Expression patterns of activin, inhibin and follistatin variants in the adult male mouse reproductive tract suggest important roles in the epididymis and vas deferens

Reproduction, Fertility and Development

Volumn 25, Issue 3, 2013, Pages 570-580

  Winnall, Wendy R ^a,c   Wu, Hui ^a   Sarraj, Mai A ^b   Rogers, Peter A W ^c   De Kretser, David M ^a   Girling, Jane E ^c   Hedger, Mark P ^a  

^a MONASH UNIVERSITY   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Fst288; Fst315; real time polymerase chain reaction (PCR)

Indexed keywords

ACTIVIN A; ACTIVIN RECEPTOR 1; ACTIVIN RECEPTOR 1B; ACTIVIN RECEPTOR 2; ACTIVIN RECEPTOR 2A; ACTIVIN RECEPTOR 2B; FOLLISTATIN; FOLLISTATIN 288; FOLLISTATIN 315; FOLLISTATIN LIKE 3; INHIBIN A; INHIBIN B; MESSENGER RNA; PROTEIN VARIANT; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDIDYMIS; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN FUNCTION; RADIOIMMUNOASSAY; VAS DEFERENS;

3' UNTRANSLATED REGIONS; ACTIVIN RECEPTORS; ACTIVINS; ANIMALS; BASE SEQUENCE; EPIDIDYMIS; EXONS; FOLLISTATIN; GENE EXPRESSION REGULATION; GENITALIA, MALE; INHIBINS; MALE; MICE; MICE, INBRED STRAINS; MOLECULAR SEQUENCE DATA; ORGAN SPECIFICITY; PROTEIN ISOFORMS; PROTEIN SUBUNITS; VAS DEFERENS;

EID: 84874886604     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11287     Document Type: Article

References (40)

1. Anawalt, B. D., Bebb, R. A., Matsumoto, A. M., Groome, N. P., Illingworth, P. J., McNeilly, A. S., and Bremner, W. J. (1996). Serum inhibin B levels reflect Sertoli cell function in normal men and men with testicular dysfunction. J. Clin. Endocrinol. Metab. 81, 3341-3345. doi:10.1210/ JC.81.9.3341
2. Anderson, R. A., Evans, L. W., Irvine, D. S., McIntyre, M. A., Groome, N. P., and Riley, S. C. (1998). Follistatin and activin A production by the male reproductive tract. Hum. Reprod. 13, 3319-3325. doi:10.1093/ HUMREP/13.12.3319
3. Bahathiq, A. O., Stewart, R. L., Baxter, L., Wells, M., Moore, H. D., and Ledger, W. L. (2005). Tissue immunoexpression and messenger ribonucleic acid localization of inhibin/activin subunit in human epididymis. Fertil. Steril. 83, 78-85. doi:10.1016/J.FERTNSTERT.2004.05.104
4. Chang, H., Lau, A. L., and Matzuk, M. M. (2001). Studying TGF-beta superfamily signaling by knockouts and knockins. Mol. Cell. Endocrinol. 180, 39-46. doi:10.1016/S0303-7207(01)00513-5
5. Craythorn, R. G., Girling, J. E., Hedger, M. P., Rogers, P. A., and Winnall, W. R. (2009). An RNA spiking method demonstrates that 18S rRNA is regulated by progesterone in the mouse uterus. Mol. Hum. Reprod. 15, 757-761. doi:10.1093/MOLEHR/GAP058
6. Da Silva,N., Cortez-Retamozo,V.,Reinecker,H. C.,Wildgruber,M.,Hill, E., Brown, D., Swirski, F. K., Pittet, M. J., and Breton, S. (2011). A dense network of dendritic cells populates the murine epididymis. Reproduction 141, 653-663. doi:10.1530/REP-10-0493
7. de Kretser, D. M., Buzzard, J. J., Okuma, Y., O'Connor, A. E., Hayashi, T., Lin, S. Y., Morrison, J. R., Loveland, K. L., and Hedger, M. P. (2004). The role of activin, follistatin and inhibin in testicular physiology. Mol. Cell. Endocrinol. 225, 57-64. doi:10.1016/J.MCE.2004.07.008
8. Eichberger, T.,Kaser,A., Pixner, C., Schmid, C.,Klingler, S.,Winklmayr,M., Hauser-Kronberger, C., Aberger, F., and Frischauf, A. M. (2008). GLI2-specific transcriptional activation of the bone morphogenetic protein/activin antagonist follistatin in human epidermal cells. J. Biol. Chem. 283, 12 426-12 437. doi:10.1074/JBC.M707117200
9. Esch, F. S., Shimasaki, S., Mercado, M., Cooksey, K., Ling, N., Ying, S., Ueno, N., and Guillemin, R. (1987). Structural characterization of follistatin: a novel follicle-stimulating hormone release-inhibiting polypeptide from the gonad. Mol. Endocrinol. 1, 849-855. doi:10.1210/ MEND-1-11-849
10. Feng, Z. M., Madigan, M. B., and Chen, C. L. (1993). Expression of type II activin receptor genes in the male and female reproductive tissues of the rat. Endocrinology 132, 2593-2600. doi:10.1210/EN.132.6.2593
11. Graham, H., and Peng, C. (2006). Activin receptor-like kinases: structure, function and clinical implications. Endocr. Metab. Immune Disord. Drug Targets 6, 45-58.
12. Hakovirta, H., Kaipia, A., Soder, O., and Parvinen, M. (1993). Effects of activin-A, inhibin-A, and transforming growth factor-beta 1 on stagespecific deoxyribonucleic acid synthesis during rat seminiferous epithelial cycle. Endocrinology 133, 1664-1668. doi:10.1210/EN.133.4.1664
13. Hedger, M. P. (2011). Immunophysiology and pathology of inflammation in the testis and epididymis. J. Androl. 32, 625-640. doi:10.2164/ JANDROL.111.012989
14. Hedger, M. P., Winnall, W. R., Phillips, D. J., and de Kretser, D. M. (2011). The regulation and functions of activin and follistatin in inflammation and immunity. Vitam. Horm. 85, 255-297. doi:10.1016/B978-0-12- 385961-7.00013-5
15. Hubner, G., Hu, Q., Smola, H., and Werner, S. (1996). Strong induction of activin expression after injury suggests an important role of activin in wound repair. Dev. Biol. 173, 490-498. doi:10.1006/DBIO.1996.0042
16. Knight, P. G., Muttukrishna, S., and Groome, N. P. (1996). Development and application of a two-site enzyme immunoassay for the determination of 'total' activin-A concentrations in serum and follicular fluid. J. Endocrinol. 148, 267-279.
17. Lerch, T. F., Shimasaki, S., Woodruff, T. K., and Jardetzky, T. S. (2007). Structural and biophysical coupling of heparin and activin binding to follistatin isoform functions. J. Biol. Chem. 282, 15 930-15 939. doi:10.1074/JBC.M700737200
18. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi:10.1006/METH.2001.1262
19. Mather, J. P., Attie, K. M., Woodruff, T. K., Rice, G. C., and Phillips, D. M. (1990). Activin stimulates spermatogonial proliferation in germ-Sertoli cell cocultures from immature rat testis. Endocrinology 127, 3206-3214. doi:10.1210/ENDO-127-6-3206
20. Mathews, L. S., and Vale, W. W. (1991). Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65, 973-982. doi:10.1016/0092-8674(91)90549-E
21. Matzuk, M. M., Kumar, T. R., and Bradley, A. (1995a). Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 374, 356-360. doi:10.1038/374356A0
22. Matzuk,M.M., Lu, N., Vogel, H., Sellheyer, K., Roop, D. R., and Bradley, A. (1995b). Multiple defects and perinatal death in mice deficient in follistatin. Nature 374, 360-363. doi:10.1038/374360A0
23. Mendis, S. H., Meachem, S. J., Sarraj, M. A., and Loveland, K. L. (2011). Activin A balances Sertoli and germ cell proliferation in the fetal mouse testis. Biol. Reprod. 84, 379-391. doi:10.1095/BIOLREPROD.110. 086231
24. Michel, U., Albiston, A., and Findlay, J. K. (1990). Rat follistatin: gonadal and extragonadal expression and evidence for alternative splicing. Biochem. Biophys. Res. Commun. 173, 401-407. doi:10.1016/S0006- 291X(05)81072-1
25. Nakamura, T., Takio, K., Eto, Y., Shibai, H., Titani, K., and Sugino, H. (1990). Activin-binding protein from rat ovary is follistatin. Science 247, 836-838. doi:10.1126/SCIENCE.2106159
26. Nistal, M., Gonzalez-Peramato, P., and De Miguel, M. P. (2010). Immunodetection of inhibin in the human testis and epididymis during normal development and in non-tumoural testicular lesions. Reprod. Fertil. Dev. 22, 558-563. doi:10.1071/RD09179
27. O'Connor, A. E., McFarlane, J. R., Hayward, S., Yohkaichiya, T., Groome, N. P., and de Kretser, D. M. (1999). Serum activin A and follistatin concentrations during human pregnancy: a cross-sectional and longitudinal study. Hum. Reprod. 14, 827-832. doi:10.1093/HUMREP/ 14.3.827
28. Okuma, Y., O'Connor, A. E., Hayashi, T., Loveland, K. L., de Kretser, D.M., and Hedger, M. P. (2006). Regulated production of activin A and inhibin B throughout the cycle of the seminiferous epithelium in the rat. J. Endocrinol. 190, 331-340. doi:10.1677/JOE.1.06706
29. Robertson, D. M., Hayward, S., Irby, D., Jacobsen, J., Clarke, L., McLachlan, R. I., and de Kretser, D. M. (1988). Radioimmunoassay of rat serum inhibin: changes after PMSG stimulation and gonadectomy. Mol. Cell. Endocrinol. 58, 1-8. doi:10.1016/0303-7207(88)90047-0
30. Schneider, O., Nau, R., and Michel, U. (2000). Comparative analysis of follistatin-, activin beta A- and activin beta B-mRNA steady-state levels in diverse porcine tissues by multiplex S1 nuclease analysis. Eur. J. Endocrinol. 142, 537-544. doi:10.1530/EJE.0.1420537
31. Schneyer, A., Sidis, Y., Xia, Y., Saito, S., del Re, E., Lin, H. Y., and Keutmann, H. (2004). Differential actions of follistatin and follistatinlike 3. Mol. Cell. Endocrinol. 225, 25-28. doi:10.1016/J.MCE. 2004.02.009
32. Shimasaki, S., Koga, M., Esch, F., Cooksey, K., Mercado, M., Koba, A., Ueno, N., Ying, S. Y., Ling, N., and Guillemin, R. (1988). Primary structure of the human follistatin precursor and its genomic organization. Proc. Natl Acad. Sci. USA 85, 4218-4222. doi:10.1073/PNAS. 85.12.4218
33. Sugino, K., Kurosawa, N., Nakamura, T., Takio, K., Shimasaki, S., Ling, N., Titani, K., and Sugino, H. (1993). Molecular heterogeneity of follistatin, an activin-binding protein. Higher affinity of the carboxyl-terminal truncated forms for heparan sulfate proteoglycans on the ovarian granulosa cell. J. Biol. Chem. 268, 15 579-15 587.
34. Thomas, T. Z., Chapman, S. M., Hong, W., Gurusingfhe, C., Mellor, S. L., Fletcher, R., Pedersen, J., and Risbridger, G. P. (1998). Inhibins, activins, and follistatins: expression of mRNAs and cellular localization in tissues from men with benign prostatic hyperplasia. Prostate 34, 34-43. doi:10.1002/(SICI) 1097-0045(19980101)34 : 1,34::AID-PROS5.3.0. CO;2-K
35. Tomaszewski, J., Joseph, A., Archambeault, D., and Yao, H. H. (2007). Essential roles of inhibin beta A in mouse epididymal coiling. Proc. Natl Acad. Sci. USA 104, 11 322-11 327. doi:10.1073/PNAS.0703445104
36. Tortoriello, D. V., Sidis, Y., Holtzman, D. A., Holmes, W. E., and Schneyer, A. L. (2001). Human follistatin-related protein: a structural homologue of follistatin with nuclear localization. Endocrinology 142, 3426-3434. doi:10.1210/EN.142.8.3426
37. Tsuchida, K., Arai, K. Y., Kuramoto, Y., Yamakawa, N., Hasegawa, Y., and Sugino, H. (2000). Identification and characterization of a novel follistatin-like protein as a binding protein for the TGF-beta family. J. Biol. Chem. 275, 40 788-40 796. doi:10.1074/JBC.M006114200
38. Veeramachaneni, D. N., Schanbacher, B. D., and Amann, R. P. (1989). Immunolocalization and concentrations of inhibin alpha in the ovine testis and excurrent duct system. Biol. Reprod. 41, 499-503. doi:10.1095/BIOLREPROD41.3.499
39. Winnall, W. R., Muir, J. A., Liew, S., Hirst, J. J., Meachem, S. J., and Hedger, M. P. (2009). Effects of chronic celecoxib on testicular function in normal and lipopolysaccharide-treated rats. Int. J. Androl. 32, 542-555.
40. Zhang, T., Guo, C. X., Hu, Z. Y., and Liu, Y. X. (1997). Localization of plasminogen activator and inhibitor, LH and androgen receptors and inhibin subunits in monkey epididymis. Mol. Hum. Reprod. 3, 945-952. doi:10.1093/MOLEHR/3.11.945