The fibroblast growth factor family: Involvement in the regulation of folliculogenesis

Reproduction, Fertility and Development

Volumn 24, Issue 7, 2012, Pages 905-915

  Chaves, Roberta Nogueira ^a   Tavares De Matos, Maria Helena ^b   Buratini, Joś ^c   Ricardo De Figueiredo, Joś ^a  

^a Faculty of Veterinary Medicine   (Brazil)

^b Federal University of so Francisco Valley   (Brazil)

^c SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

culture medium; development; follicles; ovary; survival.

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CHOLESTEROL; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 16; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 5; FIBROBLAST GROWTH FACTOR 8; FIBROBLAST GROWTH FACTOR 9; FIBROBLAST GROWTH FACTOR RECEPTOR; FOLLITROPIN; INTERLEUKIN 1; INTERLEUKIN 6; KERATINOCYTE GROWTH FACTOR; LUTEINIZING HORMONE RECEPTOR; PLASMA MEMBRANE CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PLATELET DERIVED GROWTH FACTOR B; PREGNENOLONE; PROGESTERONE; SCATTER FACTOR; SODIUM CHANNEL; STEROID HORMONE; STEROIDOGENIC ACUTE REGULATORY PROTEIN; TRANSFORMING GROWTH FACTOR ALPHA;

ALTERNATIVE RNA SPLICING; ANGIOGENESIS; BINDING AFFINITY; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL INTERACTION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CORPUS LUTEUM; ELECTRIC POTENTIAL; EMBRYO DEVELOPMENT; FEMALE FERTILITY; GENE EXPRESSION; GENITAL SYSTEM; GRANULOSA CELL; HUMAN; IN VITRO STUDY; MITOCHONDRION; NONHUMAN; OOCYTE; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; OVULATION; POSITIVE FEEDBACK; PROGESTERONE RELEASE; PROTEIN PHOSPHORYLATION; RECEPTOR BINDING; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEROIDOGENESIS; TESTIS DEVELOPMENT; THECA CELL;

ANIMALS; CELL SURVIVAL; FEMALE; FERTILITY; FIBROBLAST GROWTH FACTORS; HUMANS; LIGANDS; OVARIAN FOLLICLE; OVULATION; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

MAMMALIA;

EID: 84865841734     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD11318     Document Type: Review

References (109)

1. Aharoni, D., Meiri, I., Atzmon, R., Vlodavsky, I., and Amsterdam, A. (1997). Differential effect of components of the extracellular matrix on differentiation and apoptosis. Curr. Biol. 7, 43-51. doi:10.1016/S0960-9822(06) 00026-1
2. Almeida, A. P., Saraiva, M. V. A., Alves Filho, J. G., Silva, G. M., Goncalves, R. F. B., Brito, I. R., Silva, A. W. B., Lima, A. K. F., Cunha, R. M. S., Silva, J. R. V., and Figueiredo, J. R. (2011). Gene expression and immunolocalisation of fibroblast growth factor 2 in the ovary and its effect on the in vitro culture of caprine preantral ovarian follicles. Reprod. Domest. Anim., In press.
3. Amalric, F., Bouche, G., Bonnet, H., Brethenou, P., Roman, A. M., Truchet, I., and Quarto, N. (1994). Fibroblast growth factor-2 (FGF-2) in the nucleus: translocation process and targets. Biochem. Pharmacol. 47, 111-115. doi:10.1016/0006-2952(94)90443-X
4. Anderson, E., and Lee, G. Y. (1993). The participation of growth factors in simulating the quiescent, proliferative and differentiative stages of rat granulosa cells grown in a serum-free medium. Tissue Cell 25, 49-72. doi:10.1016/0040-8166(93)90064-R
5. Armstrong, D. G., and Webb, R. (1997). Ovarian follicular dominance: the role of intraovarian growth factors and novel proteins. Rev. Reprod. 2, 139-146. doi:10.1530/ROR.0.0
6. Beenken, A., and Mohammadi, M. (2009). The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 8, 235-253. doi:10.1038/N
7. Ben-Haroush, A., Abir, R., Aro, A., Jin, S., Kessler-Icekson, G., Feldberg, D., and Fisch, B. (2005). Expression of basic fibroblast growth factor and its receptors in human ovarian follicles from adults and fetuses. Fertil. Steril. 84, 1257-1268. doi:10.1016/J.FERTNSTERT.2005.05.0
8. Berisha, B., Sinowatz, F., and Schams, D. (2004). Expression and localisation of fibroblast growth factor (FGF) family members during the final growth of bovine ovarian follicles. Mol. Reprod. Dev. 67, 162-171. doi:10.1002/MRD.1
9. Berisha, B., Stef, M., Amselgruber, W., and Schams, D. (2006a). Changes in fibroblast growth factor 2 and its receptors in bovine follicles before and after GnRH application and after ovulation. Reproduction 131, 319-329. doi:10.1530/REP.1.0
10. Berisha, B., Welter, H., Shimizu, T., Miyamoto, A., Meyer, H., and Schams, D. (2006b). Expression of fibroblast growth factor 1 (FGF-1) and FGF-7 in mature follicles during the periovulatory period after GnRH in the cow. J. Reprod. Dev. 52, 307-313. doi:10.1262/JRD.1
11. Braw-Tal, R. (2002). The initiation of follicle growth: the oocyte or the somatic cells? Mol. Cell. Endocrinol. 187, 11-18. doi:10.1016/S0303- 7207(01)00699-2
12. Buratini, J., Jr, Glapinski, V. F., Giometti, I. C., Teixeira, A. B., Costa, I. B., Avellar, M. C., Barros, C. M., and Price, C. A. (2005a). Expression of fibroblastic growth factor-8 and its cognate receptors, fibroblastic growth factor receptor (FGFR)-3c and -4, in fetal bovine preantral follicles. Mol. Reprod. Dev. 70, 255-261. doi:10.1002/MRD.2
13. Buratini, J., Jr, Teixeira, A. B., Costa, I. B., Glapinski, V. F., Pinto, M. G. L., Giometti, I. C., Barros, C. M., Cao, M., Nicola, E. S., and Price, C. A. (2005b). Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor (FGFR)-3c and -4, in bovine antral follicles. Reproduction 130, 343-350. doi:10.1530/REP. 1.0
14. Buratini, J., Jr, Pinto, M. G. L., Castilho, A. C., Amorim, R. L., Giometti, I. C., Portela, V. M., Nicola, E. S., and Price, C. A. (2007). Expression and function of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in bovine follicles. Biol. Reprod. 77, 743- 750. doi:10.1095/BIOLREPROD.107.0
15. Campbell, W. J., Miller, K. A., and Anderson, T. M. (1992). Expression of fibroblast growth factor receptors by embryonical carcinoma cells and early mouse embryos. In Vitro Cell. Dev. Biol. 28, 61-66. doi:10.1007/B
16. Cao, M., Nicola, E., Portela, V. M., and Price, C. A. (2006). Regulation of serine protease inhibitor-E2 and plasminogen activator expression and secretion by follicle stimulating hormone and growth factors in nonluteinising bovine granulosa cells in vitro. Matrix Biol. 25, 342-354. doi:10.1016/J.MATBIO. 2006.05.0
17. Castilho, A. C., Giometti, I. C., Berisha, B., Schams, D., Price, C. A., Amorim, R. L., Papa, P. C., and Buratini, J., Jr (2008). Expression of fibroblast growth factor 10 and its receptor, fibroblast growth factor receptor 2B, in the bovine corpus luteum. Mol. Reprod. Dev. 75, 940-945. doi:10.1002/MRD.2
18. Chaves, R. N., Lima-Verde, I. B., Celestino, J. J. H., Duarte, A. B. G., Alves, A. M. C. V., Matos, M. H. T., Campello, C. C., Name, K. P. O., Ba'o, S. N., Buratini, J., Jr, and Figueiredo, J. R. (2010). Fibroblast growth factor-10 maintains the survival and promotes the growth of cultured goat preantral follicles. Domest. Anim. Endocrinol. 39, 249-258. doi:10.1016/J.DOMANIEND.2010. 06.0
19. Chen, C., Spencer, T. E., and Bazer, F. W. (2000). Fibroblast growth factor- 10: a stromal mediator of epithelial function in the ovine uterus. Biol. Reprod. 63, 959-966. doi:10.1095/BIOLREPROD63.3.9
20. Colvin, J. S., Green, R. P., Schmahl, J., Capel, B., and Ornitz, D. M. (2001). Male-to-female sex reversal in mice lacking fibroblast growth factor 9. Cell 104, 875-889. doi:10.1016/S0092-8674(01)00284-7
21. Cotton, L. M., O'Bryan,M. K., and Hinton, B. T. (2008). Cellular signalling by fibroblast growth factors (FGFs) and their receptors (FGFRs) in male reproduction. Endocr. Rev. 29, 193-216. doi:10.1210/ER. 2007-0
22. Daphna-Iken, D., Shankar, D. B., Lawshé, A., Ornitz, D. M., Shackleford, G. M., and MacArthur, C. A. (1998). MMTV-Fgf8 transgenic mice develop mammary and salivary gland neoplasia and ovarian stromal hyperplasia. Oncogene 17, 2711-2717. doi:10.1038/SJ.ONC. 1
23. Derrar, N., Price, C. A., and Sirard, M. A. (2000). Effect of growth factors and co-culture with ovarian medulla on the activation of primordial follicles in explants of bovine ovarian cortex. Theriogenology 54, 587-598. doi:10.1016/S0093-691X(00)00374-5
24. Detillieux, K. A., Sheikh, F., Kardami, E., and Cattini, P. A. (2003). Biological activities of fibroblast growth factor-2 in the adult myocardium. Cardiovasc. Res. 57, 8-19. doi:10.1016/S0008-6363(02)00708-3
25. Eswarakumar, V. P., Lax, I., and Schlessinger, J. (2005). Cellular signalling by fibroblast growth factor receptors. Cytokine Growth Factor Rev. 16, 139-149. doi:10.1016/J.CYTOGFR.2005.01.0
26. Faustino, L. R., Rossetto, R., Lima, I. M., Silva, C. M., Saraiva, M. V., Lima, L. F., Silva, A. W., Donato, M. A., Campello, C. C., Peixoto, C. A., Figueiredo, J. R., and Rodrigues, A. P. (2011). Expression of keratinocyte growth factor in goat ovaries and its effects on preantral follicles within cultured ovarian cortex. Reprod. Sci., In press. doi:10.1177/1
27. Felmeden, D. C., Blann, A. D., and Lip, G. Y. H. (2003). Angiogenesis: basic pathophysiology and implications for disease. Eur. Heart J. 24, 586-603. doi:10.1016/S0195-668X(02)00635-8
28. Fernig, D. G., and Gallagher, J. T. (1994). Fibroblast growth factors and their receptors: an information network controlling tissue growth, morphogenesis and repair. Prog. Growth Factor Res. 5, 353-377. doi:10.1016/0955-2235(94)00007-8
29. Fields, S. D., Hansen, P. J., and Ealy, A. D. (2011). Fibroblast growth factor requirements for in vitro development of bovine embryos. Theriogenology 75, 1466-1475. doi:10.1016/J.THERIOGENOLOGY. 2010.12.0
30. Gabler, C., Plath-Gabler, A., Killian, G. J., Berisha, B., and Schams, D. (2004). Expression pattern of fibroblast growth factor (FGF) and vascular endothelial growth factor (VEGF) system members in bovine corpus luteum endothelial cells during treatment with FGF-2, VEGF or oestradiol. Reprod. Domest. Anim. 39, 321-327. doi:10.1111/J.1439-0531. 2004.00517.X
31. Garcia, R. A., Sanchez, M. A., Letelier, C., Garcia, P. P., Sanchez, B., Vilar, M. P., Gonzalez-Bulnes, A., and Flores, J. M. (2006). Changes in fibroblast growth factor-2 in ovine follicle development. Reprod. Domest. Anim. 41, 105. doi:10.1111/J.1439-0531.2006.00774-1-11.X
32. Gospodarowicz, D., Plouet, J., and Fujii, D. K. (1989). Ovarian germinal epithelial cells respond to basic fibroblast growth factor and express its gene: implications for early folliculogenesis. Endocrinology 125, 1266-1276. doi:10.1210/ENDO-125-3-1
33. Grazul-Bilska, A. T., Redmer, D. A., Killilea, S. D., Kraft, K. C., and Reynolds, L. P. (1992). Production of mitogenic factor(s) by ovine corpora lutea throughout the oestrous cycle. Endocrinology 130, 3625-3632. doi:10.1210/EN.130.6.3
34. Gupta, A., Bazer, F. W., and Jaeger, L. A. (1997). Immunolocalisation of acidic and basic fibroblast growth factors in porcine uterine and conceptus tissues. Biol. Reprod. 56, 1527-1536. doi:10.1095/BIOLRE PROD56.6.1
35. Hennig, T., Mogensen, C., Kirsch, J., Pohl, U., and Gloe, T. (2011). Shear stress induces the release of an endothelial elastase: role in integrin a(v)b(3)-mediated FGF-2 release. J. Vasc. Res. 48, 453-464. doi:10. 1159/0
36. Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514-521. doi:10.1016/J.YDBIO.2006.06.0
37. Igarashi, M., Finch, P. W., and Aaronson, S. A. (1998). Characterisation of recombinant human fibroblast growth factor (FGF)-10 reveals functional similarities with keratinocyte growth factor (FGF-7). J. Biol. Chem. 273, 13 230-13 235. doi:10.1074/JBC.273.21.1
38. Ishii, K., Imamura, T., Iguchi, K., Arase, S., Yoshio, Y., Arima, K., Hirano, K., and Sugimura, Y. (2009). Evidence that androgen-independent stromal growth factor signals promote androgen-insensitive prostate cancer cell growth in vivo. Endocr. Relat. Cancer 16, 415-428. doi:10.1677/ERC-08-0
39. Itoh, N. (2007). The FGF families in humans, mice and zebra fish: their evolutional processes and roles in development, metabolism and disease. Biol. Pharm. Bull. 30, 1819-1825. doi:10.1248/BPB.30.1
40. Itoh, N. (2010). Hormone-like (endocrine) FGFs: their evolutionary history and roles in development, metabolism and disease. Cell Tissue Res. 342, 1-11. doi:10.1007/S00441-010-1024-2
41. Itoh, N., and Ornitz, D. M. (2004). Evolution of the FGF and FGFR gene families. Trends Genet. 20, 563-569. doi:10.1016/J.TIG.2004.08.0
42. Itoh, N., and Ornitz, D. M. (2008). Functional evolutionary history of the mouse FGF gene family. Dev. Dyn. 237, 18-27. doi:10.1002/DVDY. 2
43. Itoh, N., and Ornitz, D. M. (2011). Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J. Biochem. 149, 121-130. doi:10.1093/JB/M
44. Iwamoto, M., Golden, E. B. G., Adams, S. L., Noji, S., and Pacici, M. (1993). Responsiveness to retinoic acid changes during chondrocyte maturation. Exp. Cell Res. 205, 213-224. doi:10.1006/EXCR.1993.1
45. Izumi, S., Slayden, O. D., Rubin, J. S., and Brenner, R. M. (1996). Keratinocyte growth factor and its receptor in the rhesus macaque placenta during the course of gestation. Placenta 17, 123-135. doi:10.1016/S0143-4004(96) 80005-1
46. Kezele, P., Nilsson, E. E., and Skinner, M. K. (2005). Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol. Reprod. 73, 967-973. doi:10.1095/BIOLREPROD. 105.0
47. Knight, P. G., and Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191-206. doi:10.1530/REP.1.0
48. Kobayashi, S., Berisha, B., Amselgruber, W. M., Schams, D., and Miyamoto, A. (2001). Production and localisation of angiotensin II in the bovine early corpus luteum: a possible interaction with luteal angiogenic factors and prostaglandin F2 alpha. J. Endocrinol. 170, 369-380. doi:10.1677/JOE.0.1
49. Koji, T., Chedid, M., Rubin, J. S., Slayden, O. D., Csaky, K. G., Aaronson, S. A., and Brenner, R. M. (1994). Progesterone-dependent expression of keratinocyte growth factor mRNA in stromal cells of the primate endometrium: keratinocyte growth factor as a progestomedin. J. Cell Biol. 125, 393-401. doi:10.1083/JCB.125.2.3
50. Laezza, F., Lampert, A., Kozel, M. A., Gerber, B. R., Rush, A. M., Nerbonne, J. M., Waxman, S. G., Dib-Hajj, S. D., and Ornitz, D. M. (2009). F N-terminal splice variants differentially modulate Nav1.2 and Nav1.6-encoded sodium channels. Mol. Cell. Neurosci. 42, 90-101. doi:10.1016/J.MCN.2009.05.0
51. LaPolt, P. S., Day, J. R., and Lu, J. K. (1990). Effects of oestradiol and progesterone on early embryonic development in aging rats. Biol. Reprod. 43, 843-850. doi:10.1095/BIOLREPROD43.5.8
52. Lavranos, T. C., Rodgers, H. F., Bertoncello, I., and Rodgers, R. J. (1994). Anchorage-independent culture of bovine granulosa cells: the effects of basic fibroblast growth factor and dibutyryl cAMP on cell division and differentiation. Exp. Cell Res. 211, 245-251. doi:10.1006/EXCR.1994. 1
53. Lee, J., Choo, J., Choi, Y., Lee, K., Min, D., Pi, S., Seol, Y., Lee, S., Jo, I., Chung, C., and Park, Y. (2008). Characterisation of the surfaceimmobilised synthetic heparin-binding domain derived from human fibroblast growth factor-2 and its effect on osteoblast differentiation. J. Biomed. Mater. Res. 83, 970-979.
54. Li, Z., and Johnson, A. L. (1993). Expression and regulation of cytochrome P450 17 alpha-hydroxylase messenger ribonucleic acid levels and androstenedione production in hen granulosa cells. Biol. Reprod. 49, 1293-1302. doi:10.1095/BIOLREPROD49.6.1
55. Lu, W., Luo, Y., Kan, M., and McKeehan, W. L. (1999). Fibroblast growth factor-10. A second candidate stromal to epithelial cell andromedin in prostate. J. Biol. Chem. 274, 12 827-12 834. doi:10.1074/JBC.274.18. 1
56. Lumelsky, N., Blondel, O., Laeng, P., Velasco, I., Ravin, R., and McKay, R. (2001). Differentiation of embryonic stem cells to insulin-secreting structures similar to pancreatic islets. Science 292, 1389-1394. doi:10.1126/SCIENCE.1
57. Masuda, H., Otsuka, F., Matsumoto, Y., Takano, M., Miyoshi, T., Inagaki, K., Shien, T., Taira, N., Makino, H., and Doihara, H. (2011). Functional interaction of fibroblast growth factor-8, bone morphogenetic protein and oestrogen receptor in breast cancer cell proliferation. Mol. Cell. Endocrinol. 343, 7-17. doi:10.1016/J.MCE.2011.05.0
58. Matos, M. H. T., Lima-Verde, I. B., Luque, M. C. A., Maia, J. E., Silva, J. R. V., Celestino, J. J. H., Martins, F. S., Ba'o, S. N., Lucci, C. M., and Figueiredo, J. R. (2007a). Essential role of follicle-stimulating hormone in the maintenance of caprine preantral follicle viability in vitro. Zygote 15, 173-182. doi:10.1017/S
59. Matos, M. H. T., Lima-Verde, I. B., Bruno, J. B., Lopes, C. A. P., Martins, F. S., Santos, K. D. B., Rocha, R. M. P., Silva, J. R. V., Ba'o, S. N., and Figueiredo, J. R. (2007b). Follicle-stimulating hormone and fibroblast growth factor-2 interact and promote goat primordial follicle development in vitro. Reprod. Fertil. Dev. 19, 677-684. doi:10.1071/R
60. Matos, M. H. T., Bruno, J. B., Rocha, R. M., Lima-Verde, I. B., Santos, K. D., Saraiva, M. V., Silva, J. R. V., Martins, F. S., Chaves, R. N., Ba'o, S. N., and Figueiredo, J. R. (2011). In vitro development of primordial follicles after long-term culture of goat ovarian tissue. Res. Vet. Sci. 90, 404-411. doi:10.1016/J.RVSC.2010.07.0
61. Millier, S. G., Whitelaw, P. F., and Smyth, C. D. (1994). Follicular oestrogen synthesis: the 'two-cell, two-gonadotrophin' model revisited. Mol. Cell. Endocrinol. 100, 51-54. doi:10.1016/0303-7207(94)90278-X
62. Miyake, A., Konishi, M., Martin, F. H., Hernday, N. A., Ozaki, K., Yamamoto, S., and Mikami, T. (1998). Structure and expression of a novel member, FGF-16, of the fibroblast growth factor family. Biochem. Biophys. Res. Commun. 243, 148-152. doi:10.1006/BBRC.1998.8
63. Miyoshi, T., Otsuka, F., Yamashita, M., Inagaki, K., Nakamura, E., Tsukamoto, N., Takeda, M., Suzuki, J., and Makino, H. (2010). Functional relationship between fibroblast growth factor-8 and bone morphogenetic proteins in regulating steroidogenesis by rat granulosa cells. Mol. Cell. Endocrinol. 325, 84-92. doi:10.1016/J.MCE.2010.04.0
64. Neuvians, T. P., Berisha, B., and Schams, D. (2004). Vascular endothelial growth factor (VEGF) and fibroblast growth factor (FGF) expression during induced luteolysis in the bovine corpus luteum. Mol. Reprod. Dev. 67, 389-395. doi:10.1002/MRD.2
65. Nilsson, E., and Skinner, M. K. (2001). Cellular interactions that control primordial follicle development and folliculogenesis. J. Soc. Gynecol. Investig. 8, S17-S20. doi:10.1016/S1071-5576(00)00099-X
66. Ornitz, D. M., Xu, J., Colvin, J. S., McEwen, D. G., MacArthur, C. A., Coulier, F., Gao, G., and Goldfarb,M. (1996). Receptor specificity of the fibroblast growth factor family. J. Biol. Chem. 271, 15 292-15 297. doi:10.1074/JBC.M
67. Parrott, J. A., and Skinner, M. K. (1998). Developmental and hormonal regulation of keratinocyte growth factor expression and action in the ovarian follicle. Endocrinology 139, 228-235. doi:10.1210/EN.139.1.2
68. Parrott, J. A., Kim, G., Mosher, R., and Skinner, M. K. (2000). Expression and action of keratinocyte growth factor (KGF) in normal ovarian surface epithelium and ovarian cancer. Mol. Cell. Endocrinol. 167, 77-87. doi:10.1016/S0303-7207(00)00284-7
69. Pedchenko, V. K., and Imagawa, W. (2000). Oestrogen treatment in vivo increases keratinocyte growth factor expression in the mammary gland. J. Endocrinol. 165, 39-49. doi:10.1677/JOE.0.1
70. Peluso, J. (2003). Basic fibroblast growth factor (bFGF) regulation of the plasma membrane calcium ATPase (PMCA) as part of an anti-apoptotic mechanism of action. Biochem. Pharmacol. 66, 1363-1369. doi:10.1016/S0006-2952(03)00486-6
71. Peluso, J. J., and Pappalardo, A. (1999). Progesterone maintains large rat granulosa cell viability indirectly by stimulating small granulosa cells to synthesise basic fibroblast growth factor. Biol. Reprod. 60, 290-296. doi:10.1095/BIOLREPROD60.2.2
72. Peluso, J. J., Pappalardo, A., and Fernandez, G. (2001). Basic fibroblast growth factor maintains calcium homeostasis and granulosa cell viability by stimulating calcium efflux via a PKC delta-dependent pathway. Endocrinology 142, 4203-4211. doi:10.1210/EN.142.10.4
73. Portela, V. M., Machado, M., Buratini, J., Jr, Zamberlam, G., Amorim, R. L., Goncalves, P., and Price, C. A. (2010). Expression and function of fibroblast growth factor 18 in the ovarian follicle in cattle. Biol. Reprod. 83, 339-346. doi:10.1095/BIOLREPROD.110.0
74. Price, W. A. (2004). Regulation of insulin-like growth factor (IGF)-binding protein expression by growth factors and cytokines alters IGF-mediated proliferation of postnatal lung fibroblasts. Exp. Lung Res. 30, 261-283. doi:10.1080/0
75. Ribatti, D., Conconi, M. T., and Nussdorfer, G. G. (2007). Nonclassic endogenous novel (corrected) regulators of angiogenesis. Pharmacol. Rev. 59, 185-205. doi:10.1124/PR.59.2.3
76. Riedel, F., Götte, K., Bergler, W., Rojas, W., and Hörmann, K. (2000). Expression of basic fibroblast growth factor protein and its downregulation by interferons in head and neck cancer. Head Neck 22, 183-189. doi:10.1002/(SICI)1097-0347(200003)22:2,183::AIDHED11.3.0. CO;2-R
77. Roy, S. K., and Greenwald, G. S. (1991). In vitro effects of epidermal growth factor, insulin-like growth factor-I, fibroblast growth factor and folliclestimulating hormone on hamster follicular deoxyribonucleic acid synthesis and steroidogenesis. Biol. Reprod. 44, 889-896. doi:10.1095/ BIOLREPROD44.5.8
78. Salli, U., Bartol, F. F., Wiley, A. A., Tarleton, B. J., and Braden, T. D. (1998). Keratinocyte growth factor expression by the bovine corpus luteum. Biol. Reprod. 59, 77-83. doi:10.1095/BIOLREPROD59.1.7
79. Samathanam, C. A., Adesanya, O. O., Zhou, J., Wang, J., and Bondy, C. A. (1998). Fibroblast growth factors 1 and 2 in the primate uterus. Biol. Reprod. 59, 491-496. doi:10.1095/BIOLREPROD59.3.4
80. Sa'nchez, F., Adriaenssens, T., Romero, S., and Smitz, J. (2009). Quantification of oocyte-specific transcripts in follicle-enclosed oocytes during antral development and maturation in vitro. Mol. Hum. Reprod. 15, 539-550. doi:10.1093/MOLEHR/G
81. Schteingart, H. F., Meroni, S. B., Ca'nepa, D. F., Pellizzari, E. H., and Cigorraga, S. B. (1999). Effects of basic fibroblast growth factor and nerve growth factor on lactate production, gamma-glutamyl transpeptidase and aromatase activities in cultured Sertoli cells. Eur. J. Endocrinol. 141, 539-545. doi:10.1530/EJE.0.1
82. Shikone, T., Yamoto, M., and Nakano, R. (1992). Follicle-stimulating hormone induces functional receptors for basic fibroblast growth factor in rat granulosa cells. Endocrinology 131, 1063-1068. doi:10.1210/EN. 131.3.1
83. Shimizu, T., Jiang, J. Y., Sasada, H., and Sato, E. (2002). Changes of messenger RNA expression of angiogenic factors and related receptors during follicular development in gilts. Biol. Reprod. 67, 1846-1852. doi:10.1095/BIOLREPROD.102.0
84. Song, J., and Slack, J. M. (1996). XFGF-9: a new fibroblast growth factor from Xenopus embryos. Dev. Dyn. 206, 427-436. doi:10.1002/(SICI) 1097-0177(199608)206:4,427::AID-AJA8.3.0.CO;2-K
85. Song, Y., McFarland, D. C., and Velleman, S. G. (2012). Fibroblast growth factor 2 and protein kinase C alpha are involved in syndecan-4 cytoplasmic domain modulation of turkey myogenic satellite cell proliferation. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 161, 44-52.
86. Speirs, V., Jenkins, S., and White, M. C. (1993). Growth factor regulation of 17 beta-hydroxysteroid dehydrogenase activity in a human ovarian cell line: modulation by 17 beta-oestradiol. Anticancer Res. 13, 1399-1403.
87. Spicer, L. J., and Stewart, R. E. (1996). Interactions among basic fibroblast growth factor, epidermal growth factor, insulin and insulin-like growth factor-I (IGF-I) on cell numbers and steroidogenesis of bovine thecal cells: role of IGF-I receptors. Biol. Reprod. 54, 255-263. doi:10.1095/ BIOLREPROD54.1.2
88. Stevenson, K. R., and Wathes, D. C. (1996). Insulin-like growth factors and their binding proteins in the ovine oviduct during the oestrous cycle. J. Reprod. Fertil. 108, 31-40. doi:10.1530/JRF.0.1
89. Stirling, D., Waterman, M. R., and Simpson, E. R. (1991). Expression of mRNA encoding basic fibroblast growth factor (bFGF) in bovine corpora lutea and cultured luteal cells. J. Reprod. Fertil. 91, 1-8. doi:10.1530/JRF.0.0
90. Sugiura, K., Su, Y. Q., Diaz, F. J., Pangas, S. A., Sharma, S., Wigglesworth, K., O'Brien, M. J., Matzuk, M. M., Shimasaki, S., and Eppig, J. J. (2007). Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134, 2593-2603. doi:10.1242/DEV. 0
91. Taylor, M. J., and Clark, C. L. (1992). Basic fibroblast growth factor inhibits basal and stimulated relaxin secretion by cultured porcine luteal cells: analysis by reverse haemolytic plaque assay. Endocrinology 130, 1951-1956. doi:10.1210/EN.130.4.1
92. Tilly, J. L., Billig, H., Kowalski, K. I., and Hsueh, A. J. (1992). Epidermal growth factor and basic fibroblast growth factor suppress the spontaneous onset of apoptosis in cultured rat ovarian granulosa cells and follicles by a tyrosine kinase-dependent mechanism. Mol. Endocrinol. 6, 1942-1950. doi:10.1210/ME.6.11.1
93. Tsafriri, A., and Adashi, E. Y. (1994). 'Local Nonsteroidal Regulators of Ovarian Function'. (Eds E. Knobil and J. Neill) pp. 817-860. (Raven Press, Ltd.: New York.)
94. Tsai, S. J., Wu, M. H., Chen, H. M., Chuang, P. C., and Wing, L. Y. (2002). Fibroblast growth factor-9 is an endometrial stromal growth factor. Endocrinology 143, 2715-2721. doi:10.1210/EN.143.7.2
95. Turner, N., and Grose, R. (2010). Fibroblast growth factor signalling: from development to cancer. Nat. Rev. Cancer 10, 116-129. doi:10.1038/N
96. Valve, E., Penttilä, T. L., Paranko, J., and Härkönen, P. (1997). FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem. Biophys. Res. Commun. 232, 173-177. doi:10.1006/BBRC.1997.6
97. Van den Hurk, R., and Zhao, J. (2005). Formation of mammalian oocytes and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717-1751. doi:10.1016/J.THERIOGENOLOGY. 2004.08.0
98. van Wezel, I. L., Umapathysivam, K., Tilley, W. D., and Rodgers, R. J. (1995). Immunohistochemical localisation of basic fibroblast growth factor in bovine ovarian follicles. Mol. Cell. Endocrinol. 115, 133-140. doi:10.1016/0303-7207(95)03678-4
99. Vernon, R. K., and Spicer, L. J. (1994). Effects of basic fibroblast growth factor and heparin on follicle-stimulating hormone-induced steroidogenesis by bovine granulosa cells. J. Anim. Sci. 72, 2696-2702.
100. Vesterlund, L., Töhönen, V., Hovatta, O., and Kere, J. (2011). Colocalisation of neural cell adhesion molecule and fibroblast growth factor receptor 2 in early embryo development. Int. J. Dev. Biol. 55, 313-319. doi:10.1387/IJDB.103240LV
101. Wandji, S. A., Eppig, J. J., and Fortune, J. E. (1996). FSH and growth factors affect the growth and endocrine function in vitro of granulosa cells of bovine preantral follicles. Theriogenology 45, 817-832. doi:10.1016/0093- 691X(96)00011-8
102. Ware, L. B., and Matthay, M. A. (2002). Keratinocyte and hepatocyte growth factors in the lung: roles in lung development, inflammation and repair. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, 924-940.
103. Watson, J. B., Getzler, S. B., and Mosher, D. F. (1994). Platelet factor-4 modulates the mitogenic activity of basic fibroblast growth factor. J. Clin. Invest. 94, 261-268. doi:10.1172/J
104. Wing, L.-Y. C., Chuang, P.-C., Wu, M.-H., Chen, H.-M., and Tsai, S.-J. (2003). Expression and mitogenic effect of fibroblast growth factor-9 in human endometriotic implant is regulated by aberrant production of oestrogen. J. Clin. Endocrinol. Metab. 88, 5547-5554. doi:10.1210/JC. 2003-0
105. Woad, K. J., Hunter, M. G., Mann, G. E., Laird, M., Hammond, A. J., and Robinson, R. S. (2011). Fibroblast growth factor (FGF) 2 is a key determinant of vascular sprouting during bovine luteal angiogenesis. Reproduction, In press.
106. Wright, T. J., and Mansour, S. L. (2003). FGF-3 and FGF-10 are required for mouse otic placode induction. Development 130, 3379-3390. doi:10.1242/DEV.0
107. Xu, R. H., Peck, R. M., Li, D. S., Feng, X., Ludwig, T., and Thomson, J. A. (2005). Basic FGF and suppression of BMP signalling sustain undifferentiated proliferation of human ES cells. Nat. Methods 2, 185-190. doi:10.1038/N
108. Zhang, X., Ibrahimi,O. A., Olsen, S. K., Umemori, H., Mohammadi, M., and Ornitz, D. M. (2006). Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J. Biol. Chem. 281, 15 694-15 700. doi:10.1074/JBC.M
109. Zhou, H., and Zhang, Y. (2005). Regulation of in vitro growth of preantral follicles by growth factors in goats. Domest. Anim. Endocrinol. 28, 235-242. doi:10.1016/J.DOMANIEND.2004.09.0