Gene expression changes in human prostate carcinoma cells exposed to genotoxic and nongenotoxic aryl hydrocarbon receptor ligands

Toxicology Letters

Volumn 206, Issue 2, 2011, Pages 178-188

  Hrubá, Eva ^a   Vondráček, Jan ^a,b   Líbalová, Helena ^c   Topinka, Jan ^c   Bryja, Vítězslav ^b   Souček, Karel ^b   Machala, Miroslav ^a  

^a VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^b INSTITUTE OF BIOPHYSICS   (Czech Republic)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin; Benzo a pyrene; Cell cycle; E2F1; LNCaP cells; WNT5A

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; BENZO[A]PYRENE; CELL CYCLE PROTEIN 20; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; LIGAND; POLYCYCLIC AROMATIC HYDROCARBON; PROTEIN; PROTEIN ADD3; PROTEIN AURKA; PROTEIN BCL 6; PROTEIN CCNA2; PROTEIN CENPA; PROTEIN ERCC6L; PROTEIN EXO1; PROTEIN FEN1; PROTEIN KIF15; PROTEIN MAD2L1; PROTEIN PCNA; PROTEIN RAD21; PROTEIN TOP2A; RAD51 PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR E2F2; TRANSCRIPTOME; UNCLASSIFIED DRUG; WNT5A PROTEIN;

ARTICLE; CANCER GROWTH; CARCINOMA CELL; CELL CYCLE PROGRESSION; CELL STRAIN LNCAP; CONTROLLED STUDY; DNA REPAIR; DNA REPLICATION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENOTOXICITY; HUMAN; HUMAN CELL; MALE; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION;

BENZO(A)PYRENE; CARCINOGENS, ENVIRONMENTAL; CARCINOMA; CELL CYCLE; CELL LINE, TUMOR; DNA REPAIR; DNA REPLICATION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIGANDS; MALE; MITOTIC SPINDLE APPARATUS; MUTAGENS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROSTATIC NEOPLASMS; PROTO-ONCOGENE PROTEINS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; TIME FACTORS; WNT PROTEINS;

EID: 80052088782     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2011.07.011     Document Type: Article

References (51)

1. ACS Cancer Facts & Figures 2008 2009, American Cancer Society, Atlanta.
2. Andersson P., McGuire J., Rubio C., Gradin K., Whitelaw M.L., Pettersson S., Hanberg A., Poellinger L. A constitutively active dioxin/aryl hydrocarbon receptor induces stomach tumors. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:9990-9995.
3. Barnes-Ellerbe S., Knudsen K.E., Puga A. 2,3,7,8-Tetrachlorodibenzo-p-dioxin blocks androgen-dependent cell proliferation of LNCaP cells through modulation of pRB phosphorylation. Mol. Pharmacol. 2004, 66:502-511.
4. Binková B., Giguere Y., Rössner P., Dostál M., Šrám R.J. The effect of dibenzo[a,1]pyrene and benzo[a]pyrene on human diploid lung fibroblasts: the induction of DNA adducts, expression of p53 and p21(WAF1) proteins and cell cycle distribution. Mutat. Res. 2000, 471:57-70.
5. Cao J., Chiarelli C., Richman O., Zarrabi K., Kozarekar P., Zucker S. Membrane type 1 matrix metalloproteinase induces epithelial-to-mesenchymal transition in prostate cancer. J. Biol. Chem. 2008, 283:6232-6240.
6. Chan C.Y., Kim P.M., Winn L.M. TCDD affects DNA double strand-break repair. Toxicol. Sci. 2004, 81:133-138.
7. Dai J., Hall C.L., Escara-Wilke J., Mizokami A., Keller J.M., Keller E.T. Prostate cancer induces bone metastasis through Wnt-induced bone morphogenetic protein-dependent and independent mechanisms. Cancer Res. 2008, 68:5785-5794.
8. Dietrich C., Kaina B. The aryl hydrocarbon receptor (AhR) in the regulation of cell-cell contact and tumor growth. Carcinogenesis 2010, 31:1319-1328.
9. Diry M., Tomkiewicz C., Koehle C., Coumoul X., Bock K.W., Barouki R., Transy C. Activation of the dioxin/aryl hydrocarbon receptor (AhR) modulates cell plasticity through a JNK-dependent mechanism. Oncogene 2006, 25:5570-5574.
10. Endo F., Monsees T.K., Akaza H., Schill W.B., Pflieger-Bruss S. Effects of single non-ortho, mono-ortho, and di-ortho chlorinated biphenyls on cell functions and proliferation of the human prostatic carcinoma cell line, LNCaP. Reprod. Toxicol. 2003, 17:229-236.
11. Fan Y., Boivin G.P., Knudsen E.S., Nebert D.W., Xia Y., Puga A. The aryl hydrocarbon receptor functions as a tumor suppressor of liver carcinogenesis. Cancer Res. 2010, 70:212-220.
12. Fritz W.A., Lin T.M., Cardiff R.D., Peterson R.E. The aryl hydrocarbon receptor inhibits prostate carcinogenesis in TRAMP mice. Carcinogenesis 2007, 28:497-505.
13. Fritz W.A., Lin T.M., Safe S., Moore R.W., Peterson R.E. The selective aryl hydrocarbon receptor modulator 6-methyl-1,3,8-trichlorodibenzofuran inhibits prostate tumor metastasis in TRAMP mice. Biochem. Pharmacol. 2009, 77:1151-1160.
14. Hockley S.L., Arlt V.M., Brewer D., Te Poele R., Workman P., Giddings I., Phillips D.H. AHR- and DNA-damage-mediated gene expression responses induced by benzo(a)pyrene in human cell lines. Chem. Res. Toxicol. 2007, 20:1797-1810.
15. Hockley S.L., Arlt V.M., Jahnke G., Hartwig A., Giddings I., Phillips D.H. Identification through microarray gene expression analysis of cellular responses to benzo(a)pyrene and its diol-epoxide that are dependent or independent of p53. Carcinogenesis 2008, 29:202-210.
16. Hrubá E., Trilecová L., Marvanová S., Krčmář P., Vykopalová L., Milcová A., Líbalová H., Topinka J., Staršíchová A., Souček K., Vondráček J., Machala M. Genotoxic polycyclic aromatic hydrocarbons fail to induce the p53-dependent DNA damage response, apoptosis or cell-cycle arrest in human prostate carcinoma LNCaP cells. Toxicol. Lett. 2010, 197:227-235.
17. Huang L., Pu Y., Hu W.Y., Birch L., Luccio-Camelo D., Yamaguchi T., Prins G.S. The role of Wnt5a in prostate gland development. Dev. Biol. 2009, 328:188-199.
18. IARC IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, Vol. 92: Some Non-heterocyclic Polycyclic Aromatic Hydrocarbons and Some Related Industrial Exposures 2010, IARC, Lyon.
19. Jana N.R., Sarkar S., Ishizuka M., Yonemoto J., Tohyama C., Sone H. Cross-talk between 2,3,7,8-tetrachlorodibenzo-p-dioxin and testosterone signal transduction pathways in LNCaP prostate cancer cells. Biochem. Biophys. Res. Commun. 1999, 256:462-468.
20. Khan Q.A., Vousden K.H., Dipple A. Cellular response to DNA damage from a potent carcinogen involves stabilization of p53 without induction of p21(waf1/cip1). Carcinogenesis 1997, 18:2313-2318.
21. Kizu R., Okamura K., Toriba A., Kakishima H., Mizokami A., Burnstein K.L., Hayakawa K. A role of aryl hydrocarbon receptor in the antiandrogenic effects of polycyclic aromatic hydrocarbons in LNCaP human prostate carcinoma cells. Arch. Toxicol. 2003, 77:335-343.
22. Kung T., Murphy K.A., White L.A. The aryl hydrocarbon receptor (AhR) pathway as a regulatory pathway for cell adhesion and matrix metabolism. Biochem. Pharmacol. 2009, 77:536-546.
23. Kurosu T., Fukuda T., Miki T., Miura O. BCL6 overexpression prevents increase in reactive oxygen species and inhibits apoptosis induced by chemotherapeutic reagents in B-cell lymphoma cells. Oncogene 2003, 22:4459-4468.
24. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
25. Luch A., Kudla K., Seidel A., Doehmer J., Greim H., Baird W.M. The level of DNA modification by (+)-syn-(11S,12R,13S,14R)- and (-)-anti-(11R,12S,13S,14R)-dihydrodiol epoxides of dibenzo[a,l]pyrene determined the effect on the proteins p53 and p21WAF1 in the human mammary carcinoma cell line MCF-7. Carcinogenesis 1999, 20:859-865.
26. Machala M., Vondráček J., Bláha L., Ciganek M., Neča J. Aryl hydrocarbon receptor-mediated activity of mutagenic polycyclic aromatic hydrocarbons determined using in vitro reporter gene assay. Mutat. Res. 2001, 497:49-62.
27. Moennikes O., Loeppen S., Buchmann A., Andersson P., Ittrich C., Poellinger L., Schwarz M. A constitutively active dioxin/aryl hydrocarbon receptor promotes hepatocarcinogenesis in mice. Cancer Res. 2004, 64:4707-4710.
28. Morrow D., Qin C., Smith R., 3rd, Safe S. Aryl hydrocarbon receptor-mediated inhibition of LNCaP prostate cancer cell growth and hormone-induced transactivation. J. Steroid Biochem. Mol. Biol. 2004, 88:27-36.
29. Nebert D.W., Dalton T.P., Okey A.B., Gonzalez F.J. Role of aryl hydrocarbon receptor-mediated induction of the CYP1 enzymes in environmental toxicity and cancer. J. Biol. Chem. 2004, 279:23847-23850.
30. Ohtake F., Baba A., Takada I., Okada M., Iwasaki K., Miki H., Takahashi S., Kouzmenko A., Nohara K., Chiba T., Fujii-Kuriyama Y., Kato S. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 2007, 446:562-566.
31. Phan R.T., Dalla-Favera R. The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature 2004, 432:635-639.
32. Plíšková M., Vondráček J., Vojtěšek B., Kozubík A., Machala M. Deregulation of cell proliferation by polycyclic aromatic hydrocarbons in human breast carcinoma MCF-7 cells reflects both genotoxic and nongenotoxic events. Toxicol. Sci. 2005, 83:246-256.
33. Puga A., Ma C., Marlowe J.L. The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem. Pharmacol. 2009, 77:713-722.
34. Qiao Y., Jiang X., Lee S.T., Karuturi R.K., Hooi S.C., Yu Q. FOXQ1 regulates epithelial-mesenchymal transition in human cancers. Cancer Res. 2011, 71:3076-3086.
35. Ramet M., Castren K., Jarvinen K., Pekkala K., Turpeenniemi-Hujanen T., Soini Y., Paakko P., Vahakangas K. p53 protein expression is correlated with benzo[a]pyrene-DNA adducts in carcinoma cell lines. Carcinogenesis 1995, 16:2117-2124.
36. Ray S., Swanson H.I. Activation of the aryl hydrocarbon receptor by TCDD inhibits senescence: a tumor promoting event?. Biochem. Pharmacol. 2009, 77:681-688.
37. Rybicki B.A., Neslund-Dudas C., Bock C.H., Rundle A., Savera A.T., Yang J.J., Nock N.L., Tang D. Polycyclic aromatic hydrocarbon--DNA adducts in prostate and biochemical recurrence after prostatectomy. Clin. Cancer Res. 2008, 14:750-757.
38. Schreck I., Chudziak D., Schneider S., Seidel A., Platt K.L., Oesch F., Weiss C. Influence of aryl hydrocarbon- (Ah) receptor and genotoxins on DNA repair gene expression and cell survival of mouse hepatoma cells. Toxicology 2009, 259:91-96.
39. Sinha R., Park Y., Graubard B.I., Leitzmann M.F., Hollenbeck A., Schatzkin A., Cross A.J. Meat and meat-related compounds and risk of prostate cancer in a large prospective cohort study in the United States. Am. J. Epidemiol. 2009, 170:1165-1177.
40. Smyth G.K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 2004, 3(1). Article 3.
41. Solhaug A., Refsnes M., Lag M., Schwarze P.E., Husoy T., Holme J.A. Polycyclic aromatic hydrocarbons induce both apoptotic and anti-apoptotic signals in Hepa1c1c7 cells. Carcinogenesis 2004, 25:809-819.
42. Stanbrough M., Bubley G.J., Ross K., Golub T.R., Rubin M.A., Penning T.M., Febbo P.G., Balk S.P. Increased expression of genes converting adrenal androgens to testosterone in androgen-independent prostate cancer. Cancer Res. 2006, 66:2815-2825.
43. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. PNAS 2005, 102:15545-15550.
44. Tekpli X., Rissel M., Huc L., Catheline D., Sergent O., Rioux V., Legrand P., Holme J.A., Dimanche-Boitrel M.T., Lagadic-Gossmann D. Membrane remodeling, an early event in benzo[a]pyrene-induced apoptosis. Toxicol. Appl. Pharmacol. 2010, 243:68-76.
45. Topinka J., Marvanová S., Vondráček J., Sevastyanova O., Nováková Z., Krčmář P., Pencikova K., Machala M. DNA adducts formation and induction of apoptosis in rat liver epithelial "stem-like" cells exposed to carcinogenic polycyclic aromatic hydrocarbons. Mutat. Res. 2008, 638:122-132.
46. Vezina C.M., Lin T.M., Peterson R.E. AHR signaling in prostate growth, morphogenesis, and disease. Biochem. Pharmacol. 2009, 77:566-576.
47. Wang Q., Symes A.J., Kane C.A., Freeman A., Nariculam J., Munson P., Thrasivoulou C., Masters J.R., Ahmed A. A novel role for Wnt/Ca2+ signaling in actin cytoskeleton remodeling and cell motility in prostate cancer. PLoS One 2010, 5:e10456.
48. Wu Z., Zheng S., Yu Q. The E2F family and the role of E2F1 in apoptosis. Int. J. Biochem. Cell. Biol. 2009, 41:2389-2397.
49. Xue W., Warshawsky D. Metabolic activation of polycyclic and heterocyclic aromatic hydrocarbons and DNA damage: a review. Toxicol. Appl. Pharmacol. 2005, 206:73-93.
50. Yamamoto H., Oue N., Sato A., Hasegawa Y., Matsubara A., Yasui W., Kikuchi A. Wnt5a signaling is involved in the aggressiveness of prostate cancer and expression of metalloproteinase. Oncogene 2010, 29:2036-2046.
51. Zhang H., Meng F., Liu G., Zhang B., Zhu J., Wu F., Ethier S.P., Miller F., Wu G. Forkhead transcription factor foxq1 promotes epithelial-mesenchymal transition and breast cancer metastasis. Cancer Res. 2011, 71:1292-1301.