Inhibin α-subunit N terminus interacts with activin type IB receptor to disrupt activin signaling

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8060-8070

  Zhu, Jie ^a   Lin, S Jack ^b   Zou, Chao ^b   Makanji, Yogeshwar ^a   Jardetzky, Theodore S ^b   Woodruff, Teresa K ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETAGLYCAN; CELL LINES; COMBINED MECHANISMS; COMPETITIVE BINDING; COMPLEX ASSEMBLY; DELETION MUTANTS; DIRECT INTERACTIONS; DOSE-DEPENDENT MANNER; HETERODIMERS; N-TERMINAL EXTENSION; N-TERMINALS; PEPTIDE HORMONES; RECEPTOR-LIGAND BINDING; TYPE II;

CELL CULTURE; PEPTIDES; SIGNALING;

GLYCOPROTEINS;

ACTIVIN; ACTIVIN A; ACTIVIN RECEPTOR 1; ACTIVIN RECEPTOR 1B; FOLLITROPIN; INHIBIN; INHIBIN A; INHIBIN ALPHA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BIOTINYLATION; CHICKEN; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; GONADOTROPIN SECRETING CELL; HORMONE SYNTHESIS; HYPOPHYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SUBUNIT;

ACTIVIN RECEPTORS, TYPE I; ACTIVIN RECEPTORS, TYPE II; ANIMALS; CHICKENS; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; INHIBINS; MALE; MICE; MUTATION; PEPTIDES; SIGNAL TRANSDUCTION;

EID: 84863229722     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.293381     Document Type: Article

References (61)

1. Massagué, J. (1998) TGF-β signal transduction. Annu. Rev. Biochem. 67, 753-791
2. Chang, H., Brown, C. W., and Matzuk, M. M. (2002) Genetic analysis of the mammalian transforming growth factor-β superfamily. Endocr. Rev. 23, 787-823 (Pubitemid 35454589)
3. Massagué, J. (2008) A very private TGF-β receptor embrace. Mol Cell 29, 149-150
4. Fischer, W. H., Greenwald, J., Park, M., Craig, A. G., Choe, S., and Vale, W. (1999) The disulfide bond arrangement in the extracellular domain of the activin type II receptor. J. Protein Chem. 18, 437-446 (Pubitemid 29382097)
5. Lebrun, J. J., and Vale, W. W. (1997) Activin and inhibin have antagonistic effects on ligand-dependent heteromerization of the type I and type II activin receptors and human erythroid differentiation. Mol. Cell. Biol. 17, 1682-1691 (Pubitemid 27097397)
6. Chapman, S. C., Bernard, D. J., Jelen, J., and Woodruff, T. K. (2002) Properties of inhibin binding to betaglycan, InhBP/p120 and the activin type II receptors. Mol. Cell. Endocrinol. 196, 79-93 (Pubitemid 35254108)
7. Thompson, T. B., Woodruff, T. K., and Jardetzky, T. S. (2003) Structures of an ActRIIB:activin A complex reveal a novel binding mode for TGF-β ligand:receptor interactions. EMBO J. 22, 1555-1566 (Pubitemid 36417404)
8. Bernard, D. J., Chapman, S. C., and Woodruff, T. K. (2001) Mechanisms of inhibin signal transduction. Recent Prog. Horm. Res. 56, 417-450
9. Robertson, D. M., Hertan, R., and Farnworth, P. G. (2000) Is the action of inhibin mediated via a unique receptor? Rev Reprod 5, 131-135
10. Wiater, E., and Vale, W. (2003) Inhibin is an antagonist of bone morphogenetic protein signaling. J. Biol. Chem. 278, 7934-7941 (Pubitemid 36800530)
11. Xu, J., McKeehan, K., Matsuzaki, K., and McKeehan, W. L. (1995) Inhibin antagonizes inhibition of liver cell growth by activin by a dominant-negative mechanism. J. Biol. Chem. 270, 6308-6313
12. Cook, R. W., Thompson, T. B., Jardetzky, T. S., and Woodruff, T. K. (2004) Molecular biology of inhibin action. Semin. Reprod. Med. 22, 269-276 (Pubitemid 39122131)
13. Lewis, K. A., Gray, P. C., Blount, A. L., MacConell, L. A., Wiater, E., Bilezikjian, L. M., and Vale, W. (2000) Betaglycan binds inhibin and can mediate functional antagonism of activin signaling. Nature 404, 411-414 (Pubitemid 30164345)
14. Makanji, Y., Walton, K. L., Wilce, M. C., Chan, K. L., Robertson, D. M., and Harrison, C. A. (2008) Suppression of inhibin A biological activity by alterations in the binding site for betaglycan. J. Biol. Chem. 283, 16743-16751
15. Mason, A. J., Niall, H. D., and Seeburg, P. H. (1986) Structure of two human ovarian inhibins. Biochem. Biophys. Res. Commun. 135, 957-964 (Pubitemid 16039991)
16. Ling, N., Ying, S. Y., Ueno, N., Shimasaki, S., Esch, F., Hotta, M., and Guillemin, R. (1986) Pituitary FSH is released by a heterodimer of the β-subunits from the two forms of inhibin. Nature 321, 779-782 (Pubitemid 16077905)
17. Rivier, C., Vale, W., and Rivier, J. (1987) Studies of the inhibin family of hormones: a review. Horm. Res. 28, 104-118
18. Thompson, T. B., Cook, R. W., Chapman, S. C., Jardetzky, T. S., and Woodruff, T. K. (2004) Beta A versus beta B: is it merely a matter of expression? Mol. Cell. Endocrinol. 225, 9-17 (Pubitemid 39297049)
19. Xia, Y., and Schneyer, A. L. (2009) The biology of activin: recent advances in structure, regulation, and function. J. Endocrinol. 202, 1-12
20. Zhu, J., Braun, E. L., Kohno, S., Antenos, M., Xu, E. Y., Cook, R. W., Lin, S. J., Moore, B. C., Guillette, L. J., Jr., Jardetzky, T. S., and Woodruff, T. K. (2010) Phylogenomic analyses reveal the evolutionary origin of the inhibin α-subunit, a unique TGFβ superfamily antagonist. PLoS ONE 5, e9457
21. Rivier, C., Rivier, J., and Vale, W. (1986) Inhibin-mediated feedback control of follicle-stimulating hormone secretion in the female rat. Science 234, 205-208 (Pubitemid 17186100)
22. Findlay, J. K., Doughton, B., Robertson, D. M., and Forage, R. G. (1989) Effects of immunization against recombinant bovine inhibin α-subunit on circulating concentrations of gonadotrophins in ewes. J. Endocrinol. 120, 59-65 (Pubitemid 19022040)
23. Findlay, J. K., Sai, X., and Shukovski, L. (1990) Role of inhibin-related peptides as introgonadal regulators. Reprod. Fertil. Dev. 2, 205-218 (Pubitemid 20271099)
24. Glencross, R. G., Bleach, E. C., Wood, S. C., and Knight, P. G. (1994) Active immunization of heifers against inhibin: effects on plasma concentrations of gonadotrophins, steroids and ovarian follicular dynamics during prostaglandin-synchronized cycles. J. Reprod. Fertil. 100, 599-605 (Pubitemid 24151397)
25. Shelling, A. N., Burton, K. A., Chand, A. L., van Ee, C. C., France, J. T., Farquhar, C. M., Milsom, S. R., Love, D. R., Gersak, K., Aittomäki, K., and Winship, I. M. (2000) Inhibin: a candidate gene for premature ovarian failure. Hum. Reprod. 15, 2644-2649 (Pubitemid 32000524)
26. Marozzi, A., Porta, C., Vegetti, W., Crosignani, P. G., Tibiletti, M. G., Dalprà, L., and Ginelli, E. (2002) Mutation analysis of the inhibin alpha gene in a cohort of Italian women affected by ovarian failure. Hum. Reprod. 17, 1741-1745 (Pubitemid 34790294)
27. Dixit, H., Deendayal, M., and Singh, L. (2004) Mutational analysis of the mature peptide region of inhibin genes in Indian women with ovarian failure. Hum. Reprod. 19, 1760-1764 (Pubitemid 39144618)
28. Dixit, H., Rao, K. L., Padmalatha, V., Kanakavalli, M., Deenadayal, M., Gupta, N., Chakravarty, B. N., and Singh, L. (2006) Expansion of the germline analysis for the INHA gene in Indian women with ovarian failure. Hum. Reprod. 21, 1643-1644 (Pubitemid 44445049)
29. Rebar, R. W. (2008) Premature ovarian "failure" in the adolescent. Ann. N.Y. Acad. Sci. 1135, 138-145
30. Chand, A. L., Ooi, G. T., Harrison, C. A., Shelling, A. N., and Robertson, D. M. (2007) Functional analysis of the human inhibin α-subunit variant A257T and its potential role in premature ovarian failure. Hum. Reprod. 22, 3241-3248 (Pubitemid 351696784)
31. Yamashiro, D., Li, C. H., Ramasharma, K., and Sairam, M. R. (1984) Synthesis and biological activity of human inhibin-like peptide-(1-31). Proc. Natl. Acad. Sci. U.S.A. 81, 5399-5402 (Pubitemid 14048755)
32. Hillier, S. G., Tsonis, C. G., Wickings, E. J., and Eidne, K. A. (1987) Inhibition of FSH-stimulated granulosa cell function by a synthetic fragment of the porcine inhibin α-subunit: evidence for involvement of GnRH receptors. J. Endocrinol. 113, R3-R5 (Pubitemid 17071616)
33. Jimenez-Krassel, F., Winn, M. E., Burns, D., Ireland, J. L., and Ireland, J. J. (2003) Evidence for a negative intrafollicular role for inhibin in regulation of estradiol production by granulosa cells. Endocrinology 144, 1876-1886 (Pubitemid 36543327)
34. Geng, L. Y., Fang, M., Yi, J. M., Jiang, F., Moeen-ud-Din, M., and Yang, L. G. (2008) Effect of overexpression of inhibin alpha (1-32) fragment on bovine granulosa cell proliferation, apoptosis, steroidogenesis, and development of co-cultured oocytes. Theriogenology 70, 35-43
35. 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, 15930-15939 (Pubitemid 47093312)
36. Thompson, T. B., Lerch, T. F., Cook, R. W., Woodruff, T. K., and Jardetzky, T. S. (2005) The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev Cell 9, 535-543 (Pubitemid 41430736)
37. Cook, R. W., Thompson, T. B., Kurup, S. P., Jardetzky, T. S., and Woodruff, T. K. (2005) Structural basis for a functional antagonist in the transforming growth factor β superfamily. J. Biol. Chem. 280, 40177-40186 (Pubitemid 41779154)
38. Antenos, M., Stemler, M., Boime, I., and Woodruff, T. K. (2007) N-linked oligosaccharides direct the differential assembly and secretion of inhibin α- and βA-subunit dimers. Mol. Endocrinol. 21, 1670-1684 (Pubitemid 47001090)
39. Suszko, M. I., Lo, D. J., Suh, H., Camper, S. A., and Woodruff, T. K. (2003) Regulation of the rat follicle-stimulating hormone β-subunit promoter by activin. Mol. Endocrinol. 17, 318-332 (Pubitemid 36315627)
40. Scott, R. S., Burger, H. G., and Quigg, H. (1980) A simple and rapid in vitro bioassay for inhibin. Endocrinology 107, 1536-1542 (Pubitemid 10029750)
41. Vale, W., Rivier, C., Hsueh, A., Campen, C., Meunier, H., Bicsak, T., Vaughan, J., Corrigan, A., Bardin, W., and Sawchenko, P. (1988) Chemical and biological characterization of the inhibin family of protein hormones. Recent Prog. Horm. Res. 44, 1-34
42. Woodruff, T. K., D'Agostino, J., Schwartz, N. B., and Mayo, K. E. (1988) Dynamic changes in inhibin messenger RNAs in rat ovarian follicles during the reproductive cycle. Science 239, 1296-1299
43. Woodruff, T. K., and Mayo, K. E. (1990) Regulation of inhibin synthesis in the rat ovary. Annu. Rev. Physiol. 52, 807-821 (Pubitemid 20103570)
44. Bilezikjian, L. M., Blount, A. L., Donaldson, C. J., and Vale, W. W. (2006) Pituitary actions of ligands of the TGF-β family: activins and inhibins. Reproduction 132, 207-215 (Pubitemid 44269703)
45. Rivier, J., Spiess, J., McClintock, R., Vaughan, J., and Vale, W. (1985) Purification and partial characterization of inhibin from porcine follicular fluid. Biochem. Biophys. Res. Commun. 133, 120-127 (Pubitemid 16155336)
46. Carroll, R. S., Kowash, P. M., Lofgren, J. A., Schwall, R. H., and Chin, W. W. (1991) In vivo regulation of FSH synthesis by inhibin and activin. Endocrinology 129, 3299-3304
47. Rivier, C., Schwall, R., Mason, A., Burton, L., and Vale, W. (1991) Effect of recombinant inhibin on gonadotropin secretion during proestrus and estrus in the rat. Endocrinology 128, 2223-2228
48. Gray, P. C., Greenwald, J., Blount, A. L., Kunitake, K. S., Donaldson, C. J., Choe, S., and Vale, W. (2000) Identification of a binding site on the type II activin receptor for activin and inhibin. J. Biol. Chem. 275, 3206-3212 (Pubitemid 30083020)
49. Phillips, D. J., and Woodruff, T. K. (2004) Inhibin: actions and signaling. Growth Factors 22, 13-18
50. Greenwald, J., Vega, M. E., Allendorph, G. P., Fischer, W. H., Vale, W., and Choe, S. (2004) A flexible activin explains the membrane-dependent cooperative assembly of TGF-β family receptors. Mol. Cell 15, 485-489 (Pubitemid 39092763)
51. Knight, P. G., Beard, A. J., Wrathall, J. H., and Castillo, R. J. (1989) Evidence that the bovine ovary secretes large amounts of monomeric inhibin α-subunit and its isolation from bovine follicular fluid. J. Mol. Endocrinol. 2, 189-200 (Pubitemid 19117455)
52. Lee, V. W., Kraft, N. C., Atkins, R. C., and Burger, H. G. (1986) Monoclonal antibody to rat ovarian inhibin. J. Endocrinol. 109, 379-383 (Pubitemid 16085832)
53. Schneyer, A. L., Fujiwara, T., Fox, J., Welt, C. K., Adams, J., Messerlian, G. M., and Taylor, A. E. (2000) Dynamic changes in the intrafollicular inhibin/activin/follistatin axis during human follicular development: relationship to circulating hormone concentrations. J. Clin. Endocrinol. Metab. 85, 3319-3330
54. DePaolo, L. V., Bicsak, T. A., Erickson, G. F., Shimasaki, S., and Ling, N. (1991) Follistatin and activin: a potential intrinsic regulatory system within diverse tissues. Proc. Soc. Exp. Biol. Med. 198, 500-512
55. Besecke, L. M., Guendner, M. J., Sluss, P. A., Polak, A. G., Woodruff, T. K., Jameson, J. L., Bauer-Dantoin, A. C., and Weiss, J. (1997) Pituitary follistatin regulates activin-mediated production of follicle-stimulating hormone during the rat estrous cycle. Endocrinology 138, 2841-2848
56. Woodruff, T. K., Krummen, L. A., Lyon, R. J., Stocks, D. L., and Mather, J. P. (1993) Recombinant human inhibin A and recombinant human activin A regulate pituitary and ovarian function in the adult female rat. Endocrinology 132, 2332-2341 (Pubitemid 23156880)
57. Schneyer, A. L., Rzucidlo, D. A., Sluss, P. M., and Crowley, W. F., Jr. (1994) Characterization of unique binding kinetics of follistatin and activin or inhibin in serum. Endocrinology 135, 667-674 (Pubitemid 24241249)
58. Faddy, M. J., Gosden, R. G., Gougeon, A., Richardson, S. J., and Nelson, J. F. (1992) Accelerated disappearance of ovarian follicles in mid-life: implications for forecasting menopause. Hum. Reprod. 7, 1342-1346 (Pubitemid 23042150)
59. Woodruff, T. K., Besecke, L. M., Groome, N., Draper, L. B., Schwartz, N. B., and Weiss, J. (1996) Inhibin A and inhibin B are inversely correlated to follicle-stimulating hormone, yet are discordant during the follicular phase of the rat estrous cycle, and inhibin A is expressed in a sexually dimorphic manner. Endocrinology 137, 5463-5467
60. Robertson, D. M., Hale, G. E., Fraser, I. S., Hughes, C. L., and Burger, H. G. (2008) A proposed classification system for menstrual cycles in the menopause transition based on changes in serum hormone profiles. Menopause 15, 1139-1144
61. Chapman, S. C., and Woodruff, T. K. (2003) Betaglycan localization in the female rat pituitary: implications for the regulation of follicle-stimulating hormone by inhibin. Endocrinology 144, 5640-5649 (Pubitemid 37476093)