Are expression and localization of tight and adherens junction proteins in testes of adult boar affected by foetal and neonatal exposure to flutamide?

International Journal of Andrology

Volumn 35, Issue 3, 2012, Pages 340-352

  Hejmej, A ^a   Kopera, I ^a   Kotula Balak, M ^a   Lydka, M ^a   Lenartowicz, M ^a   Bilinska, B ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

Author keywords

catenin; Blood testis barrier; Boar; Flutamide; N cadherin; Occludin; Testis; ZO 1

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; BETA CATENIN; ESTRADIOL; FLUTAMIDE; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; OCCLUDIN; PROTEIN ZO1; TESTOSTERONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESTROGEN SYNTHESIS; EXPERIMENTAL PIG; FEMALE; GESTATION PERIOD; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; LEYDIG CELL; MALE; NONHUMAN; PRENATAL DRUG EXPOSURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TESTIS; TESTOSTERONE SYNTHESIS;

ADHERENS JUNCTIONS; ANDROGEN ANTAGONISTS; ANIMALS; ANIMALS, NEWBORN; BETA CATENIN; BLOOD-TESTIS BARRIER; CADHERINS; ESTRADIOL; FLUTAMIDE; MALE; MEMBRANE PROTEINS; PHOSPHOPROTEINS; RECEPTORS, ANDROGEN; RNA, MESSENGER; SEMINIFEROUS TUBULES; SUS SCROFA; TESTIS; TESTOSTERONE; TIGHT JUNCTIONS;

EID: 84861459588     PISSN: 01056263     EISSN: 13652605     Source Type: Journal    
DOI: 10.1111/j.1365-2605.2011.01206.x     Document Type: Article

References (75)

1. Allrich RD, Christenson RK, Ford JJ & Zimmerman DR. (1983) Pubertal development of the boar: age-related changes in testicular morphology and in vitro production of testosterone and estradiol-17 beta. Biol Reprod 28, 902-909.
2. Beardsley A & O'Donnell L. (2003) Characterization of normal spermiation and spermiation failure induced by hormone suppression in adult rats. Biol Reprod 68, 1299-1307.
3. Benbrahim-Tallaa L, Siddeek B, Bozec A, Tronchon V, Florin A, Friry C, Tabone E, Mauduit C & Benahmed M. (2008) Alterations of Sertoli cell activity in the long-term testicular germ cell death process induced by fetal androgen disruption. J Endocrinol 196, 21-31.
4. Bilinska B, Kotula-Balak M, Gancarczyk M, Sadowska J, Tabarowski Z & Wojtusiak A. (2003) Androgen aromatization in cryptorchid mouse testes. Acta Histochem 105, 57-65.
5. Bradford MM. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
6. Brehm R, Zeiler M, Rüttinger C, Herde K, Kibschull M, Winterhager E et al. (2007) A Sertoli cell-specific knockout of connexin43 prevents initiation of spermatogenesis. Am J Pathol 171, 19-31.
7. Burek M, Duda M, Knapczyk K, Koziorowski M & Słomczyńska M. (2007) Tissue-specific distribution of the androgen receptor (AR) in the porcine fetus. Acta Histochem 109, 358-365.
8. Cardenas H & Pope WF. (2002) Androgen receptor and follicle stimulating hormone receptor in the pig ovary during the follicular phase of the estrous cycle. Mol Reprod Dev 62, 92-98.
9. Carette D, Weider K, Gilleron J, Giese S, Dompierre J, Bergmann M, Brehm R, Denizot JP, Segretain D & Pointis G. (2010) Major involvement of connexin 43 in seminiferous epithelial junction dynamics and male fertility. Dev Biol 346, 54-67.
10. Carreau S & Hess RA. (2010) Oestrogens and spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365, 1517-1535.
11. Carreau S, Genissel C, Bilinska B & Levallet J. (1999) Sources of oestrogen in the testis and reproductive tract of the male. Int J Androl 22, 211-223.
12. Chen M, Cai H, Yang JL, Lu CL, Liu T, Yang W et al. (2008) Effect of heat stress on expression of junction-associated molecules and upstream factors androgen receptor and Wilms' tumor 1 in monkey Sertoli cells. Endocrinology 149, 4871-4882.
13. Cheng CY & Mruk DD. (2009) An intracellular trafficking pathway in the seminiferous epithelium regulating spermatogenesis: A biochemical and molecular perspective. Crit Rev Biochem Mol Biol 44, 245-263.
14. Cheng Y, Inoue N, Matsuda-Minehata F, Goto Y, Maeda A & Manabe N. (2005) Changes in expression and localization of connexin 43 RNA and protein in porcine ovary granulose cells during follicular atresia. J Reprod Dev 51, 627-637.
15. Chihara M, Otsuka S, Ichii O, Hashimoto Y & Kon Y. (2010) Molecular dynamics of the blood-testis barrier components during murine spermatogenesis. Mol Reprod Dev 77, 630-639.
16. Durlej M, Kopera I, Knapczyk-Stwora K, Hejmej A, Duda M, Koziorowski M, Słomczyńska M & Bilińska B. (2011) Connexin 43 gene expression in male and female gonads of porcine offspring following in utero exposure to an anti-androgen flutamide. Acta Histochem 40, 19-29.
17. Fink C, Weigel R, Hembes T, Lauke-Wettwer H, Kliesch S, Bergmann M & Brehm RH. (2006) Altered expression of ZO-1 and ZO-2 in Sertoli cells and loss of blood-testis barrier integrity in testicular carcinoma in situ. Neoplasia 8, 1019-1027.
18. Fiorini C, Tilloy-Ellul A, Chevalier S, Charuel C & Pointis G. (2004) Sertoli cell junctional proteins as early targets for different classes of reproductive toxicants. Reprod Toxicol 18, 413-421.
19. Fiorini C, Gilleron J, Carette D, Valette A, Tilloy A, Chevalier S, Segretain D & Pointis G. (2008) Accelerated internalization of junctional membrane proteins (connexin 43, N-cadherin and ZO-1) within endocytic vacuoles: an early event of DDT carcinogenicity. Biochim Biophys Acta 1778, 56-67.
20. Fisher JS. (2004) Environmental anti-androgens and male reproductive health: focus on phthalates and testicular dysgenesis syndrome. Reproduction 127, 305-315.
21. FlorCruz SV & Lapwood KR. (1978) A longitudinal study of pubertal development in boars. Int J Androl 1, 317-330.
22. Florin A, Maire M, Bozec A, Hellani A, Chater S, Bars R, Chuzel F & Benahmed M. (2005) Androgens and postmeiotic germ cells regulate claudin-11 expression in rat Sertoli cells. Endocrinology 146, 1532-1540.
23. Fraczek B, Kotula-Balak M, Wojtusiak A, Pierściński A & Bilińska B. (2001) Cytochrome P450 aromatase in the testis of immature and mature pigs. Reprod Biol 1, 51-59.
24. Gray LE Jr, Wilson VS, Stoker T, Lambright C, Furr J, Noriega N, Howdeshell K, Ankley GT & Guillette L. (2006) Adverse effects of environmental antiandrogens and androgens on reproductive development in mammals. Int J Androl 29, 96-104.
25. Gye MC & Ohsako S. (2003) Effects of flutamide in the rat testis on the expression of occludin, an integral member of the tight junctions. Toxicol Lett 143, 217-222.
26. Hejmej A, Gorazd M, Kosiniak-Kamysz K, Wiszniewska B, Sadowska J & Bilinska B. (2005) Expression of aromatase and oestrogen receptors in reproductive tissues of the stallion and a single cryptorchid visualised by means of immunohistochemistry. Domest Anim Endocrinol 29, 534-547.
27. Hejmej A, Kotula-Balak M, Sadowska J & Bilinska B. (2007) Expression of connexin 43 protein in testes, epididymides and prostates of stallions. Equine Vet J 39, 122-127.
28. Hejmej A, Kotula-Balak M, Galas J & Bilinska B. (2011) Effects of 4-tert-octylphenol on the testes and seminal vesicles in adult male bank voles. Reprod Toxicol 31, 95-105.
29. Hermo L, Pelletier RM, Cyr DG & Smith CE. (2010) Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 5: intercellular junctions and contacts between germs cells and Sertoli cells and their regulatory interactions, testicular cholesterol, and genes/proteins associated with more than one germ cell generation. Microsc Res Tech 73, 409-494.
30. Ikenouchi J, Umeda K, Tsukita S, Furuse M & Tsukita S. (2007) Requirement of ZO-1 for the formation of belt-like adherens junctions during epithelial cell polarization. J Cell Biol 176, 779-786.
31. Kaitu'u-Lino TJ, Sluka P, Foo CF & Stanton PG. (2007) Claudin-11 expression and localisation is regulated by androgens in rat Sertoli cells in vitro. Reproduction 133, 1169-1179.
32. Kaminski MA, Corbin CJ & Conley AJ. (1999) Development and differentiation of the interstitial and tubular compartments of fetal porcine testes. Biol Reprod 60, 119-127.
33. Knapczyk K, Duda M, Czaplicki D & Słomczyńska M. (2007) The presence of 3beta-hydroxysteroid dehydrogenase in the ovarian follicles and corpora lutea of pregnant swine. Exp Clin Endocrinol Diabetes 115, 411-416.
34. Knapczyk K, Duda M, Durlej M, Galas J, Koziorowski M & Słomczyńska M. (2008) Expression of estrogen receptor alpha (ERalpha) and estrogen receptor beta (ERbeta) in the ovarian follicles and corpora lutea of pregnant swine. Domest Anim Endocrinol 35, 170-179.
35. Kopera IA, Su L, Bilinska B, Cheng CY & Mruk DD. (2009) An in vivo study on adjudin and blood-testis barrier dynamics. Endocrinology 150, 4724-4733.
36. Kopera IA, Bilinska B, Cheng CY & Mruk DD. (2010a) Sertoli-germ cell junctions in the testis: a review of recent data. Philos Trans R Soc Lond B Biol Sci 365, 1593-1605.
37. Kopera I, Durlej M, Hejmej A, Knapczyk-Stwora K, Duda M, Koziorowski M, Słomczyńska M & Bilińska B. (2010b) Effects of pre- or postnatal exposure to flutamide on connexin 43 expression in testes and ovaries of prepubertal pigs. Eur J Histochem 54, 67-72.
38. Kopera I, Durlej M, Hejmej A, Knapczyk-Stwora K, Duda M, Slomczynska M & Bilinska B. (2011) Differential expression of connexin 43 in adult pig testes during normal spermatogenic cycle and after flutamide treatment. Reprod Domest Anim [Article in press; doi: ]
39. Lee YF, Lin WJ, Huang J, Messing EM, Chan FL, Wilding G & Chang C. (2002) Activation of mitogen-activated protein kinase pathway by the antiandrogen hydroxyflutamide in androgen receptor-negative prostate cancer cells. Cancer Res 62, 6039-6044.
40. Lee JH, Choi KW, Lee SJ & Gye MC. (2005) Expression of beta-catenin in human testes with spermatogenic defects. Arch Androl 51, 271-276.
41. Li X-H, Lou X, Liu R-X, Yang Y-J & Yang G-S. (2008) Roles of Wnt/β-catenin signaling in adipogenic differentiation potential of adipose-derived mesenchymal stem cells. Mol Cell Endo 291, 116-124.
42. Li MW, Mruk DD, Lee WM & Cheng CY. (2009a) Connexin 43 and plakophilin-2 as a protein complex that regulates blood-testis barrier dynamics. Proc Natl Acad Sci USA 106, 10213-10218.
43. Li MW, Mruk DD, Lee WM & Cheng CY. (2009b) Disruption of the blood-testis barrier integrity by bisphenol A in vitro: is this a suitable model for studying blood-testis barrier dynamics? Int J Biochem Cell Biol 41, 2302-2314.
44. Li MW, Mruk DD, Lee WM & Cheng CY. (2010) Connexin 43 is critical to maintain the homeostasis of the blood-testis barrier via its effects on tight junction reassembly. Proc Natl Acad Sci USA 107, 17998-18003.
45. Livak KJ & Schmittgen TD. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
46. Magnusson U. (2005) Can farm animals help to study endocrine disruption? Domest Anim Endocrinol 29, 430-435.
47. Maire M, Florin A, Kaszas K, Regnier D, Contard P, Tabone E, Mauduit C, Bars R & Benahmed M. (2005) Alteration of transforming growth factor-beta signaling system expression in adult rat germ cells with a chronic apoptotic cell death process after fetal androgen disruption. Endocrinology 146, 5135-5143.
48. Mazaud-Guittot S, Meugnier E, Pesenti S, Wu X, Vidal H, Gow A & Le Magueresse-Battistoni B. (2010) Claudin 11 deficiency in mice results in loss of the Sertoli cell epithelial phenotype in the testis. Biol Reprod 82, 202-213.
49. McCoard SA, Wise TH, Fahrenkrug SC & Ford JJ. (2001) Temporal and spatial localization patterns of Gata4 during porcine gonadogenesis. Biol Reprod 65, 366-374.
50. McIntyre BS, Barlow NJ & Foster PM. (2001) Androgen-mediated development in male rat offspring exposed to flutamide in utero: permanence and correlation of early postnatal changes in anogenital distance and nipple retention with malformations in androgen-dependent tissues. Toxicol Sci 62, 236-249.
51. Meng J, Holdcraft RW, Shima JE, Griswold MD & Braun RE. (2005) Androgens regulate the permeability of the blood-testis barrier. Proc Natl Acad Sci USA 102, 16696-16700.
52. Mruk DD & Cheng CY. (2010) Tight junctions in the testis: new perspectives. Philos Trans R Soc Lond B Biol Sci 365, 1621-1635.
53. Mutembei HM, Pesch S, Schuler G & Hoffmann B. (2005) Expression of oestrogen receptors alpha and beta and of aromatase in the testis of immature and mature boars. Reprod Domest Anim 40, 228-236.
54. Neri R. (1989) Pharmacology and pharmacokinetics of flutamide. Urology 34, 19-21.
55. O'Donnell L, Robertson KM, Jones ME & Simpson ER. (2001) Estrogen and spermatogenesis. Endocr Rev 22, 289-318.
56. Omezzine A, Chater S, Mauduit C, Florin A, Tabone E, Chuzel F, Bars R & Benahmed M. (2003) Long-term apoptotic cell death process with increased expression and activation of caspase-3 and -6 in adult rat germ cells exposed in utero to flutamide. Endocrinology 144, 648-661.
57. Rey RA, Musse M, Venara M & Chemes HE. (2009) Ontogeny of the androgen receptor expression in the fetal and postnatal testis: its relevance on Sertoli cell maturation and the onset of adult spermatogenesis. Microsc Res Tech 72, 787-795.
58. Rivas A, Fisher JS, McKinnell C, Atanassova N & Sharpe RM. (2002) Induction of reproductive tract developmental abnormalities in the male rat by lowering androgen production or action in combination with a low dose of diethylstilbestrol: evidence for importance of the androgen-estrogen balance. Endocrinology 143, 4797-4808.
59. Salian S, Doshi T & Vanage G. (2009) Neonatal exposure of male rats to Bisphenol A impairs fertility and expression of Sertoli cell junctional proteins in the testis. Toxicology 265, 56-67.
60. Sharpe RM. (2010) Environmental/lifestyle effects on spermatogenesis. Philos Trans R Soc Lond B Biol Sci 365, 1697-1712.
61. Sharpe RM, McKinnell C, Kivlin C & Fisher JS. (2003) Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction 125, 769-784.
62. Sobarzo CM, Lustig L, Ponzio R & Denduchis B. (2006) Effect of di-(2-ethylhexyl) phthalate on N-cadherin and catenin protein expression in rat testis. Reprod Toxicol 22, 77-86.
63. Sobarzo CM, Lustig L, Ponzio R, Suescun MO & Denduchis B. (2009) Effects of di(2-ethylhexyl) phthalate on gap and tight junction protein expression in the testis of prepubertal rats. Microsc Res Tech 72, 868-877.
64. Sonderman JP & Luebbe JJ. (2008) Semen production and fertility issues related to differences in genetic lines of boars. Theriogenology 70, 1380-1383.
65. Su L, Mruk DD, Lee WM & Cheng CY. (2010) Differential effects of testosterone and TGF-β3 on endocytic vesicle-mediated protein trafficking events at the blood-testis barrier. Exp Cell Res 316, 2945-2960.
66. Trudeau VL, Meijer JC, Erkens JH, van de Wiel DF & Wensing CJ. (1992) Pubertal development in the male pig: effects of treatment with a long-acting gonadotropin-releasing hormone agonist on plasma luteinizing hormone, follicle stimulating hormone and testosterone. Can J Vet Res 56, 102-109.
67. Uzumcu M, Suzuki H & Skinner MK. (2004) Effect of the anti-androgenic endocrine disruptor vinclozolin on embryonic testis cord formation and postnatal testis development and function. Reprod Toxicol 18, 765-774.
68. Wang RS, Yeh S, Chen LM, Lin HY, Zhang C, Ni J et al. (2006) Androgen receptor in Sertoli cell is essential for germ cell nursery and junctional complex formation in mouse testes. Endocrinology 147, 5624-5633.
69. Willems A, Batlouni SR, Esnal A, Swinnen JV, Saunders PT, Sharpe RM, França LR, De Gendt K & Verhoeven G. (2010) Selective ablation of the androgen receptor in mouse Sertoli cells affects Sertoli cell maturation, barrier formation and cytoskeletal development. PLoS ONE 5, e14168.
70. Williams K, McKinnell C, Saunders PT, Walker M, Fisher JS, Turner KJ, Atanassova N & Sharpe M. (2001) Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. Hum Reprod Update 7, 236-247.
71. Wong CH, Mruk DD, Lui WY & Cheng CY. (2004) Regulation of blood-testis barrier dynamics: an in vivo study. J Cell Sci 117, 783-798.
72. Wong EW, Mruk DD & Cheng CY. (2007) Biology and regulation of ectoplasmic specialization, an atypical adherens junction type, in the testis. Biochim Biophys Acta 1778, 692-708.
73. Yan HH, Mruk DD, Lee WM & Cheng CY. (2008) Blood-testis barrier dynamics are regulated by testosterone and cytokines via their differential effects on the kinetics of protein endocytosis and recycling in Sertoli cells. FASEB J 22, 1945-1959.
74. Zhang B & Guo Y. (2009) Supplemental zinc reduced intestinal permeability by enhancing occluding and zonula occludens protein-1 (ZO-1) expression in weaning piglets. Brit J Nutrit 102, 687-693.
75. Zhang YH, Lin L, Liu ZW, Jiang XZ & Chen BH. (2008) Disruption effects of monophthalate exposures on inter-Sertoli tight junction in a two-compartment culture model. Environ Toxicol 23, 302-308.