Perinatal exposure to low doses of tributyltin chloride advances puberty and affects patterns of estrous cyclicity in female mice

Environmental Toxicology

Volumn 27, Issue 11, 2012, Pages 662-670

  Si, Jiliang ^a   Han, Xiaoying ^a,b   Zhang, Fengmei ^a   Xin, Quanbin ^a   An, Lihong ^a   Li, Guozhen ^a   Li, Chen ^a,c  

^a SHANDONG UNIVERSITY   (China)

^b SHANDONG NORMAL UNIVERSITY   (China)

^c SHANDONG UNIVERSITY   (China)

Author keywords

Endocrine disruptor; Low dose; Mouse; Organotin; Precocious puberty

Indexed keywords

ENDOCRINE DISRUPTOR; LOW DOSE; MOUSE; ORGANOTINS; PRECOCIOUS PUBERTY;

CHLORINE COMPOUNDS; ORGANOMETALLICS;

MAMMALS;

TRIBUTYLTIN CHLORIDE;

CHLORIDE; DAM; DOSE-RESPONSE RELATIONSHIP; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; FEMALE; GASTROPOD; POLLUTION EXPOSURE; PREGNANCY; RODENT;

ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESTRUS; ESTRUS CYCLE; FEMALE; LACTATION; MOUSE; NONHUMAN; ONSET AGE; PERINATAL PERIOD; PRENATAL EXPOSURE; PRIORITY JOURNAL; PROGENY; PUBERTY; VAGINA; WEIGHT REDUCTION;

ANIMALS; BODY WEIGHT; ENDOCRINE DISRUPTORS; ESTROUS CYCLE; ESTRUS; FEMALE; LACTATION; MICE; ORGAN SIZE; OVARY; PREGNANCY; SEXUAL MATURATION; TRIALKYLTIN COMPOUNDS; VAGINA;

GASTROPODA; MUS;

EID: 84867900583     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.21756     Document Type: Article

References (50)

1. Adeeko A, Li D, Forsyth DS, Casey V, Cooke GM, Barthelemy J, Cyr DG, Trasler JM, Robaire B, Hales BF.2003.Effects of in utero tributyltin chloride exposure in the rat on pregnancy outcome.Toxicol Sci 74:407-415.
2. Akin L, Kendirci M, Doganay S, Kurtoglu S, Tucer B, Coskun A.2011.Pituitary duplication: A rare cause of precocious puberty.Childs Nerv Syst 2011:12.
3. Aksglaede L, Olsen LW, Sorensen TI, Juul A.2008.Forty years trends in timing of pubertal growth spurt in 157, 000 Danish school children.PLoS One 3:e2728.
4. Antizar-Ladislao B.2008.Environmental levels, toxicity and human exposure to tributyltin (TBT)-contaminated marine environment: A review.Environ Int 34:292-308.
5. Ashby J, Tinwell H, Stevens J, Pastoor T, Breckenridge CB.2002.The effects of atrazine on the sexual maturation of female rats.Regul Toxicol Pharmacol 35:468-473.
6. Brawer JR, Munoz J, Farookhi R.1986.Development of the polycystic ovarian condition (PCO) in the estradiol valerate-treated rat.Biol Reprod 35:647-655.
7. Brawer JR, Richard M, Farookhi R.1989.Pattern of human chorionic gonadotropin binding in the polycystic ovary.Am J Obstet Gynecol 161:474-480.
8. Caligioni CS.2009.Assessing reproductive status/stages in mice.Curr Protoc Neurosci (Appendix 4: Appendix 4I).
9. Chen Y, Zuo Z, Chen S, Yan F, Yang Z, Wang C.2008.Reduction of spermatogenesis in mice after tributyltin administration.Toxicology 251:21-27.
10. Cooke GM, Tryphonas H, Pulido O, Caldwell D, Bondy GS, Forsyth D.2004.Oral (gavage), in utero and postnatal exposure of Sprague-Dawley rats to low doses of tributyltin chloride. Part 1: Toxicology, histopathology and clinical chemistry.Food Chem Toxicol 42:211-220.
11. Cooke GM, Forsyth DS, Bondy GS, Tachon R, Tague B, Coady L.2008.Organotin speciation and tissue distribution in rat dams, fetuses, and neonates following oral administration of tributyltin chloride.J Toxicol Environ Health A 71:384-395.
12. Grote K, Stahlschmidt B, Talsness CE, Gericke C, Appel KE, Chahoud I.2004.Effects of organotin compounds on pubertal male rats.Toxicology 202:145-158.
13. Hammes A, Andreassen TK, Spoelgen R, Raila J, Hubner N, Schulz H, Metzger J, Schweigert FJ, Luppa PB, Nykjaer A, Willnow TE.2005.Role of endocytosis in cellular uptake of sex steroids.Cell 122:751-762.
14. He C, Kraft P, Chasman DI, Buring JE, Chen C, Hankinson SE, Pare G, Chanock S, Ridker PM, Hunter DJ.2010.A large-scale candidate gene association study of age at menarche and age at natural menopause.Hum Genet 128:515-527.
15. Howdeshell KL, Hotchkiss AK, Thayer KA, Vandenbergh JG, vom Saal FS.1999.Exposure to bisphenol A advances puberty.Nature 401:763-764.
16. Iguchi T, Watanabe H, Ohta Y, Blumberg B.2008.Developmental effects: Oestrogen-induced vaginal changes and organotin-induced adipogenesis.Int J Androl 31:263-268.
17. Kanemoto Y, Ishibashi H, Matsuo S, Oyama Y, Akaike N.2002.Modification of NMDA responses by tri-n-butyltin in rat brain neurons.Br J Pharmacol 136:201-206.
18. Kannan K, Senthilkumar K, Giesy JP.1999.Occurrence of butyltin compounds in human blood.Environ Sci Technol 33:1776-1779.
19. Kishimoto K, Matsuo SI, Kanemoto Y, Ishibashi H, Oyama Y, Akaike N.2001.Nanomolar concentrations of tri-n-butyltin facilitate gamma-aminobutyric acidergic synaptic transmission in rat hypothalamic neurons.J Pharmacol Exp Ther 299:171-177.
20. Lavastre V, Girard D.2002.Tributyltin induces human neutrophil apoptosis and selective degradation of cytoskeletal proteins by caspases.J Toxicol Environ Health A 65:1013-1024.
21. Laws SC, Carey SA, Ferrell JM, Bodman GJ, Cooper RL.2000.Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats.Toxicol Sci 54:154-167.
22. Luebke RW, Chen DH, Dietert R, Yang Y, King M, Luster MI.2006.The comparative immunotoxicity of five selected compounds following developmental or adult exposure.J Toxicol Environ Health B Crit Rev 9:1-26.
23. Makita Y, Tanaka A, Omura M, Ogata R.2003.Effects of simultaneous administration of tributyltin (TBT) and p, p(′)-DDE on female offspring of Wistar rats.J Toxicol Environ Health A 66:2337-2347.
24. Makita Y, Omura M, Ogata R.2004.Effects of perinatal simultaneous exposure to tributyltin (TBT) and p, p′-DDE [1, 1-dichloro-2, 2-bis(p-chlorophenyl) ethylene) on male offspring of Wistar rats.J Toxicol Environ Health A 67:385-395.
25. Markey CM, Michaelson CL, Veson EC, Sonnenschein C, Soto AM.2001.The mouse uterotrophic assay: A reevaluation of its validity in assessing the estrogenicity of bisphenol A.Environ Health Perspect 109:55-60.
26. McDonald PG, Doughty C.1972.Inhibition of androgen-sterilization in the female rat by administration of an antioestrogen.J Endocrinol 55:455-456.
27. Nakanishi T, Nishikawa J, Hiromori Y, Yokoyama H, Koyanagi M, Takasuga S, Ishizaki J, Watanabe M, Isa S, Utoguchi N, Kohno Y, Nishihara T, Tanaka K.2005.Trialkyltin compounds bind retinoid X receptor to alter human placental endocrine functions.Mol Endocrinol 19:2502-2516.
28. Nakatsu Y, Kotake Y, Takishita T, Ohta S.2009.Long-term exposure to endogenous levels of tributyltin decreases GluR2 expression and increases neuronal vulnerability to glutamate.Toxicol Appl Pharmacol 240:292-298.
29. Oetken M, Bachmann J, Schulte-Oehlmann U, Oehlmann J.2004.Evidence for endocrine disruption in invertebrates.Int Rev Cytol 236:1-44.
30. Ogata R, Omura M, Shimasaki Y, Kubo K, Oshima Y, Aou S, Inoue N.2001.Two-generation reproductive toxicity study of tributyltin chloride in female rats.J Toxicol Environ Health A 63:127-144.
31. Ojeda SR, Dubay C, Lomniczi A, Kaidar G, Matagne V, Sandau US, Dissen GA.2009.Gene networks and the neuroendocrine regulation of puberty.Mol Cell Endocrinol 324:3-11.
32. Omura M, Ogata R, Kubo K, Shimasaki Y, Aou S, Oshima Y, Tanaka A, Hirata M, Makita Y, Inoue N.2001.Two-generation reproductive toxicity study of tributyltin chloride in male rats.Toxicol Sci 64:224-232.
33. Palanza PL, Howdeshell KL, Parmigiani S, vom Saal FS.2002.Exposure to a low dose of bisphenol A during fetal life or in adulthood alters maternal behavior in mice.Environ Health Perspect 110 (Suppl 3):415-422.
34. Parent AS, Teilmann G, Juul A, Skakkebaek NE, Toppari J, Bourguignon JP.2003.The timing of normal puberty and the age limits of sexual precocity: Variations around the world, secular trends, and changes after migration.Endocr Rev 24:668-693.
35. Parent AS, Matagne V, Bourguignon JP.2005.Control of puberty by excitatory amino acid neurotransmitters and its clinical implications.Endocrine 28:281-286.
36. Penninks AH.1993.The evaluation of data-derived safety factors for bis(tri-nbutyltin) oxide.Food Additives Contam 10:351-361.
37. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM.2001.Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels.Environ Health Perspect 109:675-680.
38. Saitoh M, Yanase T, Morinaga H, Tanabe M, Mu YM, Nishi Y, Nomura M, Okabe T, Goto K, Takayanagi R, Nawata H.2001.Tributyltin or triphenyltin inhibits aromatase activity in the human granulosa-like tumor cell line KGN.Biochem Biophys Res Commun 289:198-204.
39. Si J, Li J, Zhang F, Li G, Xin Q, Dai B.2011a.Effects of perinatal exposure to low doses of tributyltin chloride on pregnancy outcome and postnatal development in mouse offspring.Environ Toxicol. doi: 10.1002/tox.20753
40. Si J, Wu X, Wan C, Zeng T, Zhang M, Xie K, Li J.2011b.Peripubertal exposure to low doses of tributyltin chloride affects the homeostasis of serum T, E2, LH, and body weight of male mice.Environ Toxicol 26:307-314.
41. Slyper AH.2006.The pubertal timing controversy in the USA, and a review of possible causative factors for the advance in timing of onset of puberty.Clin Endocrinol (Oxf) 65:1-8.
42. Smith BS.1981.Male characteristics on female mud snails caused by antifouling bottom paints.J Appl Toxicol 1:22-25.
43. Snoeij NJ, Penninks AH, Seinen W.1987.Biological activity of organotin compounds-An overview.Environ Res 44:335-353.
44. Stoker TE, Gibson EK, Zorrilla LM.2010.Triclosan exposure modulates estrogen-dependent responses in the female wistar rat.Toxicol Sci 117:45-53.
45. Takahashi S, Mukai H, Tanabe S, Sakayama K, Miyazaki T, Masuno H.1999.Butyltin residues in livers of humans and wild terrestrial mammals and in plastic products.Environ Pollut 106:213-218.
46. Tyl RW, Myers CB, Marr MC, Sloan CS, Castillo NP, Veselica MM, Seely JC, Dimond SS, Van Miller JP, Shiotsuka RN, Beyer D, Hentges SG, Waechter JMJr.2008a.Two-generation reproductive toxicity study of dietary bisphenol A in CD-1 (Swiss) mice.Toxicol Sci 104:362-384.
47. Tyl RW, Myers CB, Marr MC, Sloan CS, Castillo NP, Veselica MM, Seely JC, Dimond SS, Van Miller JP, Shiotsuka RS, Stropp GD, Waechter JMJr, Hentges SG.2008b.Two-generation reproductive toxicity evaluation of dietary 17beta-estradiol (E2; CAS No. 50-28-2) in CD-1 (Swiss) mice.Toxicol Sci 102:392-412.
48. US EPA.2009. OPPTS 890.1450. Pubertal Development and Thyroid Function in Intact Juvenile/Peripubertal Female Rats. EPA 740-C-09-009. Washington, DC: US EPA (Available at: http://www.epa.gov/endo/).
49. van Weissenbruch MM, Engelbregt MJ, Veening MA, Delemarre-van de Waal HA.2005.Fetal nutrition and timing of puberty.Endocr Dev 8:15-33.
50. Wang RY, Needham LL, Barr DB.2005.Effects of environmental agents on the attainment of puberty: Considerations when assessing exposure to environmental chemicals in the National Children's Study.Environ Health Perspect 113:1100-1107.