Growth differentiation factor 9 (GDF9) suppresses follistatin and Follistatin-Like 3 production in human Granulosa-Lutein cells

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Shi, Feng Tao ^a,c   Cheung, Anthony P ^a   Huang, He Feng ^b   Leung, Peter C K ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN A; BONE MORPHOGENETIC PROTEIN RECEPTOR 2; FOLLISTATIN; FOLLISTATIN LIKE 3 PROTEIN; FOLLISTATIN RELATED PROTEIN; GROWTH DIFFERENTIATION FACTOR 9; INHIBIN B; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; PRIMER DNA; XANTHOPHYLL;

ARTICLE; CELL CULTURE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; EXTRACELLULAR SPACE; FEMALE; FERTILIZATION IN VITRO; GENETIC TRANSFECTION; GRANULOSA CELL; HORMONE INHIBITION; HORMONE SYNTHESIS; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; INTRACELLULAR SPACE; LUTEAL CELL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; ANALYSIS OF VARIANCE; BIOSYNTHESIS; DRUG ANTAGONISM; GENE SILENCING; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; POLYMERASE CHAIN REACTION;

ANALYSIS OF VARIANCE; BASE SEQUENCE; DNA PRIMERS; FEMALE; FOLLISTATIN; FOLLISTATIN-RELATED PROTEINS; GENE KNOCKDOWN TECHNIQUES; GRANULOSA CELLS; GROWTH DIFFERENTIATION FACTOR 9; HUMANS; LUTEIN; POLYMERASE CHAIN REACTION;

EID: 79960970116     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022866     Document Type: Article

References (54)

1. Welt C, Sidis Y, Keutmann H, Schneyer A, (2002) Activins, inhibins, and follistatins: from endocrinology to signaling. A paradigm for the new millennium. Exp Biol Med 227: 724-752.
2. DePaolo LV, (1997) Inhibins, activins, and follistatins: the saga continues. Proc Soc Exp Biol Med 214: 328-339.
3. Phillips DJ, (2000) Regulation of activin's access to the cell: why is mother nature such a control freak? Bioessays 22: 689-696.
4. Ueno N, Ling N, Ying SY, Esch F, Shimasaki S, et al. (1987) Isolation and partial characterization of follistatin: a single-chain Mr 35,000 monomeric protein that inhibits the release of follicle-stimulating hormone. Proc Natl Acad Sci U S A 84: 8282-8286.
5. Hayette S, Gadoux M, Martel S, Bertrand S, Tigaud I, et al. (1998) FLRG (follistatin-related gene), a new target of chromosomal rearrangement in malignant blood disorders. Oncogene 16: 2949-2954.
6. Magill C, Reist NE, Fallon JR, Nitkin RM, Wallace BG, et al. (1987) Agrin. Prog Brain Res 71: 391-396.
7. Tsuchida K, Arai KY, Kuramoto Y, Yamakawa N, Hasegawa Y, et al. (2000) Identification and characterization of a novel follistatin-like protein as a binding protein for the TGF-beta family. J Biol Chem 275: 40788-40796.
8. Tortoriello DV, Sidis Y, Holtzman DA, Holmes WE, Schneyer AL, (2001) Human follistatin-related protein: a structural homologue of follistatin with nuclear localization. Endocrinology 142: 3426-3434.
9. McPherron AC, Lee SJ, (1993) GDF-3 and GDF-9: two new members of the transforming growth factor-beta superfamily containing a novel pattern of cysteines. J Biol Chem 268: 3444-3449.
10. Aaltonen J, Laitinen MP, Vuojolainen K, Jaatinen R, Horelli-Kuitunen N, et al. (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.
11. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, et al. (1996) Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383: 531-535.
12. Hayashi M, McGee EA, Min G, Klein C, Rose UM, et al. (1999) Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 140: 1236-1244.
13. Jaatinen R, Laitinen MP, Vuojolainen K, Aaltonen J, Louhio H, et al. (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.
14. McGrath SA, Esquela AF, Lee SJ, (1995) Oocyte-specific expression of growth/differentiation factor-9. Mol Endocrinol 9: 131-136.
15. 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.
16. Shi FT, Cheung AP, Leung PC, (2009) Growth differentiation factor 9 enhances activin A-induced inhibin B production in human granulosa cells. Endocrinology 150: 3540-3546.
17. Shi FT, Cheung AP, Huang HF, Leung PC, (2009) Effects of endogenous growth differentiation factor 9 on activin A-induced inhibin B production in human granulosa-lutein cells. J Clin Endocrinol Metab 94: 5108-5116.
18. Shintani Y, Dyson M, Drummond AE, Findlay JK, (1997) Regulation of follistatin production by rat granulosa cells in vitro. Endocrinology 138: 2544-2551.
19. Liu ZH, Shintani Y, Sakamoto Y, Harada K, Zhang CY, et al. (1996) Effects of LHRH, FSH and activin A on follistatin secretion from cultured rat anterior pituitary cells. Endocr J 43: 321-327.
20. Bartholin L, Maguer-Satta V, Hayette S, Martel S, Gadoux M, et al. (2002) Transcription activation of FLRG and follistatin by activin A, through Smad proteins, participates in a negative feedback loop to modulate activin A function. Oncogene 21: 2227-2235.
21. 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.
22. Gilchrist RB, Ritter LJ, Myllymaa S, Kaivo-Oja N, Dragovic RA, et al. (2006) Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation. J Cell Sci 119: 3811-3821.
23. Gilchrist RB RL, Myllymaa S, Kaivo-Oja N, Amato F, Ritvos O, et al. (2004) Mouse oocyte-secreted factors and GDF-9 stimulate granulosa cell proliferation via BMPR-II and activate smad2/3 pathway. Biol Reprod Special Issue pp. 568.
24. Shimonaka M, Inouye S, Shimasaki S, Ling N, (1991) Follistatin binds to both activin and inhibin through the common subunit. Endocrinology 128: 3313-3315.
25. Cataldo NA, Rabinovici J, Fujimoto VY, Jaffe RB, (1994) Follistatin antagonizes the effects of activin-A on steroidogenesis in human luteinizing granulosa cells. J Clin Endocrinol Metab 79: 272-277.
26. Tano M, Minegishi T, Nakamura K, Nakamura M, Karino S, et al. (1995) Regulation of follistatin messenger ribonucleic acid in cultured rat granulosa cells. Mol Cell Endocrinol 109: 167-174.
27. Stamler R, Keutmann HT, Sidis Y, Kattamuri C, Schneyer A, et al. (2008) The structure of FSTL3.activin A complex. Differential binding of N-terminal domains influences follistatin-type antagonist specificity. J Biol Chem 283: 32831-32838.
28. Kogawa K, Nakamura T, Sugino K, Takio K, Titani K, et al. (1991) Activin-binding protein is present in pituitary. Endocrinology 128: 1434-1440.
29. Shimasaki S, Koga M, Esch F, Cooksey K, Mercado M, et al. (1988) Primary structure of the human follistatin precursor and its genomic organization. Proc Natl Acad Sci U S A 85: 4218-4222.
30. Michel U, Albiston A, Findlay JK, (1990) Rat follistatin: gonadal and extragonadal expression and evidence for alternative splicing. Biochem Biophys Res Commun 173: 401-407.
31. Inouye S, Guo Y, DePaolo L, Shimonaka M, Ling N, et al. (1991) Recombinant expression of human follistatin with 315 and 288 amino acids: chemical and biological comparison with native porcine follistatin. Endocrinology 129: 815-822.
32. Sugino K, Kurosawa N, Nakamura T, Takio K, Shimasaki S, et al. (1993) 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.
33. Sumitomo S, Inouye S, Liu XJ, Ling N, Shimasaki S, (1995) The heparin binding site of follistatin is involved in its interaction with activin. Biochem Biophys Res Commun 208: 1-9.
34. Hashimoto O, Nakamura T, Shoji H, Shimasaki S, Hayashi Y, et al. (1997) 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 acceleration by follistatin associated with cell-surface heparan sulfate. J Biol Chem 272: 13835-13842.
35. Schneyer AL, Hall HA, Lambert-Messerlian G, Wang QF, Sluss P, et al. (1996) Follistatin-activin complexes in human serum and follicular fluid differ immunologically and biochemically. Endocrinology 137: 240-247.
36. Schneyer AL, Rzucidlo DA, Sluss PM, Crowley WF Jr, (1994) Characterization of unique binding kinetics of follistatin and activin or inhibin in serum. Endocrinology 135: 667-674.
37. Sidis Y, Tortoriello DV, Holmes WE, Pan Y, Keutmann HT, et al. (2002) Follistatin-related protein and follistatin differentially neutralize endogenous vs. exogenous activin. Endocrinology 143: 1613-1624.
38. Saito S, Sidis Y, Mukherjee A, Xia Y, Schneyer A, (2005) Differential biosynthesis and intracellular transport of follistatin isoforms and follistatin-like-3. Endocrinology 146: 5052-5062.
39. Onichtchouk D, Chen YG, Dosch R, Gawantka V, Delius H, et al. (1999) Silencing of TGF-beta signalling by the pseudoreceptor BAMBI. Nature 401: 480-485.
40. McConnell DS, Wang Q, Sluss PM, Bolf N, Khoury RH, et al. (1998) A two-site chemiluminescent assay for activin-free follistatin reveals that most follistatin circulating in men and normal cycling women is in an activin-bound state. J Clin Endocrinol Metab 83: 851-858.
41. Thadhani R, Powe CE, Tjoa ML, Khankin E, Ye J, et al. (2010) First-trimester follistatin-like-3 levels in pregnancies complicated by subsequent gestational diabetes mellitus. Diabetes Care 33: 664-669.
42. Guo Q, Kumar TR, Woodruff T, Hadsell LA, DeMayo FJ, et al. (1998) Overexpression of mouse follistatin causes reproductive defects in transgenic mice. Mol Endocrinol 12: 96-106.
43. Eldar-Geva T, Spitz IM, Groome NP, Margalioth EJ, Homburg R, (2001) Follistatin and activin A serum concentrations in obese and non-obese patients with polycystic ovary syndrome. Hum Reprod 16: 2552-2556.
44. Urbanek M, Wu X, Vickery KR, Kao LC, Christenson LK, et al. (2000) Allelic variants of the follistatin gene in polycystic ovary syndrome. J Clin Endocrinol Metab 85: 4455-4461.
45. Teixeira Filho FL, Baracat EC, Lee TH, Suh CS, Matsui M, et al. (2002) Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin Endocrinol Metab 87: 1337-1344.
46. Jardin F, Ruminy P, Parmentier F, Troussard X, Vaida I, et al. (2011) TET2 and TP53 mutations are frequently observed in blastic plasmacytoid dendritic cell neoplasm. Br J Haematol 153: 413-416.
47. Shi FT, Cheung AP, Klausen C, Huang HF, Leung PC, (2010) Growth differentiation factor 9 reverses activin A suppression of steroidogenic acute regulatory protein expression and progesterone production in human granulosa-lutein cells. J Clin Endocrinol Metab 95: E172-180.
48. Myers M, Gay E, McNeilly AS, Fraser HM, Duncan WC, (2007) In vitro evidence suggests activin-A may promote tissue remodeling associated with human luteolysis. Endocrinology 148: 3730-3739.
49. Myers M, van den Driesche S, McNeilly AS, Duncan WC, (2008) Activin A reduces luteinisation of human luteinised granulosa cells and has opposing effects to human chorionic gonadotropin in vitro. J Endocrinol 199: 201-212.
50. Hutchinson LA, Findlay JK, de Vos FL, Robertson DM, (1987) Effects of bovine inhibin, transforming growth factor-beta and bovine Activin-A on granulosa cell differentiation. Biochem Biophys Res Commun 146: 1405-1412.
51. Shukovski L, Findlay JK, (1990) Activin-A inhibits oxytocin and progesterone production by preovulatory bovine granulosa cells in vitro. Endocrinology 126: 2222-2224.
52. Miro F, Smyth CD, Hillier SG, (1991) Development-related effects of recombinant activin on steroid synthesis in rat granulosa cells. Endocrinology 129: 3388-3394.
53. Demura R, Suzuki T, Tajima S, Mitsuhashi S, Odagiri E, et al. (1993) Human plasma free activin and inhibin levels during the menstrual cycle. J Clin Endocrinol Metab 76: 1080-1082.
54. Welt CK, (2004) Regulation and function of inhibins in the normal menstrual cycle. Semin Reprod Med 22: 187-193.