NAD(P)H:quinone oxidoreductase 1 Arg139Trp and Pro187Ser polymorphisms imbalance estrogen metabolism towards DNA adduct formation in human mammary epithelial cells

Journal of Steroid Biochemistry and Molecular Biology

Volumn 117, Issue 1-3, 2009, Pages 56-66

  Singh, Seema ^a   Zahid, Muhammad ^a   Saeed, Muhammad ^a   Gaikwad, Nilesh W ^a   Meza, Jane L ^b   Cavalieri, Ercole L ^a   Rogan, Eleanor G ^a,c   Chakravarti, Dhrubajyoti ^a  

^a NEBRASKA MEDICAL CENTER   (United States)

^b Preventive and Societal Medicine   (United States)

^c UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

DNA adduct; Estrogen; Metabolism; NQO1; Polymorphism

Indexed keywords

2' FLUORO 3,4 DIHYDROXY 5 NITROBENZOPHENONE; ARGININE; CATECHOL DERIVATIVE; COMPLEMENTARY DNA; ESTRADIOL; ESTROGEN; ESTRONE; GLUTATHIONE; PROLINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SERINE; TRYPTOPHAN;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CATALYSIS; CELL LINE; CONJUGATE; CONTROLLED STUDY; CYTOTOXICITY; DNA ADDUCT; ELECTROCHEMICAL ANALYSIS; ENZYME ACTIVITY; ESTROGEN METABOLISM; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETIC TRANSFECTION; GENOTOXICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; METABOLITE; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; WILD TYPE;

AMINO ACID SUBSTITUTION; BASE SEQUENCE; BREAST; BREAST NEOPLASMS; DNA ADDUCTS; DNA PRIMERS; EPITHELIAL CELLS; ESTRADIOL; ESTROGENS; FEMALE; HUMANS; MODELS, BIOLOGICAL; NAD(P)H DEHYDROGENASE (QUINONE); POLYMORPHISM, SINGLE NUCLEOTIDE; RECOMBINANT PROTEINS; TRANSFECTION;

EID: 70249147174     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2009.07.003     Document Type: Article

References (53)

1. Chen S., Wu K., and Knox R. Structure-function studies of DT-diaphorase (NQO1) and NRH: quinone oxidoreductase (NQO2). Free Radic. Biol. Med. 29 (2000) 276-284
2. Nioi P., and Hayes J.D. Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat. Res. 555 (2004) 149-171
3. Siegelmann-Danieli N., and Buetow K.H. Significance of genetic variation at the glutathione S-transferase M1 and NAD(P)H:quinone oxidoreductase 1 detoxification genes in breast cancer development. Oncology 62 (2002) 39-45
4. Menzel H.J., Sarmanova J., Soucek P., Berberich R., Grunewald K., Haun M., and Kraft H.G. Association of NQO1 polymorphism with spontaneous breast cancer in two independent populations. Br. J. Cancer 90 (2004) 1989-1994
5. Singh S., Chakravarti D., Edney J.A., Hollins R.R., Johnson P.J., West W.W., Higginbotham S.M., Cavalieri E.L., and Rogan E.G. Relative imbalances in the expression of estrogen-metabolizing enzymes in the breast tissue of women with breast carcinoma. Oncol. Rep. 14 (2005) 1091-1096
6. Chakravarti D., Mailander P.C., Li K.-M., Higginbotham S., Zhang H.L., Gross M.L., Meza J.L., Cavalieri E.L., and Rogan E.G. Evidence that a burst of DNA depurination in SENCAR mouse skin induces error-prone repair and forms mutations in the H-ras gene. Oncogene 20 (2001) 7945-7953
7. Mailander P.C., Meza J.L., Higginbotham S., and Chakravarti D. Induction of A.T to G.C mutations by erroneous repair of depurinated DNA following estrogen treatment of the mammary gland of ACI rats. J. Steroid Biochem. Mol. Biol. 101 (2006) 204-215
8. Gaikwad N.W., Rogan E.G., and Cavalieri E.L. Evidence from ESI-MS for NQO1-catalyzed reduction of estrogen ortho-quinones. Free Radic. Biol. Med. 43 (2007) 1289-1298
9. Gaikwad N.W., Yang L., Rogan E.G., and Cavalieri E.L. Evidence for NQO2-mediated reduction of the carcinogenic estrogen ortho-quinones. Free Radic. Biol. Med. 46 (2009) 253-262
10. Talalay P., Fahey J.W., Holtzclaw W.D., Prestera T., and Zhang Y. Chemoprotection against cancer by phase 2 enzyme induction. Toxicol. Lett. 82-83 (1995) 173-179
11. Egner P.A., Kensler T.W., Prestera T., Talalay P., Libby A.H., Joyner H.H., and Curphey T.J. Regulation of phase 2 enzyme induction by oltipraz and other dithiolethiones. Carcinogenesis 15 (1994) 177-181
12. Jeffery E.H., and Stewart K.E. Upregulation of quinone reductase by glucosinolate hydrolysis products from dietary broccoli. Methods Enzymol. 382 (2004) 457-469
13. Lee Y.Y., Westphal A.H., de Haan L.H., Aarts J.M., Rietjens I.M., and van Berkel W.J. Human NAD(P)H:quinone oxidoreductase inhibition by flavonoids in living cells. Free Radic. Biol. Med. 39 (2005) 257-265
14. Moon Y.J., Wang X., and Morris M.E. Dietary flavonoids: effects on xenobiotic and carcinogen metabolism. Toxicol. In Vitro 20 (2006) 187-210
15. Hsieh T.C., Lu X., Wang Z., and Wu J.M. Induction of quinone reductase NQO1 by resveratrol in human K562 cells involves the antioxidant response element ARE and is accompanied by nuclear translocation of transcription factor Nrf2. Med. Chem. 2 (2006) 275-285
16. Montano M.M., Chaplin L.J., Deng H., Mesia-Vela S., Gaikwad N., Zahid M., and Rogan E. Protective roles of quinone reductase and tamoxifen against estrogen-induced mammary tumorigenesis. Oncogene 26 (2007) 3587-3590
17. Lu F., Zahid M., Wang C., Saeed M., Cavalieri E.L., and Rogan E.G. Resveratrol prevents estrogen-DNA adduct formation and neoplastic transformation in MCF-10F cells. Cancer Prev. Res. (Phila. Pa.) 1 (2008) 135-145
18. Hamajima N., Matsuo K., Iwata H., Shinoda M., Yamamura Y., Kato T., Hatooka S., Mitsudomi T., Suyama M., Kagami Y., Ogura M., Ando M., Sugimura Y., and Tajima K. NAD(P)H: quinone oxidoreductase 1 (NQO1) C609T polymorphism and the risk of eight cancers for Japanese. Int. J. Clin. Oncol. 7 (2002) 103-108
19. Sarmanova J., Susova S., Gut I., Mrhalova M., Kodet R., Adamek J., Roth Z., and Soucek P. Breast cancer: role of polymorphisms in biotransformation enzymes. Eur. J. Hum. Genet. 12 (2004) 848-854
20. Fowke J.H., Shu X.O., Dai Q., Jin F., Cai Q., Gao Y.T., and Zheng W. Oral contraceptive use and breast cancer risk: modification by NAD(P)H:quinone oxoreductase (NQO1) genetic polymorphisms. Cancer Epidemiol. Biomarkers Prev. 13 (2004) 1308-1315
21. Kelsey K.T., Ross D., Traver R.D., Christiani D.C., Zuo Z.F., Spitz M.R., Wang M., Xu X., Lee B.K., Schwartz B.S., and Wiencke J.K. Ethnic variation in the prevalence of a common NAD(P)H quinone oxidoreductase polymorphism and its implications for anti-cancer chemotherapy. Br. J. Cancer 76 (1997) 852-854
22. Pan S.S., Forrest G.L., Akman S.A., and Hu L.T. NAD(P)H:quinone oxidoreductase expression and mitomycin C resistance developed by human colon cancer HCT 116 cells. Cancer Res. 55 (1995) 330-335
23. Hu L.T., Stamberg J., and Pan S. The NAD(P)H:quinone oxidoreductase locus in human colon carcinoma HCT 116 cells resistant to mitomycin C. Cancer Res. 56 (1996) 5253-5259
24. Siegel D., Beall H., Senekowitsch C., Kasai M., Arai H., Gibson N.W., and Ross D. Bioreductive activation of mitomycin C by DT-diaphorase. Biochemistry 31 (1992) 7879-7885
25. Calaf G., and Russo J. Transformation of human breast epithelial cells by chemical carcinogens. Carcinogenesis 14 (1993) 483-492
26. Russo J., Hasan Lareef M., Balogh G., Guo S., and Russo I.H. Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 87 (2003) 1-25
27. Lu F., Zahid M., Saeed M., Cavalieri E.L., and Rogan E.G. Estrogen metabolism and formation of estrogen-DNA adducts in estradiol-treated MCF-10F cells. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin induction and catechol-O-methyltransferase inhibition. J. Steroid Biochem. Mol. Biol. 105 (2007) 150-158
28. Jaiswal A.K., McBride O.W., Adesnik M., and Nebert D.W. Human dioxin-inducible cytosolic NAD(P)H:menadione oxidoreductase. cDNA sequence and localization of gene to chromosome 16. J. Biol. Chem. 263 (1988) 13572-13578
29. Morgenstern J.P., and Land H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18 (1990) 3587-3596
30. Li A., Dubey S., Varney M.L., Dave B.J., and Singh R.K. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J. Immunol. 170 (2003) 3369-3376
31. Mannisto P.T., and Kaakkola S. Rationale for selective COMT inhibitors as adjuncts in the drug treatment of Parkinson's disease. Pharmacol. Toxicol. 66 (1990) 317-323
32. Zahid M., Saeed M., Lu F., Gaikwad N., Rogan E., and Cavalieri E. Inhibition of catechol-O-methyltransferase increases estrogen-DNA adduct formation. Free Radic. Biol. Med. 43 (2007) 1534-1540
33. Gaikwad N.W., Yang L., Muti P., Meza J.L., Pruthi S., Ingle J.N., Rogan E.G., and Cavalieri E.L. The molecular etiology of breast cancer: evidence from biomarkers of risk. Int. J. Cancer 122 (2008) 1949-1957
34. Siegel D., McGuinness S.M., Winski S.L., and Ross D. Genotype-phenotype relationships in studies of a polymorphism in NAD(P)H:quinone oxidoreductase 1. Pharmacogenetics 9 (1999) 113-121
35. Siegel D., Anwar A., Winski S.L., Kepa J.K., Zolman K.L., and Ross D. Rapid polyubiquitination and proteasomal degradation of a mutant form of NAD(P)H:quinone oxidoreductase 1. Mol. Pharmacol. 59 (2001) 263-268
36. Zahid M., Kohli E., Saeed M., Rogan E., and Cavalieri E. The greater reactivity of estradiol-3,4-quinone vs estradiol-2,3-quinone with DNA in the formation of depurinating adducts: implications for tumor-initiating activity. Chem. Res. Toxicol. 19 (2006) 164-172
37. Tabakovic K., and Abul-Hajj Y.J. Reaction of lysine with estrone 3,4-o-quinone. Chem. Res. Toxicol. 7 (1994) 696-701
38. Cao K., Devanesan P.D., Ramanathan R., Gross M.L., Rogan E.G., and Cavalieri E.L. Covalent binding of catechol estrogens to glutathione catalyzed by horseradish peroxidase, lactoperoxidase, or rat liver microsomes. Chem. Res. Toxicol. 11 (1998) 917-924
39. Tabakovic K., Gleason W.B., Ojala W.H., and Abul-Hajj Y.J. Oxidative transformation of 2-hydroxyestrone. Stability and reactivity of 2,3-estrone quinone and its relationship to estrogen carcinogenicity. Chem. Res. Toxicol. 9 (1996) 860-865
40. Venugopal D., Zahid M., Mailander P.C., Meza J.L., Rogan E.G., Cavalieri E.L., and Chakravarti D. Reduction of estrogen-induced transformation of mouse mammary epithelial cells by N-acetylcysteine. J. Steroid Biochem. Mol. Biol. 109 (2008) 22-30
41. Samuni A.M., Chuang E.Y., Krishna M.C., Stein W., DeGraff W., Russo A., and Mitchell J.B. Semiquinone radical intermediate in catecholic estrogen-mediated cytotoxicity and mutagenesis: chemoprevention strategies with antioxidants. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 5390-5395
42. Cavalieri E.L., Stack D.E., Devanesan P.D., Todorovic R., Dwivedy I., Higginbotham S., Johansson S.L., Patil K.D., Gross M.L., Gooden J.K., Ramanathan R., Cerny R.L., and Rogan E.G. Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 10937-10942
43. Li R., Bianchet M.A., Talalay P., and Amzel L.M. The three-dimensional structure of NAD(P)H:quinone reductase, a flavoprotein involved in cancer chemoprotection and chemotherapy: mechanism of the two-electron reduction. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 8846-8850
44. Faig M., Bianchet M.A., Talalay P., Chen S., Winski S., Ross D., and Amzel L.M. Structures of recombinant human and mouse NAD(P)H:quinone oxidoreductases: species comparison and structural changes with substrate binding and release. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 3177-3182
45. Bianchet M.A., Faig M., and Amzel L.M. Structure and mechanism of NAD[P]H:quinone acceptor oxidoreductases (NQO). Methods Enzymol. 382 (2004) 144-174
46. Chen S., Wu K., Zhang D., Sherman M., Knox R., and Yang C.S. Molecular characterization of binding of substrates and inhibitors to DT-diaphorase: combined approach involving site-directed mutagenesis, inhibitor-binding analysis, and computer modeling. Mol. Pharmacol. 56 (1999) 272-278
47. Ryk C., Kumar R., Sanyal S., de Verdier P.J., Hemminki K., Larsson P., Steineck G., and Hou S.M. Influence of polymorphism in DNA repair and defence genes on p53 mutations in bladder tumours. Cancer Lett. 241 (2006) 142-149
48. Cavalieri E., Frenkel K., Liehr J.G., Rogan E., and Roy D. Estrogens as endogenous genotoxic agents-DNA adducts and mutations. J. Natl. Cancer Inst. Monogr. 27 (2000) 75-93
49. Zheng W., Xie D.W., Jin F., Cheng J.R., Dai Q., Wen W.Q., Shu X.O., and Gao Y.T. Genetic polymorphism of cytochrome P450-1B1 and risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 9 (2000) 147-150
50. Wen W., Cai Q., Shu X.O., Cheng J.R., Parl F., Pierce L., Gao Y.T., and Zheng W. Cytochrome P450 1B1 and catechol-O-methyltransferase genetic polymorphisms and breast cancer risk in Chinese women: results from the shanghai breast cancer study and a meta-analysis. Cancer Epidemiol. Biomarkers Prev. 14 (2005) 329-335
51. Long J.R., Kataoka N., Shu X.O., Wen W., Gao Y.T., Cai Q., and Zheng W. Genetic polymorphisms of the CYP19A1 gene and breast cancer survival. Cancer Epidemiol. Biomarkers Prev. 15 (2006) 2115-2122
52. Long J.R., Cai Q., Shu X.O., Cai H., Gao Y.T., and Zheng W. Genetic polymorphisms in estrogen-metabolizing genes and breast cancer survival. Pharmacogenet Genomics 17 (2007) 331-338
53. Gaikwad N.W., Yang L., Pruthi S., Ingle J., Sandhu N., Rogan E.G., and Cavalieri E.L. Urine biomarkers of risk in the molecular etiology of breast cancer. Breast Cancer: Basic Clin. Res. 3 (2009) 1-8