Characterization of endocrine-disrupting chemicals based on hormonal balance disruption in male and female adult rats

Reproductive Toxicology

Volumn 33, Issue 3, 2012, Pages 339-352

  Quignot, Nadia ^a   Arnaud, Marine ^a   Robidel, Franck ^a   Lecomte, Anthony ^a   Tournier, Mikaël ^b   Cren Olivé, Cécile ^b   Barouki, Robert ^c,d   Lemazurier, Emmanuel ^a  

^a INSTITUT NATIONAL DE L ENVIRONNEMENT INDUSTRIEL ET DES RISQUES INERIS   (France)

^b Service Central d'Analyse   (France)

^c INSERM   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Aromatase; Endocrine disrupting chemicals; Hormonal balance; In vitro in vivo correlation; Toxicity

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; ANDROGEN; AROMATASE; ATRAZINE; ENDOCRINE DISRUPTOR; ESTROGEN; MESSENGER RNA; METHOXYCHLOR; SEX HORMONE; VINCLOZOLIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONJUGATION; CONTROLLED STUDY; DOSIMETRY; DRUG EFFICACY; ENDOCRINE DISEASE; ENZYME ACTIVITY; ENZYME REGULATION; ESTROGEN BLOOD LEVEL; FEMALE; GENITAL SYSTEM DISEASE; GONAD FUNCTION; HORMONAL REGULATION; HORMONE ACTION; HORMONE BLOOD LEVEL; IN VITRO STUDY; IN VIVO STUDY; MALE; NONHUMAN; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; STEROIDOGENESIS; UPREGULATION;

ADRENAL GLANDS; ANIMALS; AROMATASE; ATRAZINE; BODY WEIGHT; ENDOCRINE DISRUPTORS; ESTROUS CYCLE; FEMALE; GENITALIA, MALE; GONADAL STEROID HORMONES; LIVER; MALE; METHOXYCHLOR; MICROSOMES; ORGAN SIZE; OVARY; OXAZOLES; PHENOLS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPERM MOTILITY; UTERUS;

ANIMALIA; RATTUS;

EID: 84859769139     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2012.01.004     Document Type: Article

References (68)

1. Bretveld R.W., Thomas C.M., Scheepers P.T., Zielhuis G.A., Roeleveld N. Pesticide exposure: the hormonal function of the female reproductive system disrupted?. Reprod Biol Endocrinol 2006, 4:30.
2. Guillette L.J., Moore B.C. Environmental contaminants, fertility, and multioocytic follicles: a lesson from wildlife. Semin Reprod Med 2006, 24:134-141.
3. Rogan W.J., Ragan N.B. Some evidence of effects of environmental chemicals on the endocrine system in children. Int J Hyg Environ Health 2007, 210:659-667.
4. Toppari J., Larsen J.C., Christiansen P., Giwercman A., Grandjean P., Guillette L.J., et al. Male reproductive health and environmental xenoestrogens. Environ Health Perspect 1996, 104(Suppl. 4):741-803.
5. 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.
6. 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.
7. Simpson E.R., Mahendroo M.S., Nichols J.E., Bulun S.E. Aromatase gene expression in adipose tissue: relationship to breast cancer. Int J Fertil Menopausal Stud 1994, 39(Suppl 2):75-83.
8. Fan W., Yanase T., Morinaga H., Gondo S., Okabe T., Nomura M., et al. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. Molina-Molina J.M., Hillenweck A., Jouanin I., Zalko D., Cravedi J.P., Fernandez M.F., et al. Steroid receptor profiling of vinclozolin and its primary metabolites. Toxicol Appl Pharmacol 2006, 216:44-54.
14. Wong C., Kelce W.R., Sar M., Wilson E.M. Androgen receptor antagonist versus agonist activities of the fungicide vinclozolin relative to hydroxyflutamide. J Biol Chem 1995, 270:19998-20003.
15. Gray L.E., Ostby J., Monosson E., Kelce W.R. Environmental antiandrogens: low doses of the fungicide vinclozolin alter sexual differentiation of the male rat. Toxicol Ind Health 1999, 15:48-64.
16. Kelce W.R., Monosson E., Gamcsik M.P., Laws S.C., Gray L.E. Environmental hormone disruptors: evidence that vinclozolin developmental toxicity is mediated by antiandrogenic metabolites. Toxicol Appl Pharmacol 1994, 126:276-285.
17. Shelby M.D., Newbold R.R., Tully D.B., Chae K., Davis V.L. Assessing environmental chemicals for estrogenicity using a combination of in vitro and in vivo assays. Environ Health Perspect 1996, 104:1296-1300.
18. Cummings A.M. Methoxychlor as a model for environmental estrogens. Crit Rev Toxicol 1997, 27:367-379.
19. Gaido K.W., Maness S.C., McDonnell D.P., Dehal S.S., Kupfer D., Safe S. Interaction of methoxychlor and related compounds with estrogen receptor alpha and beta, and androgen receptor: structure-activity studies. Mol Pharmacol 2000, 58:852-858.
20. Hiroi H., Tsutsumi O., Momoeda M., Takai Y., Osuga Y., Taketani Y. Differential interactions of bisphenol A and 17beta-estradiol with estrogen receptor alpha (ERalpha) and ERbeta. Endocr J 1999, 46:773-778.
21. 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.
22. EPA. Integrated summary report on aromatase; 2007.
23. Simpson E.R., Clyne C., Rubin G., Boon W.C., Robertson K., Britt K., et al. Aromatase - a brief overview. Annu Rev Physiol 2002, 64:93-127.
24. Bouraima H., Lireux B., Mittre H., Benhaim A., Herrou M., Mahoudeau J., et al. Major hyperestrogenism in a feminizing adrenocortical adenoma despite a moderate overexpression of the aromatase enzyme. Eur J Endocrinol 2003, 148:457-461.
25. 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.
26. Bourguiba S., Genissel C., Lambard S., Bouraima H., Carreau S. Regulation of aromatase gene expression in Leydig cells and germ cells. J Steroid Biochem Mol Biol 2003, 86:335-343.
27. Stocco C. Aromatase expression in the ovary: hormonal and molecular regulation. Steroids 2008, 73:473-487.
28. Richards J.S., Fitzpatrick S.L., Clemens J.W., Morris J.K., Alliston T., Sirois J. Ovarian cell differentiation: a cascade of multiple hormones, cellular signals, and regulated genes. Recent Prog Horm Res 1995, 50:223-254.
29. Simpson E., Lauber M., Demeter M., Stirling D., Rodgers R., Means G., et al. Regulation of expression of the genes encoding steroidogenic enzymes. J Steroid Biochem Mol Biol 1991, 40:45-52.
30. Lievertz R.W. Pharmacology and pharmacokinetics of estrogens. Am J Obstet Gynecol 1987, 156:1289-1293.
31. Stokes W.S. Selecting appropriate animal models and experimental designs for endocrine disruptor research and testing studies. Ilar J 2004, 45:387-393.
32. Charles G.D. In vitro models in endocrine disruptor screening. Ilar J 2004, 45:494-501.
33. Massaad C., Entezami F., Massade L., Benahmed M., Olivennes F., Barouki R., et al. How can chemical compounds alter human fertility. Eur J Obstet Gynecol Reprod Biol 2002, 100:127-137.
34. Dorfman R.I., Dorfman A.S. Estrogen assays using the rat uterus. Endocrinology 1954, 55:65-69.
35. Hershberger L.G., Shipley E.G., Meyer R.K. Myotrophic activity of 19-nortestosterone and other steroids determined by modified levator ani muscle method. Proc Soc Exp Biol Med 1953, 83:175-180.
36. Hecker M., Hollert H., Cooper R., Vinggaard A.M., Akahori Y., Murphy M., et al. The OECD validation program of the H295R steroidogenesis assay: Phase 3. Final inter-laboratory validation study. Environ Sci Pollut Res Int. 2010, 18:503-515.
37. Williams K., McKinnell C., Saunders P.T., Walker M., Fisher J.S., Turner K.J., et al. Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. Hum Reprod Update 2001, 7:236-247.
38. Amato M.C., Verghi M., Nucera M., Galluzzo A., Giordano C. Low estradiol-to-testosterone ratio is associated with oligo-anovulatory cycles and atherogenic lipidic pattern in women with polycystic ovary syndrome. Gynecol Endocrinol 2011, 27:579-586.
39. Chapin R.E., Harris M.W., Davis B.J., Ward S.M., Wilson R.E., Mauney M.A., et al. The effects of perinatal/juvenile methoxychlor exposure on adult rat nervous, immune, and reproductive system function. Fundam Appl Toxicol 1997, 40:138-157.
40. Kniewald J., Jakominic M., Tomljenovic A., Simic B., Romac P., Vranesic D., et al. Disorders of male rat reproductive tract under the influence of atrazine. J Appl Toxicol 2000, 20:61-68.
41. Okazaki K., Okazaki S., Nishimura S., Nakamura H., Kitamura Y., Hatayama K., et al. A repeated 28-day oral dose toxicity study of methoxychlor in rats, based on the 'enhanced OECD test guideline 407' for screening endocrine-disrupting chemicals. Arch Toxicol 2001, 75:513-521.
42. Shibayama H., Kotera T., Shinoda Y., Hanada T., Kajihara T., Ueda M., et al. Collaborative work on evaluation of ovarian toxicity. 14) Two- or four-week repeated-dose studies and fertility study of atrazine in female rats. J Toxicol Sci 2009, 34(Suppl 1):SP 147-SP 155.
43. Shin J.H., Moon H.J., Kim T.S., Kang I.H., Ki H.Y., Choi K.S., et al. Repeated 28-day oral toxicity study of vinclozolin in rats based on the draft protocol for the " Enhanced OECD Test Guideline No. 407" to detect endocrine effects. Arch Toxicol 2006, 80:547-554.
44. Xu L.C., Wang S.Y., Yang X.F., Wang X.R. Effects of cadmium on rat sperm motility evaluated with computer assisted sperm analysis. Biomed Environ Sci 2001, 14:312-317.
45. Slott V.L., Suarez J.D., Poss P.M., Linder R.E., Strader L.F., Perreault S.D. Optimization of the Hamilton-Thorn computerized sperm motility analysis system for use with rat spermatozoa in toxicological studies. Fundam Appl Toxicol 1993, 21:298-307.
46. Chapin R.E., Filler R.S., Gulati D., Heindel J.J., Katz D.F., Mebus C.A., et al. Methods for assessing rat sperm motility. Reprod Toxicol 1992, 6:267-273.
47. Oko R., Clermont Y. Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec 1989, 225:46-55.
48. Costain R.M., Fesser A.C., McKenzie D., Mizuno M., MacNeil J.D. Identification of hormone esters in injection site in muscle tissues by LC/MS/MS. Food Addit Contam A: Chem Anal Control Expo Risk Assess 2008, 25:1520-1529.
49. Stubbings G., Bigwood T. The development and validation of a multiclass liquid chromatography tandem mass spectrometry (LC-MS/MS) procedure for the determination of veterinary drug residues in animal tissue using a QuEChERS (QUick, Easy, CHeap, Effective, Rugged and Safe) approach. Anal Chim Acta 2009, 637:68-78.
50. Leblond C.P., Clermont Y. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 1952, 55:548-573.
51. Creasy D.M. Evaluation of testicular toxicity in safety evaluation studies: the appropriate use of spermatogenic staging. Toxicol Pathol 1997, 25:119-131.
52. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
53. Lephart E.D., Simpson E.R. Assay of aromatase activity. Methods Enzymol 1991, 206:477-483.
54. Untergasser A., Nijveen H., Rao X., Bisseling T., Geurts R., Leunissen J.A. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res 2007, 35:W71-W74.
55. Fraites M.J., Cooper R.L., Buckalew A., Jayaraman S., Mills L., Laws S.C. Characterization of the hypothalamic-pituitary-adrenal axis response to atrazine and metabolites in the female rat. Toxicol Sci 2009, 112:88-99.
56. Laws S.C., Hotchkiss M., Ferrell J., Jayaraman S., Mills L., Modic W., et al. Chlorotriazine herbicides and metabolites activate an ACTH-dependent release of corticosterone in male Wistar rats. Toxicol Sci 2009, 112:78-87.
57. Rivest P., Devine P.J., Sanderson J.T. Evaluation of a bioluminescent mouse model expressing aromatase PII-promoter-controlled luciferase as a tool for the study of endocrine disrupting chemicals. Toxicol Appl Pharmacol 2010, 249:33-40.
58. Quignot N., Desmots S., Barouki R., Lemazurier E. A comparison of two human cell lines and two rat gonadal cell primary cultures as in vitro screening tools for aromatase modulation. Toxicol In Vitro 2011, 10.1016/j.tiv.2011.11.004.
59. Means G.D., Kilgore M.W., Mahendroo M.S., Mendelson C.R., Simpson E.R. Tissue-specific promoters regulate aromatase cytochrome P450 gene expression in human ovary and fetal tissues. Mol Endocrinol 1991, 5:2005-2013.
60. Murono E.P., Derk R.C. The effects of the reported active metabolite of methoxychlor, 2,2-bis(p-hydroxyphenyl)-1,1,1-trichloroethane, on testosterone formation by cultured Leydig cells from young adult rats. Reprod Toxicol 2004, 19:135-146.
61. Murono E.P., Derk R.C., Akgul Y. In vivo exposure of young adult male rats to methoxychlor reduces serum testosterone levels and ex vivo Leydig cell testosterone formation and cholesterol side-chain cleavage activity. Reprod Toxicol 2006, 21:148-153.
62. Akingbemi B.T., Sottas C.M., Koulova A.I., Klinefelter G.R., Hardy M.P. Inhibition of testicular steroidogenesis by the xenoestrogen bisphenol A is associated with reduced pituitary luteinizing hormone secretion and decreased steroidogenic enzyme gene expression in rat Leydig cells. Endocrinology 2004, 145:592-603.
63. Nakamura D., Yanagiba Y., Duan Z., Ito Y., Okamura A., Asaeda N., et al. Bisphenol A may cause testosterone reduction by adversely affecting both testis and pituitary systems similar to estradiol. Toxicol Lett 2010, 194:16-25.
64. Shan L.X., Bardin C.W., Hardy M.P. Immunohistochemical analysis of androgen effects on androgen receptor expression in developing Leydig and Sertoli cells. Endocrinology 1997, 138:1259-1266.
65. Arase S., Ishii K., Igarashi K., Aisaki K., Yoshio Y., Matsushima A., et al. Endocrine disrupter bisphenol A increases in situ estrogen production in the mouse urogenital sinus. Biol Reprod 2011, 84:734-742.
66. Carson C., Rittmaster R. The role of dihydrotestosterone in benign prostatic hyperplasia. Urology 2003, 61:2-7.
67. Rainey W.E., Parker C.R., Rehman K., Carr B.R. The adrenal genetic puzzle: how do the fetal and adult pieces differ. Endocr Res 2002, 28:611-622.
68. Kubota K., Ohsako S., Kurosawa S., Takeda K., Qing W., Sakaue M., et al. Effects of vinclozolin administration on sperm production and testosterone biosynthetic pathway in adult male rat. J Reprod Dev 2003, 49:403-412.