Effect of lindane on CYP-mediated steroid hormone metabolism in male mice following in utero exposure

Journal of Applied Toxicology

Volumn 29, Issue 8, 2009, Pages 648-655

  Di Consiglio, Emma ^a   De Angelis, Giovanna ^a   Traina, Maria Elsa ^a   Urbani, Elisabetta ^a   Testai, Emanuela ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Cytochrome P 450; In utero exposure; Lindane; Male reproductive toxicity; Steroid hormones

Indexed keywords

AROMATASE; CYTOCHROME P450; CYTOCHROME P450 2C; CYTOCHROME P450 3A; CYTOCHROME P450 3A4; LINDANE; OXYGENASE; TESTOSTERONE 2ALPHA HYDROXYLASE; TESTOSTERONE HYDROXYLASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; DEHYDROGENATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; FEMALE; GESTATIONAL AGE; HOMEOSTASIS; HYDROXYLATION; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PARAMETER; PRENATAL DEVELOPMENT; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; REPRODUCTIVE TOXICITY; SEXUAL MATURATION; SPERMATID; STEROID METABOLISM; TESTIS; TESTIS WEIGHT; TESTOSTERONE METABOLISM;

AGING; ANIMALS; AROMATASE; BODY WEIGHT; CYTOCHROME P-450 ENZYME SYSTEM; FEMALE; GONADAL STEROID HORMONES; INSECTICIDES; LINDANE; LIVER; MALE; MATERNAL EXPOSURE; MICE; MICROSOMES, LIVER; ORGAN SIZE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RANDOM ALLOCATION; SEMEN ANALYSIS; TESTIS; TESTOSTERONE;

MUS;

EID: 74549198474     PISSN: 0260437X     EISSN: 10991263     Source Type: Journal    
DOI: 10.1002/jat.1452     Document Type: Article

References (61)

1. ATSDR Agency for toxic substances and disease Registry. 2005. Toxicological Profile for Alpha-, Beta-, Gamma-, and Delta- hexachlorocyclohexane. Draft for Public Comment. US Public Health Service, Atlanta, GA.
2. Baum MJ. 1979. Differentiation of coital behavior in mammals: a comparative analysis. Neurosci. Biobehav. Rev. 3: 265-284.
3. Canistro D, Pozzetti L, Sapone A, Broccoli M, Affatato AA, Stradiotti A, Longo V, Menichini P, Barale R, Paolini M. 2008. Perturbation of murine liver cyp-superfamily of isoforms by different combinations of pesticide mixtures. Food Chem. Toxicol. 46: 34-42.
4. Chowdhury AR, Gautam AK. 1994. Steroidogenic impairment after lindane treatment in male rats. Sangyo Ika Daigaku Zasshi 16: 145-152.
5. Conley A, Hinshelwood M. 2001. Mammalian aromatases. Reproduction 121: 685-695.
6. Czerniak R. 2001. Gender-based differences in pharmacokinetics in laboratory animal models. Int. J. Toxicol. 20: 161-163.
7. Dalsenter PR, Faqi AS, Webb J, Merker HJ, Chahoud I. 1996. Reproductive toxicity and tissue concentrations of lindane in adult male rats. Hum. Exp. Toxicol. 15: 406-410.
8. Dalsenter PR, Faqi AS, Chahoud I. 1997a. Serum testosterone and sexual behavior in rats after prenatal exposure to lindane. Bull. Environ. Contam. Toxicol. 59: 360-366.
9. Dalsenter PR, Faqi AS, Webb J, Merker HJ, Chahoud I. 1997b. Reproductive toxicity and toxicokinetics of lindane in the male offspring of rats exposed during lactation. Hum. Exp. Toxicol. 16: 146-153.
10. Danzo BJ. 1997. Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ. Health Perspect. 105: 294-301.
11. EFSA scientific panel. 2005. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to gamma-hch and other hexachlorocyclohexanes as undesirable substances in animal feed. Question nø EFSA-Q-2003-067. EFSA J. 250:1-39.
12. FAO/WHO. 2002. Pesticide residues in food: Lindane. Report of the Joint Meeting of the FAO Panel of Experts on Pesticide Residues in Food and the Environment and the WHO Core Assessment Group on Pesticide Residues, pp. 181-186.
13. Faustman EM, Silbernagel SM, Fenske RA, Burbacher TM, Ponce RA. 2000. Mechanisms underlying children's susceptibility to environmental toxicants. Environ. Health Perspect. 108: 13-21.
14. Gerall AA, Ward IL. 1966. Effect of prenatal exogenous androgen on the sexual behavior of the female albino rat. J. Comp. Physiol. Psychol. 62:370-375.
15. Ginsberg G, Hattis D, Sonawane B. 2004. Incorporating pharmacokinetic differences between children and adults in assessing children's risks to environmental toxicants. Toxicol. Appl. Pharmacol. 198: 164-183.
16. Gunderson EL. 1995. FDA Total Diet Study, July 1986-April 1991, dietary intakes of pesticides, selected elements, and other chemicals. J. Assoc. Off. Anal. Chem. 78: 1353-1363.
17. Hines RN. 2008. The ontogeny of drug metabolism enzymes and implications for adverse drug event. Pharmacol. Ther. 118: 250-267.
18. Hodgson E, Rose RL. 2006. Organophosphorus chemicals: potent inhibitors of the human metabolism of steroid hormones and xenobiotics. Drug Met. Dispos. 38: 149-162.
19. Johri A, Dhawan A, Singh RL, Parmar D. 2008. Persistence in alterations in the ontogeny of cerebral and hepatic cytochrome P450s following prenatal exposure to low doses of lindane. Toxicol. Sci. 101: 331-340.
20. Juchau MR, Boutelet-Bouchan H. 1998. Cytochrome-P450-dependent biotransformation of xenobiotics in human and rodent embryonic tissues. Drug Metab. Rev. 30: 541-568.
21. Kamataki T, Maeda K, Yamazoe Y, Nagai T, Kato R. 1982. Evidence for the involvement of multiple forms of cytochrome P-450 in the occurrence of sex-related differences of drug metabolism in the rat. Life Sci. 31: 2603-2610.
22. Kamataki T, Maeda K, Yamazoe Y, Nagai T, Kato R. 1983. Sex difference of cytochrome P-450 in rat: purification, characterization, and quantitation of constitutive forms of cytochrome P-450 from liver microsomes of male and female rats. Arch. Biochem. Biophys. 225: 758-770.
23. Laurenzana EM, Weis CC, Bryant CW, Newbold RR, Delclos KB. 2002. Effect of dietary administration of genistein, nonylphenol or ethinyl estradiol on hepatic testosterone metabolism, cytochrome P-450 enzymes, and estrogen receptor alpha expression. Food Chem. Toxicol. 40: 53-63.
24. Mably TA, Bjerke DL, Moore RW, Gendron-Fitzpatrick A, Peterson RE. 1992. In utero and lactational exposure of male rats to 2,3,7,8-tetrachlorodibenzo-p- dioxin. 3. Effects on spermatogenesis and reproductive capability. Toxicol. Appl. Pharmacol. 114: 118-126.
25. Maranghi F, Rescia M, Macrì C, Di Consiglio E, De Angelis G, Testai E, Farini D, De Felici M, Lorenzetti S, Mantovani A. 2007. Lindane may modulate the female reproductive development through the interaction with ER-β: an in vivo-in vitro approach. Chem. Biol. Interact. 169: 1-14.
26. Matsuura I, Saitoh T, Tani E, Wako Y, Iwata H, Toyota N, Ishizuka Y, Namiki M, Hoshino N, Tsuchitani M, Ikeda Y. 2005. Evaluation of a twogeneration reproduction toxicity study adding endpoints to detect endocrine disrupting activity using lindane. J. Toxicol. Sci. 30: S135-S161.
27. McKinlay R, Plant JA, Bell JNB, Voulvoulis N. 2008. Endocrine disrupting pesticides: implications for risk assessment. Environ. Int. 34: 168-183.
28. Meera P, Rao PR, Shanker R, Tripathi O. 1992. Immunomodulatory effects of gamma-HCH (lindane) in mice. Immunopharmacol. Immunotoxicol. 14: 261-282.
29. Meistrich ML. 1989. Evaluation of reproductive toxicity by testicular sperm head counts. J. Am. Coll. Toxicol. 8: 551-566.
30. Morfod LL, Henck JW, Breslin WJ, DeSesso JM. 2004. Hazard Identification and Predictability of Children's Health Risk from Animal Data. Environ. Health Perspect. 112: 266-271.
31. National Toxicology Program. 2001. National Toxicology Program's report of the endocrine disruptors low dose peer review, pp. 207-214. http:// ntp.niehs.nih.gov (accessed 5 September 2006).
32. Nativelle-Serpentini C, Richard S, Sèralini GE, Sourdaine P. 2003. Aromatase activity modulation by lindane and bisphenol-A in human placental JEG-3 and transfected kidney E293 cells. Toxicol. in Vitro 17: 413-422.
33. Oyama VI, Eagle H. 1956. Measurement of cell growth in tissue culture with a phenol reagent (folin-ciocalteau). Proc. Soc. Exp. Biol. Med. 91: 305-307.
34. Pages N, Suviat MP, Bouvet S, Goudey-Perriere F. 2002. Reproductive toxicity of lindane. J. Soc. Biol. 196: 325-338.
35. Parmar D, Yadav S, Dayal M, Johri A, Dhawan PK, Seth PK. 2003. Effect of lindane on hepatic and brain cytochrome P450s and influence of P450 modulation in lindane induced neurotoxicity. Food Chem. Toxicol. 41: 1077-1087.
36. Pryor JL, Hughes C, Foster W, Hales BF, Robaire B. 2000. Critical windows of exposure for children's health: the reproductive system in animals and humans. Environ. Health Perspect. 108: 491-503.
37. Ronco AM, Valdès K, Marcus D, Llanos M. 2001. The mechanism for lindane-induced inhibition of steroidogenesis in cultured rat Leydig cells. Toxicology 159: 99-106.
38. Sanwald P, Blankson EA, Dulèry BD, Schoun J, Huebert ND, Dow J. 1995. Isocratic high-performance liquid chromatographic method for the separation to testosterone metabolites. J. Chromatogr. B 672: 207-215.
39. Saradha B, Mathur PP. 2006a. Induction of oxidative stress by lindane in epididymis of adult male rats. Environ. Toxicol. Pharmacol. 22: 90-96.
40. Saradha B, Mathur PP. 2006b. Effect of environmental contaminants on male reproduction. Environ. Toxicol. Pharmacol. 21: 34-41.
41. Scascitelli M, Pacchierotti F. 2003. Effects of lindane on oocyte maturation and preimplantation embryonic development in the mouse. Reprod. Toxicol. 17: 299-303.
42. Schrader TJ, Cooke GM. 2000. Examination of selected food additives and organochlorine food contaminants for androgenic activity in vitro. Toxicol. Sci. 53: 278-288.
43. Sharpe RM. 2001. Hormones and testis development and the possible adverse effects of environmental chemicals. Toxicol. Lett. 120: 221-232.
44. Sharpe RM, Rivas A, Walker M, McKinnell C, Fisher JS. 2003. Effect of neonatal treatment of rats with potent or weak (environmental) oestrogens, or with a GnRH antagonist, on Leydig cell development and function through puberty into adulthood. Int. J. Androl. 26: 26-36.
45. Shen R, Lee IP. 1976. Development patterns of enzymes in mouse testis. J. Reprod. Fertil. 48: 301-305.
46. Sobel V, Zhu YS, McGinley JI. 2004. Fetal hormones and sexual differentiation. Obstet. Gynecol. Clin. N. Am. 31: 837-856.
47. Sujatha R, Chitra KC, Latchoumycandane C, Mathur PP. 2001. Effect of lindane on testicular antioxidant system and steroidogenic enzymes in adult rats. Asian. J. Androl. 3: 135-138.
48. Testai E, Vittozzi L. 1986. Biochemical alterations elicited in rat liver microsomes by oxidation and reduction products of chloroform metabolism. Chem. Biol. Interact. 59: 157-171.
49. Toppari J, Larsen JC, Christiansen P. 1996. Male reproductive health and environmental xenooestrogens. Environ. Health Perspect. 104: 741-803.
50. Traina ME, Rescia M, Urbani E, Mantovani A, Macrì C, Ricciardi C, Stazi AV, Fazzi P, Cordelli E, Eleuteri P, Leter G, Spanò M. 2002. Long-lasting effects of lindane on mouse spermatogenesis induced by in utero exposure. Reprod. Toxicol. 5495: 1-11.
51. Usmani KA, Rose RL, Hodgson E. 2003. Inhibition and activation of the human liver microsomal and human cytochrome P450 3A4 metabolism of testosterone by deployment-related chemicals. Drug Metab. Dispos. 31: 384-391.
52. Walsh LP, Stocco DM. 2000. Effects of lindane on steroidogenesis and steroidogenic acute regulatory protein expression. Biol. Reprod. 63: 1024-1033.
53. Ward IL, Renz FJ. 1972. Consequences of perinatal hormone manipulation on the adult sexual behavior of female rats. J. Comp. Physiol. Psychol. 78: 349-355.
54. Waxman DJ. 1988. Interactions of hepatic cytochromes P-450 with steroid hormones: Regioselectivity and stereoselectivity of steroid metabolism and hormonal regulation of rat P-450 enzyme expression. Biochem. Pharmacol. 37: 71-84.
55. Waxman DJ, Ko A, Walsh C. 1983. Regioselectivity and stereoselectivity of androgen hydroxylations catalyzed by cytochrome P-450 enzymes purified from phenobarbital-induced rat liver. J. Biol. Chem. 258: 11937-11947.
56. Weisz J, Ward IL. 1980. Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses and neonatal offspring. Endocrinology 106: 81-87.
57. WHO-IPCS. 1991a. Lindane. Environmental Health Criteria 124. World Health Organization: Geneva.
58. WHO-IPCS. 1991b. Lindane. Health and Safety Guide 54. World Health Organization: Geneva.
59. Wilson VS, LeBlanc GA. 2000. The contribution of hepatic inactivation of testosterone to the lowering of serum testosterone levels by ketoconazole. Toxicol. Sci. 54: 128-137.
60. You L. 2004. Steroid hormone biotransformation and xenobiotic induction of hepatic steroid metabolizing enzymes. Chem. Biol. Interact. 147: 233-246.
61. You L, Sar M, Bartolucci E, Ploch S, Whitt M. 2001. Induction of hepatic aromatase by p,p′-DDE in adult male rats. Mol. Cell. Endocrinol. 178: 207-214.