Gestational and lactational exposure to di-isobutyl phthalate via diet in maternal mice decreases testosterone levels in male offspring

Adibi, 2008, Characterization of phthalate exposure among pregnant women assessed by repeat air and urine samples, Environ. Health Perspect., 116, 467, 10.1289/ehp.10749 Akingbemi, 2001, Modulation of rat Leydig cell steroidogenic function by di(2-ethylhexyl)phthalate, Biol. Reprod., 65, 1252, 10.1095/biolreprod65.4.1252 Arocho, 2006, Validation of the 2(-Delta Delta Ct) calculation as an alternate method of data analysis for quantitative PCR of BCR-ABL P210 transcripts, Diag. Mol. Pathol., 15, 56, 10.1097/00019606-200603000-00009 Barreto, 2007, Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation, Nature, 445, 671, 10.1038/nature05515 Borch, 2006, Diisobutyl phthalate has comparable anti-androgenic effects to di-n-butyl phthalate in fetal rat testis, Toxicol. Lett., 163, 183, 10.1016/j.toxlet.2005.10.020 CDC, 2012 Culty, 2008, In utero exposure to di-(2-ethylhexyl) phthalate exerts both short-term and long-lasting suppressive effects on testosterone production in the rat, Biol. Reprod., 78, 1018, 10.1095/biolreprod.107.065649 De Gendt, 2004, A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis, P Natl. Acad. Sci. U. S. A., 101, 1327, 10.1073/pnas.0308114100 Doerge, 2010, Lactational transfer of bisphenol A in Sprague-Dawley rats, Toxicol. Lett., 199, 372, 10.1016/j.toxlet.2010.09.022 Dufau, 1998, The luteinizing hormone receptor, Annu. Rev. Physiol., 60, 461, 10.1146/annurev.physiol.60.1.461 ECHA, 2009 Fisher, 2003, Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate, Hum. Reprod., 18, 1383, 10.1093/humrep/deg273 Fromme, 2007, Intake of phthalates and di(2-ethylhexyl)adipate: results of the Integrated Exposure Assessment Survey based on duplicate diet samples and biomonitoring data, Environ. Int., 33, 1012, 10.1016/j.envint.2007.05.006 Fromme, 2011, Phthalates and their metabolites in breast milk – results from the Bavarian Monitoring of Breast Milk (BAMBI), Environ. Int., 37, 715, 10.1016/j.envint.2011.02.008 Ge, 2007, Biphasic effects of postnatal exposure to diethylhexylphthalate on the timing of puberty in male rats, J. Androl., 28, 513, 10.2164/jandrol.106.001909 Gore, 2010, Neuroendocrine targets of endocrine disruptors, Horm. (Athens), 9, 16, 10.14310/horm.2002.1249 Habert, 2001, Origin, differentiation and regulation of fetal and adult Leydig cells, Mol. Cell Endocrinol., 179, 47, 10.1016/S0303-7207(01)00461-0 Hannas, 2011, Dose-response assessment of fetal testosterone production and gene expression levels in rat testes following in utero exposure to diethylhexyl phthalate, diisobutyl phthalate, diisoheptyl phthalate, and diisononyl phthalate, Toxicol. Sci., 123, 206, 10.1093/toxsci/kfr146 Hanukoglu, 1992, Steroidogenic enzymes - structure, function, and role in regulation of steroid-hormone biosynthesis, J. Steroid Biochem., 43, 779, 10.1016/0960-0760(92)90307-5 Harris, 1997, The estrogenic activity of phthalate esters in vitro, Environ. Health Perspect., 105, 802, 10.1289/ehp.97105802 Hauser, 2006, Altered semen quality in relation to urinary concentrations of phthalate monoester and oxidative metabolites, Epidemiology, 17, 682, 10.1097/01.ede.0000235996.89953.d7 Hines, 2009, Urinary phthalate metabolite concentrations among workers in selected industries: a pilot biomonitoring study, Ann. Occup. Hyg., 53, 1 Hogberg, 2008, Phthalate diesters and their metabolites in human breast milk, blood or serum, and urine as biomarkers of exposure in vulnerable populations, Environ. Health Perspect., 116, 334, 10.1289/ehp.10788 Jiang, 2007, Study on developmental abnormalities in hypospadiac male rats induced by maternal exposure to di-n-butyl phthalate (DBP), Toxicology, 232, 286, 10.1016/j.tox.2007.01.018 Joensen, 2012, Phthalate excretion pattern and testicular function: a study of 881 healthy Danish men, Environ. Health Perspect., 120, 1397, 10.1289/ehp.1205113 Kabuto, 2004, Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice, Life Sci., 74, 2931, 10.1016/j.lfs.2003.07.060 Kalb, 2016, Maternal transfer of bisphenol a during nursing causes sperm impairment in male offspring, Arch. Environ. Contam. Toxicol., 70, 793, 10.1007/s00244-015-0199-7 Latini, 2009, Lactational exposure to phthalates in Southern Italy, Environ. Int., 35, 236, 10.1016/j.envint.2008.06.002 Lei, 2001, Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene, Mol. Endocrinol., 15, 184, 10.1210/mend.15.1.0586 Lin, 2011, Phthalate exposure in pregnant women and their children in central Taiwan, Chemosphere, 82, 947, 10.1016/j.chemosphere.2010.10.073 Manna, 2005, Regulation of the steroidogenic acute regulatory protein expression: functional and physiological consequences, Curr. Drug Targets Immune Endocr. Metabol. Disord., 5, 93, 10.2174/1568008053174714 Marsee, 2006, Estimated daily phthalate exposures in a population of mothers of male infants exhibiting reduced anogenital distance, Environ. Health Perspect., 114, 805, 10.1289/ehp.8663 Martinez-Arguelles, 2015, Mechanisms mediating environmental chemical-induced endocrine disruption in the adrenal gland, Front. Endocrinol. (Lausanne), 6, 29, 10.3389/fendo.2015.00029 Meeker, 2009, Urinary metabolites of di(2-ethylhexyl) phthalate are associated with decreased steroid hormone levels in adult men, J. Androl., 30, 287, 10.2164/jandrol.108.006403 Meng, 2005, Androgens regulate the permeability of the blood-tests barrier, P Natl. Acad. Sci. U. S. A., 102, 16696, 10.1073/pnas.0506084102 Pan, 2006, Decreased serum free testosterone in workers exposed to high levels of di-n-butyl phthalate (DBP) and di-2-ethylhexyl phthalate (DEHP): a cross-sectional study in China, Environ. Health Perspect., 114, 1643, 10.1289/ehp.9016 Pan, 2015, Association between phthalate metabolites and biomarkers of reproductive function in 1066 Chinese men of reproductive age, J. Hazard Mater, 300, 729, 10.1016/j.jhazmat.2015.08.011 Payne, 2004, Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones, Endocr. Rev., 25, 947, 10.1210/er.2003-0030 Prins, 2011, Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats, Reprod. Toxicol., 31, 1, 10.1016/j.reprotox.2010.09.009 Rone, 2009, Cholesterol transport in steroid biosynthesis: role of protein-protein interactions and implications in disease states, Biochim. Biophys. Acta, 1791, 646, 10.1016/j.bbalip.2009.03.001 Saillenfait, 2006, Developmental toxic effects of diisobutyl phthalate, the methyl-branched analogue of di-n-butyl phthalate, administered by gavage to rats, Toxicol. Lett., 165, 39, 10.1016/j.toxlet.2006.01.013 Saillenfait, 2008, Diisobutyl phthalate impairs the androgen-dependent reproductive development of the male rat, Reprod. Toxicol., 26, 107, 10.1016/j.reprotox.2008.07.006 Sedha, 2015, Determination of in vivo estrogenic potential of Di-isobutyl phthalate (DIBP) and Di-isononyl phthalate (DINP) in rats, Environ. Sci. Pollut. R., 22, 18197, 10.1007/s11356-015-5021-6 Schug, 2011, Endocrine disrupting chemicals and disease susceptibility, J. Steroid Biochem., 127, 204, 10.1016/j.jsbmb.2011.08.007 Swan, 2005, Decrease in anogenital distance among male infants with prenatal plithalate exposure (vol. 113, pg 1056, 2005), Environ. Health Perspect., 113 Tsai, 2006, Differential effects of spermatogenesis and fertility in mice lacking androgen receptor in individual testis cells, P Natl. Acad. Sci. U. S. A., 103, 18975, 10.1073/pnas.0608565103 U.S. EPA, 2009 Walker, 2009, Molecular mechanisms of testosterone action in spermatogenesis, Steroids, 74, 602, 10.1016/j.steroids.2008.11.017 Wang, 2015, Urinary excretion of phthalate metabolites in school children of China: implication for cumulative risk assessment of phthalate exposure, Environ. Sci. Technol., 49, 1120, 10.1021/es504455a Wang, 2006, Androgen receptor in sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes, Endocrinology, 147, 5624, 10.1210/en.2006-0138 Wittassek, 2008, Phthalates: metabolism and exposure, Int. J. Androl., 31, 131, 10.1111/j.1365-2605.2007.00837.x Wittassek, 2009, Fetal exposure to phthalates - a pilot study, Int. J. Hyg. Environ. Health, 212, 492, 10.1016/j.ijheh.2009.04.001 Wittassek, 2011, Assessing exposure to phthalates - the human biomonitoring approach, Mol. Nutr. Food Res., 55, 7, 10.1002/mnfr.201000121 Ye, 2009, Levels of metabolites of organophosphate pesticides, phthalates, and bisphenol A in pooled urine specimens from pregnant women participating in the Norwegian Mother and Child Cohort Study (MoBa), Int. J. Hyg. Environ. Health, 212, 481, 10.1016/j.ijheh.2009.03.004 Zirkin, 2000, Regulation of Leydig cell steroidogenic function during aging, Biol. Reprod., 63, 977, 10.1095/biolreprod63.4.977 Zota, 2014, Temporal trends in phthalate exposures: findings from the national health and nutrition examination survey, 2001–2010, Environ. Health Perspect., 122, 235, 10.1289/ehp.1306681