Restricted accessOtherFirst published online 2009-03
Recombinant Epidermal Growth Factor Maintains Follicular Ultrastructure and Promotes the Transition to Primary Follicles in Caprine Ovarian Tissue Cultured In Vitro
We investigated the effects of epidermal growth factor on the survival and growth of caprine preantral follicles. Ovarian fragments were cultured for 1 and 7 days in enriched minimal essential medium with epidermal growth factor (0, 1, 10, 50, 100, or 200 ng/mL). Non-cultured and cultured tissues were processed for histological and ultrastructural studies. Results showed that after 7 days, the epidermal growth factor (1 and 10 ng/mL) maintained the percentage of normal follicles similar to control. An increase in the percentage of primary follicles was observed with 1, 10, and 50 ng/mL of epidermal growth factor compared to enriched minimal essential medium. Ultrastructural studies confirmed follicular integrity after 7 days in epidermal growth factor (1 and 10 ng/mL). In conclusion, the low concentrations of epidermal growth factor maintain caprine follicular viability and promote the transition from primordial to primary follicles.
Bristol-Gould S., Woodruff TKFolliculogenesis in the domestic cat (Felis catus). Theriogenology. 2006;66:5-13.
2.
Fortune JEThe early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim Reprod Sci . 2003;78:135-163.
3.
Eppig JJOocyte control of ovarian follicular development and function in mammals . Reproduction. 2001;122:829-838.
4.
Toyoda T., Nakamura K., Yamada K., et al. SNP analyses of growth factor genes EGF, TGF-β1, and HGF reveal haplotypic association of EGF with autism. Biochem Bioph Res Commun. 2007;360:715-720.
5.
Silva JRV , van den Hurk R., Figueiredo JRExpression of mRNA and protein localization of epidermal growth factor and its receptor in goat ovaries. Zygote. 2006 ;14:107-117.
6.
Saha S., Shimizu M., Geshi M., Izaike Y.In vitro culture of bovine preantral follicles. Anim Reprod Sci. 2000;63:27-39.
7.
Wang Y., Li J., Wang CY, Kwok AHY, Leung FCEpidermal growth factor (EGF) receptor ligands in the chicken ovary: I. Evidence for heparin-binding EGF-like growth factor (HB-EGF) as a potential oocyte-derived signal to control granulose cell proliferation and HB-EGF and kit ligand expression . Endocrinology. 2007 ;148:3426-3440.
8.
Feng P., Knecht M., Catt K.Hormonal control of epidermal growth factor receptors by gonadotropins during granulosa cell differentiation. Endocrinology. 1987;120:1121-1126.
9.
Lonergan P., Carolan C., Van Langendonckt A., Donnay I., Khatir H., Mermillod P.Role of epidermal growth factor in bovine oocyte maturation and preimplantation embryo development in vitro. Biol Reprod. 1996;54:1420-1429.
10.
Qu J., Godin PA, Nisolle M., Donnez J.Distribution of epidermal growth factor receptor expression of primordial follicles in human ovarian tissue before and after cryopreservation. Hum Reprod. 2000;15:302-310.
11.
Garnett K., Wang J., Roy SKSpatiotemporal expression of epidermal growth factor receptor messenger RNA and protein in the hamster ovary: follicle stage-specific differential modulation by follicle-stimulating hormone, luteinizing hormone, estradiol, and progesterone . Biol Reprod. 2002;67:1593-1604.
12.
Singh B., Rutledge JM, Armstrong DTEpidermal growth factor and its receptor gene expression and peptide localisation in porcine ovarian follicles. Mol Reprod Dev . 1995;40: 391-399.
13.
Hill JL, Hammar K., Smith PJ, Gross DJStage-dependent effects of epidermal growth factor on Ca2+ efflux in mouse oocytes. Mol Reprod Dev. 1999;53:244-253.
14.
Fru KN, Cherian-Shaw M., Puttabyatappa M., Vande Voort CA, Chaffin CLRegulation of granulose cell proliferation and EGF-like ligands during the periovulatory interval in monkeys. Hum Reprod. 2007;22:1247-1252.
15.
Tekpetey FR , Singh B., Barbe G., Armstrong DTLocalisation of epidermal growth factor (EGF) receptor in the rat corpus luteum, and EGF and transforming growth factor-alpha stimulation of luteal cell steroidogenesis in vitro. Mol Cell Endocrinol. 1995;110:95-102.
16.
Singh B., Kennedy TG, Tekpetey FR, Armstrong DTGene expression and peptide localisation for epidermal growth factor receptor and its ligands in porcine luteal cells. Mol Cell Endocrinol . 1995;113:137-143.
17.
Morbeck DE, Flowers WL, Britt JHResponse of porcine granulosa cells isolated from primary and secondary follicles to FSH, 8-bromo-cAMP and EGF in vitro. J Reprod Fertil. 1993;99:577-584.
18.
Gospodarowicz D., Bialecki H.Fibroblast and epidermal growth factors are mitogenic agents for cultured granulosa cells of rodent, porcine and human origin. Endocrinology. 1979;104:757-764.
19.
Mao J., Smith MF, Rucker EB, et al. Effect of epidermal growth factor and insulin-like growth factor I on porcine preantral follicular growth, antrum formation, and stimulation of granulosal cell proliferation and suppression of apoptosis in vitro. J Anim Sci. 2004;82:1967-1975.
20.
Gutierrez CG , Ralph JH, Telfer EE, Wilmut I., Webb R.Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Biol Reprod. 2000;62:1322-1328.
21.
Romano M., Kraus ER, Boland CR, Coffey RJComparison between transforming growth factor alpha and epidermal growth factor in the protection of rat gastric mucosa against drug-induced injury. Ital J Gastroenterol. 1994;26:223-228.
22.
Roy SK, Kole AROvarian transforming growth factor-beta (TGF-beta) receptors: in vitro effects of follicle stimulating hormone, epidermal growth factor and TGF beta on receptor expression in human preantral follicles. Mol Hum Reprod. 1998;4:207-214.
23.
Zhou H., Zhang Y.Regulation of in vitro growth of preantral follicles by growth factors in goats. Domest Anim Endocrinol. 2005;28:235-242.
24.
Andrade ER, Marcondes Seneda M., Alfieri AA, et al. Interactions of indole acetic acid with EGF and FSH in the culture of ovine preantral follicles. Theriogenology. 2005;64:1104-1113.
25.
Silva JRV , van den Hurk R., de Matos MH, et al. Influences of FSH and EGF on primordial follicles during in vitro culture of caprine ovarian cortical tissue. Theriogenology . 2004;61: 1691-1704.
26.
Silva JR, van den Hurk R., Costa SH, et al. Survival and growth of goat primordial follicles after in vitro culture of ovarian cortical slices in media containing coconut water. Anim Reprod Sci. 2004;81:273-286.
27.
Steel RGD , Torrie JH, Dickey D.Principles and Procedures of Statistics: A Biometrical Approach. 3rd ed. New York, NY: McGraw-Hill; 1997 .
28.
Hsu CJ, Holmes SD, Hammond JMOvarian epidermal growth factor-like activity. Concentrations in porcine follicular fluid during follicular enlargement. Biochem Biophys Res Commun.1987;147:242-247.
29.
Demeestere I., Centner J., Gervy Y., Englert Y., Delbaere A.Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents. Reproduction. 2005;130: 147-156.
Hemamalini NC, Rao BS, Tamilmani G., et al. Influence of transforming growth factor-α, insulin-like growth factor-II, epidermal growth factor or follicle stimulating hormone on in vitro development of preantral follicles in sheep. Small Rumin Res. 2003 ;50:11-22.
32.
Zhou HM, Zhang Y.Impact of growth factors on in vitro development of caprine oocytes at pre-antral stage. Reprod Domest Anim. 2005 ;40:161-165.
33.
Van den Hurk R., Abir R., Telfer EE, Bevers MMPreantral and antral follicles as possible source for fertilizable oocytes in human and bovine. Hum Reprod Update. 2000;2: 457-474.
34.
Markstrom E. , Svensson ECh , Shao R., Svanberg B., Billig H.Survival factors regulating ovarian apoptosis-dependence on follicle differentiation. Reproduction. 2002;123:23-30.
35.
Wu J., Tian Q.Role of follicle stimulating hormone and epidermal growth factor in the development of porcine preantral follicle in vitro. Zygote. 2007;15:233-240.
36.
Talmimani G. , Rao BS, Vagdevi R., et al. Nuclear maturation of ovine oocytes in cultured preantral follicles. Small Rumin Res. 2005;60:295-305.
37.
van Wezel IL , Rodgers RJMorphological characterization of bovine primordial follicles and their environment in vivo. Biol Reprod. 1996;55:1003-1011.
38.
Bolamba D., Floyd AA, McGlone JJ, Lee VHEpidermal growth factor enhances expression of connexin 43 protein in cultured porcine preantral follicles. Biol Reprod. 2002;67:154-160.
39.
Kennedy KL, Floyd AA, Clarkson AM, Lee VHEpidermal growth factor regulation of connexin 43 in cultured granulose cells from preantral follicles rabbit follicles. Mol Reprod Dev . 2003;64:61-69.
40.
Rajarajan K. , Rao BS, Vagdevi R., et al. Effect of various growth factors on the in vitro development of goat preantral follicles. Small Rumin Res. 2006;63:204-212.
41.
Conti M., Hsieh M., Park JY, Su YQRole of the epidermal growth factor network in ovarian follicles. Mol Endocrinol. 2006;20:715-723.
42.
Wandji SA, Srsen V., Nathanielsz PW, Eppig JJ, Fortune JEInitiation of growth of baboon primordial follicles in vitro. Hum Reprod. 1997;12:1993-2001.
43.
Fortune JE, Kito S., Wandji SA, Srsen V.Activation of bovine and baboon primordial follicles in vitro. Theriogenology. 1998;49:441-449.
44.
Zhao J., Taverne MAM, van der Weijden GC, Bevers MM, van den Hurk R.Effect of activin A on in vitro development of rat preantral follicles and localization of activin A and activin receptor II. Biol Reprod . 2001;65:967-977.
45.
Galloway SM , McNatty KP, Cambridge LM, et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet. 2000;25:279-283.
46.
Hayashi M., McGee EA, Min G., et al. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early follicles. Endocrinology . 1999;140:1236-1244.
47.
Lucci CM, Silva RV, Carvalho CA, Figueiredo R., Báo N.Light microscopical and ultrastrutural characterization of goat preantral follicles. Small Rumin Res. 2001;41:61-69.
48.
Cran DG, Moor RM, Hay MFFine structure of the sheep oocyte during antral follicle development . J Reprod Fertil. 1980;59:125-132.
