., Yang F., Hang H. Rad9 plays an important role in DNA mismatch repair through physical interaction with MLH1. Nucleic Acids Res. 2008, 36:6406-6417.
8. Bai H., Madabushi A., Guan X., Lu A.L. Interaction between human mismatch repair recognition proteins and checkpoint sensor Rad9-Rad1-Hus1. DNA Repair 2010, 9:478-487.
9. Yin Y., Zhu A., Jin Y.J., Liu Y.X., Zhang X., Hopkins K.M., Lieberman H.B. Human RAD9 checkpoint control/proapoptotic protein can activate transcription of p21. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:8864-8869.
10. Ishikawa K., Ishii H., Murakumo Y., Mimori K., Kobayashi M., Yamamoto K., Mori M., Nishino H., Furukawa Y., Ichimura K. Rad9 modulates the P21WAF1 pathway by direct association with p53. BMC Mol. Biol. 2007, 8:37.
11. Komatsu K., Miyashita T., Hang H., Hopkins K.M., Zheng W., Cuddeback S., Yamada M., Lieberman H.B., Wang H.G. Human homologue of S. pombe Rad9 interacts with BCL-2/BCL-xL and promotes apoptosis. Nat. Cell Biol. 2000, 2:1-6.
12. Reardon J.T., Sancar A. Nucleotide excision repair. Prog. Nucleic Acid Res. Mol. Biol. 2005, 79:183-235.
13. Gillet L.C., Scharer O.D. Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem. Rev. 2006, 106:253-276.
14. Li R.Y., Calsou P., Jones C.J., Salles B. Interactions of the transcription/DNA repair factor TFIIH and XP repair proteins with DNA lesions in a cell-free repair assay. J. Mol. Biol. 1998, 281:211-218.
15. Yokoi M., Masutani C., Maekawa T., Sugasawa K., Ohkuma Y., Hanaoka F. The xeroderma pigmentosum group C protein complex XPC-HR23B plays an important role in the recruitment of transcription factor IIH to damaged DNA. J. Biol. Chem. 2000, 275:9870-9875.
16. Araujo S.J., Nigg E.A., Wood R.D. Strong functional interactions of TFIIH with XPC and XPG in human DNA nucleotide excision repair, without a preassembled repairosome. Mol. Cell. Biol. 2001, 21:2281-2291.
17. Mori T., Nakane M., Hattori T., Matsunaga T., Ihara M., Nikaido O. Simultaneous establishment of monoclonal antibodies specific for either cyclobutane pyrimidine dimer or (6-4)photoproduct from the same mouse immunized with ultraviolet-irradiated DNA. Photochem. Photobiol. 1991, 54:225-232.
18. Lieberman H.B., Hopkins K.M., Nass M., Demetrick D., Davey S. A human homolog of the Schizosaccharomyces pombe rad9+ checkpoint control gene. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13890-13895.
19. Hu Z., Liu Y., Zhang C., Zhao Y., He W., Han L., Yang L., Hopkins K.M., Yang X., Lieberman H.B., Hang H. Targeted deletion of Rad9 in mouse skin keratinocytes enhances genotoxin-induced tumor development. Cancer Res. 2008, 68:5552-5561.
20. Giannattasio M., Lazzaro F., Longhese M.P., Plevani P., Muzi-Falconi M. Physical and functional interactions between nucleotide excision repair and DNA damage checkpoint. EMBO J. 2004, 23:429-438.
21. Wang Z., Lu M., Wang X., Yin R., Song Y., Le X.C., Wang H. Quantum dots enhanced ultrasensitive detection of DNA adducts. Anal. Chem. 2009, 81:10285-10289.
22. Mone M.J., Volker M., Nikaido O., Mullenders L.H., van Zeeland A.A., Verschure P.J., Manders E.M., van Driel R. Local UV-induced DNA damage in cell nuclei results in local transcription inhibition. EMBO Rep. 2001, 2:1013-1017.
23. Adimoolam S., Ford J.M. p53 and DNA damage-inducible expression of the xeroderma pigmentosum group C gene. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:12985-12990.
24. Tan T., Chu G. p53 binds and activates the xeroderma pigmentosum DDB2 gene in humans but not mice. Mol. Cell. Biol. 2002, 22:3247-3254.
25. Murray J.M., Carr A.M., Lehmann A.R., Watts F.Z. Cloning and characterisation of the rad9 DNA repair gene from Schizosaccharomyces pombe. Nucleic Acids Res. 1991, 19:3525-3531.
26. Cosman M., de los Santos C., Fiala R., Hingerty B.E., Ibanez V., Luna E., Harvey R., Geacintov N.E., Broyde S., Patel D.J. Solution conformation of the (+)-cis-anti-[BP]dG adduct in a DNA duplex: intercalation of the covalently attached benzo[a]pyrenyl ring into the helix and displacement of the modified deoxyguanosine. Biochemistry 1993, 32:4145-4155.
27. Roos-Mattjus P., Vroman B.T., Burtelow M.A., Rauen M., Eapen A.K., Karnitz L.M. Genotoxin-induced Rad9-Hus1-Rad1(9-1-1) chromatin association is an early checkpoint signaling event. J. Biol. Chem. 2002, 277:43809-43812.
28. Zou L., Cortez D., Elledge S.J. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev. 2002, 16:198-208.
29. Delacroix S., Wagner J.M., Kobayashi M., Yamamoto K., Karnitz L.M. The Rad9-Hus1-Rad1(9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev. 2007, 21:1472-1477.
30. Sugasawa K. Multiple DNA damage recognition factors involved in mammalian nucleotide excision repair. Biochemistry (Moscow) 2011, 76:16-23.
31. Moser J., Volker M., Kool H., Alekseev S., Vrieling H., Yasui A., van Zeeland A.A., Mullenders L.H. The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair 2005, 4:571-582.
32. Sugasawa K., Okuda Y., Saijo M., Nishi R., Matsuda N., Chu G., Mori T., Iwai S., Tanaka K., Hanaoka F. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 2005, 121:387-400.
33. Yasuda G., Nishi R., Watanabe E., Mori T., Iwai S., Orioli D., Stefanini M., Hanaoka F., Sugasawa K. In vivo destabilization and functional defects of the xeroderma pigmentosum C protein caused by a pathogenic missense mutation. Mol. Cell. Biol. 2007, 27:6606-6614.
34. Reardon J.T., Nichols A.F., Keeney S., Smith C.A., Taylor J.S., Linn S., Sancar A. Comparative analysis of binding of human damaged DNA-binding protein (XPE) and Escherichia coli damage recognition protein (UvrA) to the major ultraviolet photoproducts: T[c,s]T, T[t,s]T, T[6-4]T, and T[Dewar]T. J. Biol. Chem. 1993, 268:21301-21308.
35. Treiber D.K., Chen Z., Essigmann J.M. An ultraviolet light-damaged DNA recognition protein absent in xeroderma pigmentosum group E cells binds selectively to pyrimidine (6-4) pyrimidone photoproducts. Nucleic Acids Res. 1992, 20:5805-5810.
36. Hwang B.J., Ford J.M., Hanawalt P.C., Chu G. Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:424-428.
37. Rapic-Otrin V., McLenigan M.P., Bisi D.C., Gonzalez M., Levine A.S. Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res. 2002, 30:2588-2598.
38. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., Liu J., Zhao X.D., Chew J.L., Lee Y.L., Kuznetsov V.A., Sung W.K., Miller L.D., Lim B., Liu E.T., Yu Q., Ng H.H., Ruan Y. A global map of p53 transcription-factor binding sites in the human genome. Cell 2006, 124:207-219.
39. St Onge R.P., Besley B.D., Pelley J.L., Davey S. A role for the phosphorylation of hRad9 in checkpoint signaling. J. Biol. Chem. 2003, 278:26620-26628.
40. He W., Ma X., Yang X., Zhao Y., Qiu J., Hang H. A role for the arginine methylation of Rad9 in checkpoint control and cellular sensitivity to DNA damage. Nucleic Acids Res. 2011, 39:4719-4727.
41. Wagner J.M., Karnitz L.M. Cisplatin-induced DNA damage activates replication checkpoint signaling components that differentially affect tumor cell survival. Mol. Pharmacol. 2009, 76:208-214.
42. Park M.J., Park J.H., Hahm S.H., Ko S.I., Lee Y.R., Chung J.H., Sohn S.Y., Cho Y., Kang L.W., Han Y.S. Repair activities of human 8-oxoguanine DNA glycosylase are stimulated by the interaction with human checkpoint sensor Rad9-Rad1-Hus1 complex. DNA Repair 2009, 8:1190-1200.
43. Medhurst A.L., Warmerdam D.O., Akerman I., Verwayen E.H., Kanaar R., Smits V.A., Lakin N.D. ATR and Rad17 collaborate in modulating Rad9 localisation at sites of DNA damage. J. Cell Sci. 2008, 121:3933-3940.
44. Warmerdam D.O., Freire R., Kanaar R., Smits V.A. Cell cycle-dependent processing of DNA lesions controls localization of Rad9 to sites of genotoxic stress. Cell Cycle 2009, 8:1765-1774.
45. He Z., Henricksen L.A., Wold M.S., Ingles C.J. RPA involvement in the damage-recognition and incision steps of nucleotide excision repair. Nature 1995, 374:566-569.
46. Li L., Lu X., Peterson C.A., Legerski R.J. An interaction between the DNA repair factor XPA and replication protein A appears essential for nucleotide excision repair. Mol. Cell. Biol. 1995, 15:5396-5402.
47. Marini F., Nardo T., Giannattasio M., Minuzzo M., Stefanini M., Plevani P., Muzi Falconi M. DNA nucleotide excision repair-dependent signaling to checkpoint activation. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:17325-17330.
48. Carcagno A.L., Ogara M.F., Sonzogni S.V., Marazita M.C., Sirkin P.F., Ceruti J.M., Canepa E.T. E2F1 transcription is induced by genotoxic stress through ATM/ATR activation. IUBMB Life 2009, 61:537-543.
49. Takimoto R., MacLachlan T.K., Dicker D.T., Niitsu Y., Mori T., el-Deiry W.S. BRCA1 transcriptionally regulates damaged DNA binding protein (DDB2) in the DNA repair response following UV-irradiation. Cancer Biol. Ther. 2002, 1:177-186.
50. Hartman A.R., Ford J.M. BRCA1 induces DNA damage recognition factors and enhances nucleotide excision repair. Nat. Genet. 2002, 32:180-184.
51. Gasch A.P., Huang M., Metzner S., Botstein D., Elledge S.J., Brown P.O. Genomic expression responses to DNA-damaging agents and the regulatory role of the yeast ATR homolog Mec1p. Mol. Biol. Cell 2001, 12:2987-3003.
52. Levine A.J. p53, the cellular gatekeeper for growth and division. Cell 1997, 88:323-331.
53. Fitch M.E., Cross I.V., Ford J.M. p53 responsive nucleotide excision repair gene products p48 and XPC, but not p53, localize to sites of UV-irradiation-induced DNA damage, in vivo. Carcinogenesis 2003, 24:843-850.