2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces oxidative stress, DNA strand breaks, and poly(ADP-ribose) polymerase-1 activation in human breast carcinoma cell lines

Toxicology Letters

Volumn 172, Issue 3, 2007, Pages 146-158

  Lin, Po Hsiung ^a   Lin, Chia Hua ^a   Huang, Chuan Chen ^a   Chuang, Ming Chien ^a   Lin, Pinpin ^b  

^a NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^b NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

Author keywords

Dioxin; DNA damage; GSH; Oxidative stress; Poly(ADP ribose) polymerase 1

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ESTROGEN RECEPTOR ALPHA; GLUTATHIONE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; BREAST CARCINOMA; CANCER CELL CULTURE; CATALYSIS; CELL VIABILITY; COMET ASSAY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DNA REPAIR; DNA STRAND BREAKAGE; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEPLETION; WESTERN BLOTTING;

BENZAMIDES; BENZOFLAVONES; BREAST NEOPLASMS; CARCINOMA; CELL LINE, TUMOR; CELL SURVIVAL; COUMARINS; DNA BREAKS; ENVIRONMENTAL POLLUTANTS; ESTROGEN RECEPTOR ALPHA; GLUTATHIONE; HUMANS; NAD; NADP; OXIDATIVE STRESS; POLY(ADP-RIBOSE) POLYMERASES; REACTIVE OXYGEN SPECIES; RECEPTORS, ARYL HYDROCARBON; TAMOXIFEN; TETRACHLORODIBENZODIOXIN;

MAMMALIA;

EID: 34547559840     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2007.06.003     Document Type: Article

References (62)

1. Alaluusua S., Calderara P., Gerthoux P.M., Lukinmaa P.L., Kovero O., Needham L., Patterson Jr. D.G., Tuomisto J., and Mocarelli P. Developmental dental aberrations after the dioxin accident in Seveso. Environ. Health Perspect. 112 (2004) 1313-1318
2. American Cancer Society [ACS]. Cancer Facts and Figures (2006), American Cancer Society, Atlanta
3. Baccarelli A., Pfeiffer R., Consonni D., Pesatori A.C., Bonzini M., Patterson Jr. D.G., Bertazzi P.A., and Landi M.T. Handling of dioxin measurement data in the presence of non-detectable values: overview of available methods and their application in the Seveso chloracne study. Chemosphere 60 (2005) 898-906
4. Balasubramanian B., Pogozelski W.K., and Tullius T.D. DNA strand breaking by the hydroxyl radical is governed by the accessible surface areas of the hydrogen atoms of the DNA backbone. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 9738-9743
5. Bertazzi P.A., Consonni D., Bachetti S., Rubagotti M., Baccarelli A., Zocchetti C., and Pesatori A.C. Health effects of dioxin exposure: a 20-year mortality study. Am. J. Epidemiol. 153 (2001) 1031-1044
6. Breen A.P., and Murphy J.A. Reactions of oxyl radicals with DNA. Free Radic. Biol. Med. 18 (1995) 1033-1077
7. Caldecott K.W., Aoufouchi S., Johnson P., and Shall S. XRCC1 polypeptide interacts with DNA polymerase beta and possibly poly (ADP-ribose) polymerase, and DNA ligase III is a novel molecular 'nick-sensor' in vitro. Nucleic Acids Res. 24 (1996) 4387-4394
8. Caldecott K.W., Tucker J.D., Stanker L.H., and Thompson L.H. Characterization of the XRCC1-DNA ligase III complex in vitro and its absence from mutant hamster cells. Nucleic Acids Res. 23 (1995) 4836-4843
9. Caldecott K.W., McKeown C.K., Tucker J.D., Ljungquist S., and Thompson L.H. An interaction between the mammalian DNA repair protein XRCC1 and DNA ligase III. Mol. Cell. Biol. 14 (1994) 68-76
10. Chen H.L., Lee C.C., Liao P.C., Guo Y.L., Chen C.H., and Su H.J. Associations between dietary intake and serum polychlorinated dibenzo-p-dioxin and dibenzofuran (PCDD/F) levels in Taiwanese. Environ. Res. 91 (2003) 172-178
11. Chen Z.H., Hurh Y.J., Na H.K., Kim J.H., Chun Y.J., Kim D.H., Kang K.S., Cho M.H., and Surh Y.J. Resveratrol inhibits TCDD-induced expression of CYP1A1 and CYP1B1 and catechol estrogen-mediated oxidative DNA damage in cultured human mammary epithelial cells. Carcinogenesis 25 (2004) 2005-2013
12. Collier A.C., Pritsos K.L., and Pritsos C.A. TCDD as a biological response modifier for Mitomycin C: oxygen tension affects enzyme activation, reactive oxygen species and cell death. Life Sci. 78 (2006) 1499-1507
13. Demple B., and Harrison L. Repair of oxidative damage to DNA: enzymology and biology. Annu. Rev. Biochem. 63 (1994) 915-948
14. de Murcia G., and de Murcia J.M. Poly(ADP) ribose polymerase: a molecular nick sensor. Trends Biochem. Sci. 19 (1994) 172-176
15. Domingo J.L., Agramunt M.C., Nadal M., Schuhmacher M., and Corbella J. Health risk assessment of PCDD/PCDF exposure for the population living in the vicinity of a municipal waste incinerator. Arch. Environ. Contam. Toxicol. 43 (2002) 461-465
16. Eskenazi B., Warner M., Marks A.R., Samuels S., Gerthoux P.M., Vercellini P., Olive D.L., Needham L., Patterson Jr. D., and Mocarelli P. Serum dioxin concentrations and age at menopause. Environ. Health Perspect. 113 (2005) 858-862
17. Giri A.K. Mutagenic and genotoxic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin, a review. Mutat. Res. 168 (1986) 241-248
18. Hassoun E.A., Vodhanel J., and Abushaban A. The modulatory effects of ellagic acid and vitamin E succinate on TCDD-induced oxidative stress in different brain regions of rats after subchronic exposure. J. Biochem. Mol. Toxicol. 18 (2004) 196-203
19. Hilscherova K., Blankenship A.L., Nie M., Coady K.K., Upham B.L., Trosko J.E., and Giesy J.P. Oxidative stress in liver and brain of the hatchling chicken (Gallus domesticus) following in ovo injection with TCDD. Comp. Biochem. Physiol. C: Toxicol. Pharmacol. 136 (2003) 29-45
20. Huff J.E., Salmon A.G., Hooper N.K., and Zeise L. Long-term carcinogenesis studies on 2,3,7,8-tetrachlorodibenzo-p-dioxin and hexachlorodibenzo-p-dioxins. Cell Biol. Toxicol. 7 (1991) 67-94
21. Iannuzzi I., Perucatti A., Di Meo G.P., Polimeno F., Ciotola F., Incarnato D., Peretti V., Caputi-Jambrenghi A., Pecoraro A., Manniti F., D'Alessandro A., and Vonghia G. Chromosome fragility in two sheep flocks exposed to dioxins during pasturage. Mutagenesis 19 (2004) 355-359
22. Ishizuka S., Martin K., Booth C., Potten C.S., de Murcia G., Burkle A., and Kirkwood T.B. Poly(ADP-ribose) polymerase-1 is a survival factor for radiation-exposed intestinal epithelial stem cells in vivo. Nucleic Acids Res. 31 (2003) 6198-6205
23. Junod A.F., Jornot L., and Petersen H. Differential effects of hyperoxia and hydrogen peroxide on DNA damage, polyadenosine diphosphate-ribose polymerase activity, and nicotinamide adenine dinucleotide and adenosine triphosphate contents in cultured endothelial cells and fibroblasts. J. Cell. Physiol. 140 (1989) 177-185
24. Knerr S., Schaefer J., Both S., Mally A., Dekant W., and Schrenk D. 2,3,7,8-Tetrachlorodibenzo-p-dioxin induced cytochrome P450s alter the formation of reactive oxygen species in liver cells. Mol. Nutr. Food Res. 50 (2006) 378-384
25. Krokan H.E., Standal R., and Slupphaug G. DNA glycosylases in the base excision repair of DNA. Biochem. J. 325 Pt 1 (1997) 1-16
26. Kubota Y., Nash R.A., Klungland A., Schar P., Barnes D.E., and Lindahl T. Reconstitution of DNA base excision-repair with purified human proteins: interaction between DNA polymerase beta and the XRCC1 protein. EMBO J. 15 (1996) 6662-6670
27. Lee C.C., Guo Y.L., Kuei C.H., Chang H.Y., Hsu J.F., Wang S.T., and Liao P.C. Human PCDD/PCDF levels near a pentachlorophenol contamination site in Tainan, Taiwan. Chemosphere 65 (2006) 436-448
28. Lin C.H., and Lin P.H. Induction of ROS formation, poly(ADP-ribose) polymerase-1 activation, and cell death by PCB126 and PCB153 in human T47D and MDA-MB-231 breast cancer cells. Chem. Biol. Interact. 162 (2006) 181-194
29. Lin C.H., Leow H.T., Huang S.C., Nakamura J., Swenberg J.A., and Lin P.H. Induction of cytotoxicity, aldehydic DNA lesions, and poly(ADP-ribose) polymerase-1 activation by catechol derivatives of pentachlorophenol in calf thymus DNA and in human breast cancer cells. Chem. Res. Toxicol. 18 (2005) 257-264
30. Lin P., Chang Y.C., Chen C.H., Yang W.J., Cheng Y.H., and Chang L.W. A comparative study on the effects of 2,3,7,8,-tetrachlorodibenzo-p-dioxin polychlorinated biphenyl126 and estrogen in human bronchial epithelial cells. Toxicol. Appl. Pharmacol. 195 (2004) 83-91
31. Liu X., Yao J., Pisha E., Yang Y., Hua Y., van Breemen R.B., and Bolton J.L. Oxidative DNA damage induced by equine estrogen metabolites: role of estrogen receptor alpha. Chem. Res. Toxicol. 15 (2002) 512-519
32. Mimura J., and Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochim. Biophys. Acta 1619 (2003) 263-268
33. Mobley J.A., and Brueggemeier R.W. Estrogen receptor-mediated regulation of oxidative stress and DNA damage in breast cancer. Carcinogenesis 25 (2004) 3-9
34. Moennikes O., Loeppen S., Buchmann A., Andersson P., Ittrich C., Poellinger L., and Schwarz M. A constitutively active dioxin/aryl hydrocarbon receptor promotes hepatocarcinogenesis in mice. Cancer Res. 64 (2004) 4707-4710
35. Musarrat J., Arezina-Wilson J., and Wani A.A. Prognostic and aetiological relevance of 8-hydroxyguanosine in human breast carcinogenesis. Eur. J. Cancer 32A (1996) 1209-1214
36. Nakamura J., Asakura S., Hester S.D., de Murcia G., Caldecott K.W., and Swenberg J.A. 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 (2003) e104
37. Park J.Y., Shigenaga M.K., and Ames B.N. Induction of cytochrome P4501A1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin or indolo(3,2-b)carbazole is associated with oxidative DNA damage. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 2322-2327
38. Parke D.V., Ioannides C., and Lewis D.F. The 1990 Pharmaceutical Manufacturers Association of Canada keynote lecture. The role of the cytochromes P450 in the detoxication and activation of drugs and other chemicals. Can. J. Physiol. Pharmacol. 69 (1991) 537-549
39. Poland A., and Glover E. An estimate of the maximum in vivo covalent binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin to rat liver protein, ribosomal RNA, and DNA. Cancer Res. 39 (1979) 3341-3344
40. Rajapakse N., Butterworth M., and Kortenkamp A. Detection of DNA strand breaks and oxidized DNA bases at the single-cell level resulting from exposure to estradiol and hydroxylated metabolites. Environ. Mol. Mutagen. 45 (2005) 397-404
41. Rosenquist T.A., Zharkov D.O., and Grollman A.P. Cloning and characterization of a mammalian 8-oxoguanine DNA glycosylase. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 7429-7434
42. Sasaki J.C., Arey J., Eastmond D.A., Parks K.K., and Grosovsky A.J. Genotoxicity induced in human lymphoblasts by atmospheric reaction products of naphthalene and phenanthrene. Mutat. Res. 393 (1997) 23-35
43. Seiler J.P. A survey on the mutagenicity of various pesticides. Experientia 29 (1973) 622-623
44. Senft A.P., Dalton T.P., Nebert D.W., Genter M.B., Puga A., Hutchinson R.J., Kerzee J.K., Uno S., and Shertzer H.G. Mitochondrial reactive oxygen production is dependent on the aromatic hydrocarbon receptor. Free Radic. Biol. Med. 33 (2002) 1268-1278
45. Shen D., Dalton T.P., Nebert D.W., and Shertzer H.G. Glutathione redox state regulates mitochondrial reactive oxygen production. J. Biol. Chem. 280 (2005) 25305-25312
46. Shima H., Nakayasu M., Aonuma S., Sugimura T., and Nagao M. Loss of the MYC gene amplified in human HL-60 cells after treatment with inhibitors of poly(ADP-ribose) polymerase or with dimethyl sulfoxide. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 7442-7445
47. Sing N.P., McCoy M.T., Tice R.R., and Schneider E.L. A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res. 175 (1988) 184-191
48. Siraki A.G., Chan T.S., and O'Brien P.J. Application of quantitative structure-toxicity relationships for the comparison of the cytotoxicity of 14 p-benzoquinone congeners in primary cultured rat hepatocytes versus PC12 cells. Toxicol. Sci. 81 (2004) 148-159
49. Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica D., Warren J.T., Bokesch H., Kenney S., and Boyd M.R. New colorimetric cytotoxicity assay for anticancer-drug screening. J. Natl. Cancer Inst. 82 (1990) 1107-1112
50. Skidmore C.J., Davies M.I., Goodwin P.M., Halldorsson H., Lewis P.J., Shall S., and Zia'ee A.A. The involvement of poly(ADP-ribose) polymerase in the degradation of NAD caused by gamma-radiation and N-methyl-N-nitrosourea. Eur. J. Biochem. 101 (1979) 135-142
51. Stohs S.J. Oxidative stress induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Free Radic. Biol. Med. 9 (1990) 79-90
52. Sugimura T., Fujimura S., Hasegawa S., and Kawamura Y. Polymerization of the adenosine 5′-diphosphate ribose moiety of NAD by rat liver nuclear enzyme. Biochim. Biophys. Acta 138 (1967) 438-441
53. Viluksela M., Bager Y., Tuomisto J.T., Scheu G., Unkila M., Pohjanvirta R., Flodstrom S., Kosma V.M., Maki-Paakkanen J., Vartiainen T., Klimm C., Schramm K.W., Warngard L., and Tuomisto J. Liver tumor-promoting activity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in TCDD-sensitive and TCDD-resistant rat strains. Cancer Res. 60 (2000) 6911-6920
54. Vodenicharov M.D., Ghodgaonkar M.M., Halappanavar S.S., Shah R.G., and Shah G.M. Mechanism of early biphasic activation of poly(ADP-ribose) polymerase-1 in response to ultraviolet B radiation. J. Cell Sci. 118 (2005) 589-599
55. Vuchetich P.J., Bagchi D., Bagchi M., Hassoun E.A., Tang L., and Stohs S.J. Naphthalene-induced oxidative stress in rats and the protective effects of vitamin E succinate. Free Radic. Biol. Med. 21 (1996) 577-590
56. Wahba Z.Z., Murray W.J., Hassan M.Q., and Stohs S.J. Comparative effects of pair-feeding and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on various biochemical parameters in female rats. Toxicology 59 (1989) 311-323
57. Warner M., Eskenazi B., Mocarelli P., Gerthoux P.M., Samuels S., Needham L., Patterson D., and Brambilla P. Serum dioxin concentrations and breast cancer risk in the Seveso Women's Health Study. Environ. Health Perspect. 110 (2002) 625-628
58. Wassom J.S., Huff J.E., and Loprieno N. A review of the genetic toxicology of chlorinated dibenzo-p-dioxins. Mutat. Res. 47 (1977) 141-160
59. Whitehouse C.J., Taylor R.M., Thistlethwaite A., Zhang H., Karimi-Busheri F., Lasko D.D., Weinfeld M., and Caldecott K.W. XRCC1 stimulates human polynucleotide kinase activity at damaged DNA termini and accelerates DNA single-strand break repair. Cell 104 (2001) 107-117
60. Wyde M.E., Cambre T., Lebetkin M., Eldridge S.R., and Walker N.J. Promotion of altered hepatic foci by 2,3,7,8-tetrachlorodibenzo-p-dioxin and 17beta-estradiol in male Sprague-Dawley rats. Toxicol. Sci. 68 (2002) 295-303
61. Wyde M.E., Wong V.A., Kim A.H., Lucier G.W., and Walker N.J. Induction of hepatic 8-oxo-deoxyguanosine adducts by 2,3,7,8-tetrachlorodibenzo-p-dioxin in Sprague-Dawley rats is female-specific and estrogen-dependent. Chem. Res. Toxicol. 14 (2001) 849-855
62. Ying W., Sevigny M.B., Chen Y., and Swanson R.A. Poly(ADP-ribose) glycohydrolase mediates oxidative and excitotoxic neuronal death. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 12227-12232