Transforming growth factor β-activated kinase 1 is a key mediator of ovine follicle-stimulating hormone β-subunit expression

Endocrinology

Volumn 146, Issue 11, 2005, Pages 4814-4824

  Safwat, Nedal ^a   Ninomiya Tsuji, Jun ^a   Gore, A Jesse ^a   Miller, William L ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

7 OXOZEANOL; ACTIVIN; ALCOHOL DERIVATIVE; FOLLITROPIN BETA SUBUNIT; LUCIFERASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN INHIBITOR; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL LINE; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; GENE CONSTRUCT; HORMONE ACTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN INDUCTION; REACTION TIME;

ACTIVINS; ANIMALS; CELL LINE; ENZYME ACTIVATION; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; HUMANS; INHIBIN-BETA SUBUNITS; KINETICS; LACTONES; LUCIFERASES; MAP KINASE KINASE KINASES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; RESORCINOLS; SHEEP; TRANSFECTION;

EID: 26844553319     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2005-0457     Document Type: Article

References (64)

1. Kumar TR, Wang Y, Lu N, Matzuk MM 1997 Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 15:201-204
2. Besecke LM, Guendner MJ, Schneyer AL, Bauer-Dantoin AC, Jameson JL, Weiss J 1996 Gonadotropin-releasing hormone regulates follicle-stimulating hormone-β gene expression through an activin/follistatin autocrine or paracrine loop. Endocrinology 137:3667-3673
3. Dalkin AC, Haisenleder DJ, Ortolano GA, Ellis TR, Marshall JC 1989 The frequency of gonadotropin-releasing-hormone stimulation differentially regulates gonadotropin subunit messenger ribonucleic acid expression. Endocrinology 125:917-924
4. Haisenleder DJ, Ortolano GA, Dalkin AC, Ellis TR, Paul SJ, Marshall JC 1990 Differential regulation of gonadotropin subunit gene expression by gonadotropin-releasing hormone pulse amplitude in female rats. Endocrinology 127:2869-2875
5. Huang HJ, Wu JC, Su P, Zhirnov O, Miller WL 2001 A novel role for bone morphogenetic proteins in the synthesis of follicle-stimulating hormone. Endocrinology 142:2275-2283
6. Krummen LA, Woodruff TK, DeGuzman G, Cox ET, Baly DL, Mann E, Garg S, Wong WL, Cossum P, Mather JP 1993 Identification and characterization of binding proteins for inhibin and activin in human serum and follicular fluids. Endocrinology 132:431-443
7. Ling N, Ying SY, Ueno N, Esch F, Denoroy L, Guillemin R 1985 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
8. Otsuka F, Shimasaki S 2002 A novel function of bone morphogenetic protein-15 in the pituitary: selective synthesis and secretion of FSH by gonadotropes. Endocrinology 143:4938-4941
9. Rivier J, Spiess J, McClintock R, Vaughan J, Vale W 1985 Purification and partial characterization of inhibin from porcine follicular fluid. Biochem Biophys Res Commun 133:120-127
10. Vale W, Rivier J, Vaughan J, McClintock R, Corrigan A, Woo W, Karr D, Spiess J 1986 Purification and characterization of an FSH releasing protein from porcine ovarian follicular fluid. Nature 321:776-779
11. Carroll RS, Corrigan AZ, Gharib SD, Vale W, Chin WW 1989 Inhibin, activin, and follistatin: regulation of follicle-stimulating hormone messenger ribonucleic acid levels. Mol Endocrinol 3:1969-1976
12. Norwitz ER, Xu S, Jeong KH, Bedecarrats GY, Winebrenner LD, Chin WW, Kaiser UB 2002 Activin A augments GnRH-mediated transcriptional activation of the mouse GnRH receptor gene. Endocrinology 143:985-997
13. Norwitz ER, Xu S, Xu J, Spiryda LB, Park JS, Jeong KH, McGee EA, Kaiser UB 2002 Direct binding of AP-1 (Fos/Jun) proteins to a SMAD binding element facilitates both gonadotropin-releasing hormone (GnRH)- and activin-mediated transcriptional activation of the mouse GnRH receptor gene. J Biol Chem 277:37469-37478
14. Attisano L, Wrana JL, Cheifetz S, Massague J 1992 Novel activin receptors: distinct genes and alternative mRNA splicing generate a repertoire of serine/threonine kinase receptors. Cell 68:97-108
15. Mathews LS, Vale WW 1991 Expression cloning of an activin receptor, a predicted transmembrane serine kinase. Cell 65:973-982
16. ten Dijke P, Ichijo H, Franzen P, Schulz P, Saras J, Toyoshima H, Heldin CH, Miyazono K 1993 Activin receptor-like kinases: a novel subclass of cell-surface receptors with predicted serine/threonine kinase activity. Oncogene 8:2879-2887
17. Attisano L, Carcamo J, Ventura F, Weis FM, Massague J, Wrana JL 1993 Identification of human activin and TGFβ type I receptors that form heteromeric kinase complexes with type II receptors. Cell 75:671-680
18. Attisano L, Wrana JL, Montalvo E, Massague J 1996 Activation of signalling by the activin receptor complex. Mol Cell Biol 16:1066-1073
19. Carcamo J, Weis FM, Ventura F, Wieser R, Wrana JL, Attisano L, Massague J 1994 Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor β and activin. Mol Cell Biol 14:3810-3821
20. Mathews LS, Vale WW, Kintner CR 1992 Cloning of a second type of activin receptor and functional characterization in Xenopus embryos. Science 255:1702-1705
21. Chen X, Rubock MJ, Whitman M 1996 A transcriptional partner for MAD proteins in TGF-β signalling. Nature 383:691-696
22. Hua X, Liu X, Ansari DO, Lodish HF 1998 Synergistic cooperation of TFE3 and smad proteins in TGF-β-induced transcription of the plasminogen activator inhibitor-1 gene. Genes Dev 12:3084-3095
23. Labbe E, Silvestri C, Hoodless PA, Wrana JL, Attisano L 1998 Smad2 and Smad3 positively and negatively regulate TGFβ-dependent transcription through the forkhead DNA-binding protein FAST2. Mol Cell 2:109-120
24. Massague J 1998 TGF-β signal transduction. Annu Rev Biochem 67:753-791
25. Pouponnot C, Jayaraman L, Massague J 1998 Physical and functional interaction of SMADs and p300/CBP. J Biol Chem 273:22865-22868
26. Shi Y, Wang YF, Jayaraman L, Yang H, Massague J, Pavletich NP 1998 Crystal structure of a Smad MH1 domain bound to DNA: insights on DNA binding in TGF-β signaling. Cell 94:585-594
27. Wotton D, Lo RS, Lee S, Massague J 1999 A Smad transcriptional corepressor. Cell 97:29-39
28. Zhou S, Zawel L, Lengauer C, Kinzler KW, Vogelstein B 1998 Characterization of human FAST-1, a TGFβ and activin signal transducer. Mol Cell 2:121-127
29. Bailey JS, Rave-Harel N, McGillivray SM, Coss D, Mellon PL 2004 Activin regulation of the follicle-stimulating hormone β-subunit gene involves Smads and the TALE homeodomain proteins Pbx1 and Prep1. Mol Endocrinol 18:1158-1170
30. Suszko MI, Lo DJ, Suh H, Camper SA, Woodruff TK 2003 Regulation of the rat follicle-stimulating hormone β-subunit promoter by activin. Mol Endocrinol 17:318-332
31. Gregory SJ, Lacza CT, Detz AA, Xu S, Petrillo LA, Kaiser UB 2005 Synergy between activin A and gonadotropin-releasing hormone in transcriptional activation of the rat follicle-stimulating hormone-β gene. Mol Endocrinol 19:237-254
32. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K 1995 Identification of a member of the MAPKKK family as a potential mediator of TGF-β signal transduction. Science 270:2008-2011
33. Shibuya H, Yamaguchi K, Shirakabe K, Tonegawa A, Gotoh Y, Ueno N, Irie K, Nishida E, Matsumoto K 1996 TAB1: an activator of the TAK1 MAPKKK in TGF-β signal transduction. Science 272:1179-1182
34. Cheung PC, Nebreda AR, Cohen P 2004 TAB3, a new binding partner of the protein kinase TAK1. Biochem J 378:27-34
35. Jin G, Klika A, Callahan M, Faga B, Danzig J, Jiang Z, Li X, Stark GR, Harrington J, Sherf B 2004 Identification of a human NF-κB-activating protein, TAB3. Proc Natl Acad Sci USA 101:2028-2033
36. Kanayama A, Seth RB, Sun L, Ea CK, Hong M, Shaito A, Chiu YH, Deng L, Chen ZJ 2004 TAB2 and TAB3 activate the NF-κB pathway through binding to polyubiquitin chains. Mol Cell 15:535-548
37. Ishitani T, Takaesu G, Ninomiya-Tsuji J, Shibuya H, Gaynor RB, Matsumoto K 2003 Role of the TAB2-related protein TAB3 in IL-1 and TNF signaling. EMBO J 22:6277-6288
38. Munoz-Sanjuan I, Bell E, Altmann CR, Vonica A, Brivanlou AH 2002 Gene profiling during neural induction in Xenopus laevis: regulation of BMP signaling by post-transcriptional mechanisms and TAB3, a novel TAK1-binding protein. Development 129:5529-5540
39. Qiao B, Padilla SR, Benya PD 2005 TGF-β activated kinase 1 (TAK1) mimics and mediates TGF-β-induced stimulation of type II collagen synthesis in chondrocytes independent of Col2a1 transcription and Smad3 signaling. J Biol Chem
40. Hanafusa H, Ninomiya-Tsuji J, Masuyama N, Nishita M, Fujisawa J, Shibuya H, Matsumoto K, Nishida E 1999 Involvement of the p38 mitogenactivated protein kinase pathway in transforming growth factor-β-induced gene expression. J Biol Chem 274:27161-27167
41. Sano Y, Harada J, Tashiro S, Gotoh-Mandeville R, Maekawa T, Ishii S 1999 ATF-2 is a common nuclear target of Smad and TAK1 pathways in transforming growth factor-β signaling. J Biol Chem 274:8949-8957
42. Schnabl B, Bradham CA, Bennett BL, Manning AM, Stefanovic B, Brenner DA 2001 TAK1/JNK and p38 have opposite effects on rat hepatic stellate cells. Hepatology 34:953-963
43. Akiyama S, Yonezawa T, Kudo TA, Li MG, Wang H, Ito M, Yoshioka K, Ninomiya-Tsuji J, Matsumoto K, Kanamaru R, Tamura S, Kobayashi T 2004 Activation mechanism of c-Jun amino-terminal kinase in the course of neural differentiation of P19 embryonic carcinoma cells. J Biol Chem 279:36616 -36620
44. Goswami M, Uzgare AR, Sater AK 2001 Regulation of MAP kinase by the BMP-4/TAK1 pathway in Xenopus ectoderm. Dev Biol 236:259-270
45. Dowdy SC, Mariani A, Janknecht R 2003 HER2/Neu- and TAK1-mediated up-regulation of the transforming growth factor β inhibitor Smad7 via the ETS protein ER81. J Biol Chem 278:44377-44384
46. Sakurai H, Nishi A, Sato N, Mizukami J, Miyoshi H, Sugita T 2002 TAK1-TAB1 fusion protein: a novel constitutively active mitogen-activated protein kinase kinase kinase that stimulates AP-1 and NF-κB signaling pathways. Biochem Biophys Res Commun 297:1277-1281
47. Chen Y, Lebrun JJ, Vale W 1996 Regulation of transforming growth factor β-and activin-induced transcription by mammalian Mad proteins. Proc Natl Acad Sci USA 93:12992-12997
48. Datto MB, Frederick JP, Pan L, Borton AJ, Zhuang Y, Wang XF 1999 Targeted disruption of Smad3 reveals an essential role in transforming growth factor β-mediated signal transduction. Mol Cell Biol 19:2495-2504
49. Yingling JM, Datto MB, Wong C, Frederick JP, Liberati NT, Wang XF 1997 Tumor suppressor Smad4 is a transforming growth factor β-inducible DNA binding protein. Mol Cell Biol 17:7019-7028
50. Wagner M, Kleeff J, Lopez ME, Bockman I, Massaque J, Korc M 1998 Transfection of the type I TGF-β receptor restores TGF-β responsiveness in pancreatic cancer. Int J Cancer 78:255-260
51. Pernasetti F, Vasilyev VV, Rosenberg SB, Bailey JS, Huang HJ, Miller WL, Mellon PL 2001 Cell-specific transcriptional regulation of follicle-stimulating hormone-β by activin and gonadotropin-releasing hormone in the LβT2 pituitary gonadotrope cell model. Endocrinology 142:2284-2295
52. Huang HJ, Sebastian J, Strahl BD, Wu JC, Miller WL 2001 The promoter for the ovine follicle-stimulating hormone-β gene (FSHβ) confers FSHβ-like expression on luciferase in transgenic mice: regulatory studies in vivo and in vitro. Endocrinology 142:2260-2266
53. Goto D, Yagi K, Inoue H, Iwamoto I, Kawabata M, Miyazono K, Kato M 1998 A single missense mutant of Smad3 inhibits activation of both Smad2 and Smad3, and has a dominant negative effect on TGF-β signals. FEBS Lett 430:201-204
54. Kakonen SM, Selander KS, Chirgwin JM, Yin JJ, Burns S, Rankin WA, Grubbs BG, Dallas M, Cui Y, Guise TA 2002 Transforming growth factor-β stimulates parathyroid hormone-related protein and osteolytic metastases via Smad and mitogen-activated protein kinase signaling pathways. J Biol Chem 277:24571-24578
55. Ninomiya-Tsuji J, Kajino T, Ono K, Ohtomo T, Matsumoto M, Shiina M, Mihara M, Tsuchiya M, Matsumoto K 2003 A resorcylic acid lactone, 5Z-7-oxozeaenol, prevents inflammation by inhibiting the catalytic activity of TAK1 MAPK kinase kinase. J Biol Chem 278:18485-18490
56. Ono K, Ohtomo T, Ninomiya-Tsuji J, Tsuchiya M 2003 A dominant negative TAK1 inhibits cellular fibrotic responses induced by TGF-β. Biochem Biophys Res Commun 307:332-337
57. Wu JC, Su P, Safwat NW, Sebastian J, Miller WL 2004 Rapid, efficient isolation of murine gonadotropes and their use in revealing control of follicle-stimulating hormone by paracrine pituitary factors. Endocrinology 145:5832-5839
58. Weiss J, Guendner MJ, Halvorson LM, Jameson JL 1995 Transcriptional activation of the follicle-stimulating hormone β-subunit gene by activin. Endocrinology 136:1885-1891
59. Wang EY, Ma EY, Woodruff TK 2003 Activin signal transduction in the fetal rat adrenal gland and in human H295R cells. J Endocrinol 178:137-148
60. Liu X, Sun Y, Constantinescu SN, Karam E, Weinberg RA, Lodish HF 1997 Transforming growth factor β-induced phosphorylation of Smad3 is required for growth inhibition and transcriptional induction in epithelial cells. Proc Natl Acad Sci USA 94:10669-10674
61. Liu C, Gaca MD, Swenson ES, Vellucci VF, Reiss M, Wells RG 2003 Smads 2 and 3 are differentially activated by transforming growth factor-β (TGF-β) in quiescent and activated hepatic stellate cells. Constitutive nuclear localization of Smads in activated cells is TGF-β-independent. J Biol Chem 278:11721-11728
62. Inagaki Y, Mamura M, Kanamaru Y, Greenwel P, Nemoto T, Takehara K, Ten Dijke P, Nakao A 2001 Constitutive phosphorylation and nuclear localization of Smad3 are correlated with increased collagen gene transcription in activated hepatic stellate cells. J Cell Physiol 187:117-123
63. Zhang L, Deng M, Parthasarathy R, Wang L, Mongan M, Molkentin JD, Zheng Y, Xia Y 2005 MEKK1 transduces activin signals in keratinocytes to induce actin stress fiber formation and migration. Mol Cell Biol 25:60-65
64. Ogihara T, Watada H, Kanno R, Ikeda F, Nomiyama T, Tanaka Y, Nakao A, German MS, Kojima I, Kawamori R 2003 p38 MAPK is involved in activin A- and hepatocyte growth factor-mediated expression of pro-endocrine gene neurogenin 3 in AR42J-B13 cells. J Biol Chem 278:21693-21700