Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5

Molecular Endocrinology

Volumn 18, Issue 3, 2004, Pages 653-665

  Mazerbourg, Sabine ^a   Klein, Cynthia ^a   Roh, Jaesook ^a   Kaivo Oja, Noora ^b,c   Mottershead, David G ^b,c   Korchynskyi, Olexander ^d,e   Ritvos, Olli ^b,c   Hsueh, Aaron J W ^a,a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Program for Developmental and Reproductive Biology   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

^e UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; GROWTH DIFFERENTIATION FACTOR 9; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD6 PROTEIN; SMAD7 PROTEIN; SMALL INTERFERING RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; FEMALE; GENE ACTIVITY; GENE FUNCTION; GENE OVEREXPRESSION; GRANULOSA CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; REPORTER GENE; SIGNAL TRANSDUCTION;

ACTIVIN RECEPTORS, TYPE I; ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEINS; CELLS, CULTURED; COS CELLS; DNA-BINDING PROTEINS; FEMALE; GRANULOSA CELLS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROMOTER REGIONS (GENETICS); RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD6 PROTEIN; SMAD7 PROTEIN; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA;

EID: 1542357571     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2003-0393     Document Type: Article

References (67)

1. Adashi EY 1992 Intraovarian peptides. Stimulators and inhibitors of follicular growth and differentiation. Endocrinol Metab Clin North Am 21:1-17
2. McGee EA, Hsueh AJ 2000 Initial and cyclic recruitment of ovarian follicles. Endocr Rev 21:200-214
3. Jaatinen R, Rosen V, Tuuri T, Ritvos O 1996 Identification of ovarian granulosa cells as a novel site of expression for bone morphogenetic protein-3 (BMP-3/osteogenin) and regulation of BMP-3 messenger ribonucleic acids by chorionic gonadotropin in cultured human granulosaluteal cells. J Clin Endocrinol Metab 81:3877-3882
4. Shimasaki S, Zachow RJ, Li D, Kim H, Iemura S, Ueno N, Sampath K, Chang RJ, Erickson GF 1999 A functional bone morphogenetic protein system in the ovary. Proc Natl Acad Sci USA 96:7282-7287
5. Liu X, Andoh K, Abe Y, Kobayashi J, Yamada K, Mizunuma H, Ibuki Y 1999 A comparative study on transforming growth factor-β and activin A for preantral follicles from adult, immature, and diethylstilbestrol-primed immature mice. Endocrinology 140:2480-2485
6. 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
7. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM 1996 Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383: 531-535
8. Hayashi M, McGee EA, Min G, Klein C, Rose UM, van Duin M, Hsueh AJ 1999 Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140: 1236-1244
9. 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
10. 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
11. Otsuka F, Yao Z, Lee T, Yamamoto S, Erickson GF, Shimasaki S 2000 Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 275:39523-39528
12. Jaatinen R, Laitinen MP, Vuojolainen K, Aaltonen J, Louhio H, Heikinheimo K, Lehtonen E, Ritvos O 1999 Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homolog GDF-9B. Mol Cell Endocrinol 156: 189-193
13. McGrath SA, Esquela AF, Lee SJ 1995 Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 9:131-136
14. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, Seppa L, Louhio H, Tuuri T, Sjoberg J, Butzow R, Hovata O, Dale L, Ritvos O 1999 Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J Clin Endocrinol Metab 84:2744-2750
15. 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
16. Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJ, 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
17. Vitt UA, Hayashi M, Klein C, Hsueh AJ 2000 Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod 62:370-377
18. Kaivo-Oja N, Bondestam J, Kamarainen M, Koskimies J, Vitt U, Cranfield M, Vuojolainen K, Kallio JP, Olkkonen VM, Hayashi M, Moustakas A, Groome NP, ten Dijke P, Hsueh AJ, Ritvos O 2003 Growth differentiation factor-9 induces Smad2 activation and inhibin B production in cultured human granulosa-luteal cells. J Clin Endocrinol Metab 88:755-762
19. Roh JS, Bondestam J, Mazerbourg S, Kaivo-Oja N, Groome N, Ritvos O, Hsueh AJ 2003 Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 144:172-178
20. Elvin JA, Clark AT, Wang P, Wolfman NM, Matzuk MM 1999 Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol 13:1035-1048
21. Solovyeva EV, Hayashi M, Margi K, Barkats C, Klein C, Amsterdam A, Hsueh AJ, Tsafriri A 2000 Growth differentiation factor-9 stimulates rat theca-interstitial cell androgen biosynthesis. Biol Reprod 63:1214-1218
22. Massague J 1998 TGF-β signal transduction. Annu Rev Biochem 67:753-791
23. Kawabata M, Imamura T, Miyazono K 1998 Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Rev 9:49-61
24. Lux A, Attisano L, Marchuk DA 1999 Assignment of transforming growth factor β1 and β3 and a third new ligand to the type I receptor ALK-1. J Biol Chem 274: 9984-9992
25. Nakao A, Afrakhte M, Moren A, Nakayama T, Christian JL, Heuchel R, Itoh S, Kawabata M, Heldin NE, Heldin CH, ten Dijke P 1997 Identification of Smad7, a TGFβ-inducible antagonist of TGF-β signalling. Nature 389: 631-635
26. Hayashi H, Abdollah S, Qiu Y, Cai J, Xu YY, Grinnell BW, Richardson MA, Topper JN, Gimbrone Jr MA, Wrana JL, Falb D 1997 The MAD-related protein Smad7 associates with the TGFβ receptor and functions as an antagonist of TGFβ signaling. Cell 89:1165-1173
27. Hata A, Lagna G, Massague J, Hemmati-Brivanlou A 1998 Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev 12:186-197
28. Ishisaki A, Yamato 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
29. Vitt UA, Mazerbourg S, Klein C, Hsueh AJ 2002 Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol Reprod 67:473-480
30. Newfeld SJ, Wisotzkey RG, Kumar S 1999 Molecular evolution of a developmental pathway: phylogenetic analyses of transforming growth factor-β family ligands, receptors and Smad signal transducers. Genetics 152: 783-795
31. Dennler S, Itoh S, Vivien D, ten Dijke P, Huet S, Gauthier JM 1998 Direct binding of Smad3 and Smad4 to critical TGF β-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J 17:3091-3100
32. Korchynskyi O, ten Dijke P 2002 Identification and functional characterization of distinct critically important bone morphogenetic protein-specific response elements in the Id1 promoter. J Biol Chem 277:4883-4891
33. Kusanagi K, Inoue H, Ishidou Y, Mishima HK, Kawabata M, Miyazono K 2000 Characterization of a bone morphogenetic protein-responsive Smad-binding element. Mol Biol Cell 11:555-565
34. Watanabe R, Yamada Y, Ihara Y, Someya Y, Kubota A, Kagimoto S, Kuroe A, Iwakura T, Shen ZP, Inada A, Adachi T, Ban N, Miyawaki K, Sunaga Y, Tsuda K, Seino Y 1999 The MH1 domains of smad2 and smad3 are involved in the regulation of the ALK7 signals. Biochem Biophys Res Commun 254:707-712
35. Macias-Silva M, Abdollah S, Hoodless PA, Pirone R, Attisano L, Wrana JL 1996 MADR2 is a substrate of the TGFβ receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87:1215-1224
36. Nakao A, Imamura T, Souchelnytskyi S, Kawabata M, Ishisaki A, Oeda E, Tamaki K, Hanai J, Heldin CH, Miyazono K, ten Dijke P 1997 TGF-β receptor-mediated signalling through Smad2, Smad3 and Smad4. EMBO J 16:5353-5362
37. Nakao A, Roijer E, Imamura T, Souchelnytskyi S, Stenman G, Heldin CH, ten Dijke P 1997 Identification of Smad2, a human Mad-related protein in the transforming growth factor β signaling pathway. J Biol Chem 272: 2896-2900
38. Jornvall H, Blokzijl A, ten Dijke P, Ibanez CF 2001 The orphan receptor serine/threonine kinase ALK7 signals arrest of proliferation and morphological differentiation in a neuronal cell line. J Biol Chem 276:5140-5146
39. Reissmann E, Jornvall H, Blokzijl A, Andersson O, Chang C, Minchiotti G, Persico MG, Ibanez CF, Brivanlou AH 2001 The orphan receptor ALK7 and the activin receptor ALK4 mediate signaling by nodal proteins during vertebrate development. Genes Dev 15:2010-2022
40. Cheifetz S, Weatherbee JA, Tsang ML, Anderson JK, Mole JE, Lucas R, Massague J 1987 The transforming growth factor-β system, a complex pattern of cross-reactive ligands and receptors. Cell 48:409-415
41. Cheifetz S, Hernandez H, Laiho M, ten Dijke P, Iwata KK, Massague J 1990 Distinct transforming growth factor-β (TGF-β) receptor subsets as determinants of cellular responsiveness to three TGF-β isoforms. J Biol Chem 265: 20533-20538
42. Rebbapragada A, Benchabane H, Wrana JL, Celeste AJ, Attisano L 2003 Myostatin signals through a transforming growth factor β-like signaling pathway to block adipogenesis. Mol Cell Biol 23:7230-7242
43. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T 2001 Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411:494-498
44. Qu J, Godin PA, Nisolle M, Donnez J 2000 Expression of receptors for insulin-like growth factor-I and transforming growth factor-β in human follicles. Mol Hum Reprod 6:137-145
45. Xu J, Oakley J, McGee EA 2002 Stage-specific expression of Smad2 and Smad3 during folliculogenesis. Biol Reprod 66:1571-1578
46. Larsson J, Goumans MJ, Sjostrand LJ, van Rooijen MA, Ward D, Leveen P, Xu X, ten Dijke P, Mummery CL, Karlsson S 2001 Abnormal angiogenesis but intact hematopoietic potential in TGF-β type I receptor-deficient mice. EMBO J 20:1663-1673
47. Tomic D, Brodie 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
48. Liu F, Ventura F, Doody J, Massague J 1995 Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol Cell Biol 15:3479-3486
49. Rosenzweig BL, Imamura T, Okadome T, Cox GN, Yamashita H, ten Dijke P, Heldin CH, Miyazono K 1995 Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc Natl Acad Sci USA 92:7632-7636
50. Nohno T, Ishikawa T, Saito T, Hosokawa K, Noji S, Wolsing DH, Rosenbaum JS 1995 Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogenetic protein type I receptors. J Biol Chem 270: 22522-22526
51. Yamashita H, ten Dijke P, Huylebroeck D, Sampath TK, Andries M, Smith JC, Heldin CH, Miyazono K 1995 Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J Cell Biol 130: 217-226
52. Koenig BB, Cook JS, Wolsing DH, Ting J, Tiesman JP, Correa PE, Olson CA, Pecquet AL, Ventura F, Grant RA, Chen G-X, Wrana JL, Massagué J, Rosenbaum JS 1994 Characterization and cloning of a receptor for BMP-2 and BMP-4 from NIH 3T3 cells. Mol Cell Biol 14:5961-5974
53. ten Dijke P, Yamashita H, Sampath T, Reddi AH, Estevez M, Riddle DL, Ichijo H, Heldin CH, Miyazono K 1994 Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J Biol Chem 269: 16985-16988
54. Oh SP, Seki T, Goss KA, Imamura T, Yi Y, Donahoe PK, Li L, Miyazono K, ten Dijke P, Kim S, Li E 2000 Activin receptor-like kinase 1 modulates transforming growth factor-β 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci USA 97:2626-2631
55. Goumans MJ, Valdimarsdottir G, Itoh S, Lebrin F, Larsson J, Mummery C, Karlsson S, ten Dijke P 2003 Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFβ/ALK5 signaling. Mol Cell 12:817-828
56. Nishitoh H, Ichijo H, Kimura M, Matsumoto T, Makishima F, Yamaguchi A, Yamashita H, Enomoto S, Miyazono K 1996 Identification of type I and type II serine/threonine kinase receptors for growth/differentiation factor-5. J Biol Chem 271:21345-21352
57. Hoodless PA, Haerry T, Abdollah S, Stapleton M, O'Connor MB, Attisano L, Wrana JL 1996 MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85:489-500
58. Attisano L, Carcamo J, Ventura F, Weis FM, Massague J, Wrana JL 1993 Identification of human activin and TGF β type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75:671-680
59. Lopez-Casillas F, Wrana JL, Massague J 1993 Betaglycan presents ligand to the TGF β signaling receptor. Cell 73:1435-1444
60. Bianco C, Adkins HB, Wechselberger C, Seno M, Normanno N, De Luca A, Sun Y, Khan N, Kenney N, Ebert A, Williams KP, Sanicola M, Salomon DS 2002 Cripto-1 activates nodal-and ALK4-dependent and -independent signaling pathways in mammary epithelial cells. Mol Cell Biol 22:2586-2597
61. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie AE, Davis GH, Ritvos O 2000 Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 25:279-283
62. Otsuka F, Yamamoto S, Erickson GF, Shimasaki S 2001 Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J Biol Chem 276:11387-11392
63. Findlay JK, Drummond AE, Dyson M, Baillie AJ, Robertson DM, Ethier JF 2001 Production and actions of inhibin and activin during folliculogenesis in the rat. Mol Cell Endocrinol 180:139-144
64. Piek E, Westermark U, Kastemar M, Heldin CH, van Zoelen EJ, Nister M, Ten Dijke P 1999 Expression of transforming-growth-factor (TGF)-β receptors and Smad proteins in glioblastoma cell lines with distinct responses to TGF-β1. Int J Cancer 80:756-763
65. 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 Lett 434:83-87
66. Wilkes MC, Murphy SJ, Garamszegi N, Leof EB 2003 Cell-type-specific activation of PAK2 by transforming growth factor β independent of Smad2 and Smad3. Mol Cell Biol 23:8878-8889
67. Hsueh AJ, Adashi EY, Jones PB, Welsh Jr TH 1984 Hormonal regulation of the differentiation of cultured ovarian granulosa cells. Endocr Rev 5:76-127