Follistatin and its role as an activin-binding protein

Journal of Medical Investigation

Volumn 44, Issue 1-2, 1997, Pages 1-14

  Sugino, Hiromu ^a   Sugino, Kishiko ^a   Hashimoto, Osamu ^b   Shoji, Hiroki ^c   Nakamura, Takanori ^c  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^c KAGAWA UNIVERSITY   (Japan)

Author keywords

Activin; Follistatin; Heparan sulfate

Indexed keywords

ACTIVIN; FOLLISTATIN; GLYCOPROTEIN; INHIBIN;

AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMISTRY; FEMALE; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; RAT; REVIEW; SIGNAL TRANSDUCTION;

ACTIVINS; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; FEMALE; FOLLISTATIN; GLYCOPROTEINS; HUMANS; INHIBINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; RATS; SIGNAL TRANSDUCTION;

EID: 0031196169     PISSN: 13431420     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, Karr D, Spiess J: Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 321: 776-779, 1986
2. Ling N, Ying SY, Ueno N, Shimasaki S, Esch F, Hotta M, Guillemin R: Pituitary FSH is released by a heterodimer of the β-subunits from the two forms of inhibin. Nature 321: 779-782, 1986
3. Robertson DM, Foulds LM, Leversha L, Morgan FJ, Hearn MTW, Burger HG, Wettenhall REH, de Kretser DM: Isolation of inhibin from bovine follicular fluid. Biochem Biophys Res Commun 126: 220-226, 1985
4. Miyamoto K, Hasegawa Y, Fukuda M, Nomura M, Igarashi M, Kangawa K, Matuo H: Isolation of porcine follicular fluid inhibin of 32 K daltons. Biochem Biophys Res Commun 129: 396-403,1985
5. Ling N, Ying SY, Ueno N, Esch F, Denoroy L, Guillemin R: Isolation and partial characterization of a Mr 32,000 protein with inhibin activity from porcine follicular fluid. Proc Natl Acad Sci USA 82: 7217-7221, 1985
6. Rivier J, Spiess J, McClintock R, Vaughan J, Vale W: Purification and partial characterization of inhibin from porcine follicular fluid. Biochem Biophys Res Commun 133: 120-127, 1985
7. Ueno N, Ling N, Ying SY, Esch F, Shimasaki S, Guillemin R: Isolation and partial characterization of follistatin: A signal-chain Mr 35,000 monomeric protein that inhibits the release of follicle-stimulating hormone. Proc Natl Acad Sci USA 84: 8282-8286, 1987
8. Mason AJ, Hayflick JS, Ling N, Esch F, Ueno N, Ying SY, Guillemin R, Niall H, Seeburg PH: Complementary DNA sequences of ovarian follicular fluid inhibin show precursor structure and homology with transforming growth factor-β. Nature 318: 659-663, 1985
9. Forage RG, Ring JM, Brown RW, McInerney BV, Cobon GS, Gregson RP, Robertson DM, Morgan FJ, Hearn MTW, Findlay JK, Wettenhall REH, Burger HG, de Kretser DM: Cloning and sequence analysis of cDNA species coding for the two subunits of inhibin from bovine follicular fluid. Proc Natl Acad Sci USA 83: 3091-3095, 1986
10. Mayo KE, Cerelli GM, Spiess J, Rivier J, Rosenfeld MG, Evans RM, Vale W: Inhibin A-subunit cDNAs from porcine ovary and human placenta. Proc Natl Acad Sci USA 83: 5849-5853, 1986
11. Mason AJ, Niall HD, Seeburg PH: Structure of two human ovarian inhibins. Biochem Biophys Res Commun 135: 957-964, 1986
12. Esch FS, Shimasaki S, Cooksey K, Mercado M, Mason AJ, Ying SY, Ueno N, Ling N: Complementary deoxyribonucleic acid (cDNA) cloning and DNA sequence analysis of rat ovarian inhibins. Molec Endocrinol 1: 388-396, 1987
13. Mason AJ, Berkemeier LM, Schmelzer CH, Schwall RH: Activin B: Precursor sequences, genomic structure and in vitro activities. Molec Endocrinol 3: 1352-1358, 1989
14. Höten G, Neidhart H, Shneider C, Pohl J: Cloning of a new member of the TGF-β family: A putative new activin βC chain. Biochem Biophys Res Commun 206: 608-613, 1995
15. Oda S, Nishimatsu S, Murakami K, Ueno N: Molecular cloning and functional analysis of a new activin β subunit: A dorsal mesoderm-inducing activity in Xenopus. Biochem Biophys Res Commun 210: 581-588, 1995
16. Fang J, Yin W, Smiley E, Wang SQ, Bonadio J: Molecular cloning of the mouse activin βE subunit gene. Biochem Biophys Res Commun 228: 669-674, 1996
17. Nakamura T, Asashima M, Eto Y, Takio K, Uchiyama H, Moriya N, Ariizumi T, Yashiro T, Sugino K, Titani K, Sugino H: Isolation and characterization of native activin B. J Biol Chem 267: 16385-16389, 1992
18. Murata T, Ying YS: Transforming growth factor-β and activin inhibit basal secretion of prolactin in a pituitary monolayer culture system. Proc Soc Exp Biol Med 198: 599-605, 1991
19. Kitaoka M, Kojima I, Ogata E: Activin A: A modulator of multiple types of anterior pituitary cells. Biochem Biophys Res Commun 157: 48-54, 1988
20. Billestrup N, Gonzalez-Manchon C, Potter E, Vale W: Inhibition of somatotroph growth and GH biosynthesis by activin in vitro. Mol Endocrinol 4: 356-362, 1990
21. Bilezikjian LM, Corrigan A, Vale W: Activin A modulates growth hormone secretion from cultures of rat anterior pituitary cells. Endocrnology 126: 2369-2376, 1990
22. Bilezikjian LM, Blount AL, Campen CA, Gonzalez-Manchon C, Vale W: Activin A inhibits POMC mRNA accumulation and ACTH secretion of AtT20 cells. Mol Endocrinol 5: 1389-1395, 1991
23. Eto Y, Tsuji T, Takezawa M, Takano S, Yokozawa Y, Shibai H: Purification and characterization of erythroid differentiation factor (EDF) isolatied from human leukemia cell line THP-1.Biochem Biophys Res Commun 142: 1095-1103, 1987
24. Yu J, Shao L, Lemas V, Yu AL, Vaughan J, Rivier J, Vale W: Importance of FSH-releasing protein and inhibin in erythrodifferentiation. Nature 330: 765-767, 1987
25. Broxmeyer HE, Lu L, Cooper S, Schwall RH, Mason AJ, Nikolics K: Selective and indirect modulation of human multipotential and erythroid hematopoietic progenitor cell proliferation by recombinant human activin and inhibin. Proc Natl Acad Sci USA 85: 9052-9056, 1988
26. Lebrun JJ, Vale WW: 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, 1997
27. Sugino H, Nakamura T, Hasegawa Y, Miyamoto K, Abe Y, Igarashi M, Eto Y, Shibai H, Titani K: Erythroid differentiation factor can modulate follicular granulosa cell functions. Biochem Biophys Res Commun 153: 281-288, 1988
28. Hutchinson LA, Findlay JK, de Vos FL, Robertson DM: Effects of bovine inhibin, transforming growth factor-β and bovine activin-A on granulosa cell differentiation. Biochem Biophys Res Commun 146: 1405-1412, 1987
29. Hasegawa Y, Miyamoto K, Abe Y, Nakamura T, Sugino H, Eto Y, Shibai H, Igarashi M: Induction of follicle stimulating hormone receptor by erythroid differentiation factor on rat granulosa cell. Biochem Biophys Res Commun 156: 668-674, 1988
30. Hsueh AJW, Dahl KD, Vaughan J, Tucker E, Rivier J, Bardin CW, Vale W: Heterodimers and homodimers of inhibin subunits have different paracrine action in the modulation of luteinizing hormone-stimulated androgen biosynthesis. Proc Natl Acad Sci USA 84: 5082-5086, 1987
31. Mather JP, Attie KM, Woodruff TK, Rice GC, Philiips DM: Activin stimulates spermatogonial proliferation in germ-Sertoli cell cocultures from immature rat testis. Endocrinology 127: 3206-3214, 1990
32. Schubert D, Kimura H, LaCorbiere M, Vaughan J, Karr D, Fischer WH: Activin is a nerve cell survival molecule. Nature 344: 868-870, 1990
33. Hashimoto M, Kondo S, Sakurai T, Etoh Y, Shibai H, Muramatsu M: Activin/EDF as an inhibitor of neural differentiation. Biochem Biophys Res Commun 173: 193-200, 1990
34. Asashima M, Nakano H, Shimada K, Kinoshita K, Ishii K, Shibai H, Ueno N: Mesodermal induction in early amphibian embryos by activin A (erthroid differentiation factor). Roux's Arch Dev Biol 198: 330-335, 1990
35. Asashima M, Nakano H, Uchiyama H, Davids M, Plessow S, Loppnow-Blinde B, Hoppe P, Dan H, Tiedemann H: The vegitalizing factor belongs to a family of mesoderm-inducing proteins related to erythroid differentiation factor. Naturwissenschaften 77: 389-391, 1990
36. Smith JC, Price BMJ, Van Nimmen K, Huylebroeck D: Identification of a potent Xenopus mesoderm-inducing factor as a homologue of activin A. Nature 345: 729-731, 1990
37. van den Eijnden-Van Raaij AJM, van Zoelent EJJ, van Nimmen K, Koster CH, Snoek GT, Durston AJ, Huylebroeck D: Activin-like factor from a Xenopus laevis cell line responsible for mesoderm induction. Nature 345: 732-734, 1990
38. Thomsen G, Woolf T, Whitman M, Sokol S, Vaughan J, Vale W, Melton DA: Activins are expressed early in Xenopus embryogenesis and can induce axial mesoderm and anterior structures. Cell 63: 485-493, 1990
39. Mitrani E, Ziv T, Thomsen G, Shimoni Y, Melton DA, Bril A: Activin can induce the formation of axial structures and is expressed in the hypoblast of the chick. Cell 63: 495-501, 1990
40. Asashima M, Nakano H, Uchiyama H, Sugino H, Nakamura T, Eto Y, Ejima D, Nishimatsu S, Ueno N, Kinoshita K: Presence of activin (erythroid differentiation factor) in unfertilized eggs and blastulae of Xenopus laevis. Proc Natl Acad Sci USA 88: 6511-6514, 1991
41. Totsuka Y, Tabuchi M, Kojima I, Shibai H, Ogata E: A novel action of activin A: Stimulation of insulin secretion in rat pancreatic islets. Biochem Biophys Res Commun 156: 335-339, 1988
42. Centrella M, McCarthy TL, Canalis E: Activin-A binding and biochemical effects in osteoblast-enriched cultures from fetal-rat parietal bone. Mol Cell Biol 11: 250-258, 1991
43. Hashimoto M, Shoda A, Inoue S, Yamada R, Kondo T, Sakurai T, Ueno N, Muramatsu M: Functional regulation of osteoblastic cells by the interaction of activin A with follistatin. J Biol Chem 267: 4999-5004, 1992
44. Ogawa Y, Schmidt DK, Nathan RM, Armstrong RM, Miller KL, Sawamura SJ, Ziman JM, Erickson KL, de Leon ER, Rosen DM, Seyedin SM, Glaser CB, Chang RJ, Corrigan AZ, Vale W: Bovine bone activin enhances bone morphogenetic protein-induced ectopic bone formation. J Biol Chem 267: 14233-14237, 1992
45. Meunier H, Rivier C, Evans RM, Vale W: Gonadal and extragonadal expression of inhibin α, βA and βB subunits in various tissues predicts diverse functions. Proc Natl Acad Sci USA 85: 247-251, 1988
46. Mathews LS, Vale WW: Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65: 973-982, 1991
47. Mathews LS: Activin receptors and cellular signaling by the receptor serine kinase family. Endocr Rev 15: 310-325, 1994
48. Robertson DM, Klein R, de Vos FL, McLachlan RI, Wettenhall RE, Hearn MT, Burger HG, de Kretser DM: The isolation of polypeptides with FSH suppressing activity from bovine follicular fluid which are structually different to inhibin. Biochem Biophys Res Commun 149: 744-749, 1987
49. Nakamura T, Takio K, Eto Y, Shibai H, Titani K, Sugino H: Activin-binding protein from rat ovary is follistatin. Science 247: 836-838, 1990
50. Kogawa T, Nakamura T, Sugino K, Takio K, Titani K, Sugino H: Activin-binding protein is present in pituitary. Endocrinology 128: 1434-1440, 1991
51. Shimasaki S, Koga M, Esch F, Mercado M, Cooksey K, Koba A, Ling N: Porcine follistatin gene structure supports two forms of mature follistatin produced by alternative splicing. Biochem Biophys Rec Commun 152: 717-723, 1988
52. Shimasaki S, Koga M, Esch F, Cooksey K, Mercado M, Koba A, Ueno N, Ying SY, Ling N, Guilemin R: Primary structure of the human follistatin precursor and its genomic organization. Proc Natl Acad Sci USA 85: 4218-4222, 1988
53. Yokoyama Y, Nakamura T, Nakamura R, Ihara M, Aono T, Sugino H: Identification of activins and follistatin proteins in human follicular fluid and placenta. J Clin Endocrinol Metab 80: 915-921, 1995
54. Fukui A, Nakamura T, Sugino K, Takio K, Uchiyama H, Asashima M, Sugino H: Isolation and characterization of Xenopus follistatin and activins. Dev Biol 159: 131-139, 1993
55. Sugino K, Kurosawa N, Nakamura T, Takio K, Shimasaki S, Ling N, Titani K, Sugino H: 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: 15579-15587, 1993
56. Kogawa K, Ogawa K, Hayashi Y, Nakamura T, Titani K, Sugino H: Immunohistochemical localization of follistatin in rat tissues. Endocrinnol Jpn 38: 383-391, 1991
57. Kogawa K: Function and localization of follistatin, a binding protein for activin. Ph. D. Thesis Acta, University of Tokyo, 1992
58. Shimasaki S, Koga M, Buscaglia ML, Simmons DM, Bicsak TA, Ling N: Follistatin gene expression in the ovary and extragonadal tissues. Mol Endocrinol 3: 651-659, 1989
59. Nakamura T, Hasegawa Y, Sugino K, Kogawa K, Titani K, Sugino H: Follistatin inhibits activin-induced differentiation of rat follicular granulosa cells in vitro. Biochem Biophys Acta 1135: 103-109, 1992
60. Shiozaki M, Sakai R, Tabuchi M, Nakamura T, Sugino K, Sugino H, Eto Y: Evidence for the participation of endogenous activin A/erythroid differentiation factor in the regulation of erythropoiesis. Proc Natl Acad Sci USA 89: 1553-1556, 1992
61. Asashima M, Nakano H, Uchiyama H, Sugino H, Nakamura T, Eto Y, Ejima D, Davids M, Plessow S, Cinchocka I, Kinoshita K: Follistatin inhibits the mesoderm-inducing activity of activin A and the vegetalizing factor from chicken embyo. Roux's Arch Dev Biol 200: 4-7, 1991
62. Shimonaka M, Inouye S, Shimasaki S, Ling N: Follistatin binds to both activin and inhibin through the common subunit. Endocrinology 128: 3313-3315, 1991
63. Krummen LA, Woodruff TK, DeGuzman G, Cox ED, Baly DL, Mann E, Garg S, Wong WE, Cossum P, Mather JP: Identification and characterization of binding proteins for inhibin and activin in human serum and follicular fluids. Endcrinology 132: 431-443, 1993
64. 2-Macroglobulin is a binding protein of inhibin and activin. Endocrinology 132: 2038-2050, 1993
65. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM: Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64: 841-848, 1991
66. Nakamura T, Sugino K, Titani K, Sugino H: Follistatin, an activin-binding protein, associates with heparan sulfate chains of proteoglycans on follicular granulosa cells. J Biol Chem 266: 19432-19437, 1991
67. Inouye S, Guo Y, DePaolo L, Shimonaka M, Ling N, Shimasaki S: Recombinant expression of human follistatin with 315 and 288 amino acids: chemical and biological comparison with native porcine follistatin. Endocrinology 129: 815-822, 1991
68. Dalkin AC, Haisenleder DJ, Yasin M, Gilrain JT, Marshall JC: Pituitary activin receptor subtypes and follistatin gene expression in female rats: Differential regulation by activin and follistatin. Endocrinology 137: 548-554, 1996
69. Hashimoto O, Nakamura T, Shoji H, Shimasaki S, Hayashi Y, Sugino H: A novel role of follistatin, an activin-binding protein, in the inhibition of activin action in rat pituitary cells: Endocytotic degradation of activin and its accelaration by follistatin associated with cell-surface heparan sulfate. J Biol Chem 272: 13835-13842, 1997
70. de Winter JP, ten Dijke P, de Vries CJ, van Achterberg TA, Sugino H, de Waele P, Huylebroeck D, Verschueren K, van den Eijnden-van Raaij AJ: Follistatins neutralize activin bioactivity by inhibition of activin binding to its type II receptors. Mol Cell Endocrinol 116: 105-114, 1996
71. Saito S, Nakamura T, Titani K, Sugino H: Production of activin-binding protein by rat granulosa cells in vitro. Biochem Biophys Rec Commun 176: 413-422, 1991
72. Hemmati-Brivanlou A, Melton DA: Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 77: 273-281, 1994
73. Hemmati-Brivanlou A, Kelly OG, Melton DA: Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neutralizing activity. Cell 77: 283-295, 1994
74. Furuya S, Sera M, Tohno-Oka R, Sugahara K, Shiokawa K, Hirabayashi Y: Elimination of heparan sulfate by heparitinases induces abnormal mesodemal and neural formation in Xenopus embyos. Develop Growth Differ 37: 337-346, 1995
75. Piccolo S, Sasai Y, Lu B, De Robertis EM: Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589-598, 1996
76. Zimmerman LB, De Jesús-Escobar JM, Harland RM: The Spemann organazer signal noggin binds and inactivates bone morphogenetic protein 4. Cell 86: 599-606, 1996