Response of human mammary epithelial cells to DNA damage induced by BPDE: Involvement of novel regulatory pathways

Carcinogenesis

Volumn 24, Issue 2, 2003, Pages 225-234

  Wang, Aijin ^a   Gu, Jing ^a   Judson Kremer, Kimberly ^a   Powell, K Leslie ^a   Mistry, Harsha ^a   Simhambhatla, Padmaja ^a   Aldaz, C Marcelo ^a   Gaddis, Sally ^a   Mac Leod, Michael C ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARCINOGEN; DIHYDROXYBENZO[A]PYRENE OXIDE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; PROTEIN P21; PROTEIN P53; SERINE; TRANSCRIPTION FACTOR;

ADULT; ANALYTIC METHOD; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CASE REPORT; CELL COUNT; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EXCISION REPAIR; FLOW CYTOMETRY; GENE EXPRESSION; GENE TARGETING; GENETIC ANALYSIS; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; UPREGULATION;

7,8-DIHYDRO-7,8-DIHYDROXYBENZO(A)PYRENE 9,10-OXIDE; BREAST; CARCINOGENS; CELL CYCLE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA; DNA ADDUCTS; DNA DAMAGE; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; HUMANS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0037325927     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/24.2.225     Document Type: Article

References (68)

1. Friedberg,E.C. (2001) How nucleotide excision repair protects against cancer. Nature Rev. Cancer, 1, 22-33.
2. de Laat,W.L., Jaspers,N.G. and Hoeijmakers,J.H. (1999) Molecular mechanism of nucleotide excision repair. Genes Dev., 13, 768-785.
3. Lindahl,T. and Wood,R.D. (1999) Quality control by DNA repair. Science, 286, 1897-1905.
4. Zhang,Y., Yuan,F., Wu,X., Rechkoblit,O., Taylor,J.S., Geacintov,N.E. and Wang,Z. (2000) Error-prone lesion bypass by human DNA polymerase eta. Nucleic Acids Res., 28, 4717-4724.
5. Zhang,Y., Yuan,F., Wu,X., Wang,M., Rechkoblit,O., Taylor,J.S., Geacintov,N.E. and Wang,Z. (2000) Error-free and error-prone lesion bypass by human DNA polymerase kappa in vitro. Nucleic Acids Res., 28, 4138-4146.
6. Johnson,R.E., Haracska,L., Prakash,S. and Prakash,L. (2001) Role of DNA polymerase zeta in the bypass of a (6-4) TT photoproduct. Mol. Cell. Biol., 21, 3558-3563.
7. Johnson,R.E., Prakash,S. and Prakash,L. (1999) Efficient bypass of a thymine-thymine dimer by yeast DNA polymerase, Poleta. Science, 283, 1001-1004.
8. Washington,M.T., Johnson,R.E., Prakash,S. and Prakash,L. (2001) Mismatch extension ability of yeast and human DNA polymerase eta. J. Biol. Chem., 276, 2263-2266.
9. Washington,M.T., Johnson,R.E., Prakash,L. and Prakash,S. (2002) Human DINB1-encoded DNA polymerase kappa is a promiscuous extender of mispaired primer termini. Proc. Natl Acad. Sci. USA, 99, 1910-1914.
10. Yang,L.L., Maher,V.M. and McCormick,J.J. (1982) Relationship between excision repair and the cytotoxic and mutagenic effect of the 'anti' 7,8-diol-9,10-epoxide of benzo[a]pyrene in human cells. Mutat. Res., 94, 435-447.
11. MacLeod,M.C., Adair,G., Daylong,A., Lew,L. and Humphrey,R.M. (1991) Low absolute mutagenic efficiency but high cytotoxicity of a non-bay region diol epoxide derived from benzo[a]pyrene. Mutat. Res., 261, 281-293.
12. Brookes,P. and Osborne,M.R. (1982) Mutation in mammalian cells by stereoisomers of anti-benzo[a]pyrene-diolepoxide in relation to the extent and nature of the DNA reaction products. Carcinogenesis, 3, 1223-1226.
13. MacLeod,M.C., Adair,G. and Humphrey,R.M. (1988) Differential efficiency of mutagenesis at three genetic loci in CHO cells by a benzo[a]pyrene diol epoxide. Mutat. Res., 199, 243-254.
14. Kastan,M.B., Onyekwere,O., Sidransky,D., Vogelstein,B. and Craig,R.W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51, 6304-6311.
15. Oren,M. (1999) Regulation of the p53 tumor suppressor protein. J. Biol. Chem., 274, 36031-36034.
16. Sionov,R.V. and Haupt,Y. (1999) The cellular response to p53: the decision between life and death. Oncogene, 18, 6145-6157.
17. Vousden,K.H. (2000) p53: death star. Cell, 103, 691-694.
18. Harper,J.W., Adami,G.R., Wei,N., Keyomarsi,K. and Elledge,S.J. (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell, 75, 805-816.
19. Waldman,T., Kinzler,K.W. and Vogelstein,B. (1995) p21 is necessary for the p53-mediated G1 arrest in human cancer cells. Cancer Res., 55, 5187-5190.
20. Wang,X.W., Zhan,Q., Coursen,J.D., Khan,M.A., Kontny,H.U., Yu,L., Hollander,M.C., O'Connor,P.M., Fornace,A.J. Jr and Harris,C.C. (1999) GADD45 induction of a G2/M cell cycle checkpoint. Proc. Natl Acad. Sci. USA, 96, 3706-3711.
21. Oda,K., Arakawa,H., Tanaka,T., Matsuda,K., Tanikawa,C., Mori,T., Nishimori,H., Tamai,K., Tokino,T., Nakamura,Y. and Taya,Y. (2000) p53AIP1, a potential mediator of p53-dependent apoptosis and its regulation by Ser-46-phosphorylated p53. Cell, 102, 849-862.
22. Polyak,K., Xia,Y., Zweier,J.L., Kinzler,K.W. and Vogelstein,B. (1997) A model for p53-induced apoptosis. Nature, 389, 300-305.
23. Banin,S., Moyal,L., Shieh,S., Taya,Y., Anderson,C.W., Chessa,L., Smorodinsky,N.I., Prives,C., Reiss,Y., Shiloh,Y. and Ziv,Y. (1998) Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science, 281, 1674-1677.
24. Lakin,N.D., Hann,B.C. and Jackson,S.P. (1999) The ataxia-telangiectasia related protein ATR mediates DNA-dependent phosphorylation of p53. Oncogene, 18, 3989-3995.
25. Ramet,M., Castren,K., Jarvinen,K., Pekkala,K., Turpeenniemi-Hujanen,T., Soini,Y., Paakko,P. and Vahakangas,K. (1995) p53 protein expression is correlated with benzo[a]pyrene-DNA adducts in carcinoma cell lines. Carcinogenesis, 16, 2117-2124.
26. Khan,Q.A., Vousden,K.H. and Dipple,A. (1999) Lack of p53-mediated G1 arrest in response to an environmental carcinogen. Oncology, 57, 258-264.
27. Khan,Q.A., Vousden,K.H. and Dipple,A. (1997) Cellular response to DNA damage from a potent carcinogen involves stabilization of p53 without induction of p21 (waf1/cip1). Carcinogenesis, 18, 2313-2318.
28. Khan,Q.A. and Dipple,A. (2000) Diverse chemical carcinogens fail to induce G (1) arrest in MCF-7 cells. Carcinogenesis, 21, 1611-1618.
29. Meyer,K.M., Hess,S.M., Tlsty,T.D. and Leadon,S.A. (1999) Human mammary epithelial cells exhibit a differential p53-mediated response following exposure to ionizing radiation or UV light. Oncogene, 18, 5795-5805.
30. Flatt,P.M., Price,J.O., Shaw,A. and Pietenpol,J.A. (1998) Differential cell cycle checkpoint response in normal human keratinocytes and fibroblasts. Cell Growth Differ, 9, 535-543.
31. Wang,A., Pierce,A., Judson-Kremer,K., Gaddis,S., Aldaz,C.M., Johnson,D.G. and MacLeod,M.C. (1999) Rapid analysis of gene expression (RAGE) facilitates universal expression profiling. Nucleic Acids Res., 27, 4609-4618.
32. Gazdar,A.F., Kurvari,V., Virmani,A. et al. (1998) Characterization of paired tumor and non-tumor cell lines established from patients with breast cancer. Int. J. Cancer, 78, 766-774.
33. MacLeod,M.C. and Lew,L. (1988) A rapid, spectrophotometric assay for the integrity of diol epoxides. Carcinogenesis, 9, 2133-2135.
34. MacLeod,M.C., Adair,G., Dickson-Black,D., Pevny,T. and Humphrey,R.M. (1987) Stabilization of a reactive, electrophilic carcinogen, benzo[a]pyrene diol epoxide, by mammalian cells. Chem. Biol. Interact., 63, 279-289.
35. Hai,T., Wolfgang,C.D., Marsee,D.K., Allen,A.E. and Sivaprasad,U. (1999) ATF3 and stress responses. Gene Exp., 7, 321-335.
36. Fornace,A.J. Jr, Nebert,D.W., Hollander,M.C., Luethy,J.D., Papathanasiou,M., Fargnoli,J. and Holbrook,N.J. (1989) Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell. Biol., 9, 4196-4203.
37. Zhao,R., Gish,K., Murphy,M., Yin,Y., Notterman,D., Hoffman,W.H., Tom,E., Mack,D.H. and Levine,A.J. (2000) Analysis of p53-regulated gene expression patterns using oligonucleotide arrays. Genes Dev., 14, 981-993.
38. Yu,J., Zhang,L., Hwang,P.M., Rago,C., Kinzler,K.W. and Vogelstein,B. (1999) Identification and classification of p53-regulated genes. Proc. Natl Acad. Sci. USA, 96, 14517-14522.
39. Sugasawa,K., Ng,J.M., Masutani,C., Iwai,S., van der Spek,P.J., Eker,A.P., Hanaoka,F., Bootsma,D. and Hoeijmakers,J.H. (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell, 2, 223-232.
40. Unger,T., Juven-Gershon,T., Moallem,E., Berger,M., Vogt Sionov,R., Lozano,G., Oren,M. and Haupt,Y. (1999) Critical role for Ser20 of human p53 in the negative regulation of p53 by Mdm2. EMBO J., 18, 1805-1814.
41. Kapoor,M., Hamm,R., Yan,W., Taya,Y. and Lozano,G. (2000) Cooperative phosphorylation at multiple sites is required to activate p53 in response to UV radiation. Oncogene, 19, 358-364.
42. Chehab,N.H., Malikzay,A., Stavridi,E.S. and Halazonetis,T.D. (1999) Phosphorylation of Ser-20 mediates stabilization of human p53 in response to DNA damage. Proc. Natl Acad. Sci. USA, 96, 13777-13782.
43. Liang,G., Wolfgang,C.D., Chen,B.P., Chen,T.H. and Hai,T. (1996) ATF3 gene. Genomic organization, promoter and regulation. J. Biol. Chem., 271, 1695-1701.
44. van Dam,H., Wilhelm,D., Herr,I., Steffen,A., Herrlich,P. and Angel,P. (1995) ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J., 14, 1798-1811.
45. Smeal,T., Binetruy,B., Mercola,D.A., Birrer,M. and Karin,M. (1991) Oncogenic and transcriptional cooperation with Ha-Ras requires phosphorylation of c-Jun on serines 63 and 73. Nature, 354, 494-496.
46. Adler,V., Fuchs,S.Y., Kim,J., Kraft,A., King,M.P., Pelling,J. and Ronai,Z. (1995) jun-NH2-terminal kinase activation mediated by UV-induced DNA lesions in melanoma and fibroblast cells. Cell Growth Differ., 6, 1437-1446.
47. Khan,Q.A., Agarwal,R., Seidel,A., Frank,H., Vousden,K.H. and Dipple,A. (1998) DNA adduct levels associated with p53 induction and delay of MCF-7 cells in S phase after exposure to benzo[g]chrysene dihydrodiol epoxide enantiomers. Mol. Carcinogen., 23, 115-120.
48. Wani,M., El-Mahdy,M., Hamada,F., Wani,G., Zhu,Q., Wang,Q. and Wani,A. (2002) Efficient repair of bulky anti-BPDE DNA adducts from non-transcribed DNA strand requires functional p53 but not p21 (waf1/cip1) and pRb. Mutat. Res., 505, 13.
49. Buzek,J., Latonen,L., Kurki,S., Peltonen,K. and Laiho,M. (2002) Redox state of tumor suppressor p53 regulates its sequence-specific DNA binding in DNA-damaged cells by cysteine 277. Nucleic Acids Res., 30, 2340-2348.
50. Wolfgang,C.D., Chen,B.P., Martindale,J.L., Holbrook,N.J. and Hai,T. (1997) gadd153/Chop10, a potential target gene of the transcriptional repressor ATF3. Mol. Cell. Biol., 17, 6700-6707.
51. Wolfgang,C.D., Liang,G., Okamoto,Y., Allen,A.E. and Hai,T. (2000) Transcriptional autorepression of the stress-inducible gene ATF3. J. Biol. Chem., 275, 16865-16870.
52. Yan,C., Wang,H. and Boyd,D.D. (2002) ATF3 represses 72-kDa type IV collagenase (MMP-2) expression by antagonizing p53-dependent transactivation of the collagenase promoter. J. Biol. Chem., 277, 10804-10812.
53. Bain,G., Maandag,E.C., Izon,D.J. et al. (1994) E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell, 79, 885-892.
54. Funato,N., Ohtani,K., Ohyama,K., Kuroda,T. and Nakamura,M. (2001) Common regulation of growth arrest and differentiation of osteoblasts by helix-loop-helix factors. Mol. Cell. Biol., 21, 7416-7428.
55. Herblot,S., Aplan,P.D. and Hoang,T. (2002) Gradient of E2A activity in B-cell development. Mol. Cell. Biol., 22, 886-900.
56. Prabhu,S., Ignatova,A., Park,S.T. and Sun,X.H. (1997) Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol. Cell. Biol., 17, 5888-5896.
57. 2/M checkpoint. J. Biol. Chem., 275, 36892-36898.
58. 2/M transition by p53. Oncogene, 20, 1803-1815.
59. Takekawa,M., Adachi,M., Nakahata,A., Nakayama,I., Itoh,F., Tsukuda,H., Taya, Y. and Imai,K. (2000) p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J., 19, 6517-6526.
60. Mita,H., Tsutsui,J., Takekawa,M., Witten,E.A. and Saito,H. (2002) Regulation of MTK1/MEKK4 kinase activity by its N-terminal autoinhibitory domain and GADD45 binding. Mol. Cell. Biol., 22, 4544-4555.
61. Amundson,S.A., Bittner,M., Chen,Y., Trent,J., Meltzer,P. and Fornace,A.J. Jr (1999) Fluorescent cDNA microarray hybridization reveals complexity and heterogeneity of cellular genotoxic stress responses. Oncogene, 18, 3666-3672.
62. Kawauchi,J., Zhang,C., Nobori,K., Hashimoto,Y., M,T.A., Noda,A., Sunamori,M. and Kitajima,S. (2002) Transcriptional repressor ATF3 protects human umbilical vein endothelial cells from TNF-alpha-induced apoptosis through down-regulation of p53 transcription. J Biol Chem.
63. Allen-Jennings,A.E., Hartman,M.G., Kociba,G.J. and Hai.T. (2002) The roles of ATF3 in liver dysfunction and the regulation of phosphoenolpyruvate carboxykinase gene expression. J. Biol. Chem., 26, 26.
64. Mashima,T., Udagawa,S. and Tsuruo,T. (2001) Involvement of transcriptional repressor ATF3 in acceleration of caspase protease activation during DNA damaging agent-induced apoptosis. J. Cell. Physiol., 188, 352-358.
65. Zhang,C., Kawauchi,J., Adachi,M.T., Hashimoto,Y., Oshiro,S., Aso,T. and Kitajima,S. (2001) Activation of JNK and transcriptional repressor ATF3/LRF1 through the IRE1/TRAF2 pathway is implicated in human vascular endothelial cell death by homocysteine. Biochem. Biophys. Res. Commun., 289, 718-724.
66. Okamoto,Y., Chaves,A., Chen,J. et al. (2001) Transgenic mice with cardiac-specific expression of activating transcription factor 3, a stress-inducible gene, have conduction abnormalities and contractile dysfunction. Am. J. Pathol., 159, 639-650.
67. Allan,A.L., Albanese,C., Pestell,R.G. and LaMarre,J. (2001) Activating transcription factor 3 induces DNA synthesis and expression of cyclin D1 in hepatocytes. J. Biol. Chem., 276, 27272-27280.
68. Chu,H.M., Tan,Y., Kobierski,L.A., Balsam,L.B. and Comb,M.J. (1994) Activating transcription factor-3 stimulates 3,5-cyclic adenosine monophosphate-dependent gene expression. Mol. Endocrinol., 8, 59-68.