Sequential Gonadotropin Treatment of Immature Mice Leads to Amplification of Transforming Growth Factor β Action, Via Upregulation of Receptor-Type 1, Smad 2 and 4, and Downregulation of Smad 6

Biology of Reproduction

Volumn 70, Issue 3, 2004, Pages 640-648

  Guéripel, Xavier ^a   Benahmed, Mohamed ^a   Gougeon, Alain ^a,b  

^a INSERM   (France)

^b CENTRE HOSPITALIER LYON SUD   (France)

Author keywords

Follicle; Follicle stimulating hormone; Growth factors; Luteinizing hormone; Ovary

Indexed keywords

GONADOTROPIN; LUTEINIZING HORMONE; MESSENGER RNA; RECOMBINANT FOLLITROPIN; SMAD2 PROTEIN; SMAD4 PROTEIN; SMAD6 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; GENE ACTIVATION; GENE AMPLIFICATION; GENE EXPRESSION; GRANULOSA CELL; IMMUNOHISTOCHEMISTRY; LUTEAL CELL; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE MATURATION; OVULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THECA CELL; WESTERN BLOTTING;

ANIMALIA;

EID: 1242298817     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.103.021162     Document Type: Article

References (53)

1. Dunker N, Krieglstein K. Targeted mutations of transforming growth factor-beta genes reveal important roles in mouse development and adult homeostasis. Eur J Biochem 2000; 267:6982-6988.
2. Chang H, Lau AL, Matzuk MM. Studying TGF-beta superfamily signaling by knockouts and knockins. Mol Cell Endocrinol 2001; 180:39-46.
3. Ueno S, Kuroda T, Maclaughlin DT, Ragin RC, Manganaro TF, Donahoe PK. Mullerian inhibiting substance in the adult rat ovary during various stages of the estrous cycle. Endocrinology 1989; 125:1060-1066.
4. Elvin JA, Yan C, Matzuk MM. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol Cell Endocrinol 2000; 159:1-5.
5. Findlay JK, Drummond AE, Dyson M, Baillie AJ, Robertson DM, Ethier JE. Production and actions of inhibin and activin during folliculogenesis in the rat. Mol Cell Endocrinol 2001; 180:139-144.
6. Juneja SC, Chegini N, Williams RS, Ksander GA. Ovarian intrabursal administration of transforming growth factor beta 1 inhibits follicle rupture in gonadotropin-primed mice. Biol Reprod 1996; 55:1444-1451.
7. Wrana JL, Attisano L, Wieser R, Ventura F, Massagué J. Mechanism of activation of the TGF-β receptor. Nature 1994; 370:341-347.
8. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997; 390:465-471.
9. Attisano L, Lee-Hoeflich ST. The Smads. Genome Biol 2001; 2:1-8.
10. Ghiglieri C, Khatchadourian C, Tabone E, Hendrick JC, Benahmed M, Ménézo Y. Immunolocalization of TGF-β1 and TGF-β2 in the mouse ovary during gonadotropin-induced follicular maturation. Hum Reprod 1995; 10:2115-2119.
11. Hernandez ER, Hurwitz A, Payne DW, Dharmarajan AM, Purchio AF, Adashi EY. Transforming growth factor-β1 inhibits ovarian androgen production: gene expression, cellular localization, mechanism(s), and site(s) of action. Endocrinology 1990; 127:2804-2811.
12. Mulheron GW, Danielpour D, Schomberg DW. Rat thecal/interstitial cell express transforming growth factor-β type 1 and 2, but only type 2 is regulated by gonadotropin in vitro. Endocrinology 1991; 129:368-374.
13. Teerds KJ, Dorrington JH. Immunohistochemical localization of transforming growth factor-β1 and β2 during follicular development in the adult rat ovary. Mol Cell Endocrinol 1992; 84:R7-R13.
14. Levacher C, Gautier C, Saez JM, Habert R. Immunohistochemical localization of transforming growth factor beta 1 and beta 2 in the fetal and neonatal rat ovary. Differentiation 1996; 61:45-51.
15. Roy SK, Ogren C, Roy C, Lu B. Cell-type localization of transforming growth factor-β2 and transforming growth factor-β1 in the hamster ovary: differential regulation by follicle-stimulating hormone and luteinizing hormone. Biol Reprod 1992; 46:595-606.
16. Roy SK, Hughes J. Ontogeny of granulosa cells in the ovary: lineage-specific expression of transforming growth factor-β2 and transforming growth factor-β1. Biol Reprod 1994; 51:821-830.
17. Massagué J, Blain SW, Lo RS. TGF-β signaling in growth control, cancer and heritable disorders. Cell 2000; 103:295-309.
18. Schmid P, Cox D, Van Der Putten H, McMaster GK, Bilbe G. Expression of TGF-βs and TGF-β type II receptor mRNAs in mouse folliculogenesis: stored maternal TGF-β2 message in oocytes. Biochem Biophys Res Commun 1994; 201:649-656.
19. Li M, Li J, Hoodless PA, Tzukazaki T, Wrana JL, Attisano L, Tsang BK. Mothers against decapentaplegic-related protein 2 expression in avian granulosa cells is up-regulated by transforming growth factor beta during ovarian follicular development. Endocrinology 1997; 138:3659-3665.
20. Osterlund C, Fried G. TGFbeta receptor types I and II and the substrate proteins Smad 2 and 3 are present in human oocytes. Mol Hum Reprod 2000; 6:498-503.
21. Drummond AE, Le MT, Ethier JF, Dyson M, Findlay JK. Expression and localization of activin receptors, Smads, and betaglycan to the postnatal rat ovary. Endocrinology 2002; 143:1423-1433.
22. Xu J, Oakley J, McGee EA. Stage-specific expression of Smad2 and Smad3 during folliculogenesis. Biol Reprod 2002; 66:1571-1578.
23. Kano K, Notani A, Nam SY, Fujisawa M, Kurohmaru M, Hayashi Y. Cloning and studies of the mouse cDNA encoding Smad3. J Vet Med Sci 1999; 61:213-219.
24. Liu X, Andoh K, Abe Y, Kobayashi J, Yamada K, Mizunuma H, Ibuki Y. A comparative study on transforming growth factor-beta and activin A for preantral follicles from adult, immature, and diethylstilbestrolprimed immature mice. Endocrinology 1999; 140:2480-2485.
25. Dorrington JH, Chuma AV, Bendell JJ. Transforming growth factor β and follicle-stimulating hormone promote rat granulosa cell proliferation. Endocrinology 1988; 123:353-359.
26. Roy SK. Transforming growth factor-β potentiation of follicle-stimulating hormone-induced deoxyribonucleic acid synthesis in hamster preantral follicles is mediated by a latent induction of epidermal growth factor. Biol Reprod 1993; 48:558-563.
27. Saragueta PE, Lanuza GM, Baranao JL. Autocrine role of transforming growth factor beta I on rat granulosa cell proliferation. Biol Reprod 2002; 66:1862-1868.
28. Magoffin DA, Gancedo B, Erickson GE. Transforming growth factor-β promotes differentiation of ovarian theca-interstitial cells but inhibits androgen production. Endocrinology 1989; 125:1951-1958.
29. Mulheron GW, Schomberg DW. Rat granulosa cells express transforming growth factor-β type 2 messenger ribonucleic acid which is regulatable by follicle-stimulating hormone in vitro. Endocrinology 1990; 126:1777-1779.
30. Magoffin DA, Hubert-Leslie D, Zachow R. Estradiol-17β, insulin-like growth factor-I, and luteinizing hormone inhibit secretion of transforming growth factor β by rat theca-interstitial cells. Biol Reprod 1995; 53:627-635.
31. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987; 162:156-159.
32. Greenwald GS, Roy SK. Follicular development and its control. In: Knobil E, Neill JD (eds.), Physiology of Reproduction, vol. 1, 2nd ed. New York: Raven Press; 1994:629-724.
33. May JV, Turzcynski CJ, Ramos L, Mau YH. Differential involvement of protein kinase C in the regulation of transforming growth factor-beta (TGF-beta) secretion by porcine theca and granulosa cells in vitro. Endocrinology 1995; 136:1319-1322.
34. Kingsley-Kallesen ML, Kelly D, Rizzino A. Transcriptional regulation of the transforming growth factor-beta2 promoter by cAMP-responsive element-binding protein (CREB) and activating transcription factor-1 (ATF-1) is modulated by protein kinases and the coactivators p300 and CREB-binding protein. J Biol Chem 1999; 274:34020-34028.
35. Wilder PJ, Desler MM, Nowling TK, Rizzino A. Isolation and characterization of the murine transforming growth factor-beta2 promoter. Gene 2001; 270:201-209.
36. Boussouar E, Grataroli R, Ji J, Benahmed M. Tumor necrosis factor-a stimulates lactate dehydrogenase A expression in porcine cultured Sertoli cells: mechanisms of action. Endocrinology 1999; 140:3054-3062.
37. Benbrahim-Tallaa L, Tabone E, Tosser-Klopp G, Hatey E, Benahmed M. Glutathione S-transferase alpha expressed in porcine Sertoli cells is under the control of follicle-stimulating hormone and testosterone. Biol Reprod 2002; 66:1734-1742.
38. Kim SJ, Angel P, Lafyatis R, Hattori K, Kim KY, Sporn MB, Karin M, Roberts AB. Autoinduction of transforming growth factor beta 1 is mediated by the AP-1 complex. Mol Cell Biol 1990; 10:1492-1497.
39. Moreland RB, Gupta S, Goldstein I, Traish A. Cyclic AMP modulates TGF-beta 1-induced fibrillar collagen synthesis in cultured human corpus cavernosum smooth muscle cells. Int J Impot Res 1998; 10:159-163.
40. Ji C, Casinghino S, Chang D, Chen Y, Javed A, Ito Y, Hiebert SW, Lian JB, McCarthy TL, Centrella M. CBFa (AML/PEBP2)-related elements in the TGF-β type I receptor promoter and expression with osteoblast differentiation. J Cell Biol 1998; 69:353-363.
41. Bloom BB, Humphries DE, Kuang PP, Fine A, Goldstein RH. Structure and expression of the promoter for the R4/ALK5 human type I transforming growth factor-beta receptor: regulation by TGF-beta. Biochim Biophys Acta 1996; 1312:243-248.
42. Kleeff J, Korc M. Up-regulation of transforming growth factor (TGF)-β receptors by TGF-β1 in COLO-357 cells. J Biol Chem 1998; 273:7495-7500.
43. Ariazi EA, Satomi Y, Ellis MJ, Haag JD, Shi W, Sattler CA, Gould MN. Activation of the transforming growth factor beta signaling pathway and induction of cytostasis and apoptosis in mammary carcinomas treated with the anticancer agent perillyl alcohol. Cancer Res 1999; 59:1917-1928.
44. Imamura T, Takase M, Nishihara A, Oeda E, Hanai J, Kawabata M, Miyazono K. Smad 6 inhibits signalling by the TGF-beta superfamily. Nature 1997; 389:622-626.
45. Afrakhte M, Moren A, Jossan S, Itoh S, Sampath K, Westermark B, Heldin CH, Heldin NE, ten Dijke P. Induction of inhibitory Smad6 and Smad7 mRNA by TGF-beta family members. Biochem Biophys Res Commun 1998; 249:505-511.
46. Topper JN, Cai J, Qiu Y, Anderson KR, Xu YY, Deeds JD, Feeley R, Gimeno CJ, Woolf EA, Tayber O, Mays GG, Sampson BA, Schoen FJ, Gimbrone MA Jr, Falb D. Vascular MADs: two novel MAD-related genes selectively inducible by flow in human vascular endothelium. Proc Natl Acad Sci U S A 1997; 94:9314-9319.
47. Stopa M, Benes V, Ansorge W, Gressner AM, Dooley S. Genomic locus and promoter region of rat Smad7, an important antagonist of TGFbeta signaling. Mamm Genome 2000; 11:169-176.
48. Ishida W, Hamamoto T, Kusanagi K, Yagi K, Kawabata M, Takehara K, Sampath TK, Kato M, Miyazono K. Smad6 is a Smad1/5-induced Smad inhibitor. Characterization of bone morphogenetic protein-responsive element in the mouse Smad6 promoter. J Biol Chem 2000; 275:6075-6079.
49. Johnsen SA, Subramaniam M, Janknecht R, Spelsberg TC. TGFbeta inducible early gene enhances TGFbeta/Smad-dependent transcriptional responses. Oncogene 2002; 21:5783-5790.
50. Johnsen SA, Subramaniam M, Katagiri T, Janknecht R, Spelsberg TC. Transcriptional regulation of Smad2 is required for enhancement of TGFbeta/Smad signaling by TGFbeta inducible early gene. J Cell Biochem 2002; 87:233-241.
51. Shull MM, Doetschman T. Transforming growth factor-β1 in reproduction and development. Mol Reprod Dev 1994; 39:239-246.
52. Feng P, Catt KJ, Knecht M. Transforming growth factor-beta stimulated meiotic maturation of the rat oocyte. Endocrinology 1988; 122:181-186.
53. Tsafriri A, Vale W, Hsueh AJW. Effects of transforming growth factors and inhibin-related proteins on rat preovulatory graafian follicles in vitro. Endocrinology 1989; 125:1857-1862.