The endocrine disruptors dibutyl phthalate (DBP) and diethylstilbestrol (DES) influence Leydig cell regeneration following ethane dimethane sulphonate treatment of adult male rats

International Journal of Andrology

Volumn 35, Issue 3, 2012, Pages 353-363

  Heng, K ^a   Anand Ivell, R ^b,c   Teerds, K ^d   Ivell, R ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF SOUTH AUSTRALIA   (Australia)

^c LEIBNIZ INSTITUTE FOR FARM ANIMAL BIOLOGY FBN   (Germany)

^d WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Endocrine disruptors; Leydig cell; Rat < animal models; Testicular dysgenesis syndrome

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CYTOCHROME P450 17; DIETHYLSTILBESTROL; ETHYLENE GLYCOL DIMESYLATE; LUTEINIZING HORMONE RECEPTOR; MESSENGER RNA; NICOTINIC RECEPTOR ALPHA4; NUCLEAR RECEPTOR NUR77; PHTHALIC ACID DIBUTYL ESTER;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL REGENERATION; CONTROLLED STUDY; IN VIVO STUDY; LEYDIG CELL; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RAT; STEM CELL; STEROIDOGENESIS; TESTIS;

ANIMALS; CELL DIFFERENTIATION; DIBUTYL PHTHALATE; DIETHYLSTILBESTROL; ENDOCRINE DISRUPTORS; INSULIN; LEYDIG CELLS; MALE; MESYLATES; PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; REGENERATION; TESTOSTERONE;

EID: 84861457016     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2011.01231.x     Document Type: Article

References (41)

1. Anand-Ivell R, Wohlgemuth J, Haren MT, Hope PJ, Hatzinikolas G, Wittert G & Ivell R. (2006) Peripheral INSL3 concentrations decline with age in a large population of Australian men. Int J Androl 29, 618-626.
2. Anand-Ivell R, Heng K, Hafen B, Setchell B & Ivell R. (2009) Dynamics of INSL3 peptide expression in the rodent testis. Biol Reprod 81, 480-487.
3. Akingbemi BT, Youker RT, Sottas CM, Ge R, Katz E, Klinefelter GR, Zirkin BR & Hardy MP. (2004) Modulation of rat Leydig cell steroidogenic function by di(2-ethylhexyl)phthalate. Biol Reprod 65, 1252-1259.
4. Ariyaratne HB, Mills N, Mason JI & Mendis-Handagama SM. (2000) Effects of thyroid hormone on Leydig cell regeneration in the adult rat following ethane dimethane sulphonate treatment. Biol Reprod 63, 1115-1123.
5. Duckett RJ, Hedger MP, McLachlan RI & Wreford NG. (1997) The effects of gonadotropin-releasing hormone immunization and recombinant follicle-stimulating hormone on the Leydig cell and macrophage populations of the adult rat testis. J Androl 18, 417-423.
6. Emmen JM, McLuskey A, Adham IM, Engel W, Verhoef-Post M, Themmen AP, Grootegoed JA & Brinkmann AO. (2000) Involvement of insulin-like factor 3 (Insl3) in diethylstilbestrol-induced cryptorchidism. Endocrinology 141, 846-849.
7. Foster PM. (2006) Disruption of reproductive development in male rat offspring following in utero exposure to phthalate esters. Int J Androl 29, 140-147.
8. Foster PM, Mylchreest E, Gaido KW & Sar M. (2001) Effects of phthalate esters on the developing reproductive tract of male rats. Hum Reprod Update 7, 231-235.
9. Ge RS & Hardy MP. (2007) Regulation of Leydig cells during pubertal development. In: The Leydig Cell in Health and Disease (eds Payne AH & Hardy MP ), pp. 55-70. Human Press, Totowa, NJ.
10. Ge RS, Dong Q, Sottas CM, Chen H, Zirkin BR & Hardy MP. (2005) Gene expression in rat leydig cells during development from the progenitor to adult stage: a cluster analysis. Biol Reprod 72, 1405-1415.
11. Gundersen HJG. (1977) Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J Microsc 111, 219-223.
12. Hardy MP, Zirkin BR & Ewing LL. (1989) Kinetic studies on the development of the adult population of Leydig cells in testes of the pubertal rat. Endocrinology 124, 762-770.
13. Ivell R & Anand-Ivell R. (2009) The biology of insulin-like factor 3 (INSL3) in human reproduction. Hum Reprod Update 15, 463-476.
14. Ivell R & Spiess AN. (2002) Analysing differential gene expression in the testis. In: Testicular Tangrams (eds Rommerts FFG & Teerds KJ ), pp 99-120. Ernst Schering Research Foundation Workshop, Supplement 9. Springer-Verlag, Berlin.
15. Ivell R, Tillmann G, Wang H, Nicol M, Stewart PM, Bartlick B, Walther N, Mason JI & Morley SD. (2000) Acute regulation of the bovine gene for steroidogenic acute regulatory (StAR) protein in ovarian theca and adrenocortical cells. J Mol Endocrinol 24, 109-118.
16. Ivell R, Balvers M, Anand RJ, Paust HJ, McKinnell C & Sharpe R. (2003) Differentiation-dependent expression of 17beta-hydroxysteroid dehydrogenase, type 10, in the rodent testis: effect of aging in Leydig cells. Endocrinology 144, 3130-3137.
17. Joensen UMN, Jorgensen N, Rajpert-De Meyts E & Skakkebaek NE. (2008) Testicular dysgenesis syndrome and Leydig cell function. Basic Clin Pharmacol Toxicol 102, 155-161.
18. Johnson KJ, Hensley JB, Kelso MD, Wallace DG & Gaido KW. (2007) Mapping gene expression changes in the fetal rat testis following acute dibutyl phthalate exposure defines a complex temporal cascade of responding cell types. Biol Reprod 77, 978-989.
19. Mahood KI, McKinnell C, Walker M, Hallmark N, Scott H, Fisher JS, et al. (2006) Cellular origins of testicular dysgenesis in rats exposed in utero to di(n-butyl) phthalate. Int J Androl 29, 148-154.
20. McKinnell C, Sharpe RM, Mahood K, Hallmark N, Scott H, Ivell R et al. (2005) Expression of Insulin-like factor 3 (Insl3) protein in the rat testis during fetal and postnatal development and in relation to cryptorchidism induced by in utero exposure to Di (n-butyl) phthalate. Endocrinology 146, 4536-4544.
21. Mendis-Handagama SM & Ariyaratne HB. (2001) Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 65, 660-671.
22. Molenaar R, de Rooij DG, Rommerts FF, Reuvers PJ & van der Molen HJ. (1985) Specific destruction of Leydig cells in mature rats after in vivo administration of ethane dimethyl sulfonate. Biol Reprod 33, 1213-1222.
23. Morris ID, Phillips DM & Bardin CW. (1986) Ethylene dimethanesulfonate destroys Leydig cells in the rat testis. Endocrinology 118, 709-719.
24. Muller PY, Janovjak H, Miserez AR & Dobbieet Z. (2002) Processing of gene expression data generated by quantitative real-time RT-PCR. BioTechniques 32, 1372-1379.
25. O'Leary PC, Jackson AE, Irby DC & de Kretser DM. (1987) Effects of ethane dimethane sulphonate (EDS) on seminiferous tubule function in rats. Int J Androl 10, 625-634.
26. Palmer JR, Herbst AL, Noller KL, Boggs DA, Troisi R, Titus-Ernstoff L, Hatch EE, Wise LA, Strohsnitter WC & Hoover RN. (2009) Urogenital abnormalities in men exposed to diethylstilbestrol in utero: a cohort study. Environ Health 8, 37.
27. Risbridger G, Kerr J & de Kretser D. (1989) Differential effects of the destruction of Leydig cells by administration of ethane dimethane sulphonate to postnatal rats. Biol Reprod 40, 801-809.
28. Sharpe RM & Skakkebaek NE. (2008) Testicular dysgenesis syndrome: mechanistic insights and potential new downstream effects. Fertil Steril 89(2 Suppl), e33-e38.
29. Sterio DC. (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134, 127-136.
30. Teerds K & Rijntjes E. (2007) Dynamics of Leydig cell regeneration after EDS: a model for postnatal Leydig cell development. In: The Leydig Cell in Health and Disease (eds Payne AH & Hardy MP ), pp. 91-116. Human Press, Totowa, NJ.
31. Teerds KJ, De Rooij DG, Rommerts FF, van den Hurk R & Wensing CJ. (1989) Stimulation of the proliferation and differentiation of Leydig cell precursors after the destruction of existing Leydig cells with ethane dimethyl sulphonate (EDS) can take place in the absence of LH. J Androl 10, 472-477.
32. Teerds KJ, de Boer-Brouwer M, Dorrington JH, Balvers M & Ivell R. (1999) Identification of markers for precursor and Leydig cell differentiation in the adult rat testis following ethane dimethyl sulphonate administration. Biol Reprod 60, 1437-1445.
33. Teerds KJ, Rijntjes E, Veldhuizen-Tsoerkan MB, Rommerts FF & de Boer-Brouwer M. (2007) The development of rat Leydig cell progenitors in vitro: how essential is luteinizing hormone? J Endocrinol 194, 579-593.
34. Tena-Sempere M, Zhang FP & Huhtaniemi I. (1994) Persistent expression of a truncated form of the luteinizing hormone receptor messenger ribonucleic acid in the rat testis after selective Leydig cell destruction by ethylene dimethane sulfonate. Endocrinology 135, 1018-1024.
35. Travison TG, Araujo AB, O'Donnell AB, Kupelian V & McKinlay JB. (2007) A population-level decline in serum testosterone levels in American men. J Clin Endocrinol Metab 92, 196-202.
36. Turner KJ, Morley M, MacPherson S, Millar MR, Wilson JA, Sharpe RM & Saunders PT. (2001) Modulation of gene expression by androgen and oestrogens in the testis and prostate of the adult rat following androgen withdrawal. Mol Cell Endocrinol 178, 73-87.
37. Veldhuizen-Tsoerkan MB, Ivell R & Teerds KJ. (1994) hCG-induced changes in LH/CG receptor mRNA transcript levels in the testis of adult hypophysectomized, ethane dimethyl sulphonate-treated rats. Mol Cell Endocrinol 105, 37-44.
38. Wilson VS, Lambright C, Furr J, Ostby J, Wood C, Held G & Gray LE Jr. (2004) Phthalate ester-induced gubernacular lesions are associated with reduced insl3 gene expression in the fetal rat testis. Toxicol Lett 146, 207-215.
39. Woolveridge I, de Boer-Brouwer M, Taylor MF, Teerds KJ, Wu FC & Morris ID. (1999) Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biol Reprod 60, 461-470.
40. Wreford NG. (1995) Theory and practice of stereological techniques applied to the estimation of cell number and nuclear volume in the testis. Microsc Res Tech 32, 423-436.
41. Yasuda Y, Konishi H & Tanimura T. (1986) Leydig cell hyperplasia in fetal mice treated transplacentally with ethinyl estradiol. Teratology 33, 281-288.