Mapping the follicle-stimulating hormone-induced signaling networks

Frontiers in Endocrinology

Volumn 2, Issue OCT, 2011, Pages

  Gloaguen, Pauline ^a,b,c,d   Crépieux, Pascale ^a,b,c,d   Heitzler, Domitille ^a,b,c,d   Poupon, Anne ^a,b,c,d   Reiter, Eric ^a,b,c,d  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE TOURS   (France)

^d Institut Francais du Cheval et de l'Equitation   (France)

Author keywords

Follicle stimulating hormone; Receptor; Signaling network; Systems biology; Topological map

Indexed keywords

EID: 84874053202     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2011.00045     Document Type: Review

References (106)

1. Agrawal, G., and Dighe, R. R. (2009). Critical involvement of the hinge region of the follicle-stimulating hormonereceptorintheactivation of the receptor. J. Biol. Chem. 284, 2636-2647.
2. Aittomaki, K., Lucena, J. L., Pakarinen, P., Sistonen, P., Tapanainen, J., Gromoll, J., Kaskikari, R., Sankila, E. M., Lehvaslaiho, H., Engel, A. R., Nieschlag, E., Huhtaniemi, I., and De La Chapelle, A. (1995). Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 82, 959-968.
3. Alam, H., Maizels, E. T., Park, Y., Ghaey, S., Feiger, Z. J., Chandel, N. S., and Hunzicker-Dunn, M. (2004). Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT/Ras homolog enriched in brain (Rheb)/ mammalian target of rapamycin (mTOR) pathway is necessary for induction of select protein markers of follicular differentiation. J. Biol. Chem. 279, 19431-19440.
4. Alam, H., Weck, J., Maizels, E., Park, Y., Lee, E. J., Ashcroft, M., and Hunzicker-Dunn, M. (2009). Role of the phosphatidylinositol-3- kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)- 1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 150, 915-928.
5. Andric, N., and Ascoli, M. (2006). A delayed gonadotropin-dependent and growth factor-mediated activation of the extracellular signal- regulated kinase 1/2 cascade negatively regulates aromatase expression in granulosa cells. Mol. Endocrinol. 20, 3308-3320.
6. Arey, B. J., Stevis, P. E., Deecher, D. C., Shen, E. S., Frail, D. E., Negro-Vilar, A., and Lopez, F. J. (1997). Induction of promiscuous G protein coupling of the follicle-stimulating hormone (FSH) receptor: a novel mechanism for transducing pleiotropic actions of FSH isoforms. Mol. Endocrinol. 11, 517-526.
7. Arey, B. J.,Yanofsky, S. D., Claudia Perez, M., Holmes, C. P., Wrobel, J., Gopalsamy,A., Stevis, P. E., Lopez, F. J., and Winneker, R. C. (2008). Differing pharmacological activities of thiazolidinone analogs at the FSH receptor. Biochem. Biophys. Res. Commun. 368, 723-728.
8. Cameron, M. R., Foster, J. S., Bukovsky, A., and Wimalasena, J. (1996). Activation of mitogen-activated protein kinases by gonadotropins and cyclic adenosine 5'-monophosphates in porcine granulosa cells. Biol. Reprod. 55, 111-119.
9. Chen, Y.-J., Hsiao, P.-W., Lee, M.- T., Mason, J. I., Ke, F.-C., and Hwang, J.-J. (2007). Interplay of PI3K and cAMP/PKA signaling, and rapamycin-hypersensitivity in TGFbeta1 enhancement of FSH-stimulated steroidogenesis in rat ovarian granulosa cells. J. Endocrinol. 192, 405-419.
10. Choi, J.-H., Chen, C.-L., Poon, S. L., Wang, H.-S., and Leung, P. C. K. (2009). Gonadotropin-stimulated epidermal growth factor receptor expression in human ovarian surface epithelial cells: involvement of cyclic AMP-dependent exchange protein activated by cAMP pathway. Endocr. Relat. Cancer 16, 179-188.
11. Choi, J. H., Wong, A. S., Huang, H. F., and Leung, P. C. (2007). Gonadotropins and ovarian cancer. Endocr. Rev. 28, 440-461.
12. Cohen, B. D., Nechamen, C. A., and Dias, J. A. (2004). Human follitropin receptor (FSHR) interacts with the adapter protein 14-3-3tau. Mol. Cell. Endocrinol. 220, 1-7.
13. Cottom, J., Salvador, L. M., Maizels, E. T., Reierstad, S., Park, Y., Carr, D. W., Davare, M. A., Hell, J. W., Palmer, S. S., Dent, P., Kawakatsu, H., Ogata, M., and Hunzicker-Dunn, M. (2003). Follicle-stimulating hormone activates extracellular signal- regulated kinase but not extracellular signal-regulated kinase kinase through a 100-kDa phosphotyrosine phosphatase. J. Biol. Chem. 278, 7167-7179.
14. Crépieux, P., Marion, S., Martinat, N., Fafeur, V., Vern, Y. L., Kerboeuf, D., Guillou,F.,and Reiter, E. (2001). The ERK-dependent signalling is stage- specifically modulated by FSH, during primary Sertoli cell maturation. Oncogene 20, 4696-4709.
15. Cunningham, M. A., Zhu, Q., Unterman, T. G., and Hammond, J. M. (2003). Follicle-stimulating hormone promotes nuclear exclusion of the forkhead transcription factor FoxO1a via phosphatidylinositol 3-kinase in porcine granulosa cells. Endocrinology 144, 5585-5594.
16. Dattatreyamurty, B., Figgs, L. W., and Reichert, L. E. (1987). Physical and functional association of follitropin receptors with cholera toxin-sensitive guanine nucleotide- binding protein. J. Biol. Chem. 262, 11737-11745.
17. Dias, J. A., Bonnet, B., Weaver, B. A., Watts, J., Kluetzman, K., Thomas, R. M., Poli, S., Mutel, V., and Campo, B. (2011). A negative allosteric modulator demonstrates biased antagonism of the follicle stimulating hormone receptor. Mol. Cell. Endocrinol. 333, 143-150.
18. Dias, J. A., Mahale, S. D., Nechamen, C. A., Davydenko, O., Thomas, R. M., and Ulloa-Aguirre, A. (2010). Emerging roles for the FSH receptor adapter protein APPL1 and overlap of a putative 14-3-3tau interaction domain with a canonical G- protein interaction site. Mol. Cell. Endocrinol. 329, 17-25.
19. Dias, J. A., Nechamen, C. A., and Atari, R. (2005). Identifying protein interactors in gonadotropin action. Endocrine 26, 241-247.
20. Dierich, A., Sairam, M. R., Monaco, L., Fimia, G. M., Gansmuller, A., Lemeur, M., and Sassone- Corsi, P. (1998). Impairing follicle- stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc. Natl. Acad. Sci. U.S.A. 95, 13612-13617.
21. Dupont, J., Musnier, A., Decourtye, J., Boulo, T., Lécureuil, C., Guillou, H., Valet, S., Fouchécourt, S., Pitetti, J.- L., Nef, S., Reiter, E., and Crépieux, P. (2010). FSH-stimulated PTEN activity accounts for the lack of FSH mitogenic effect in prepubertal rat Sertoli cells. Mol. Cell. Endocrinol. 315, 271-276.
22. Escamilla-Hernandez, R., Little-Ihrig, L., Orwig, K. E., Yue, J., Chandran, U., and Zeleznik, A. J. (2008a). Constitutively active protein kinase A qualitatively mimics the effects of follicle-stimulating hormone on granulosa cell differentiation. Mol. Endocrinol. 22, 1842-1852.
23. Escamilla-Hernandez, R., Little-Ihrig, L., and Zeleznik, A. J. (2008b). Inhibition of rat granulosa cell differentiation by overexpression of Galphaq. Endocrine 33, 21-31.
24. Fakunding, J. L., Tindall, D. J., Dedman, J. R., Mena, C. R., and Means, A. R. (1976). Biochemical actions of follicle-stimulating hormone in the Sertoli cell of the rat testis. Endocrinology 98, 392-402.
25. Fan, H.-Y., Liu, Z., Cahill, N., and Richards, J. S. (2008). Targeted disruption of Pten in ovarian granulosa cells enhances ovulation and extends the life span of luteal cells. Mol. Endocrinol. 22, 2128-2140.
26. Fan, H.-Y., O'Connor, A., Shitanaka, M., Shimada, M., Liu, Z., and Richards, J. S. (2010). Beta-catenin (CTNNB1) promotes preovulatory follicular development but represses LH-mediated ovulation and luteinization. Mol. Endocrinol. 24, 1529-1542.
27. Flores, J. A., Veldhuis, J. D., and Leong, D. A. (1990). Follicle-stimulating hormone evokes an increase in intra- cellular free calcium ion concentrations in single ovarian (granulosa) cells. Endocrinology 127, 3172-3179.
28. Gonzalez-Robayna, I. J., Falender, A. E., Ochsner, S., Firestone, G. L., and Richards, J. S. (2000). Follicle- Stimulating hormone (FSH) stimulates phosphorylation and activation of protein kinase B (PKB/Akt) and serum and glucocorticoid-lnduced kinase (Sgk): evidence for A kinase- independent signaling by FSH in granulosa cells. Mol. Endocrinol. 14, 1283-1300.
29. Guan, R., Wu, X., Feng, X., Zhang, M., Hebert, T. E., and Segaloff, D. L. (2010). Structural determinants underlying constitutive dimerization of unoccupied human follitropin receptors. Cell. Signal. 22, 247-256.
30. Hans, F., and Dimitrov, S. (2001). Histone H3 phosphorylation and cell division. Oncogene 20, 3021-3027.
31. Huhtaniemi, I., Ahtiainen, P., Pakarainen, T., Rulli, S. B., Zhang, F. P., and Poutanen, M. (2006). Genetically modified mouse models in studies of luteinising hormone action. Mol. Cell. Endocrinol. 252, 126-135.
32. Jayes, F. C., Day, R. N., Garmey, J. C., Urban, R. J., Zhang, G., and Veldhuis, J. D. (2000). Calcium ions positively modulate follicle-stimulating hormone- and exogenous cyclic 3',5'-adenosine monophosphate-driven transcription of the P450(scc) gene in porcine granulosa cells. Endocrinology 141, 2377-2384.
33. Kara, E., Crépieux, P., Gauthier, C., Martinat, N., Piketty, V., Guillou, F., and Reiter, E. (2006). A phosphorylation cluster of five serine and threonine residues in the C-terminus of the follicle-stimulating hormone receptor is important for desensitization but not for beta-arrestin-mediated ERK activation. Mol. Endocrinol. 20, 3014-3026.
34. Kayampilly, P. P., and Menon, K. M. J. (2007). Follicle-stimulating hormone increases tuberin phosphorylation and mammalian target of rapamycin signaling through an extracellular signal-regulated kinase-dependent pathway in rat granulosa cells. Endocrinology 148, 3950-3957.
35. Kayampilly, P. P., and Menon, K. M. J. (2009). Follicle-stimulating hormone inhibits adenosine 5'- monophosphate-activated protein kinase activation and promotes cell proliferation of primary granulosa cells in culture through an Akt- dependent pathway. Endocrinology 150, 929-935.
36. Kenakin, T. (2005). New concepts in drug discovery: collateral efficacy and permissive antagonism. Nat. Rev. Drug Discov. 4, 919-927.
37. Kishi, H., Krishnamurthy, H., Galet, C., Bhaskaran, R. S., and Ascoli, M. (2002). Identification of a short linear sequence present in the C- terminal tail of the rat follitropin receptor that modulates arrestin- 3 binding in a phosphorylation- independent fashion. J. Biol. Chem. 277, 21939-21946.
38. Kitano, H., Funahashi, A., Matsuoka, Y., and Oda, K. (2005). Using process diagrams for the graphical representation of biological networks. Nat. Biotechnol. 23, 961-966.
39. Kluetzman, K. S., Thomas, R. M., Nechamen, C. A., and Dias, J. A. (2011). Decreased degradation of internalized follicle-stimulating hormone caused by mutation of aspartic acid 6.30550 in a protein kinase-CK2 consensus sequence in the third intracellular loop of human follicle-stimulating hormone receptor. Biol. Reprod. 84, 1154-1163.
40. Krishnamurthy, H., Galet, C., and Ascoli, M. (2003a). The association of arrestin-3 with the follitropin receptor depends on receptor activation and phosphorylation. Mol. Cell. Endocrinol. 204, 127-140.
41. Krishnamurthy, H., Kishi, H., Shi, M., Galet,C.,Bhaskaran,R. S.,Hirakawa, T., and Ascoli, M. (2003b). Posten-docytotic trafficking of the follicle-stimulating hormone (FSH)-FSH receptor complex. Mol. Endocrinol. 17, 2162-2176.
42. Kumar, T. R., Wang, Y., Lu, N., and Matzuk, M. M. (1997). Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 15, 201-204.
43. Lai, T.-H., Lin, Y.-F., Wu, F.-C., and Tsai, Y.-H. (2008). Folliclestimulating hormone-induced Galphah/phospholipase C-delta1 signaling mediating a noncapacitative Ca2+ influx through T-type Ca2+ channels in rat sertoli cells. Endocrinology 149, 1031-1037.
44. Landmark, B. F., Fauske, B., Eskild, W., Skalhegg, B., Lohmann, S. M., Hansson, V., Jahnsen, T., and Beebe, S. J. (1991). Identification, characterization, and hormonal regulation of 3',5'-cyclic adenosine monophosphate-dependent protein kinases in rat Sertoli cells. Endocrinology 129, 2345-2354.
45. Layman, L. C., Lee, E. J., Peak, D. B., Namnoum, A. B., Vu, K. V., Van Lingen, B. L., Gray, M. R., Mcdonough, P. G., Reindollar, R. H., and Jameson, J. L. (1997). Delayed puberty and hypogonadism caused by mutations in the follicle-stimulating hormone beta-subunit gene. N.Engl.J.Med. 337, 607-611.
46. Lazari, M. F., Liu, X., Nakamura, K., Benovic, J. L., and Ascoli, M. (1999). Role of G protein-coupled receptor kinases on the agonist-induced phosphorylation and internalization of the follitropin receptor. Mol. Endocrinol. 13, 866-878.
47. Lécureuil, C., Tesseraud, S., Kara, E., Martinat, N., Sow, A., Fontaine, I., Gauthier, C., Reiter, E., Guillou, F., and Crépieux, P. (2005). Follicle- stimulating hormone activates p70 ribosomal protein S6 kinase by protein kinase A-mediated dephosphorylation of Thr 421/Ser 424 in primary Sertoli cells. Mol. Endocrinol. 19, 1812-1820.
48. Lefkowitz, R. J., and Shenoy, S. K. (2005). Transduction of receptor signals by beta-arrestins. Science 308, 512-517.
49. Lin, Y. F., Tseng, M. J., Hsu, H. L., Wu, Y. W., Lee, Y. H., and Tsai, Y. H. (2006). A novel follicle-stimulating hormone-induced G alpha h/phospholipase C-delta1 signaling pathway mediating rat sertoli cell Ca2+-influx. Mol. Endocrinol. 20, 2514-2527.
50. Loutradis, D., Drakakis, P., Milingos, S., Stefanidis, K., and Michalas, S. (2003). Alternative approaches in the management of poor response in controlled ovarian hyperstimulation (COH). Ann. N. Y. Acad. Sci. 997, 112-119.
51. Loutradis, D., Elsheikh, A., Kallianidis, K., Drakakis, P., Stefanidis, K., Milingos,S.,and Michalas,S. (2004). Results of controlled ovarian stimulation for ART in poor responders according to the short protocol using different gonadotrophins combinations. Arch. Gynecol. Obstet. 270, 223-226.
52. Lunenfeld, B. (2004). Historical perspectives in gonadotrophin therapy. Hum. Reprod. Update 10, 453-467.
53. Macklon, N. S., Stouffer, R. L., Giudice, L. C., and Fauser, B. C. (2006). The science behind 25 years of ovarian stimulation for in vitro fertilization. Endocr. Rev. 27, 170-207.
54. Maizels,E. T.,Cottom,J.,Jones,J. C.,and Hunzicker-Dunn, M. (1998). Follicle stimulating hormone (FSH) activates the p38 mitogen-activated protein kinase pathway, inducing small heat shock protein phosphorylation and cell rounding in immature rat ovarian granulosa cells. Endocrinology 139, 3353-3356.
55. Marion, S., Kara, E., Crepieux, P., Piketty, V., Martinat, N., Guillou, F., and Reiter, E. (2006). G protein-coupled receptor kinase 2 and beta-arrestins are recruited to FSH receptor in stimulated rat primary Sertoli cells. J. Endocrinol. 190, 341-350.
56. Marion, S., Robert, F., Crepieux, P., Martinat, N., Troispoux, C., Guillou, F., and Reiter, E. (2002). G protein-coupled receptor kinases and beta arrestins are relocalized and attenuate cyclic 3',5'-adenosine monophosphate response to folliclestimulating hormone in rat primary Sertoli cells. Biol. Reprod. 66, 70-76.
57. Matthews, C. H., Borgato, S., Beck-Peccoz, P., Adams, M., Tone, Y., Gambino, G., Casagrande, S., Tedeschini, G., Benedetti, A., and Chatter- jee, V. K. (1993). Primary amenor- rhoea and infertility due to a mutation in the beta-subunit of follicle- stimulating hormone. Nat. Genet. 5, 83-86.
58. McDonald, C. A., Millena, A. C., Reddy, S., Finlay, S., Vizcarra, J., Khan, S. A., and Davis, J. S. (2006). Follicle-stimulating hormone-induced aro-matase in immature rat Sertoli cells requires an active phosphatidylinositol 3-kinase pathway and is inhibited via the mitogen-activated protein kinase signaling pathway. Mol. Endocrinol. 20, 608-618.
59. Means, A. R., Macdougall, E., Soderling, T. R., and Corbin, J. D. (1974). Testicular adenosine 3':5'- monophosphate-dependent protein kinase. Regulation by follicle- stimulating hormone. J. Biol. Chem. 249, 1231-1238.
60. Meroni, S. B., Riera, M. F., Pellizzari, E. H., and Cigorraga, S. B. (2002). Regulation of rat Sertoli cell function by FSH: possible role of phosphatidylinositol 3-kinase/protein kinase B pathway. J. Endocrinol. 174, 195-204.
61. Meroni, S. B., Riera, M. F., Pellizzari, E. H., Galardo, M. N., and Cigorraga, S. B. (2004). FSH activates phosphatidylinositol 3- kinase/protein kinase B signaling pathway in 20-day-old Sertoli cells independently of IGF-I. J. Endocrinol. 180, 257-265.
62. Musnier, A., Heitzler, D., Boulo, T., Tesseraud, S., Durand, G., Lécureuil, C., Guillou, H., Poupon, A., Reiter, E., and Crépieux, P. (2009). Developmental regulation of p70 S6 kinase byaGprotein-coupled receptor dynamically modelized in primary cells. Cell.Mol.LifeSci.66, 3487-3503.
63. Nakamura, K., Krupnick, J. G., Benovic, J. L., and Ascoli, M. (1998). Signaling and phosphorylation-impaired mutants of the rat follitropin receptor reveal an activationand phosphorylation-independent but arrestin-dependent pathway for internalization. J. Biol. Chem. 273, 24346-24354.
64. Naz, R. K., Gupta, S. K., Gupta, J. C., Vyas, H. K., and Talwar, G. P. (2005). Recent advances in contraceptive vaccine development: a mini-review. Hum. Reprod. 20, 3271-3283.
65. Nechamen, C. A., Thomas, R. M., Cohen, B. D., Acevedo, G., Poulikakos, P. I., Testa, J. R., and Dias, J. A. (2004). Human follicle-stimulating hormone (FSH) receptor interacts with the adaptor protein APPL1 in HEK 293 cells: potential involvement of the PI3K pathway in FSH signaling. Biol. Reprod. 71, 629-636.
66. Nechamen, C. A., Thomas, R. M., and Dias, J. A. (2007). APPL1, APPL2, Akt2 and FOXO1a interact with FSHR in a potential signaling complex. Mol. Cell. Endocrinol. 260-262, 93-99.
67. Northup, J. K., Sternweis, P. C., Smigel, M. D., Schleifer, L. S., Ross, E. M., and Gilman, A. G. (1980). Purification of the regulatory component of adenylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 77, 6516-6520.
68. Ongeri, E. M., Verderame, M. F., and Hammond, J. M. (2007). The TATA binding protein associated factor 4b (TAF4b) mediates FSH stimulation of the IGFBP-3 promoter in cultured porcine ovarian granulosa cells. Mol. Cell. Endocrinol. 278, 29-35.
69. Papkoff, H., and Ekblad, M. (1970). Ovine follicle stimulating hormone: preparation and characterization of its subunits. Biochem. Biophys. Res. Commun. 40, 614-621.
70. Park, Y., Maizels, E. T., Feiger, Z. J., Alam, H., Peters, C. A., Woodruff, T. K., Unterman, T. G., Lee, E. J., Jameson, J. L., and Hunzicker-Dunn, M. (2005). Induction of cyclin D2 in rat granulosa cells requires FSH-dependent relief from FOXO1 repression coupled with positive signals from Smad. J. Biol. Chem. 280, 9135-9148.
71. Piketty, V., Kara, E., Guillou, F., Reiter, E., and Crepieux, P. (2006). Follicle-stimulating hormone (FSH) activates extracellular signalregulated kinase phosphorylation independently of beta-arrestin- and dynamin-mediated FSH receptor internalization. Reprod. Biol. Endocrinol. 4, 33-44.
72. Quintana, J., Hipkin, R. W., Sanchez- Yague, J., and Ascoli, M. (1994). Follitropin (FSH) and a phorbol ester stimulate the phosphorylation of the FSH receptor in intact cells. J. Biol. Chem. 269, 8772-8779.
73. Radu, A., Pichon, C., Camparo, P., Antoine, M., Allory, Y., Couvelard, A., Fromont, G., Hai, M. T., and Ghinea, N. (2010). Expression of follicle-stimulating hormone receptor in tumor blood vessels. N. Engl. J. Med. 363, 1621-1630.
74. Rajagopal, S., Rajagopal, K., and Lefkowitz, R. J. (2010). Teaching old receptors new tricks: biasing seven- transmembrane receptors. Nat. Rev. Drug Discov. 9, 373-386.
75. Rangel-Aldao, R., and Rosen, O. M. (1976). Dissociation and reassociation of the phosphorylated and nonphosphorylated forms of adenosine 3':5'-monophosphate- dependent protein kinase from bovine cardiac muscle. J. Biol. Chem. 251, 3375-3380.
76. Reiter, E., and Lefkowitz, R. J. (2006). GRKs and beta-arrestins: roles in receptor silencing, trafficking and signaling. Trends Endocrinol. Metab. 17, 159-165.
77. Reiter, E., Marion, S., Robert, F., Troispoux, C., Boulay, F., Guillou, F., and Crepieux, P. (2001). Kinase- inactive G-protein-coupled receptor kinases are able to attenuate follicle-stimulating hormone- induced signaling. Biochem. Biophys. Res. Commun. 282, 71-78.
78. Salvador, L. M., Park, Y., Cottom, J., Maizels, E. T., Jones, J. C., Schillace, R. V., Carr, D. W., Cheung, P., Allis, C. D., Jameson, J. L., and Hunzicker-Dunn, M. (2001). Follicle-stimulating hormone stimulates protein kinase A- mediated histone H3 phosphorylation and acetylation leading to select gene activation in ovarian granulosa cells. J. Biol. Chem. 276, 40146-40155.
79. Santos, N. C., and Kim, K. H. (2010). Activity of retinoic acid receptor-alpha is directly regulated at its protein kinase A sites in response to follicle-stimulating hormone signaling. Endocrinology 151, 2361-2372.
80. Shimada, M., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., and Richards, J. S. (2006). Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol. Endocrinol. 20, 1352-1365.
81. Shupe, J., Cheng, J., Puri, P., Kostereva, N., and Walker, W. H. (2011). Regulation of sertoli-germ cell adhesion and sperm release by FSH and nonclassical testosterone signaling. Mol. Endocrinol. 25, 238-252.
82. Simoni, M., Gromoll, J., and Nieschlag, E. (1997). The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology, and pathophysiology. Endocr. Rev. 18, 739-773.
83. Themmen, A. P. N., and Huhtaniemi, I. T. (2000). Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary- gonadal function. Endocr. Rev. 21, 551-583.
84. Thomas, R. M., Nechamen, C. A., Mazurkiewicz, J. E., Muda, M., Palmer, S., and Dias, J. A. (2007). Follice-stimulating hormone receptor forms oligomers and shows evidence of carboxyl-terminal proteolytic processing. Endocrinology 148, 1987-1995.
85. Thomas, R. M., Nechamen, C. A., Mazurkiewicz, J. E., Ulloa-Aguirre, A., and Dias, J. A. (2011). The Adapter Protein APPL1 Links FSH Receptor to inositol 1,4,5- trisphosphate production and is implicated in intracellular Ca2+ mobilization. Endocrinology 152, 1691-1701.
86. Tranchant, T., Durand, G., Gauthier, C., Crépieux, P., Ulloa-Aguirre, A., Royère, D., and Reiter, E. (2011). Preferential β-arrestin signalling at low receptor density revealed by functional characterization of the human FSH receptor A189 V mutation. Mol. Cell. Endocrinol. 331, 109-118.
87. Troispoux, C., Guillou, F., Elalouf, J. M., Firsov, D., Iacovelli, L., Blasi, A. D., Combarnous, Y., and Reiter, E. (1999). Involvement of G protein-coupled receptor kinases and arrestins in desensitization to follicle-stimulating hormone action. Mol. Endocrinol. 13, 1599-1614.
88. Ulloa-Aguirre,A., Crépieux, P., Poupon, A., Maurel, M.-C., and Reiter, E. (2011). Novel pathways in gonadotropin receptor signaling and biased agonism. Rev. Endocr. Metab. Disord. doi: 10.1007/s11154-011- 9176-2. [Epub ahead of print].
89. Vloeberghs, V., Peeraer, K., Pexsters, A., and D'Hooghe, T. (2009). Ovarian hyperstimulation syndrome and complications of ART. Best Pract. Res. Clin. Obstet. Gynaecol. 23, 691-709.
90. Wang, W., Chen, X., Li, X., Wang, L., Zhang, H., He, Y., Wang, J., Zhao, Y., Zhang, B., and Xu, Y. (2011). Interference RNA (RNAi)-based silencing of endogenous Smad4 in porcine granulosa cells resulted in decreased FSH-mediated GCs proliferation and steroidogenesis. Reproduction 141, 643-651.
91. Wang, Y., Chan, S., and Tsang, B. K. (2002). Involvement of inhibitory nuclear factor-kappaB (NFkappaB)- independent NFkappaB activation in the gonadotropic regulation of X-linked inhibitor of apoptosis expression during ovarian follicular development in vitro. Endocrinology 143, 2732-2740.
92. Wayne, C. M., Fan, H.-Y., Cheng, X., and Richards, J. S. (2007). Follicle- stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for granulosa cell differentiation. Mol. Endocrinol. 21, 1940-1957.
93. Wehbi, V., Decourtye, J., Piketty, V., Durand, G., Reiter, E., and Maurel, M.-C. (2010a). Selective modulation of follicle-stimulating hormone signaling pathways with enhancing equine chorionic gonadotropin/antibody immune complexes. Endocrinology 151, 2788-2799.
94. Wehbi, V., Tranchant, T., Durand, G., Musnier, A., Decourtye, J., Piketty, V., Butnev, V. Y., Bousfield, G. R., Crépieux, P., Maurel, M.-C., and Reiter, E. (2010b). Partially deglycosylated equine LH preferentially activates beta- arrestin-dependent signaling at the follicle-stimulating hormone receptor. Mol. Endocrinol. 24, 561-573.
95. Whalen, E. J., Rajagopal, S., and Lefkowitz, R. J. (2011). Therapeutic potential of beta-arrestin- and G protein-biased agonists. Trends. Mol. Med. 17, 126-139.
96. Xiao, K., Mcclatchy, D. B., Shukla, A. K., Zhao, Y., Chen, M., Shenoy, S. K., Yates, J. R. III, and Lefkowitz, R. J. (2007). Functional specialization of beta-arrestin interactions revealed by proteomic analysis. Proc. Natl. Acad. Sci. U.S.A. 104, 12011-12016.
97. Xiao, K., Sun, J., Kim, J., Rajagopal, S., Zhai, B., Villen, J., Haas, W., Kovacs, J. J., Shukla, A. K., Hara, M. R., Hernandez, M., Lachmann, A., Zhao, S., Lin, Y., Cheng, Y., Mizuno, K., Ma'ayan, A., Gygi, S. P., and Lefkowitz, R. J. (2010). Global phosphorylation analysis of beta-arrestin-mediated signaling downstream of a seven transmembrane receptor (7TMR). Proc. Natl. Acad. Sci. U.S.A. 107, 15299-15304.
98. Xu, P., and Derynck, R. (2010). Direct activation of TACE-mediated ectodomain shedding by p38 MAP kinase regulates EGF receptordependent cell proliferation. Mol. Cell 37, 551-566.
99. Yamashita, Y., Hishinuma, M., and Shimada, M. (2009). Activation of PKA, p38 MAPK and ERK1/2 by gonadotropins in cumulus cells is critical for induction of EGF-like factor and TACE/ADAM17 gene expression during in vitro maturation of porcine COCs. J. Ovarian Res. 2, 20.
100. Yamashita, Y., Kawashima, I., Gunji, Y., Hishinuma, M., and Shimada, M. (2010). Progesterone is essential for maintenance of Tace/Adam17 mRNA expression, but not EGF- like factor, in cumulus cells, which enhances the EGF receptor signaling pathway during in vitro maturation of porcine COCs. J. Reprod. Dev. 56, 315-323.
101. Yamashita, Y., Kawashima, I., Yanai, Y., Nishibori, M., Richards, J. S., and Shimada, M. (2007). Hormone-induced expression of tumor necrosis factor alpha- converting enzyme/A disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. Endocrinology 148, 6164-6175.
102. Yang, P., and Roy, S. K. (2006). A novel mechanism of FSH regulation of DNA synthesis in the granulosa cells of hamster preantral follicles: involvement of a protein kinase C-mediated MAP kinase 3/1 self- activation loop. Biol. Reprod. 75, 149-157.
103. Yang, W., Lu, C.-L., Yu, F.-Q., Liu, T., Hu, Z.-Y., and Liu, Y.-X. (2008). Mitogen-activated protein kinase regulates FSH-induced expression of tissue-type plasminogen activator through an activator protein 1 response element. Endocrine 34, 101-107.
104. Yu, F.-Q., Han, C.-S., Yang, W., Jin, X., Hu,Z.-Y.,and Liu,Y.-X. (2005).Activation of the p38 MAPK pathway by follicle-stimulating hormone regulates steroidogenesis in granulosa cells differentially. J. Endocrinol. 186, 85-96.
105. Zeleznik, A. J., Saxena, D., and Little-Ihrig, L. (2003). Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology 144, 3985-3994.
106. Zhang, Q., Thomas, S. M., Lui, V. W. Y., Xi,S.,Siegfried,J. M.,Fan,H.,Smithgall, T. E., Mills, G. B., and Grandis, J. R. (2006). Phosphorylation of TNFalpha converting enzyme by gastrinreleasing peptide induces amphiregulin release and EGF receptor activation. Proc. Natl. Acad. Sci. U.S.A. 103, 6901-6906.