Evaluation of a bioluminescent mouse model expressing aromatase PII-promoter-controlled luciferase as a tool for the study of endocrine disrupting chemicals

Toxicology and Applied Pharmacology

Volumn 249, Issue 1, 2010, Pages 33-40

  Rivest, Patricia ^a   Devine, Patrick J ^a   Sanderson, J Thomas ^a  

^a UNIVERSITÉ LAVAL   (Canada)

Author keywords

Aromatase (CYP19); Atrazine; Bioluminescence; Endocrine disruption; In vivo imaging; PII promoter

Indexed keywords

AROMATASE; AROMATASE PII; ATRAZINE; ENDOCRINE DISRUPTOR; ESTRADIOL; FORSKOLIN; GONADOTROPIN; LUCIFERASE; UNCLASSIFIED DRUG; PHOTOPROTEIN;

ADRENAL CORTEX; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; CARCINOMA CELL; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; EPIDIDYMIS; ESTRADIOL BLOOD LEVEL; EX VIVO STUDY; FEMALE; GONAD; IN VIVO STUDY; MALE; MARE; MOUSE; NONHUMAN; OVARY; PREGNANCY; PROTEIN EXPRESSION; SCREENING; TESTIS; ANIMAL; BIOSYNTHESIS; ENZYMOLOGY; EVALUATION STUDY; GENE EXPRESSION REGULATION; GENETICS; HORSE; HUMAN; PHYSIOLOGY; PROMOTER REGION; TRANSGENIC MOUSE;

ANIMALS; AROMATASE; ENDOCRINE DISRUPTORS; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HORSES; HUMANS; LUCIFERASES; LUMINESCENT PROTEINS; MALE; MICE; MICE, TRANSGENIC; MODELS, ANIMAL; OVARY; PROMOTER REGIONS, GENETIC; TESTIS;

MUS;

EID: 77957882569     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2010.08.011     Document Type: Article

References (55)

1. Agarwal V.R., Bulun S.E., Simpson E.R. Quantitative detection of alternatively spliced transcripts of the aromatase cytochrome P450 (CYP19) gene in aromatase-expressing human cells by competitive RT-PCR. Mol. Cell. Probes 1995, 9:453-464.
2. Agarwal V.R., Bulun S.E., Leitch M., Rohrich R., Simpson E.R. Use of alternative promoters to express the aromatase cytochrome P450 (CYP19) gene in breast adipose tissues of cancer-free and breast cancer patients. J. Clin. Endocrinol. Metab. 1996, 81:3843-3849.
3. Andersen H.R., Vinggaard A.M., Rasmussen T.H., Gjermandsen I.M., Bonefeld-Jorgensen E.C. Effects of currently used pesticides in assays for estrogenicity, androgenicity, and aromatase activity in vitro. Toxicol. Appl. Pharmacol. 2002, 179:1-12.
4. Babic-Gojmerac T., Kniewald Z., Kniewald J. Testosterone metabolism in neuroendocrine organs in male rats under atrazine and deethylatrazine influence. J. Steroid Biochem. 1989, 33:141-146.
5. Bulun S.E. Aromatase deficiency and estrogen resistance: from molecular genetics to clinic. Semin. Reprod. Med. 2000, 18:31-39.
6. Bulun S.E., Sebastian S., Takayama K., Suzuki T., Sasano H., Shozu M. The human CYP19 (aromatase P450) gene: update on physiologic roles and genomic organization of promoters. J. Steroid Biochem. Mol. Biol. 2003, 86:219-224.
7. Bulun S.E., Lin Z., Imir G., Amin S., Demura M., Yilmaz B., Martin R., Utsunomiya H., Thung S., Gurates B., Tamura M., Langoi D., Deb S. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol. Rev. 2005, 57:359-383.
8. Campbell D.R., Kurzer M.S. Flavonoid inhibition of aromatase enzyme activity in human preadipocytes. J. Steroid Biochem. Mol. Biol. 1993, 46:381-388.
9. Canton R.F., Sanderson J.T., Letcher R.J., Bergman A., van den Berg M. Inhibition and induction of aromatase (CYP19) activity by brominated flame retardants in H295R human adrenocortical carcinoma cells. Toxicol. Sci. 2005, 88:447-455.
10. Coady K.K., Murphy M.B., Villeneuve D.L., Hecker M., Jones P.D., Carr J.A., Solomon K.R., Smith E.E., Van Der Kraak G., Kendall R.J., Giesy J.P. Effects of atrazine on metamorphosis, growth, laryngeal and gonadal development, aromatase activity, and sex steroid concentrations in Xenopus laevis. Ecotoxicol. Environ. Saf. 2005, 62:160-173.
11. Crain D.A., Guillette L.J., Rooney A.A., Pickford D.B. Alterations in steroidogenesis in alligators (Alligator mississippiensis) exposed naturally and experimentally to environmental contaminants. Environ. Health Perspect. 1997, 105:528-533.
12. Crain D.A., Spiteri I.D., Guillette L.J. The functional and structural observations of the neonatal reproductive system of alligators exposed in ovo to atrazine, 2, 4-D, or estradiol. Toxicol. Ind. Health 1999, 15:180-185.
13. Demura M., Bulun S.E. CpG dinucleotide methylation of the CYP19 I.3/II promoter modulates cAMP-stimulated aromatase activity. Mol. Cell. Endocrinol. 2008, 283:127-132.
14. Drenth H.-J., Bouwman C.A., Seinen W., Van den Berg M. Effects of some persistent halogenated environmental contaminants on aromatase (CYP19) activity in the human choriocarcinoma cell line JEG-3. Toxicol. Appl. Pharmacol. 1998, 148:50-55.
15. Fan W., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., Hayes T.B., Takayanagi R., Nawata H. Herbicide atrazine activates SF-1 by direct affinity and concomitant co-activators recruitments to induce aromatase expression via promoter II. Biochem. Biophys. Res. Commun. 2007, 355:1012-1018.
16. Fan W., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., Komatsu T., Morohashi K., Hayes T.B., Takayanagi R., Nawata H. Atrazine-induced aromatase expression is SF-1 dependent: implications for endocrine disruption in wildlife and reproductive cancers in humans. Environ. Health Perspect. 2007, 115:720-727.
17. Fernandez-Canton R., Letcher R.J., Sanderson J.T., Bergman A., van den Berg M. Effects of brominated flame retardants on activity of the steroidogenic enzyme aromatase (CYP19) in H295R human adrenocortical carcinoma cells in culture. Organohalogen Compd. 2003, 61:104-107.
18. Guillette L.J., Gunderson M.P. Alterations in development of reproductive and endocrine systems of wildlife populations exposed to endocrine-disrupting contaminants. Reproduction 2001, 122:857-864.
19. Guillette L.J., Gross T.S., Masson G.R., Matter J.M., Percival H.F., Woodward A.R. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ. Health Perspect. 1994, 102:680-688.
20. Harada N., Utsumi T., Takagi Y. Tissue-specific expression of the human aromatase cytochrome P-450 gene by alternative use of multiple exons 1 and promoters, and switching of tissue-specific exons 1 in carcinogenesis. Proc. Natl Acad. Sci. USA 1993, 90:11312-11316.
21. He Y., Murphy M.B., Yu R.M., Lam M.H., Hecker M., Giesy J.P., Wu R.S., Lam P.K. Effects of 20 PBDE metabolites on steroidogenesis in the H295R cell line. Toxicol. Lett. 2008, 176:230-238.
22. Hecker M., Park J.W., Murphy M.B., Jones P.D., Solomon K.R., Van Der Kraak G., Carr J.A., Smith E.E., du Preez L., Kendall R.J., Giesy J.P. Effects of atrazine on CYP19 gene expression and aromatase activity in testes and on plasma sex steroid concentrations of male African clawed frogs (Xenopus laevis). Toxicol. Sci. 2005, 86:273-280.
23. Heneweer M., van den Berg M., Sanderson J.T. A comparison of human H295R and rat R2C cell lines as in vitro screening tools for effects on aromatase. Toxicol. Lett. 2004, 146:183-194.
24. Heneweer M., van den Berg M., de Geest M.C., de Jong P.C., Bergman A., Sanderson J.T. Inhibition of aromatase activity by methyl sulfonyl PCB metabolites in primary culture of human mammary fibroblasts. Toxicol. Appl. Pharmacol. 2005, 202:50-58.
25. Holloway A.C., Anger D.A., Crankshaw D.J., Wu M., Foster W.G. Atrazine-induced changes in aromatase activity in estrogen sensitive target tissues. J. Appl. Toxicol. 2008, 28:260-270.
26. Ibrahim A.R., Abul-Hajj Y.J. Aromatase inhibition by flavonoids. J. Steroid Biochem. Mol. Biol. 1990, 37:257-260.
27. Kamat A., Hinshelwood M.M., Murry B.A., Mendelson C.R. Mechanisms in tissue-specific regulation of estrogen biosynthesis in humans. Trends Endocrinol. Metab. 2002, 13:122-128.
28. Laws S.C., Ferrell J.M., Stoker T.E., Schmid J., Cooper R.L. The effects of atrazine on female wistar rats: an evaluation of the protocol for assessing pubertal development and thyroid function. Toxicol. Sci. 2000, 58:366-376.
29. Le Bail J.C., Laroche T., Marre-Fournier F., Habrioux G. Aromatase and 17beta-hydroxysteroid dehydrogenase inhibition by flavonoids. Cancer Lett. 1998, 133:101-106.
30. Letcher R.J., Sanderson J.T., Bokkers A., Giesy J.P., van den Berg M. Effects of bisphenol A-related diphenylalkanes on vitellogenin production in male carp (Cyprinus carpio) hepatocytes and aromatase (CYP19) activity in human H295R adrenocortical carcinoma cells. Toxicol. Appl. Pharmacol. 2005, 209:95-104.
31. Mahendroo M.S., Mendelson C.R., Simpson E.R. Tissue-specific and hormonally controlled alternative promoters regulate aromatase cytochrome P450 gene expression in human adipose tissue. J. Biol. Chem. 1993, 268:19463-19470.
32. Mason J.I., Carr B.R., Murry B.A. Imidazole antimycotics: selective inhibitors of steroid aromatization and progesterone hydroxylation. Steroids 1987, 50:179-189.
33. Miller W.R., Dixon J.M. Antiaromatase agents: preclinical data and neoadjuvant therapy. Clin. Breast Cancer 2000, 1(Suppl 1):S9-S14.
34. Morinaga H., Yanase T., Nomura M., Okabe T., Goto K., Harada N., Nawata H. A benzimidazole fungicide, benomyl, and its metabolite, carbendazim, induce aromatase activity in a human ovarian granulose-like tumor cell line (KGN). Endocrinology 2004, 145:1860-1869.
35. Ohno K., Araki N., Yanase T., Nawata H., Iida M. A novel nonradioactive method for measuring aromatase activity using a human ovarian granulosa-like tumor cell line and an estrone ELISA. Toxicol. Sci. 2004, 82:443-450.
36. Pasqualini J.R., Chetrite G., Blacker C., Feinstein M.C., Delalonde L., Talbi M., Maloche C. Concentrations of estrone, estradiol, and estrone sulfate and evaluation of sulfatase and aromatase activities in pre- and postmenopausal breast cancer patients. J. Clin. Endocrinol. Metab. 1996, 81:1460-1464.
37. Pezzi V., Sirianni R., Chimento A., Maggiolini M., Bourguiba S., Delalande C., Carreau S., Ando S., Simpson E.R., Clyne C.D. Differential expression of steroidogenic factor-1/adrenal 4 binding protein and liver receptor homolog-1 (LRH-1)/fetoprotein transcription factor in the rat testis: LRH-1 as a potential regulator of testicular aromatase expression. Endocrinology 2004, 145:2186-2196.
38. Saarinen N., Joshi S.C., Ahotupa M., Li X., Ammala J., Makela S., Santti R. No evidence for the in vivo activity of aromatase-inhibiting flavonoids. J. Steroid Biochem. Mol. Biol. 2001, 78:231-239.
39. Sanderson J.T. The steroid hormone biosynthesis pathway as a target for endocrine-disrupting chemicals. Toxicol. Sci. 2006, 94:3-21.
40. Sanderson J.T., Seinen W., Giesy J.P., van den Berg M. 2-Chloro-s-triazine herbicides induce aromatase (CYP19) activity in H295R human adrenocortical carcinoma cells: a novel mechanism for estrogenicity?. Toxicol. Sci. 2000, 54:121-127.
41. Sanderson J.T., Letcher R.J., Heneweer M., Giesy J.P., van den Berg M. Effects of chloro-s-triazine herbicides and metabolites on aromatase activity in various human cell lines and on vitellogenin production in male carp hepatocytes. Environ. Health Perspect. 2001, 109:1027-1031.
42. Sanderson J.T., Boerma J., Lansbergen G.W., van den Berg M. Induction and inhibition of aromatase (CYP19) activity by various classes of pesticides in H295R human adrenocortical carcinoma cells. Toxicol. Appl. Pharmacol. 2002, 182:44-54.
43. Sanderson J.T., Hordijk J., Denison M.S., Springsteel M.F., Nantz M.H., Van Den Berg M. Induction and Inhibition of aromatase (CYP19) activity by natural and synthetic flavonoid compounds in H295R human adrenocortical carcinoma cells. Toxicol. Sci. 2004, 82:70-79.
44. Siegfried Z., Cedar H. DNA methylation: a molecular lock. Curr. Biol. 1997, 7:R305-R307.
45. Simpson E.R. Sources of estrogen and their importance. J. Steroid Biochem. Mol. Biol. 2003, 86:225-230.
46. Sirianni R., Seely J.B., Attia G., Stocco D.M., Carr B.R., Pezzi V., Rainey W.E. Liver receptor homologue-1 is expressed in human steroidogenic tissues and activates transcription of genes encoding steroidogenic enzymes. J. Endocrinol. 2002, 174:R13-R17.
47. Stoker T.E., Laws S.C., Guidici D.L., Cooper R.L. The effect of atrazine on puberty in male wistar rats: an evaluation in the protocol for the assessment of pubertal development and thyroid function. Toxicol. Sci. 2000, 58:50-59.
48. Stoker T.E., Guidici D.L., Laws S.C., Cooper R.L. The effects of atrazine metabolites on puberty and thyroid function in the male Wistar rat. Toxicol. Sci. 2002, 67:198-206.
49. Vinggaard A.M., Hnida C., Breinholt V., Larsen J.C. Screening of selected pesticides for inhibition of CYP19 aromatase activity in vitro. Toxicol. In Vitro 2000, 14:227-234.
50. Watanabe M., Nakajin S. Forskolin up-regulates aromatase (CYP19) activity and gene transcripts in the human adrenocortical carcinoma cell line H295R. J. Endocrinol. 2004, 180:125-133.
51. Yue W., Brodie A.M. Mechanisms of the actions of aromatase inhibitors 4-hydroxyandrostenedione, fadrozole, and aminoglutethimide on aromatase in JEG-3 cell culture. J. Steroid Biochem. Mol. Biol. 1997, 63:317-328.
52. Zar J.H. Biostatistical Analysis 1999, Prentice-Hall, N.J.
53. Zhao Y., Nichols J.E., Bulun S.E., Mendelson C.R., Simpson E.R. Aromatase P450 gene expression in human adipose tissue. Role of a Jak/STAT pathway in regulation of the adipose-specific promoter. J. Biol. Chem. 1995, 270:16449-16457.
54. Zhao Y., Agarwal V.R., Mendelson C.R., Simpson E.R. Transcriptional regulation of CYP19 gene (aromatase) expression in adipose stromal cells in primary culture. J. Steroid Biochem. Mol. Biol. 1997, 61:203-210.
55. Zhou J., Gurates B., Yang S., Sebastian S., Bulun S.E. Malignant breast epithelial cells stimulate aromatase expression via promoter II in human adipose fibroblasts: an epithelial-stromal interaction in breast tumors mediated by CCAAT/enhancer binding protein beta. Cancer Res. 2001, 61:2328-2334.