A role for selective androgen response elements in the development of the epididymis and the androgen control of the 5α reductase II gene

FASEB Journal

Volumn 26, Issue 10, 2012, Pages 4360-4372

  Kerkhofs, Stefanie ^a   Dubois, Vanessa ^a   De Gendt, Karel ^a   Helsen, Christine ^a   Clinckemalie, Liesbeth ^a   Spans, Lien ^a   Schuit, Frans ^a   Boonen, Steven ^a   Vanderschueren, Dirk ^a   Saunders, Philippa T K ^b   Verhoeven, Guido ^a   Claessens, Frank ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Androgen receptor binding site; Male fertility; Sperm maturation; Srd5 2

Indexed keywords

ANDROGEN RECEPTOR; ANDROSTANOLONE; SPECIFICITY AFFECTING ANDROGEN RECEPTOR KNOCK IN; STEROID 5ALPHA REDUCTASE 2; TESTOSTERONE; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANDROGEN RESPONSE ELEMENT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA BINDING; DNA STRUCTURE; EPIDIDYMIS; GENE EXPRESSION REGULATION; GENE MUTATION; HORMONAL REGULATION; IMMUNOHISTOCHEMISTRY; MALE; MALE FERTILITY; MOUSE; NONHUMAN; ORCHIECTOMY; PHENOTYPE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SEMEN ANALYSIS; SPERMATOZOON MOTILITY; TRANSGENIC MOUSE;

3-OXO-5-ALPHA-STEROID 4-DEHYDROGENASE; ANDROGENS; ANIMALS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; EPIDIDYMIS; HELA CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; ORCHIECTOMY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ANDROGEN; RESPONSE ELEMENTS;

MUS;

EID: 84868142107     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-202283     Document Type: Article

References (53)

1. Nef, S., and Parada, L. F. (2000) Hormones in male sexual development. Genes Dev. 14, 3075-3086
2. Wilson, J. D., Griffin, J. E., and Russell, D. W. (1993) Steroid 5α-reductase 2 deficiency. Endocr. Rev. 14, 577-593
3. Robinson-Rechavi, M., Escriva Garcia, H., and Laudet, V. (2003) The nuclear receptor superfamily. J. Cell Sci. 116, 585-586
4. Claessens, F., Denayer, S., Van Tilborgh, N., Kerkhofs, S., Helsen, C., and Haelens, A. (2008) Diverse roles of androgen receptor (AR) domains in AR-mediated signaling. Nucl. Recept. Signal. 6, e008
5. De Vos, P., Claessens, F., Peeters, B., Rombauts, W., Heyns, W., and Verhoeven, G. (1993) Interaction of androgen and gluco-corticoid receptor DNA-binding domains with their response elements. Mol. Cell. Endocrinol. 90, R11-16
6. Adler, A. J., Danielsen, M., and Robins, D. M. (1992) Androgen-specific gene activation via a consensus glucocorticoid response element is determined by interaction with nonreceptor factors. Proc. Natl. Acad. Sci. U. S. A. 89, 11660-11663
7. Rennie, P. S., Bruchovsky, N., Leco, K. J., Sheppard, P. C., McQueen, S. A., Cheng, H., Snoek, R., Hamel, A., Bock, M. E., and MacDonald, B. S. (1993) Characterization of two cis-acting DNA elements involved in the androgen regulation of the probasin gene. Mol. Endocrinol. 7, 23-36
8. Schoenmakers, E., Alen, P., Verrijdt, G., Peeters, B., Verhoeven, G., Rombauts, W., and Claessens, F. (1999) Differential DNA binding by the androgen and glucocorticoid receptors involves the second Zn-finger and a C-terminal extension of the DNA-binding domains. Biochem. J. 341(Pt 3), 515-521
9. Haelens, A., Verrijdt, G., Callewaert, L., Christiaens, V., Schauwaers, K., Peeters, B., Rombauts, W., and Claessens, F. (2003) DNA recognition by the androgen receptor: evidence for an alternative DNA-dependent dimerization, and an active role of sequences flanking the response element on transactivation. Biochem. J. 369, 141-151
10. Tanner, T. M., Denayer, S., Geverts, B., Van Tilborgh, N., Kerkhofs, S., Helsen, C., Spans, L., Dubois, V., Houtsmuller, A. B., Claessens, F., and Haelens, A. (2010) A 629RKLKK633 motif in the hinge region controls the androgen receptor at multiple levels. Cell. Mol. Life Sci. 67, 1919-1927
11. Denayer, S., Helsen, C., Thorrez, L., Haelens, A., and Claessens, F. (2010) The rules of DNA recognition by the androgen receptor. Mol. Endocrinol. 24, 898-913
12. Schauwaers, K., De Gendt, K., Saunders, P. T., Atanassova, N., Haelens, A., Callewaert, L., Moehren, U., Swinnen, J. V., Verhoeven, G., Verrijdt, G., and Claessens, F. (2007) Loss of androgen receptor binding to selective androgen response elements causes a reproductive phenotype in a knockin mouse model. Proc. Natl. Acad. Sci. U. S. A. 104, 4961-4966
13. Cooper, T. G. (2007) Sperm maturation in the epididymis: a new look at an old problem. Asian J. Androl. 9, 533-539
14. Turner, T. T., Bomgardner, D., Jacobs, J. P., and Nguyen, Q. A. (2003) Association of segmentation of the epididymal interstitium with segmented tubule function in rats and mice. Reproduction 125, 871-878
15. Hermo, L., and Robaire, B. (2002) Epididymal Cell Types and Their Functions, Kluwer Academic/Plenum Press, New York
16. Mahendroo, M. S., Cala, K. M., Hess, D. L., and Russell, D. W. (2001) Unexpected virilization in male mice lacking steroid 5α-reductase enzymes. Endocrinology 142, 4652-4662
17. Vanderschueren, D., Vandenput, L., Boonen, S., Van Herck, E., Swinnen, J. V., and Bouillon, R. (2000) An aged rat model for partial androgen deficiency: prevention of both loss of bone and lean body mass by low-dose androgen replacement. Endocrinology 141, 1642-1647
18. World Health Organization (2010) WHO Laboratory Manual for the Examination and Processing of Human Semen, 5th Ed., World Health Organization, Geneva, http://www.who.int/reproductivehealth/publications/infertility/ 9789241547789/en/index.html
19. Venken, K., Schuit, F., Van Lommel, L., Tsukamoto, K., Kopchick, J. J., Coschigano, K., Ohlsson, C., Moverare, S., Boonen, S., Bouillon, R., and Vanderschueren, D. (2005) Growth without growth hormone receptor: estradiol is a major growth hormone-independent regulator of hepatic IGF-I synthesis. J. Bone Miner. Res. 20, 2138-2149
20. Verrijdt, G., Schauwaers, K., Haelens, A., Rombauts, W., and Claessens, F. (2002) Functional interplay between two response elements with distinct binding characteristics dictates androgen specificity of the mouse sex-limited protein enhancer. J. Biol. Chem. 277, 35191-35201
21. Scheller, A., Hughes, E., Golden, K. L., and Robins, D. M. (1998) Multiple receptor domains interact to permit, or restrict, androgen-specific gene activation. J. Biol. Chem. 273, 24216-24222
22. Hsia, N., and Cornwall, G. A. (2004) DNA microarray analysis of region-specific gene expression in the mouse epididymis. Biol. Reprod. 70, 448-457
23. Jelinsky, S. A., Turner, T. T., Bang, H. J., Finger, J. N., Solarz, M. K., Wilson, E., Brown, E. L., Kopf, G. S., and Johnston, D. S. (2007) The rat epididymal transcriptome: comparison of segmental gene expression in the rat and mouse epididymides. Biol. Reprod. 76, 561-570
24. Thimon, V., Koukoui, O., Calvo, E., and Sullivan, R. (2007) Region-specific gene expression profiling along the human epididymis. Mol. Hum. Reprod. 13, 691-704
25. Chauvin, T. R., and Griswold, M. D. (2004) Androgen-regulated genes in the murine epididymis. Biol. Reprod. 71, 560-569
26. Kaunisto, K., Parkkila, S., Parkkila, A. K., Waheed, A., Sly, W. S., and Rajaniemi, H. (1995) Expression of carbonic anhydrase isoenzymes IV and II in rat epididymal duct. Biol. Reprod. 52, 1350-1357
27. Henderson, N. A., Cooke, G. M., and Robaire, B. (2006) Region-specific expression of androgen and growth factor pathway genes in the rat epididymis and the effects of dual 5α- reductase inhibition. J. Endocrinol. 190, 779-791
28. Jervis, K. M., and Robaire, B. (2001) Dynamic changes in gene expression along the rat epididymis. Biol. Reprod. 65, 696-703
29. Johnston, D. S., Jelinsky, S. A., Bang, H. J., DiCandeloro, P., Wilson, E., Kopf, G. S., and Turner, T. T. (2005) The mouse epididymal transcriptome: transcriptional profiling of segmental gene expression in the epididymis. Biol. Reprod. 73, 404-413
30. Jin, Y., and Penning, T. M. (2001) Steroid 5α-reductases and 3α-hydroxysteroid dehydrogenases: key enzymes in androgen metabolism. Best Pract. Res. Clin. Endocrinol. Metab. 15, 79-94
31. Hu, S., Yao, G., Guan, X., Ni, Z., Ma, W., Wilson, E. M., French, F. S., Liu, Q., and Zhang, Y. (2010) Research resource: genomewide mapping of in vivo androgen receptor binding sites in mouse epididymis. Mol. Endocrinol. 24, 2392-2405
32. Verrijdt, G., Schoenmakers, E., Haelens, A., Peeters, B., Verhoeven, G., Rombauts, W., and Claessens, F. (2000) Change of specificity mutations in androgen-selective enhancers. Evidence for a role of differential DNA binding by the androgen receptor. J. Biol. Chem. 275, 12298-12305
33. Helsen, C., Kerkhofs, S., Clinckemalie, L., Spans, L., Laurent, M., Boonen, S., Vanderschueren, D., and Claessens, F. (2011) Structural basis for nuclear hormone receptor DNA binding. Mol. Cell. Endocrinol. 348, 411-417
34. Hinton, B. T., Palladino, M. A., Rudolph, D., and Labus, J. C. (1995) The epididymis as protector of maturing spermatozoa. Reprod. Fertil. Dev. 7, 731-745
35. Jones, R. C. (1999) To store or mature spermatozoa? The primary role of the epididymis. Int. J. Androl. 22, 57-67
36. Turner, T. T. (1995) On the epididymis and its role in the development of the fertile ejaculate. J. Androl. 16, 292-298
37. De Gendt, K., Swinnen, J. V., Saunders, P. T., Schoonjans, L., Dewerchin, M., Devos, A., Tan, K., Atanassova, N., Claessens, F., Lecureuil, C., Heyns, W., Carmeliet, P., Guillou, F., Sharpe, R. M., and Verhoeven, G. (2004) A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc. Natl. Acad. Sci. U. S. A. 101, 1327-1332
38. Yeh, S., Tsai, M. Y., Xu, Q., Mu, X. M., Lardy, H., Huang, K. E., Lin, H., Yeh, S. D., Altuwai jr, S., Zhou, X., Xing, L., Boyce, B. F., Hung, M. C., Zhang, S., Gan, L., and Chang, C. (2002) Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc. Natl. Acad. Sci. U. S. A. 99, 13498-13503
39. Ezer, N., and Robaire, B. (2002) Androgenic Regulation of the Structure and Functions of the Epididymis, Kluwer Academic/Plenum Press, New York
40. Krutskikh, A., De Gendt, K., Sharp, V., Verhoeven, G., Poutanen, M., and Huhtaniemi, I. Targeted inactivation of the androgen receptor gene in murine proximal epididymis causes epithelial hypotrophy and obstructive azoospermia. Endocrinology 152, 689-696
41. Itoh, M., Miyamoto, K., Satriotomo, I., and Takeuchi, Y. (1999) Spermatic granulomata are experimentally induced in epididymides of mice receiving high-dose testosterone implants. I. A light-microscopical study. J. Androl. 20, 551-558
42. Snyder, E. M., Small, C. L., Li, Y., and Griswold, M. D. (2009) Regulation of gene expression by estrogen and testosterone in the proximal mouse reproductive tract. Biol. Reprod. 81, 707-716
43. Wandernoth, P. M., Raubuch, M., Mannowetz, N., Becker, H. M., Deitmer, J. W., Sly, W. S., and Wennemuth, G. Role of carbonic anhydrase IV in the bicarbonate-mediated activation of murine and human sperm. PLoS One 5, e15061
44. Ekstedt, E., Holm, L., and Ridderstrale, Y. (2004) Carbonic anhydrase in mouse testis and epididymis; transfer of isozyme IV to spermatozoa during passage. J. Mol. Histol. 35, 167-173
45. + channel blockers on volume regulation of murine spermatozoa. Biol. Reprod. 72, 1275-1281
46. Yeung, C. H., Wagenfeld, A., Nieschlag, E., and Cooper, T. G. (2000) The cause of infertility of male c-ros tyrosine kinase receptor knockout mice. Biol. Reprod. 63, 612-618
47. Jakobsson, A., Westerberg, R., and Jacobsson, A. (2006) Fatty acid elongases in mammals: their regulation and roles in metabolism. Prog. Lipid Res. 45, 237-249
48. Tvrdik, P., Westerberg, R., Silve, S., Asadi, A., Jakobsson, A., Cannon, B., Loison, G., and Jacobsson, A. (2000) Role of a new mammalian gene family in the biosynthesis of very long chain fatty acids and sphingolipids. J. Cell Biol. 149, 707-718
49. Kobayashi, T., Zadravec, D., and Jacobsson, A. (2007) ELOVL2 overexpression enhances triacylglycerol synthesis in 3T3-L1 and F442A cells. FEBS Lett. 581, 3157-3163
50. Toth, M., and Zakar, T. (1982) Different binding of testosterone, 19-nortestosterone and their 5α-reduced derivatives to the androgen receptor of the rat seminal vesicle: a step toward the understanding of the anabolic action of nortestosterone. Endokrinologie 80, 163-172
51. Bolton, E. C., So, A. Y., Chaivorapol, C., Haqq, C. M., Li, H., and Yamamoto, K. R. (2007) Cell- and gene-specific regulation of primary target genes by the androgen receptor. Genes Dev. 21, 2005-2017
52. Massie, C. E., Adryan, B., Barbosa-Morais, N. L., Lynch, A. G., Tran, M. G., Neal, D. E., and Mills, I. G. (2007) New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. EMBO Rep. 8, 871-878
53. Wang, Q., Li, W., Liu, X. S., Carroll, J. S., Janne, O. A., Keeton, E. K., Chinnaiyan, A. M., Pienta, K. J., and Brown, M. (2007) A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 27, 380-392