Aromatase and 11β-hydroxysteroid dehydrogenase 2 localisation in the testes of pigs from birth to puberty linked to changes of hormone pattern and testicular morphology

Reproduction, Fertility and Development

Volumn 20, Issue 4, 2008, Pages 505-512

  Wagner, A ^a   Claus, R ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

Pig testis; Postnatal development

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE; 11BETA HYDROXYSTEROID DEHYDROGENASE 2; AROMATASE; ESTRADIOL; FOLLITROPIN; HYDROCORTISONE; LUTEINIZING HORMONE; TESTOSTERONE; UNCLASSIFIED DRUG; SEX HORMONE;

ANIMAL TISSUE; ARTICLE; AUTOPSY; BIRTH; BLOOD SAMPLING; CONTROLLED STUDY; ENZYME LOCALIZATION; INTRAVENOUS CATHETER; LEYDIG CELL; MORPHOLOGY; NONHUMAN; PERINATAL PERIOD; POSTNATAL DEVELOPMENT; PROTEIN EXPRESSION; PUBERTY; SERTOLI CELL; SWINE; TESTIS DEVELOPMENT; AGE; ANIMAL; BLOOD; CELL COUNT; CYTOLOGY; ENZYMOLOGY; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; PHYSIOLOGY; SEXUAL MATURATION; TESTIS; TISSUE DISTRIBUTION;

SUIDAE;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; AGE FACTORS; ANIMALS; AROMATASE; CELL COUNT; GONADAL STEROID HORMONES; LEYDIG CELLS; MALE; PARTURITION; SERTOLI CELLS; SEXUAL MATURATION; SWINE; TESTIS; TISSUE DISTRIBUTION;

EID: 42149190626     PISSN: 10313613     EISSN: None     Source Type: Journal    
DOI: 10.1071/RD07136     Document Type: Article

References (56)

1. Abercrombie, M. (1946). Estimation of nuclear population from microtome sections. Anat. Rec. 94, 239-246. doi:10.1002/AR.1090940210
2. Allrich, R. D., Christenson, R. K., Ford, J. J., and Zimmermann, D. R. (1982). Pubertal development of the boar: testosterone, estradiol-17β, cortisol and LH concentrations before and after castrations at various ages. J. Anim. Sci. 55, 1139-1146.
3. Altucci, L., Addeo, R., Cicatiello, L., Germano, D., Pacilio, C., Battista, T., Cancemi, M., Petrizzi, V.B., Bresciani, F., and Weisz, A. (1997). Estrogen induces early and timed activation of cyclin-dependent kinase 4, 5, and 6 and increases cyclin messenger ribonucleic acid expression in rat uterus. Endocrinology 138, 978-984. doi:10.1210/EN.138.3.978
4. Attal, J., Andre, D., and Engels, J. A. (1972). Testicular androgen and oestrogen levels during the postnatal period in rams. J. Reprod. Fertil. 28, 207-212.
5. Bagu, E. T., Madgwick, S., Duggavathi, R., Bartlewski, P. M., Barrett, D. M. W., Huchkowsky, S., Cook, S. J., and Rawlings, N. C. (2004). Effects of treatment with LH or FSH from 4 to 8 weeks of age on the attainment of puberty in bull calves. Theriogenology 62, 861-873. doi:10.1016/J. THERIOGENOLOGY.2003.12.021
6. Booth, W. D. (1988). Hormones, pheromones and sexual behaviour in the boar. Pig News and Information 5, 251-255.
7. Bubenik, G. A., Morris, J. M., Schams, D., and Claus, R. (1982). Photoperiodicity and circannual levels of LH, FSH and testosterone in normal and castrated male, white-tailed deer. Can. J. Physiol. Pharmacol. 60, 788-793.
8. Claus, R., and Hoffmann, B. (1980). Oestrogens compared to other steroids of testicular origin in blood plasma of boars. Acta Endocrinol. (Copenh.) 94, 404-411.
9. Claus, R., and Weiler, U. (1996). Relationship between IGF-I, cortisol, and osteocalcin in peripheral plasma of growing pigs. Exp. Clin. Endocrinol. Diab. 104, 344-349.
10. Claus, R., Schopper, D., and Wagner, H. G. (1983). Seasonal effects on steroids in blood plasma and seminal plasma of boars. J. Steroid Biochem. 19, 725-729. doi:10.1016/0022-4731(83)90003-1
11. Claus, R., Hoang-Vu, C., Ellendorff, F., Meyer, H. D., Schopper, D., and Weiler, U. (1987). Seminal oestrogens in the boar: origin and functions in the sow. J. Steroid Biochem. 27, 331-335. doi:10.1016/0022-4731(87) 90324-4
12. Claus, R., Bingel, A., Hofäcker, S., and Weiler, U. (1990). Twenty-four hour profiles of growth hormone (GH) concentrations in mature female and entire male domestic pigs in comparison to mature wild boars (Sus scrofa L.). Livest. Prod. Sci. 25, 247-255. doi:10.1016/0301-6226(90)90020-7
13. Claus, R., Wagner, A., and Lambert, T. (2005). Characterization of 11β-hydroxysteroid dehydrogenase activity in testicular tissue of control and GnRH-immunized boars as a possible regulator of spermatogenesis. Exp. Clin. Endocrinol. Diabetes 113, 262-267. doi:10.1055/S-2005-837554
14. Claus, R., Lacorn, M., Welter, H., Lekhkota, O., Messe, N., Wagner, A., and Bergmann, M. (2007). Expression of 11-hydroxysteroid-dehydrogenase in Sertoli cells of boar testes. Mol. Cell. Endocrinol. 272, 86-92. doi:10.1016/J.MCE.2007.04.010
15. Corpechot, C., Baulieu, E. E., and Robel, P. (1981). Testosterone, dihydrotestosterone and androstanediols in plasma, testes and prostates of rats during development. Acta Endocrinol. (Copenh.) 96, 127-135.
16. Courot, M. (1962). Développement du testicule chez l'agneau. Établissement de la spermatogénèse. Ann. Biol. Anim. Bioch. Biophys. 2, 25-41. doi:10.1051/RND:19620104
17. Courot, M. (1965). Action des hormones gonadotropes sur le testicule de l'agneau. Ann. Biol. Anim. Bioch. Biophys. 5, 145-149. doi:10.1051/RND:19650110
18. Ford, J. J. (1983). Postnatal differentiation of sexual preference in male pigs. Horm. Behav. 17, 152-162. doi:10.1016/0018-506X(83) 90003-X
19. Ford, J. J. (1990). Differentiation of sexual behaviour in pigs. In 'Control of Pig Reproduction KKK'. (Eds D. J. A. Cole, G. R. Foxcroft and J. Weir.) J. Reprod. Fertil. Suppl. 40, 311-321.
20. Ford, J. J., Christenson, R. K., and Maurer, R. R. (1980). Serum testosterone concentrations in embryonic and fetal pigs during sexual differentiation. Biol. Reprod. 23, 583-587. doi:10.1095/ BIOLREPROD23.3.583
21. Fraçzek, B., Kotula-Balak, M., Wojtusiak, A., Pierś ciński, A., and Bilińska, B. (2001). Cytochrome P450 aromatase in the testis of immature and mature pigs. Reprod. Biol. 1, 51-59.
22. França, L. R., Silva, V.A., Chiarini-Garcia, H., Garcia, S. K., and Debeljuk, L. (2000). Cell proliferation and hormonal changes during postnatal development of the testis in the pig. Biol. Reprod. 63, 1629-1636. doi:10.1095/BIOLREPROD63.6.1629
23. Ge, R.-S., Gao, H.-B., Nacharaju, V. L., Gunsalus, G. L., and Hardy, M. P. (1997). Identification of a kinetically-distinct activity of 11β-hydroxysteroid dehydrogenase in rat Leydig cells. Endocrinology 138, 2435-2442. doi:10.1210/EN.138.6.2435
24. Geley, S., Fiegl, M., Hartmann, B. L., and Kofler, R. (1996). Genes mediating glucocorticoid effects and mechanisms of their regulation. Rev. Physiol. Biochem. Pharmacol. 128, 1-97.
25. Haeussler, S., and Claus, R. (2007). Expression of the glucocorticoid receptor and 11β-hydroxysteroid dehydrogenase 2 in pig testes cells along fetal development. Reprod. Fertil. Dev. 19, 664-669. doi:10.1071/RD07033
26. Haeussler, S., Wagner, A., Welter, H., and Claus, R. (2007). Changes of testicular aromatase expression during fetal development in male pigs (Sus scrofa). Reproduction 133, 323-330. doi:10.1530/REP.1.01169
27. Johnston, H., Baker, P. J., Aberl, M., Charlton, H. M., Jackson, G., Fleming, L., Kumar, T. R., and O'Shaughnessy, P. J. (2004). Regulation of Sertoli cell number and activity by follicle-stimulating hormone and androgen during postnatal development in the mouse. Endocrinology 145, 318-329. doi:10.1210/EN.2003-1055
28. Joshi, H. S., and Raeside, J. I. (1973). Synergistic effects of testosterone and oestrogens on accessory sex glands and sexual behaviour of the boar. J. Reprod. Fertil. 33, 411-423.
29. Kilgour, R. J., Courot, M., Pisselet, C., Dubois, M. P., and Sairam, M. R. (1993). Inhibition of FSH affects spermatogenesis in the mature ram. Anim. Reprod. Sci. 32, 213-225. doi:10.1016/0378-4320(93)90093-7
30. Kusakabe, M., Nakamura, I., and Young, G. (2003). 11β-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. Endocrinology 144, 2534-2545. doi:10.1210/EN.2002-220446
31. Martin, T. E., Baker, B., Miller, H.W., and Kellogg, T. F. (1984). Circulating androgen levels in the developing boar. Theriogenology 21, 357-363. doi:10.1016/0093-691X(84)90420-5
32. Mastorakos, G., and Ilias, I. (2003). Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann. N.Y. Acad. Sci. 997, 136-149. doi:10.1196/ANNALS.1290.016
33. McCoard, S. A., Lunstra, D. D., Wise, T. H., and Ford, J. J. (2001). Specific staining of Sertoli cell nuclei and evaluation of Sertoli cell number and proliferative activity in meishan and white comosite boars during the neonatal period. Biol. Reprod. 64, 689-695. doi:10.1095/ BIOLREPROD64.2.689
34. McCoard, S. A., Wise, T. H., Lunstra, D. D., and Ford, J. J. (2003). Stereological evaluation of Sertoli cell ontogeny during fetal and neonatal life in two diverse breeds of swine. J. Endocrinol. 178, 395-403. doi:10.1677/JOE.0.1780395
35. McMillen, I. C., Phillips, I. D., Ross, J. T., Robinson, J. S., and Owens, J. A. (1995). Chronic stress - the key to parturition? Reprod. Fertil. Dev. 7, 499-507. doi:10.1071/RD9950499
36. Meachem, S. J., McLachlan, R. I., deKretser, D. M., Robertson, D. M., and Wreford, N. G. (1996). Neonatal exposure of rats to recombinant follicle stimulating hormone increases adult sertoli and spermatogenic cell numbers. Biol. Reprod. 54, 36-44. doi:10.1095/BIOLREPROD54.1.36
37. Mentschel, J., Leiser, R., Mülling, C., Pfarrer, C., and Claus, R. (2001). Butyric acid stimulates rumen mucosa development in the calf mainly by a reduction of apoptosis. Arch. Tierernahr. 55, 85-102.
38. Monder, C. (1990). Characterization and biological significance of corticosteroid 11β-dehydrogenase, the oxidizing component of 11beta-hydroxysteroid dehydrogenase. Ann. N. Y. Acad. Sci. 595, 26-39. doi:10.1111/J.1749-6632.1990.TB34280.X
39. Moran, T. J., Gray, S., Mikosz, C.A., and Conzen, S.D. (2000). The glucocorticoid receptor mediates a survival signal in human mammary epithelial cells. Cancer Res. 60, 867-872.
40. Mutembei, H. M., Pesch, S., Schuler, G., and Hoffmann, B. (2005). Expression of oestrogen receptors alpha and p and of aromatase in the testis of immature and mature boars. Reprod. Domest. Anim. 40, 228-236. doi:10.1111/J.1439-0531.2005.00586.X
41. Parrott, R. F., and Booth, W. D. (1984). Behavioural and morphological effects of 5α-dihydrotestosterone and oestradiol-17β in the prepubertally castrated boar. J. Reprod. Fertil. 71, 453-461.
42. Riccardi, C., Cifone, M. G., and Migliorati, G. (1999). Glucocorticoid hormone-induced modulation of gene expression and regulation of T-cell death: role of GITR and GILZ, two dexamethasone-induced genes. Cell Death Differ. 6, 1182-1189. doi:10.1038/SJ.CDD.4400609
43. Romeis, B. (1989). Chapt. V. Einbetten der fixierten Präparate. In 'Mikroskopische Technik'. 17th edn. (Ed. P. Böck.) pp. 113-133. (Urban und Schwarzenberg : München Wien Baltimore.)
44. Rommerts, F. F. G., de Jong, F. H., Brinkmann, A.O., and van der Molen, H. J. (1982). Development and cellular localization of rat testicular aromatase activity. J. Reprod. Fertil. 65, 281-288.
45. Sanchez, I., Goya, I., Vallerga, A. K., and Firestone, G. L. (1993). Glucocorticoids reversibly arrest rat hepatoma cell growth by inducing an early G1 block in cell cycle progression. Cell Growth Differ. 4, 215-225.
46. Schwarzenberger, F., Toole, G. S., Christie, H. L., and Raeside, J. I. (1993). Plasma levels of several androgens and estrogens from birth to puberty in male domestic pigs. Acta Endocrinol. (Copenh.) 128, 173-177.
47. Swanlund, D. J., N'Diaye, M. R., Loseth, K. J., Pryor, J. L., and Crabo, B. G. (1995). Diverse testicular responses to exogenous growth hormone and follicle-stimulating hormone in prepubertal boars. Biol. Reprod. 53, 749-757. doi:10.1095/BIOLREPROD53.4.749
48. Van Straaten, H. W. M., and Wensing, C. J. G. (1978). Leydig cell development in the testis of the pig. Biol. Reprod. 18, 86-93. doi:10.1095/BIOLREPROD18.1.86
49. van Vorstenbosch, C. J., Colenbrander, B., and Wensing, C. J. G. (1982). Leydig cell development of pig testis in the early fetal period: an ultrastructural study. Am. J. Anat. 165, 305-318. doi:10.1002/AJA.1001650307
50. van Vorstenbosch, C. J., Spek, E., Colenbrander, B., and Wensing, C. J. B. (1987). The ultrastructure of normal fetal and neonatal pig testis germ cells and the influence of fetal decapitation on the germcell development. Development 99, 553-563.
51. Van Weerden, E. J., and Grandadam, J. A. (1976). The effect of an anabolic agent on N depostition, growth performance and nitrogen deposition of hybrid boars, gilts and castrated male pigs. Environmental Quality and Safety Suppl. 5, 115-122.
52. Vogl, S. E., Worda, C., Egarter, C., Bieglmayer, C., Szekeres, T., Huber, J., and Husslein, P. (2006). Mode of delivery is associated with maternal and fetal endocrine stress response. BJOG 113, 441-445. doi:10.1111/J.1471-0528.2006.00865.X
53. Wagner, A., and Claus, R. (2004). Involvement of glucocorticoids in testicular involution after active immunization of boars against GnRH. Reproduction 127, 275-283. doi:10.1530/REP.1.00072
54. Wagner, A., Messe, N., Bergmann, M., Lekhkota, O., and Claus, R. (2006). Effects of estradiol infusion in GnRH-immunized boars on spermatogenesis. J. Androl. 27, 880-889. doi:10.2164/JANDROL.106.000448
55. Welsh, T. H., Jr, Bambino, T. H., and Hsueh, A. J. (1982). Mechanism of glucocorticoid-induced suppression of testicular androgen biosynthesis in vitro. Biol. Reprod. 27, 1138-1146. doi:10.1095/BIOLREPROD27.5.1138
56. Zhang, Z., Laping, J., Glasser, S., Day, P., and Mulholland, J. (1998). Mediators of estradiol-stimulated mitosis in the rat uterine luminal epithelium. Endocrinology 139, 961-966. doi:10.1210/EN.139.3.961