In utero exposure to phthalate downregulates critical genes in Leydig cells of F1 male progeny

Journal of Cellular Biochemistry

Volumn 116, Issue 7, 2015, Pages 1466-1477

  Sekaran, Suganya ^a   Jagadeesan, Arunakaran ^a  

^a Dr ALM Postgraduate Institute of Basic Medical Sciences   (India)

Author keywords

ANDROGEN BIOSYNTHESIS; DI(2 ETHYLHEXYL)PHTHALATE; DNA METHYLTRANSFERASE; METHYLATION; TRANSCRIPTION FACTORS

Indexed keywords

3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; AROMATASE; CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; DNA METHYLTRANSFERASE 3L; ESTRADIOL; OLIVE OIL; PHTHALIC ACID; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; SPECIFIC PROTEIN 1; STEROID 5ALPHA REDUCTASE; STEROIDOGENIC FACTOR 1; TESTOSTERONE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; POLLUTANT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANOGENITAL DISTANCE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DNA METHYLATION; DOSE RESPONSE; DOWN REGULATION; EPIGENETICS; ESTRADIOL BLOOD LEVEL; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; GESTATIONAL AGE; LEYDIG CELL; MALE; NEWBORN; NONHUMAN; ORGAN WEIGHT; PERINATAL PERIOD; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROGENY; PROMOTER REGION; RAT; REAL TIME POLYMERASE CHAIN REACTION; STEROIDOGENESIS; TESTIS FUNCTION; TESTOSTERONE BLOOD LEVEL; WESTERN BLOTTING; ADMINISTRATION AND DOSAGE; ANIMAL; BLOOD; DRUG EFFECTS; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; POLLUTANT; PREGNANCY; PRENATAL EXPOSURE; TOXICITY; WISTAR RAT;

ANIMALS; DIETHYLHEXYL PHTHALATE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; GESTATIONAL AGE; LEYDIG CELLS; MALE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; TESTOSTERONE;

EID: 84929103648     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.25108     Document Type: Article

References (49)

1. Akingbemi BT, Ge RS, Klinefelter GR, Gunsalus GL, Hardy MP,. 2000. A metabolite of methoxychlor, 2,2-bis(p-hydroxyphenyl)-1,1,1-trichloroethane, reduces testosterone biosynthesis in rat leydig cells through suppression of steady-state messenger ribonucleic acid levels of the cholesterol side-chain cleavage enzyme. Biol Reprod 62: 571-578.
2. Akingbemi BT, Youker RT, Sottas CM, Ge R, Katz E, Klinefelter GR, Zirkin BR, Hardy MP,. 2001. Modulation of rat Leydig cell steroidogenic function by di(2-ethylhexyl)phthalate. Biol Reprod 65: 1252-1259.
3. Aldred LF, Cooke BA,. 1983. The effect of cell damage on the density and steroidogenic capacity of rat testis Leydig cells, using an NADH exclusion test for determination of viability. J Steroid Biochem 18: 411-414.
4. Andrade AJ, Grande SW, Talsness CE, Gericke C, Grote K, Golombiewski A, Sterner-Kock A, Chahoud I,. 2006. A dose response study following in utero and lactational exposure to di-(2-ethylhexyl)phthalate (DEHP): Reproductive effects on adult male offspring rats. Toxicology 228: 85-97.
5. Anway MD, Cupp AS, Uzumcu M, Skinner MK,. 2005. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469.
6. Bergmeyer M,. 1974. Steroid dehydrogenase. In:, Bergmeyer H, editor. Methods of enzymatic analysis. New York: Academic Press. pp 476-477.
7. Bernal AJ, Jirtle RL,. 2010. Epigenomic disruption: The effects of early developmental exposures. Birth Defects Res A Clin Mol Teratol 88: 938-944.
8. Borch J, Metzdorff SB, Vinggaard AM, Brokken L, Dalgaard M,. 2006. Mechanisms underlying the anti-androgenic effects of diethylhexyl phthalate in fetal rat testis. Toxicology 223: 144-155.
9. Calafat AM, Needham LL, Silva MJ, Lambert G,. 2004. Exposure to di-(2-ethylhexyl)phthalate among premature neonates in a neonatal intensive care unit. Pediatrics 113: e429-e434.
10. Chomczynski P, Sacchi N,. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
11. Clark BJ, Wells J, King SR, Stocco DM,. 1994. The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J Biol Chem 269: 28314-28322.
12. Crain DA, Janssen SJ, Edwards TM, Heindel J, Ho SM, Hunt P, Iguchi T, Juul A, McLachlan JA, Schwartz J, Skakkebaek N, Soto AM, Swan S, Walker C, Woodruff TK, Woodruff TJ, Giudice LC, Guillette LJ, Jr., 2008. Female reproductive disorders: The roles of endocrine-disrupting compounds and developmental timing. Fertil Steril 90: 911-940.
13. Fisher JS,. 2004. Environmental anti-androgens and male reproductive health: Focus on phthalates and testicular dysgenesis syndrome. Reproduction 127: 305-315.
14. Frederiksen H, Skakkebaek NE, Andersson AM,. 2007. Metabolism of phthalates in humans. Mol Nutr Food Res 51: 899-911.
15. Gray LE, Jr, Ostby J, Furr J, Price M, Veeramachaneni DN, Parks L,. 2000. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 58: 350-365.
16. Hauser R, Meeker JD, Singh NP, Silva MJ, Ryan L, Duty S, Calafat AM,. 2007. DNA damage in human sperm is related to urinary levels of phthalate monoester and oxidative metabolites. Hum Reprod 22: 688-695.
17. Ho SM, Tang WY, Belmonte de Frausto J, Prins GS,. 2006. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 66: 5624-5632.
18. Hu GX, Lian QQ, Ge RS, Hardy DO, Li XK,. 2009. Phthalate-induced testicular dysgenesis syndrome: Leydig cell influence. Trends Endocrinol Metab 20: 139-145.
19. Huang PC, Kuo PL, Guo YL, Liao PC, Lee CC,. 2007. Associations between urinary phthalate monoesters and thyroid hormones in pregnant women. Hum Reprod 22: 2715-2722.
20. Kim HS, Saito K, Ishizuka M, Kazusaka A, Fujita S,. 2003. Short period exposure to di-(2-ethylhexyl)phthalate regulates testosterone metabolism in testis of prepubertal rats. Arch Toxicol 77: 446-451.
21. La Salle S, Mertineit C, Taketo T, Moens PB, Bestor TH, Trasler JM,. 2004. Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev Biol 268: 403-415.
22. Latini G, De Felice C, Presta G, Del Vecchio A, Paris I, Ruggieri F, Mazzeo P,. 2003. In utero exposure to di-(2-ethylhexyl)phthalate and duration of human pregnancy. Environ Health Perspect 111: 1783-1785.
23. Lehmann KP, Phillips S, Sar M, Foster PM, Gaido KW,. 2004. Dose-dependent alterations in gene expression and testosterone synthesis in the fetal testes of male rats exposed to di (n-butyl)phthalate. Toxicol Sci 81: 60-68.
24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ,. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
25. Lucifero D, Chaillet JR, Trasler JM,. 2004. Potential significance of genomic imprinting defects for reproduction and assisted reproductive technology. Hum Reprod Update 10: 3-18.
26. Martinez-Arguelles DB, Culty M, Zirkin BR, Papadopoulos V,. 2009. In utero exposure to di-(2-ethylhexyl)phthalate decreases mineralocorticoid receptor expression in the adult testis. Endocrinology 150: 5575-5585.
27. Moore RW, Jefcoate CR, Peterson RE,. 1991. 2,3,7,8-Tetrachlorodibenzo-p-dioxin inhibits steroidogenesis in the rat testis by inhibiting the mobilization of cholesterol to cytochrome P450scc. Toxicol Appl Pharmacol 109: 85-97.
28. Moore RW, Rudy TA, Lin TM, Ko K, Peterson RE,. 2001. Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer Di(2-ethylhexyl)phthalate. Environ Health Perspect 109: 229-237.
29. Mortensen GK, Main KM, Andersson AM, Leffers H, Skakkebaek NE,. 2005. Determination of phthalate monoesters in human milk, consumer milk, and infant formula by tandem mass spectrometry (LC-MS-MS). Anal Bioanal Chem 382: 1084-1092.
30. Newbold RR,. 2004. Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 199: 142-150.
31. Pan G, Hanaoka T, Yoshimura M, Zhang S, Wang P, Tsukino H, Inoue K, Nakazawa H, Tsugane S, Takahashi K,. 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: 1643-1648.
32. Pant N, Shukla M, Kumar Patel D, Shukla Y, Mathur N, Kumar Gupta Y, Saxena DK,. 2008. Correlation of phthalate exposures with semen quality. Toxicol Appl Pharmacol 231: 112-116.
33. Payne AH, Hales DB,. 2004. Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr Rev 25: 947-970.
34. Rakyan V, Whitelaw E,. 2003. Transgenerational epigenetic inheritance. Curr Biol 13: R6.
35. Rigaudiere N, Loubassou S, Grizard G, Boucher D,. 1988. Characterization of insulin binding and comparative action of insulin and insulin-like growth factor I on purified Leydig cells from the adult rat. Int J Androl 11: 165-178.
36. Ryu JY, Lee BM, Kacew S, Kim HS,. 2007. Identification of differentially expressed genes in the testis of Sprague-Dawley rats treated with di(n-butyl)phthalate. Toxicology 234: 103-112.
37. Schaefer CB, Ooi SK, Bestor TH, Bourc'his D,. 2007. Epigenetic decisions in mammalian germ cells. Science 316: 398-399.
38. Schmittgen TD, Livak KJ,. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108.
39. Sekaran S, Balaganapathy P, Parsanathan R, Elangovan S, Gunashekar J, Bhat F, Jagadeesan A,. 2014. Lactational exposure of phthalate causes long-term disruption in testicular architecture by altering tight junctional and apoptotic protein expression in Sertoli cells of first filial generation pubertal Wistar rats. Hum Exp Toxicol doi: 10.1177/0960327114555926.
40. Shultz VD, Phillips S, Sar M, Foster PM, Gaido KW,. 2001. Altered gene profiles in fetal rat testes after in utero exposure to di(n-butyl)phthalate. Toxicol Sci 64: 233-242.
41. Skakkebaek NE, Rajpert-De Meyts E, Main KM,. 2001. Testicular dysgenesis syndrome: An increasingly common developmental disorder with environmental aspects. Hum Reprod 16: 972-978.
42. Soto AM, Vandenberg LN, Maffini MV, Sonnenschein C,. 2008. Does breast cancer start in the womb ? Basic Clin Pharmacol Toxicol 102: 125-133.
43. Stocco DM,. 2000. The role of the StAR protein in steroidogenesis: Challenges for the future. J Endocrinol 164: 247-253.
44. Sugawara T, Saito M, Fujimoto S,. 2000. Sp1 and SF-1 interact and cooperate in the regulation of human steroidogenic acute regulatory protein gene expression. Endocrinology 141: 2895-2903.
45. Svechnikov K, Svechnikova I, Soder O,. 2008. Inhibitory effects of mono-ethylhexyl phthalate on steroidogenesis in immature and adult rat Leydig cells in vitro. Reprod Toxicol 25: 485-490.
46. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, Mao CS, Redmon JB, Ternand CL, Sullivan S, Teague JL,. 2005. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 113: 1056-1061.
47. Val P, Lefrancois-Martinez AM, Veyssiere G, Martinez A,. 2003. SF-1 a key player in the development and differentiation of steroidogenic tissues. Nucl Recept 1: 8.
48. Vo TT, Jung EM, Dang VH, Jung K, Baek J, Choi KC, Jeung EB,. 2009. Differential effects of flutamide and di-(2-ethylhexyl)phthalate on male reproductive organs in a rat model. J Reprod Dev 55: 400-411.
49. Wu S, Zhu J, Li Y, Lin T, Gan L, Yuan X, Xiong J, Liu X, Xu M, Zhao D, Ma C, Li X, Wei G,. 2010. Dynamic epigenetic changes involved in testicular toxicity induced by di-2-(ethylhexyl)phthalate in mice. Basic Clin Pharmacol Toxicol 106: 118-123.