Growth differentiation factor-9 induces Smad2 activation and inhibin B production in cultured human granulosa-luteal cells

Journal of Clinical Endocrinology and Metabolism

Volumn 88, Issue 2, 2003, Pages 755-762

  Kaivo Oja, Noora ^a   Bondestam, Jonas ^a   Kämäräinen, Meerit ^a   Koskimies, Janne ^a   Vitt, Ursula ^b   Cranfield, Mark ^c   Vuojolainen, Kaisa ^a   Kallio, Janne P ^a   Olkkonen, Vesa M ^d   Hayashi, Masaru ^b   Moustakas, Aristidis ^e   Groome, Nigel P ^c   Ten Dijke, Peter ^f   Hsueh, Aaron J W ^b   Ritvos, Olli ^a,g  

^a UNIVERSITY OF HELSINKI   (Finland)

^b STANFORD UNIVERSITY   (United States)

^c OXFORD BROOKES UNIVERSITY   (United Kingdom)

^d NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^e LUDWIG INSTITUTE FOR CANCER RESEARCH   (Sweden)

^f NETHERLANDS CANCER INSTITUTE   (Netherlands)

^g UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; GONADOTROPIN; GROWTH DIFFERENTIATION FACTOR 9; INHIBIN B; MESSENGER RNA; PROTEIN ANTIBODY; RECOMBINANT PROTEIN; SMAD2 PROTEIN; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GRANULOSA CELL; HUMAN; HUMAN CELL; LUTEAL CELL; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY FOLLICLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; STEADY STATE; WESTERN BLOTTING;

ADENOVIRIDAE; ANIMALS; ANTIBODIES, MONOCLONAL; CELLS, CULTURED; DIMERIZATION; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION, VIRAL; HUMANS; INHIBINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LUTEAL CELLS; MICE; PHOSPHORYLATION; RATS; RECOMBINANT PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; TRANS-ACTIVATORS;

ADENOVIRIDAE; FALLOPIA; MAMMALIA;

EID: 0037326090     PISSN: 0021972X     EISSN: None     Source Type: Journal    
DOI: 10.1210/jc.2002-021317     Document Type: Article

References (45)

1. McPherron AC, Lee SJ 1993 GDF-3 and GDF-9: two new members of the transforming growth factor-β superfamily containing a novel pattern of cysteines. J Biol Chem 268:3444-3449
2. McGrath SA, Esquela AF, Lee SJ 1995 Oocyte specific expression of growth differentiation factor-9. Mol Endocrinol 9:131-136
3. Fitzpatrick SL, Sindoni DM, Shughrue PJ, Lane MV, Merchenthaler IJ, Frail DE 1998 Expression of growth differentiation factor-9 messenger ribonucleic acid in ovarian and nonovarian rodent and human tissues. Endocrinology 139:2571-2578
4. Dong J, Albertini DF, Nishimori K, Kumar R, Lu N, Matzuk MM 1996 Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383:531-535
5. Eppig JJ 2001 Oocyte control of ovarian follicular development and function in mammals. Reproduction 122:829-938
6. Erickson GF, Shimasaki S 2000 The role of the oocyte in folliculogenesis. Trends Endocrinol Metab 11:193-198
7. Laitinen M, Vuojolainen K, Jaatinen R, Ketola I, Aaltonen J, Lehtonen E, Heikinheimo M, Ritvos O 1998 A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev 78:135-140
8. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM 1998 The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 12:1809-1817
9. Galloway SM, McNatty KP, Cambridge LM, Laitinen MPE, Juengel JL, Jokiranta S, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie A, Davis GH, Ritvos O 2000 Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertililty in a dosage-sensitive manner. Nat Genet 25:279-283
10. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppä L, Louhio H, Tuuri T, Sjöberg J, Bützow R, Hovatta O, Dale L, Ritvos O 1999 Human growth differentiation factor-9 and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab 84:2744-2750
11. Teixeira Filho FL, Baracat EC, Lee TH, Suh CS, Matsui M, Chang RJ, Shimasaki S, Erickson GF 2002 Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab 87:1337-1344
12. Hayashi M, McGee EA, Min G, Klein C, Rose UM, van Duin M, Hsueh AJW 1999 Recombinant growth and differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140:1236-1244
13. Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJW, Hovatta O 2002 Growth differentiation factor-9 promotes the growth, development and survival of human ovarian follicles in organ culture. J Clin Endocrinol Metab 87:316-321
14. Vitt UA, McGee EA, Hayashi M, Hsueh AJ 2000 In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141:3814-3820
15. Massagué J, Chen YG 2000 Controlling TGF-β signaling. Genes Dev 14:27-644
16. Miyazono K, ten Dijke P, Heldin CH 2000 TGF-β signaling by Smad proteins. Adv Immunol 75:115-157
17. Ishisaki A, Yamamoto K, Hashimoto S, Nakao A, Tamaki K, Nonaka K, ten Dijke P, Sugino H, Nishihara T 1999 Differential inhibition of Smad6 and Smad7 on bone morphogenetic protein-and activin-mediated growth arrest and apoptosis in B cells. J Biol Chem 274:13637-13642
18. Erämaa M, Hilden K, Tuuri T, Ritvos O 1995 Regulation of inhibin/activin subunit messenger ribonucleic acids (mRNAs) by activin A and expression of activin receptor mRNAs in cultured human granulosa-luteal cells. Endocrinology 136:4382-4389
19. B-subunit messenger ribonucleic acid levels in cultured human granulosa-luteal cells. Fertil Steril 65:954-960
20. B-subunit messenger ribonucleic acid and secreted inhibin B levels in cultured human granulosa-luteal cells. J Clin Endocrinol Metab 87:254-1261
21. Persson U, Izumi H, Souchelnytskyi S, Itoh S, Grimsby S, Engstrom U, Heldin CH, Funa K, ten Dijke P 1998 The L45 loop in type I receptors for TGF-β family members is a critical determinant in specifying Smad isoform activation. FEBS Left 434:83-87
22. Piek E, Westermark U, Kastemar M, Heldin C-H, van Zoelen EJ, Nister M, ten Dijke P 1999 Expression of transforming growth factor (TGF)-β receptors in glioblastoma cell lines with distinct responses to TGF-β1. Int J Cancer 80:756-763
23. Hobbs S, Jitrapakdee S, Wallace JC 1998 Development of a bicistronic vector driven by the human polypeptide chain elongation factor 1α promoter for creation of stable mammalian cell lines that express very high levels of recombinant proteins. Biochem Biophys Res Commun 252:368-372
24. Erämaa M, Heikinheimo K, Tuuri T, Hilden K, Ritvos O 1993 Inhibin/activin subunit mRNA expression in human granulosa-luteal cells. Mol Cell Endocrinol 92:R15-R20
25. Fujii M, Takeda K, Imamura T, Aoki H, Sampath TK, Enomoto S, Kawabata M, Kato M, Ichijo H, Miyazono K 1999 Roles of bone morphogenetic protein type I receptors and smad proteins in osteoblast and chondroblast differentiation. Mol Biol Cell 10:3801-3813
26. Bondestam J, Kaivo-oja N, Kallio J, Hyden-Granskog C, Groome N, Fujii M, Moustakas A, Jalanko A, ten Dijke P, Ritvos O 2002 Engagement of activin and bone morphogenetic protein signaling pathway Smad proteins in the induction of inhibin B production in cultured human granulosa-luteal cells. Mol Cell Endocrinol 195:79-88
27. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, Vogelstein B 1998 A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95:2509-2514
28. Kumar A, Novoselov V, Celeste AJ, Wolfman NM, ten Dijke P, Kuehn MR 2000 Nodal signaling uses activin and transforming growth factor-β receptor-regulated smads. J Biol Chem 276:656-661
29. Laitinen M, Rutanen EM, Ritvos O 1995 Expression of c-kit ligand messenger ribonucleic acids in human ovaries and regulation of their steady-state levels by gonadotropins in cultured granulosa-luteal cells. Endocrinology 136:4407-4414
30. Zhang Y, Feng X, We R, Derynck R 1996 Receptor-associated mad homologues synergize as effectors the TGFβ-response. Nature 383:168-172
31. Yamamoto N, Christenson LK, McAllister JM, Strauss III JF 2002 Growth differentiation factor-9 inhibits 3′5′-adenosine monophosphate-stimulated steroidogenesis in human granulosa and theca cells. J Clin Endocrinol Metab 87:2849-2856
32. Juengel JL, Hudson NL, Heath DA, Smith P, Reader KR, Lawrence SB, O'Connell AR, Laitinen MPE, Cranfield M, Groome NP, Ritvos O, McNatty KP 2002 Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol Reprod 67:1777-1789
33. Vitt UA, Mazerbourg S, Klein C, Hsueh AJW 2002 Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol Reprod 67:473-480
34. Lo R, Massague J 1999 Ubiquitin-dependent degradation of TGF-β-activated Smad2. Nat Cell Biol 1:472-478
35. Somers JP, DeLoia JA, Zeleznik AJ 1999 Adenovirus-directed expression of a nonphosphorylatable mutant of CREB (cAMP response element-binding protein) adversely affects the survival, but not the differentiation, of rat granulosa cells. Mol Endocrinol 13:1364-1372
36. Roh J-S, Bondestam J, Mazerbourg S, Kaivo-oja N, Groome N, Ritvos O, Hsueh AJW 2003 Growth differentiation factor-9 (GDF-9) stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 144:172-178.
37. Xu J, Oakley J, McGee EA 2002 Stage-specific expression of smad2 and smad3 during folliculogenesis. Biol Reprod 66:1571-1578
38. Tomic D, Biodie SG, Deng C, Hickey RJ, Babus JK, Malkas LH, Flaws JA 2002 Smad 3 may regulate follicular growth in the mouse ovary. Biol Reprod 66:917-923
39. Kano K, Notani A, Nam SY, Fujisawa M, Kurohmaru M, Hayashi Y 1999 Cloning and studies of the mouse cDNA encoding Smad3. J Vet Med Sci 61:213-219
40. Pangas SA, Rademaker AW, Fishman DA, Woodruff TK 2002 Localization of the activin signal transduction components in normal human ovarian follicles: implications for autocrine and paracrine signaling in the ovary. J Clin Endocrinol Metab 87:2644-2657
41. Lanuza GM, Groome NP, Baranao JL, Campo S 1999 Dimeric inhibin A and B production are differentially regulated by hormones and local factors in rat granulosa cells. Endocrinology 140:2549-2554
42. Vänttinen T, Liu J, Hyden-Granskog C, Parviainen M, Penttilä I, Voutilainen R 2000 Regulation of immunoreactive inhibin A and B secretion in cultured human granulosa-luteal cells by gonadotropins, activin A and insulin-like growth factor type-1 receptor. J Endocrinol 167:289-294
43. Yu L, Hebert MC, Zhang YE 2002 TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO J 21:3749-3759
44. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ 2002 Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 143:2221-2232
45. Mulsant P, Lecerf F, Fabre S, Schibler L, Monget P, Lanneluc I, Pisselet C, Riquet J, Monniaux D, Callebaut I, Cribiu E, Thimonier J, Teyssier J, Bodin L, Cognie Y, Chitour N, Elsen JM 2001 Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc Natl Acad Sci USA 98:5104-5109