Hormonal and photoperiodic modulation of testicular mRNAs coding for inhibin/activin subunits and follistatin in Clethrionomys glareolus, Schreber

Journal of Experimental Zoology

Volumn 281, Issue 4, 1998, Pages 336-345

  Tähkä, Klaus M ^a   Kaipia, Antti ^b   Toppari, Jorma ^b   Tähkä, Sinikka ^a   Tuuri, Timo ^c   Tuohimaa, Pentti ^d  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; CHORIONIC GONADOTROPIN; FOLLISTATIN; FOLLITROPIN; GLYCOPROTEIN; INHIBIN; MESSENGER RNA;

ANIMAL; ARTICLE; ARVICOLINAE; BIOSYNTHESIS; DRUG EFFECT; HISTOLOGY; MACROMOLECULE; MALE; METABOLISM; ORGAN SIZE; PHOTOPERIODICITY; PHYSIOLOGY; REPRODUCTION; SEASON; TESTIS;

ACTIVINS; ANIMALS; ARVICOLINAE; CHORIONIC GONADOTROPIN; FOLLICLE STIMULATING HORMONE; FOLLISTATIN; GLYCOPROTEINS; INHIBINS; MACROMOLECULAR SUBSTANCES; MALE; ORGAN SIZE; PHOTOPERIOD; REPRODUCTION; RNA, MESSENGER; SEASONS; TESTIS;

EID: 2642673615     PISSN: 0022104X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-010X(19980701)281:4<336::AID-JEZ8>3.0.CO;2-P     Document Type: Article

References (64)

1. Allenby, G., P.M.D. Foster, and R.M. Sharpe (1991) Evidence that secretion of immunoreactive inhibin by seminiferous tubules from adult rat testis is regulated by specific germ cell types: Correlation between in vivo and in vitro studies. Endocrinology, 128:467-476.
2. Burger, H.G., P.G. Farnworth, J.K. Findlay, C.J. Gurusinghe, D.L. Healy, P. Mamers, A. Mason, and D.M. Robertson (1995) Aspects of current and future inhibin research. Reprod. Fertil. Dev., 7:997-1002.
3. Chirgwin, J.M., A.E. Przybyla, R.J. MacDonald, and W.J. Rutter (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry, 18:5294-5299.
4. Chomczynski, P., and N. Sacchi (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162:156-159.
5. Chomczynski, P. (1992) One-hour downward alkaline capillary transfer for blotting of DNA and RNA. Anal. Biochem., 201:134-139.
6. de Kretser, D.M., B.J. Bremner, H.G. Burger, L. Eddie, B. Hudson, E.J. Keogh, and V.W.K. Lee (1977) Control of FSH secretion. Excerpta Med. Int. Congr. Ser., 402:398-403.
7. de Winter, J.P., H.M.J. Vanderstichele, G. Verhoeven, M.A. Timmerman, J.G. Wesseling, and F.H. de Jong (1994) Peritubular myoid cells from immature rat testes secrete activin-A and express activin receptor type II in vitro. Endocrinology, 13759-767.
8. Doi, M., M. Igarashi, Y. Hasegawa, Y. Eto, H. Shibai, T. Miura, and Y. Ibuki (1992) In vivo action of activin-A on pituitarygonadal system. Endocrinology, 130:139-144.
9. Esch, F.S., S. Shimasaki, K. Cooksey, M. Mercado, A.J. Mason, S.-Y. Ying, N. Ueno, and N. Ling (1987) Complementary deoxyribonucleic acid (cDNA) cloning and DNA sequence analysis of rat ovarian inhibins. Mol. Endocrinol., 1:388-396.
10. Feinberger, A.P., and B. Vogeltein (1983) A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem., 132:6-13.
11. Feng, Z.-M., C.W. Bardin, and C.-L.C. Chen (1989) Characterization and regulation of testicular inhibin β-subunit mRNA. Mol. Endocrinol., 3:939-948.
12. Groome, N.P., and M. O'Brien (1993) Immunoassays for inhibin and its subunits. Further applications of the synthetic peptide approach. J. Immunol. Methods, 165:167-176.
13. Guthrie, H.D., J.L.H. Ireland, T.E.M. Good, and J.J. Ireland (1997) Expression of different molecular mass forms of inhibin in atretic and nonatretic follicles during the early luteal phase and altrenogest-synchronized follicular phase in pigs. Biol. Reprod., 56:870-877.
14. Hakovirta, H., A. Kaipia, O. Söder, and M. Parvinen (1993) Effects of activin-A, inhibin-A, and transforming growth factor-β1 on stage-specific deoxyribonucleic acid synthesis during rat seminiferous epithelial cycle. Endocrinology, 13: 1664-1668.
15. Jenkin, G., J.R. McFarlane, and D.M. de Kretser (1995) Implication of inhibin and related proteins in fetal development. Reprod. Fertil. Dev., 7:323-331.
16. Kaipia, A., M. Parvinen, S. Shimasaki, N. Ling, and J. Toppari (1991) Stage-specific cellular regulation of inhibin α-subunit mRNA expression in the rat seminiferous tubules. Mol. Cell. Endocrinol., 82:165-173.
17. Kaipia, A., T-L. Penttilä, S. Shimasaki, N. Ling, M. Parvinen, and J. Toppari (1992) Expression of inhibin βA and βB, follistatin and activin A receptor messenger ribonucleic acids in the rat seminiferous epithelium. Endocrinology, 2703-2710.
18. 2) mRNA in the rat seminiferous epithelium. Endocrinology, 132:477-479.
19. Kaipia, A., J. Toppari, I. Huhtaniemi, and J. Paranko (1994) Sex differences in the action of activin-A on cell proliferation of differentiating rat gonad. Endocrinology, 134:2165-2170.
20. Keinan, D., M.B. Madigan, C.W. Bardin, and C.-L.C. Chen (1989) Expression and regulation of testicular inhibin α-subunit gene in vivo and in vitro. Mol. Endocrinol., 29-35.
21. Kerr, J.B., and R.M. Sharpe (1986) Effects of LH and LHRH agonist on testicular morphology and function in hypophysectomized rats. J. Reprod. Fertil., 76:175-192.
22. Kirby, J.D., A.E. Jetton, J.F. Ackland, F.W. Turek, and N.B. Schwartz, (1993) Changes in serum immunoreactive inhibin-α during photoperiod-induced testicular regression and recrudescence in the golden hamster. Biol. Reprod., 49: 483-488.
23. Klaij, I.A., A.M.W. Toebosch, A.P.N. Themmen, S. Shimasaki, and F.H. de Jong (1990) Regulation of α- and βB-subunit mRNA levels in rat Sertoli cells. Mol. Cell. Endocrinol., 68:45-52.
24. Knight, P.G., J.H.M. Wrathall, R.G. Glencross, and B.J. McLeod (1991) Effects of bovine follicular fluid on the secretion of LH and FSH in inhibin-immunized seasonally anoestrous ewes. J. Endocrinol., 128:403-410.
25. Krummen, L.A., J. Toppari, W.H. Kim, B.S Morelos, N. Ahmad, R.S. Swerdloff, N. Ling, S. Shimasaki, F. Esch, and S. Bhasin (1989) Regulation of testicular inhibin subunit messenger ribonucleic acid levels in vivo: Effects of hypophysectomy and selective follicle stimulating hormone replacement. Endocrinology, 125:1630-1637.
26. Krummen, L.A., T.K. Woodruff, G. DeGuzman E.T. Cox, D.L. Baly, E. Mann, S. Garg, W.-L. Wong, P. Cossum, and J.P. Mather (1993) Identification and characterization of binding proteins for inhibin and activin in human serum and follicular fluids. Endocrinology, 132:431-443.
27. Krummen, L.A., A. Moore, T.K. Woodruff, R. Covello, R. Taylor, P. Working, and J.P. Mather (1994) Localization of inhibin and activin binding sites in the testis during development by in situ ligand binding. Biol. Reprod., 50:734
28. Lee, W., A. Mason, R. Schwall, E. Szonyi, and J.P. Mather (1989) Secretion of activin by interstitial cells in the testis. Science, 243:396-398.
29. Lin, T., H. Calcins, P.L. Morris, W. Vale, and C.W. Bardin (1989) Regulation of Leydig cell function in primary culture by inhibin and activin. Endocrinology, 125:2134-2140.
30. Lincoln, G.A., C.E. Lincoln, and A.S. McNeilly (1990) Seasonal cycles in blood plasma concentration of FSH, inhibin and testosterone, and testicular size in rams of wild feral and domesticated breeds of sheep. J. Reprod. Fertil., 88:6-633.
31. r 32,000 protein with inhibin activity from porcine follicular fluid. Proc. Natl. Acad. Sci. USA, 82:7221.
32. Macconell, L.A., S. Barth, and V.J. Roberts (1996) Distribution of follistatin messenger ribonucleic acid in the rat brain: implications for a role in the regulation of central reproductive functions. Endocrinology, 137:2150-215.
33. Majdic, G., A.S. McNeilly, R.M. Sharpe, L.R. Evans, N.P. Groome, and P.T.K. Saunders (1997) Testicular expression of inhibin and activin subunits and follistatin in the rat and human fetus and neonate and during postnatal development in the rat. Endocrinology, 138:2136-2147.
34. Mason, A.J., J.S. Hayflick, N. Ling, F. Esch, N. Ueno, S.-Y. Ying, R. Guillemin, H. Niall, and P. Seeburg (1985) Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor-β Nature, 318:659-663.
35. Mather, J.P., K.M. Attie, T.K. Woodruff, G.C. Rice, and D.M. Phillips (1990) Activin stimulates spermatogonial proliferation in germ cell cocultures from immature rat testis. Endocrinology, 127:3206-3214.
36. Mather, J.P., T.K. Woodruff, and L.A. Krummen (1992) Paracrine regulation of reproductive function by inhibin and activin. Proc. Soc. Exp. Biol. Med., 201:1-15.
37. Matsubayashi, K., G. Watanabe, K. Taya, Y. Katakai, S. Sasamoto, J. Suzuki, and M. Nozaki (1991) Seasonal changes in plasma concentrations of immunoreactive inhibin and testicular activity in male Japanese monkeys. Biol. Reprod., 44:82-826.
38. Matzuk, M.M., M.J. Finegold, Y. Mishina, A. Bradley, and R.R. Behringer (1995) Synergistic effects of inhibins and Mullerian-inhibiting substance on testicular tumorigenesis. Mol. Endocrinol., 9:1337-1345.
39. Nakamura, T., K., Takio, Y. Eto, H. Shibai, K. Titani, and H. Sugino (1990) Activin binding protein from rat ovary is folhstatin. Science, 247:836-838.
40. Pineau, C., R.M. Sharpe, P.T.K. Saunders, N. Gerard, and B. Jegou (1990) Regulation of Sertoli cell inhibin production and of inhibin α-subunit mRNA levels by specific germ cell types. Mol. Cell. Endocrinol. 72:13-22.
41. Rabinovici, J., P.C. Goldsmith, V.J. Roberts, J. Vaughan, W.W. Vale, and R.B. Jaffe (1991) Localization and secretion of inhibin/activin subunits in the human and subhuman primate fetal gonads. J. Clin. Endocrinol. Metab., 73:1141-1149.
42. Rappolee, D.A., A. Wang, D. Mark, and Z. Werb (1989) Novel method for studying mRNA phenotypes in single or small numbers of cells. J. Cell. Biochem., 39:1-11.
43. Roberts, V., H. Meunier, P. Sawchenko, and W. Vale ( 1989) Differential production and regulation of inhibin subunits in rat testicular cell types. Endocrinology, 125:2350-2359.
44. Robertson, D.M., L.M. Foulds, L. Leversha, F.J. Morgan, M.T.W. Hearn, H.G. Burger, R.E. Wettenhall, and D.M. de Kretser (1985) Isolation of inhibin from bovine follicular fluid. Biochem. Biophys. Res. Comm., 126:220-226.
45. Robertson, D.M., M. Giacometti, L.M. Foulds, J. Lahnstein, N.H. Goss, M.T.W. Hearn, and D.M. de Kretser (1989) Isolation of inhibin α-subunit precursor proteins from bovine follicular fluid. Endocrinology. 125:2141-2149.
46. Robertson, D.M., L.M. Foulds, M. Prisk, and M.P. Hedger (1992) Inhibin/activin β-subunit monomer: Isolation and characterization. Endocrinology, 130:1680-1687.
47. Sanford, L.M., J.K. Voglmayr, W.W. Vale, and B. Robaire (1993) Photoperiod-mediated increases in serum concentrations of inhibin, follicle-stimulating hormone and luteinizing hormone are accentuated in adult shortened scrotum rams without corresponding decreasing testosterone and estradiol. Biol. Reprod., 49:365-373.
48. Schneyer, A.L., D.A. O'Neil, and W.F. Crowley (1992) Activin binding proteins in human serum and follicular fluid. J. Clin. Endocrinol. Metab., 74:1320-1324.
49. Schneyer, A.L., A.H. Hall, G. Lambert-Messerlian, Q.F. Wang, P. Sluss, and W.F. Crowley, Jr. (1996) Follistatin-activin complexes in human serum and follicular fluid differ immunologically and biochemically. Endocrinology, 137:240247.
50. Schwall, R., C.H. Schmelzer, E. Matsuyama, A.J. and Mason (1989) Multiple actions of recombinant activin-A in vivo. Endocrinology, 125:1420-1423.
51. Shaha, C., P.L. Morris, C.C. Chen, W. Vale, and C.W. Bardin (1989) Immunostainable inhibin subunits are in multiple cell types of testicular cells. Endocrinology, 125:1941-1950.
52. Smith, J.C., B.M.J. Price, K. Van Nimmen, and D. Huylebroeck (1990) Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature, 345:729-731.
53. Sugino, K., N. Kurosawa, T. Nakamura, K. Takio, S. Shimaski, N. Ling, K. Titani, and H. Sugin (1993) Molecular heterogeneity of follistatin, an activin binding protein. Higher affinity of the carboxyterminal truncated forms for heparin sulfate proteoglycans in the ovarian granulosa cell. J. Biol. Chem., 268:15579-15587.
54. Tähkä, K.M., A. Ruokonen, H. Wallgren, and T. Teräväinen (1983) Temporal changes in testicular histology and steroidogenesis in juvenile bank voles (Clethrionomys glareolus, Schreber) exposed to different photoperiods. Endocrinology, 112:1420-1426.
55. Tähkä K.M., S. Tähkä, and H. Rajaniemi (1991) Hormonal regulation of LH receptors in a seasonally breeding small mammal the bank vole (C. glareolus):Effects of photoperiod and sexual maturation. Winter meeting of the Society for the Study of Fertility, Paris France, Abstr., 73.
56. Tähkä K.M., B. Fröysa, S. Tähkä, and O. Söder (1993) Hormonal and photoperiod-induced changes in testicular interleukin-1-like factor in bank voles (Clethrionomys glareolus). J. Reprod. Fertil., 97:469474.
57. Tähkä K.M., Y.-H. Zhuang, S. Tähkä, and P. Tuohimaa (1997) Photoperiod-induced changes in androgen receptor expression in testes and accessory sex glands of the bank vole, Clethrionomys glareolus. Biol. Repro., 56:898-908.
58. Thomas, P.S. (1980) Hybridization of denaturated RNA and small DNA fragments transferred to nitrocellulose. Proc. Natl. Acad. Sci. USA, 77:5201-5205.
59. Tuohimaa, P., M. Bläuer, M. Bergman, and G. Aumüller (1993) Change in location and processing of inhibin α-subunit precursors during sexual maturation of the Djungarian hamster testis. Endocrinology, 132:629-633.
60. Ultee-van Gessel, A.M., F.G. Leemborg, F.H. de Jong, and H.J. van der Molen (1986) In vitro secretion of inhibin-like activity by Sertoli cells from normal and prenatally irradiated immature rats. J. Endocrinol., 109:411-418.
61. Vale, W., J. Rivier, J. Vaughan, R. McClintock, A. Corrigan, W. Woo, D. Karr, and J. Spiess (1986) Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature, 321:776-779.
62. van Dissel-Emiliani, F.M.F., A.J. Grootenhuis, F. de Jong, and D.G. de Rooij (1989) Inhibin reduces spermatogonial numbers in testes of adult mice and Chinese hamsters. Endocrinology, 125:1898-1903.
63. Voutilainen, R., J. Tapanainen, B. Chung, K.J. Matteson, and W.L. Miller (1986) Hormonal regulation of P450scc (20,22-desmolase) and P450c17 (17α-hydroxylase/17,20-lyase) in cultured human granulosa cells. J. Clin. Endocrinol. Metab., 63:202-207.
64. Webley, G.E., P.L. Marsden, and P.G. Knight (1994) Differential control of α-inhibin and progesterone production by marmoset luteal cells in vitro: Evidence for a paracrine action of α-inhibin on basal and gonadotropin-stimulated progesterone production. Biol. Reprod., 50:1394-1402.