Induction of the transferrin receptor gene by benzo[a]pyrene in breast cancer MCF-7 cells: Potential as a biomarker of PAH exposure

Environmental and Molecular Mutagenesis

Volumn 47, Issue 7, 2006, Pages 518-526

  Kemp, Michael Q ^a   Liu, Wenjing ^a   Thorne, Patricia A ^a   Kane, Michael D ^b   Selmin, Ornella ^a   Romagnolo, Donate F ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b Genomic Solutions Inc   (United States)

Author keywords

Aromatic hydrocarbon receptor; Benzo a pyrene; Breast cancer; Polycyclic aromatic hydrocarbons; Transferrin receptor

Indexed keywords

ALPHA NAPHTHOFLAVONE; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; BETA 2 MICROGLOBULIN; CORTACTIN; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; FLAVONOID; POLYCYCLIC AROMATIC HYDROCARBON; TRANSCRIPTION FACTOR PAX3; TRANSFERRIN RECEPTOR;

ARTICLE; BIOTRANSFORMATION; BREAST CANCER; BREAST CARCINOGENESIS; CELL STRAIN MCF 7; CONTROLLED STUDY; DISEASE MARKER; DNA DAMAGE; GENE INDUCTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; LUNG CANCER; POLYMERASE CHAIN REACTION; PROMOTER REGION; RISK FACTOR;

BENZO(A)PYRENE; BREAST NEOPLASMS; CELL LINE, TUMOR; FEMALE; GENE EXPRESSION PROFILING; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYCYCLIC HYDROCARBONS, AROMATIC; PROMOTER REGIONS (GENETICS); RECEPTORS, TRANSFERRIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION, GENETIC; TUMOR MARKERS, BIOLOGICAL;

EID: 33747872435     PISSN: 08936692     EISSN: 10982280     Source Type: Journal    
DOI: 10.1002/em.20221     Document Type: Article

References (67)

1. American Cancer Society. 2005. Cancer facts and figures. American Cancer Society, Atlanta, GA.
2. Bernasconi M, Remppis A, Fredericks WJ, Rauscher FJ, III, Schafer BW. 1996. Induction of apoptosis in rhabdomyosarcoma cells through down-regulation of PAX proteins. Proc Natl Acad Sci USA 93:13164-13169.
3. Bonner MR. Han D, Nie J, Rogerson P, Vena JE, Muti P, Trevisan M, Edge SB, Freudenheim JL. 2005. Breast cancer risk and exposure in early life to polycyclic aromatic hydrocarbons using total suspended particulates as a proxy measure. Cancer Epidemiol Biomarkers Prev 14:53-60.
4. Casey JL, Di Jeso B, Rao KK, Rouault TA, Klausner RD, Harford JB. 1988. Deletional analysis of the promoter region of the human transfer™ receptor gene. Nucleic Acids Res 16:629-646.
5. Chi N. Epstein JA. 2002. Getting your Pax straight: Pax proteins in development and disease. Trends Genet 18:41-47.
6. Cleaver JE. 2005. Cancer in xeroderma pigmentosum and related dis-orders of DNA repair. Nat Rev Cancer 5:564-573.
7. Currier N, Solomon SE, Demicco EG, Chang DL, Farago M, Ying H, Dominguez I, Sonenshein GE, Cardiff RD, Xiao ZX, Sherr DH, Seldin DC. 2005. Oncogenic signaling pathways activated in DMBA-induced mouse mammary tumors. Toxicol Pathol 33:726-737.
8. Denissenko MF. Pao A, Tang M, Pfeifer GP. 1996. Preferential formation of Benzo[a]pyrene adducts at lung cancer mutational hotspots in p53. Science 274:430-432.
9. Dipple A, Khan QA, Page JE, Ponten I, Szeliga J. 1999. DNA reactions, mutagenic action and stealth properties of polycyclic aromatic hydrocarbon carcinogens. Int J Oncol 14:103-111.
10. Dixon B. Stet RJ, van Erp SH, Pohajdak B. 1993. Characterization of β2-microglobulin transcripts from two teleost species. Immunogenetics 38:27-34.
11. Drezen JM, Babinet C, Morello D. 1993. Transcriptional control of MHC class I, β2-microglobulin genes in vivo. J Immunol 150:2805-2813.
12. D'Urso CM, Wang ZG, Cao Y, Tatake R, Zeff RA, Ferrone S. 1991. Lack of HLA class 1 antigen expression by cultured melanoma cells FO-1 due to a defect in β2m gene expression. J Clin Invest 87:284-292.
13. Eisen MB, Spellman PT, Brown PO, Botstein D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 95:14863-14868.
14. El-Bayoumy K, Chae YH, Upadhyaya P, Rivenson A, Kurtzke C, Reddy B, Hecht SS. 1995. Comparative tumorigenicity of benzo[a]pyrene, 1-nitropyrene and 2-amino-1-methyl-6-phenylimidazo[4,5-6]pyridine administered by gavage to female CD rats. Carcinogenesis 16:431-434.
15. Escalon MP, Liu NS, Yang Y, Hess M, Walker PL, Smith TL, Dang NH. 2005. Prognostic factors and treatment of patients with T-cell non-Hodgkin lymphoma: The M.D. Anderson Cancer Center experience. Cancer 103:2091-2098.
16. Fantl V, Smith R, Brookes S, Dickson C, Peters G. 1993. Chromosome 11q13 abnormalities in human breast cancer. Cancer Surv 18:77-94.
17. Fujii-Kuriyama A, Mimura J. 2005. Molecular mechanisms of AhR functions in the regulation of cytochrome P450 genes. Biochem Biophys Res Commun 338:311-317.
18. Gammon MD, Santella RM, Neugut AI, Eng SM, Teitelbaum SL, Paykin A, Levin B, Terry MB, Young TL, Wang LW, Wang Q, Britton JA, Wolff MS, Stellman SD, Hatch M. Kabat GC, Senie R, Garbowski G, Maffeo C, Montalvan P, Berkowitz G. Kemeny M, Citron M, Schnabel F, Schuss A, Hajdu S. Vinceguerra V. 2002. Environmental toxins and breast cancer on Long Island. I. Polycyclic aromatic hydrocarbon DNA adducts Cancer Epidemiol Biomarkers Prev 11:677-685.
19. Gasiewicz TA, Rucci G. 1991. α-Naphthoflavone acts as an antagonist of 2,3.7,8-Tetrachlorodibenzo-p-dioxin by forming an inactive complex with the Ah receptor. Mol Phatmacol 40:607-612.
20. Glaze ER, Flowers L, Penning TM. 2001. Polycyclic aromatic hydrocarbon (PAH) ο-quinones generate reactive oxygen species (ROS) which results in 8-oxo-deoxyguanosine formation in DNA. Proc Am Assoc Cancer Res 42:2540.
21. Gwinn MR, Keshava C, Olivero OA, Humsi JA, Poirier MC, Weston A. 2005. Transcriptional signatures of normal human mammary epithelial cells in response to benzola]pyrene exposure: A comparison of three microarray platforms. OMICS 9:334-350.
22. Hecht SS. 2003. Tobacco carcinogens, their biomarkers and tobacco-induced cancer. Nat Rev Cancer 3:733-744.
23. Hentze MW, Muckenthaler MU, Andrews NC. 2004. Balancing acts: Molecular control of mammalian iron metabolism. Cell 117:285-297.
24. Hogemann-Savellano D, Bos E, Blondet C, Sato F, Abe T, Josephson L, Weissleder R, Gaudet J, Sgroi D, Peters PJ, Basilion JP. 2003. The transferrin receptor: A potential molecular imaging marker for human cancer. Neoplasia 5:495-506.
25. Hooper K, Petreas MX, Chuvakova T, Kazbekova G, Druz N, Seminova G. Sharmanov T, Hayward D, She J, Visita P, Winkler J, McKinney M, Wade TJ, Grassman J, Stephens RD. 1998. Analysis of breast milk to assess exposure to chlorinated contaminants in Kazakhstan: High levels of 2,3.7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in agricultural villages of southern Kazakhstan. Environ Health Perspect 106:797-806.
26. Huang C, Liu J, Haudenschild CC, Zhan X. 1998. The role of tyrosine phosphorylation of cortactin in the locomotion of endothelial cells. J Biol Chem 273:25770-25776.
27. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. 2004. Tobacco smoke and involuntary smoking. IARC Monogr Eval Carcinog Risks Hum 83:1-1438.
28. Jeffy BD, Chen EJ, Gudas JM, Romagnolo DF. 2000. Disruption of the cell cycle kinetics by benzo[a]pyrene: Inverse expression patterns of BRCA-1 and p53 in MCF-7 cells arrested in S, G2. Neoplasia 2:460-470.
29. Jeffy BD, Chirnomas RB, Chen EJ, Gudas JM, Romagnolo DF. 2002. Activation of the aromatic hydrocarbon receptor pathway is not sufficient for transcriptional repression of BRCA-1: Requirements for metabolism of benzo[i/]pyrene to 7r,8t-dihydroxy-9t,10-epoxy-7,8,9,10-tetrahydrobenzo[a] pyrene. Cancer Res 62:113-121.
30. Kairouz R, Daly RJ. 2000. Tyrosine kinase signalling in breast cancer: Modulation of tyrosine kinase signalling in human breast cancer through altered expression of signalling intermediates. Breast Cancer Res 2:197-202.
31. Kosinska W, von Pressentin MD, Guttenplan JB. 1999. Mutagen induced by benzo[a]pyrene in lacZ mouse mammary and oral tissues: Comparisons with mutagenesis in other organs and relationships to previous carcinogenicity assays. Carcinogenesis 20:1103-1106.
32. Krishnan V, Porter W, Santostefano M, Wang X, Safe S. 1995. Molecular mechanism of inhibition of estrogen-induced cathepsin D gene expression by 2,3,7,8-tetrachlorordibenzo-p-dioxin (TCDD) in MCF-7 cells. Mol Cell Biol 15:6710-6719.
33. Landi S. 2000. Mammalian class theta GST, differential susceptibility to carcinogens: A review. Mutat Res 463:247-283.
34. Landi S, Hanley NM, Warren SH, Pegram RA, DeMarini DM. 1999. Induction of genetic damage in human lymphocytes and mutations in Salmonella by trihalomethanes: Role of red blood cells and GSTT1-1 polymorphism. Mutagen 14:479-482.
35. Leadon SA, Stampfer MR, Bartley J. 1988. Production of oxidative DNA damage during the metabolic activation of benzo[a]pyrene in human mammary epithelial cells correlates with cell killing. Proc Nat Acad Sci USA 85:4365-4368.
36. Lemm F, Wilhelm M, Roos PH. 2004. Occupational exposure to polycyclic aromatic hydrocarbons suppresses constitutive expression of CYP1B1 on the transcript level in human leukocytes. Int J Hyg Environ Health 207:325-335.
37. Li D, Wang M, Firozi PF, Chang P, Zhang W, Baer-Dubowska W, Moorthy B, Vulimiri SV, Goth-Goldstein R, Weyand EH, DiGiovanni J. 2002. Characterization of a major aromatic DNA adduct detected in human breast tissues. Environ Mol Mutagen 39:193-200.
38. MacLeod MC, Selkirk JK. 1982. Physical interactions of isomeric benzo[a]pyrene diol-epoxides with DNA. Carcinogenesis 3:287-292.
39. Merchant M, Arellano L, Safe S. 1990. The mechanism of action of α-naphthoflavone as an inhibitor of 2,3,7,8-tetrachlorodibenzo-p-dioxin- induced CYP1A1 gene expression. Arch Biochem Biophys 281:84-89.
40. Muratovska A, Zhou C, He S, Goodyer P, Ecoles MR. 2003. Paired-Box genes are frequently expressed in cancer and often required for cancer cell survival. Oncogene 22:7989-7997.
41. Murray SA, Yang S, Demicco E, Ying H, Sherr DH, Hafer LJ, Rogers AE, Sonenshein GE, Xiao ZX. 2005. Increased expression of MDM2, cyclin D1, and p27Kip1 in carcinogen-induced rat mammary tumors. J Cell Biochem 95:875-884.
42. Parkin DM. 2004. International variation. Oncogene 23:6329-6340.
43. Penning TM, Ohnishi ST, Ohnishi T, Harvey RG. 1996. Generation of reactive oxygen species during the enzymatic oxidation of polycyclic aromatic hydrocarbon trans-dihydrodiols catalyzed by dihydrodiol dehydrogenase. Chem Res Toxicol 9:84-92.
44. Peto J, Collins N, Barfoot R, Seal S, Warren W, Rahman N, Easton DF, Evans C, Deacon J, Sratton MR. 1999. Prevalence of BRCA1 and BRCA2 gene mutations in patients with early-onset breast cancer. J Natl Cancer Inst 91:943-949.
45. Piskorska-Pliszczynska J, Keys B, Safe S, Newman MS. 1986. The cytosolic receptor binding affinities and AHH induction potencies of 29 polynuclear aromatic hydrocarbons. 34:67-74.
46. Pliskova M, Vondracek J, Vojtesek B, Kozubik A, Machala M. 2005. Deregulation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotixic events. Toxicol Sci 83:246-256.
47. Romagnolo D, Annab LA, Thompson TE, Risinger JI, Terry LA, Barrett JC, Afshari CA. 1998. Estrogen upregulation of BRCA-1 expression with no effect on localization. Mol Carcinog 22:102-109.
48. Ronai Z, Gradia S, el-Bayoumy K, Amin S, Hecht SS. 1994. Contrasting incidence of ras mutations in rat mammary and mouse skin tumors induced by anti-benzo[r]phenanthrene-3-,4-diol-1,2-epoxide. Carcinogenesis 15:2113-2116.
49. Russo IH, Russo J. 1996. Mammary gland neoplasia in long-term rodent studies. Environ Health Perspect 104:938-967.
50. Safe S, Krishnan V. 1995. Chlorinated hydrocarbons: Estrogens and anti-estrogens. Toxicol Lett 82/83:731-736.
51. Safe S, McDougal A, Gupta MS, Ramamoorthy K. 2001. Selective Ah receptor modulators (SAhRMs): Progress towards development of a new class of inhibitors of breast cancer growth. J Women's Cancer 3:37-45.
52. Santella RM, Gammon MD, Zhang YJ, Motykiewicz G, Young TL, Hayes SC, Terry MB, Schoenberg JB, Brinton LA, Bose S, Teitelbaum SL, Hibshoosh H. 2000. Immunohistochemical analysis of polycyclic aromatic hydrocarbon-DNA adducts in breast tumor tissue. Cancer Lett 154:143-149.
53. Scherer G, Frank S, Riedel K, Meger-Kossien I, Renner T. 2000. Biomonitoring of exposure to polycyclic aromatic hydrocarbons of non-occupationally exposed persons. Cancer Epidemiol Biomarkers Prev 9:373-380.
54. Selkirk JK, MacLeod MC, Kuroki T, Drevon C, Piccoli C, Montesano R. 1982. Benzo[a]pyrene metabolites: Formation in rat liver cell-culture lines, binding to macromolecules, and mutagenesis in V79 hamster cells. Carcinogenesis 3:635-639.
55. Selmin O, Thorne PA, Blachere FM, Johnson PD, Romagnolo DF. 2005. Transcriptional activation of the membrane-bound progesterone receptor (mPR) by dioxin, in endocrine-responsive tissues. Mol Reprod Dev 70:166-174.
56. Shih HA, Nathanson KL, Seal S, Collins N, Stratton MR, Rebbeck TR, Weber BL. 2000. BRCA1 and BRCA2 mutations in breast cancer families with multiple primary cancers. Clin Cancer Res 6:4259-4264.
57. Smith CA, Smith G, Wolf CR. 1994. Genetic polymorphisms in xenobiotic metabolism. Eur J Cancer 30A:1921-1935.
58. Sram RJ, Binkova B. 2000. Molecular epidemiology studies on occupational and environmental exposure to mutagens and carcinogens, 1997-1999. Environ Health Perspect 108:57-70.
59. Tacchini L, Bianchi L, Bernelli-Zazzera A, Cairo G. 1999. Transferrin receptor induction by hypoxia. J Biol Chem 274:24142-24146.
60. Terry MB, Gammon MD, Zhang FF, Eng SM, Sagiv SK, Paykin AB. Wang Q, Hayes S, Teitelbaum SL, Neugut AI, Santella RM. 2004. Polymorphism in the DNA repair gene XPD, polycyclic aromatic hydrocarbon-DNA adducts, cigarette smoking, and breast cancer risk. Cancer Epidemiol Biomarkers Prev 13:2053-2058.
61. Thier R, Penible SE, Kramer H, Taylor JB, Guengerich FP, Ketterer B. 1996. Human glutathione S-transferase T1-1 enhances mutagenicity of 1,2-dibromoethane, dibromomethane and 1,2,3,4-diepoxybutane in Salmonella typhimurium. Carcinogenesis 17:163-166.
62. Toide K, Yamazaki H, Nagashima R, Itoh K, Iwano S, Takahashi Y, Watanabe S, Kamataki T. 2003. Aryl hydrocarbon hydroxylase represents CYP1B1, and not CYP1A1, in human freshly isolated white cells: Trimodal distribution of Japanese population according to induction of CYP1B1 mRNA by environmental dioxins. Cancer Epidemiol Biomarkers Prev 12:219-222.
63. Toyokuni S. 1996. Iron-induced Carcinogenesis: The role of redox regulation. Free Radic Biol Med 20:553-566.
64. Vanden Heuvel JP, Clark GC, Kohn MC, Tritscher AM, Greenlee WF, Lucier GW, Bell DA. 1994. Dioxin-responsive genes: Examination of dose-response relationships using quantitative reverse transcriptase-polymerase chain reaction. Cancer Res 54:62-68.
65. Weiss J, Papke O, Bignert A, Jensen S, Greyerz E, Agostoni C, Besana R, Riva E, Giovannini M, Zetterstrom R. 2003. Concentrations of dioxins and other organochlorines (PCBs, DDTs, HCHs) in human milk from Seveso, Milan and a Lombardian rural area in Italy: A study performed 25 years after the heavy dioxin exposure in Seveso. Acta Paediatr 92:467-472.
66. Wogan GN, Hecht SS, Felton JS, Conney AH, Loeb LA. 2004. Environmental and chemical Carcinogenesis. Semin Cancer Biol 14:473-486.
67. Yang DC, Jiang XP, Elliott RL, Head JF. 2001. Inhibition of growth of human breast carcinoma cells by an antisense oligonucleotide targeted to the transferrin receptor gene. Anticancer Res 21:1777-1787.