Regulation of Follicular Growth and Development in Sheep

Iranian Journal of Applied Animal Science

مقاله 2، دوره 4، شماره 1، خرداد 2014، صفحه 21-31   

نوع مقاله: Review Article

نویسنده

H.B. Ciftci^*

Department of Animal Science, School of Agriculture, Selçuk University, 42075, Konya, Turkey

چکیده

This manuscript reviews the present knowledge related to folliculogenesis in sheep.Folliculogenesis starts with formation of primordial follicles before birth, present as a pool containing a certain number of follicles. By the attainment of puberty, a group of follicles from that pool starts to grow, a process known as primordial follicle activation or recruitment. The number of growing primordial follicles directly affects the number of available oocytes for fertilization. Many studies, especially in rodents, have been performed to understand the mechanisms that control the primordial follicle growth. Therefore, many autocrine, paracrine, intacrin factors from oocyte, granulasa and surrounding stroma have been identified. These regulating factors depend on species, age, physiological condition of the gonad and the environment. Also, interactions between these regulating factors have been observed and some discrepancies among results were found. The factors regulating primordial follicle activation probably act in concert with gonadotropins and regulate follicle growth and atresia before the antrum formation. Although many studies have been performed to understand the mechanisms controlling preantral follicle growth, no precise key points have been identified. The majority of the factors that affect primordial follicle transition have not yet been studied in sheep, while many studies have been performed to understand the controlling mechanisms of follicular growth through the antral the stages. Therefore new experimental studies are needed to understand the controlling mechanisms of preantral follicle growth.

کلیدواژه‌ها

atresia؛ Follicle؛ growth؛ Ovary؛ Sheep

مراجع

Adashi E.Y. Resnick C.E., Hernandez E.R., May J.V., Knecht M., Svoboda M.E. and Van Wyk J.J. (1988). Insulin-like growth factor-I as an amplifier of follicle-stimulating hormone action: studies on mechanism(s) and site(s) of action in cultured rat granulosa cells. Endocrinology. 122, 1583-1591.
Arici A., Oral E., Bahtiyar O., Engin O., Seli E. and Jones E.E. (1997). Leukaemia inhibitory factor expression in human follicular fluid and ovarian cells. Hum. Reprod. 12,1233-1239.
Armstrong D.T., Weiss T.J., Selstam G. and Seamark R.F. (1981). Hormonal and cellular interactions in follicular steroid biosynthesis by the sheep ovary. J. Reprod. Fertil. Suppl. 30, 143-154.
Armstrong D.G. and Webb R. (1997). Ovarian follicular dominance: the role of intraovarian growth factors and novel proteins. Rev. Reprod. 2, 139-146.
Baird D.T. (1983). Factors regulating the growth of the preovulatory follicle in the sheep and human. J. Reprod. Fertil. 69,343-352.
Baird D.T., Campbell B.K. and McNeilly A.S. (1990). Ovine follicular fluid suppresses the ovarian secretion of androgens, oestradiol and inhibin. J. Endocrinol. 127,23-32.
Besnard N., Pisselet C., Monniaux D., Locatelli A., Benne F., Gasser F., Hatey F. and Monget P. (1996). Expression of messenger ribonucleic acids of insulin-like TgrowthTfactor binding protein-2, -4 and -5 in the ovine ovary: localization and changes during TgrowthTand atresia of antral follicles. Biol. Reprod. 55,1356-1367.
Bézard J., Vigier B., Tran D., Mauléon P. and Josso N. (1988). TAntiT-müllerian ThormoneTin TsheepTfollicles. Reprod. Nutr. Dev. 28, 1105-1112.
Bicsak T.A., Tucker E.M., Cappel S., Vaughan J., Rivier J., Vale W. and Hsueh A.J. (1986). Hormonal regulation of granulosa cell inhibin biosynthesis. Endocrinology. 119, 2711-2719.
Bodensteiner K.J., Clay C.M., Moeller C.L., Sawyer H.R. (1999). Molecular cloning of the ovine growth / differentiation factor-9 gene and expression of growth / differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 60,381-386.
Boone D.L. and sang B.K. (1998). Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol. Reprod. 58, 1533-1539.
Campbell B.K., Scaramuzzi R.J. and Webb R. (1995). Control of antral follicle development and selection in sheep and cattle. J. Reprod. Fertil. Suppl. 49, 335-350.
Campbell B.K., Dobson H., Baird D.T. and Scaramuzzi R.J. (1999). Examination of the relative role of TFSHTand TLHTin the mechanism of ovulatory follicle selection in sheep. J. Reprod. Fertil. 117, 355-367.
Campbell B.K., Telfer E.E., Webb R. and Baird D.T. (2000). Ovarian autografts in sheep as a model for studying folliculogenesis. Mol. Cell. Endocrinol. 163, 137-139.
Campbell B.K., Clinton M. and Webb R. (2012). The role of TantiT-müllerian ThormoneT(TAMHT) during TfollicleTdevelopment in a monovulatory species (TsheepT). Endocrinology. 153, 4533-4543.
Carlsson I.B., Laitinen M.P., Scott J.E., Louhio H., Velentzis L., Tuuri T., Aaltonen J., Ritvos O., Winston R.M. and Hovatta O. (2006). Kit ligand and c-Kit are expressed during early human ovarian follicular development and their interaction is required for the survival of follicles in long-term culture. Reproduction. 131, 641-649.
Clark D.E., Tisdall D.J., Fidler A.E. and Mc Natty K.P. (1996). Localization of mRNA encoding c-TkitTduring the initiation of folliculogenesis in ovine fetal ovaries. J. Reprod. Fertil. 106, 329-335.
Coskun S., Uzumcu M., Jaroudi K., Hollanders J.M., Parhar R. and Al-Sedairy S. (1998). Presence of leukemia inhibitory factor and interleukin-12 in human follicular fluid during follicular growth.Am. J. Reprod. Immunol. 40, 13-18.
Çiftci H.B. (2004). In vitroand in vivo effects of serine and threonine on follicle growth differentiation and atresia. Turk. J. Vet. Anim. Sci. 28, 825-830.
Da Nóbrega J.E.Jr., Gonçalves P.B., Chaves R.N., Magalhães D.De.M., Rossetto R., Lima Verde I.B., Pereira G.R., Campello C.C., Figueiredo J.R. and De Oliveira J.F. (2012).TLeukemia inhibitory factorTstimulates the transition of TprimordialTto primary follicle and supports the goat primordial follicle viability in vitro. Zygote. 20, 73-78.
Demeestere I., Centner J., Gervy C., Englert Y. and Delbaere A. (2005). Impact of various endocrine and paracrine factors on in vitroculture of preantral follicles in rodents. Reproduction. 130, 147-156.
Dissen G.A., Garcia Rudaz C. and Ojeda S.R. (2009). Role of neurotrophic factors in early ovarian development. Semin. Reprod. Med. 27, 24-31.
Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N. and Matzuk M.M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature. 383, 531-535.
Driancourt M.A., Webb R. and Fry R.C. (1991). Does follicular TdominanceToccur in ewes? J. Reprod. Fertil. 93,63-70.
Dube J.L., Wang P., Elvin J., Lyons K.M., Celeste A.J. and Matzuk M.M. (1998). The bone morphogenetic protein 15 gene is x-linked and expressed in oocytes. Mol. Endocrinol. 12, 1809-1817.
Durlinger A.L., Kramer P., Karels B., De Jong F.H., Uilenbroek J.T., Grootegoed J.A. and Themmen A.P. (1999). Control of primordial follicle recruitmentby anti-müllerian hormone in the mouse ovary. Endocrinology. 140, 5789-5796.
Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Kumar T.R., Matzuk M.M., Rose U.M., De Jong F.H., Uilenbroek J.T., Grootegoed J.A. and Themmen A.P. (2001). Anti-müllerian hormone attenuates the effects of FSH on follicle development in the  mouse ovary.  Endocrinology . 142, 4891-4899.
Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Ingraham H.A., Nachtigal M.W., Uilenbroek J.T., Grootegoed J.A. and Themmen A.P. (2002). Anti-müllerian hormone inhibits initiation of primordial follicle growth in themouse ovary. Endocrinology. 143,1076-1084.
Elvin J.A., Clark A.T., Wang P., Wolfman N.M. and Matzuk M.M. (1999). Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 13, 1035-1048.
Fair T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci.78, 203-216.
Feary E.S., Juengel J.L., Smith P., French M.C., O'Connell A.R., Lawrence S.B., Galloway S.M., Davis G.H. and Mc Natty K.P. (2007). Patterns of expression of messenger RNAs encoding GDF9, BMP15, TGFBR1, BMPR1B and BMPR2 during follicular development and characterization of TovarianTfollicular populations in ewes carrying the Woodlands FecX2W mutation. Biol. Reprod. 77,990-998.
Fenwick M.A. and Hurst P.R. (2002). Immunohistochemical localization of active caspase-3 in the mouse ovary: growth and atresia of small follicles. Reproduction. 124, 659-665.
Filicori M. (1999). The role of luteinizing hormone in folliculogenesis and ovulation induction.Fertil. Steril. 71, 405-414.
Fortune J.E. (1994). Ovarian follicular growth and development in mammals. Biol. Reprod. 50, 225-232.
Fortune J.E., Cushman R.A., Wahl C.M., Kito W.S. (2000). The primordial to primary follicle transition. Mol. Cell. Endocrinol. 163, 53-60.
Gosden R. and Spears N. (1997). Programmed cell death in the reproductive system. Br. Med. Bull. 53, 644-661.
Gutierrez C.G., Ralph J.H., Telfer E.E., Wilmut I. and Webb R. (2000). Growth and antrum formation of bovine preantral follicles in long-term culture in vitro. Mol. Cell. Endocrinol. 62,1322-1328.
Hammond J.M., Mondschein J.S., Samaras S.E. and Canning S.F. (1991). The ovarian insulin-like growth factors, a local amplification mechanism for steroidogenesis and hormone action. J. Steroid. Biochem. Mol. Biol. 40,411-416.
Hastie P.M. and Haresign W. (2008). Modulating peripheral gonadotropin levels affects follicular expression of  RNAs encoding insulin-like growth factors and  receptors in  sheep . Anim. Reprod. Sci. 109, 110-123.
Hastie P.M. and Haresign W. (2010). Modulating peripheral gonadotropin levels affects follicular expression of mRNAs encoding insulin-like  growth factor binding proteins in  sheep. Anim Reprod Sci. 119, 198-204.
Hayashi M., Mc Gee E.A., Min G., Klein C., Rose U.M., Van Duin M. and Hsueh A.J. (1999). Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarianfollicles. Endocrinology. 140, 1236-1244.
Hreinsson J.G., Scott J.E., Rasmussen C., Swahn M.L., Hsueh A.J. and Hovatta O. (2002). Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture. J. Clin. Endocrinol. Metab. 87, 316-621.
Hsueh A.J.W., Billig H. and Tsafriri A. (1994). Ovarian follicle atresia: a hormonally controlled apoptotic process. Endocrinol. Rev. 15, 707-724.
Hulshof S.C., Figueiredo J.R., Beckers J.F., Bevers M.M., Van Der Donk J.A. and Van Den Hurk R. (1995). Effects of fetal bovine serum, TFSHTand 17 beta-estradiol on the culture of bovine TpreantralTfollicles. Theriogenology. 44, 217-226.
Hurst P.R., Mora J.M. and Fenwick M.A. (2006). Caspase-3, TUNEL and ultrastructural studies of small follicles in adult human ovarian biopsies. Hum. Reprod. 21, 1974-1980.
Hussein M.R. (2005). Apoptosis in the ovary: molecular mechanisms. Hum. Reprod. Update. 11, 162-177.
Ireland J.J. (1987). Control of follicular growth and development. J. Reprod. Fertil. Suppl. 34, 39-54.
Josso N., Di Clemente N. and Gouédard L. (2001). Anti-müllerian hormone and its receptors. Mol. Cell. Endocrinol. 179, 25-32.
Juengel J.L., Hudson N.L., Whiting L. and Mc Natty K.P. (2004). Effects of immunization against bone morphogenetic protein 15 and growth differentiation factor 9 on ovulation rate, fertilization and pregnancy in ewes. Biol. Reprod. 70, 557-561.
Kaipia A. and Hsueh A.J. (1997). Regulation of ovarian follicle atresia. Annu. Rev. Physiol. 59, 349-363.
Kedem A., Fisch B., Garor R., Ben Zaken A., Gizunterman T., Felz C., Ben Haroush A., Kravarusic D. and Abir R. (2011). Growth differentiating factor 9 (GDF9) and  bone morphogenetic protein 15 both activate  development of human primordial follicles in vitro, with seemingly more beneficial effects of  GDF9 . J. Clin. Endocrinol. Metab. 96, 1246-1254.
Kezele P.R., Nilsson E.E. and Skinner M.K. (2002). Insulin but not  insulin-like growth factor-1 promotes the primordial to primary follicle transition. Mol. Cell. Endocrinol. 192, 37-43.
Kim J.Y. (2012). Control of ovarian primordial follicle activation. Clin. Exp. Reprod. Med. 39, 10-14.
Laitinen M., Vuojolainen K., Jaatinen R., Ketola I., Aaltonen J., Lehtonen E., Heikinheimo M. and Ritvos O. (1998). A novel growth differentiation factor-9 (GDF-9) related factor is co expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech. Dev. 78, 135-140.
Leeuwenberg B.R., Hurst P.R. and Mc Natty K.P. (1995). Expression of IGF-I mRNA in the ovine ovary. J. Mol. Endocrinol. 15, 251-258.
Luz V.B., Araújo V.R., Duarte A.B., Celestino J.J., Silva T.F., Magalhães Padilha D.M., Chaves R.N., Brito I.R., Almeida A.P., Campello C.C., Feltrin C., Bertolini M., Santos R.R. and Figueiredo J.R. (2012a). Eight-cell parthenotes originated from in vitro grown sheep preantral follicles. Reprod. Sci. 19, 1219-1225.
Luz V.B., Santos R., Araújo V.R., Celestino J.J., Magalhães-Padilha D.M., Chaves R.N., Brito I.R., Silva T.F., Almeida A.P., Campello C.C. and Figueiredo J.R. (2012b). The effect of LIF in the absence or presence of FSH on the in vitro development of isolated caprine preantral follicles. Reprod. Domest. Anim. 47,379-384.
Magamage M.P.S., Moniruzzaman M. and Miyano T. (2011). Effect of kit ligand on the viability of porcine primordial follicles in vitro. J. Mamm. Ova. Res. 28, 61-67.
Martins F.S., Celestino J.J., Saraiva M.V., Matos M.H., Bruno J.B., Rocha-Junior C.M., Lima-Verde I.B., Lucci C.M., Báo S.N. and Figueiredo J.R. (2008). Growth and differentiation factor-9 stimulates TactivationTof goat TprimordialTfollicles in vitro and their progression to secondary follicles. Reprod. Fertil. Dev. 20, 916-924.
Matikainen T., Perez G.I., Zheng T.S., Kluzak T.R., Rueda B.R., Flavell R.A. and Tilly J.L. (2001).Caspase-3 gene knockout defines cell lineage specificity for programmed cell death signaling in the ovary. Endocrinology. 142, 2468-2480.
Matsuda F., Inoue N., Manabe N. and Ohkura S. (2012). Follicular growth and atresia in mammalian ovaries: regulation by survival and death of granulosa cells. J. Reprod. Dev. 58,44-50.
Mc Grath S.A., Esquela A.F. and Lee S.J. (1995). Oocyte-specific expression of growth / differentiation factor-9. Mol. Endocrinol. 9, 131-136.
Mc Natty K.P., Heath D.A., Lundy T., Fidler A.E., Quirke L., O'Connell A., Smith P., Groome N.P. and Tisdall D.J. (1999). Control of early ovarian follicular development. J. Reprod. Fertil. Suppl. 54, 3-16.
Mc Natty K.P., Fidler A.E., Juengel J.L., Quirke L.D., Smith P.R., Heath D.A., Lundy T., O'Connell A. and Tisdall D.J. (2000). Growth and paracrine factors regulating follicular formation and cellular function. Mol. Cell. Endocrinol. 163, 11-20.
Mc Natty K.P., Reader K., Smith P., Heath D.A. and Juengel J.L. (2007). Control of ovarian follicular  development to the gonadotrophin-dependent phase: a 2006 perspective. Soc. Reprod. Fertil. Suppl. 64, 55-68.
Mc Neilly A.S. (1984). Changes in FSH and the pulsatile secretion of LH during the delay in oestrus induced by treatment of ewes with bovine follicular fluid. J. Reprod.Fertil. 72, 165-172.
Mc NeillyA.S. (1985). Effect of changes in FSH induced by bovine follicular fluid infusion in the preovulatory phase on subsequent ovulation rate and corpus luteum function in the ewe. J. Reprod.Fertil. 74, 661-568.
Mc Neilly A.S. and Fraser H.M. (1987). Effect of GnRH agonist-induced suppression of LH and FSH on follicle growth and corpus luteum function in the ewe. J. Endocrinol. 115, 273-282.
Mc PherronA.C. and Lee S.J. (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.
Mery L., Lefevre A., Benchaib M., Demirci B., Salle B., Guerin J.F. and Lornage J. (2007). Follicular growth in  vitro: detection of  growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 ( BMP15 ) during in  vitro culture of ovine cortical slices. Mol. Reprod. Dev. 74, 767-774.
Monniaux D., Huet C., Besnard N., Clément F., Bosc M., Pisselet C., Monget P. and Mariana J.C (1997). Follicular growth and TovarianTdynamics in mammals. J. Reprod. Fertil. Suppl. 51, 3-23.
Nicholas B., Alberio R., Fouladi Nashta A.A. and Webb R. (2005). Relationship between low molecular weight insulin-like growth factor-binding proteins, caspase-3 activity and oocyte quality. Biol. Reprod.72,796-804.
Nilsson E., Parrott J.A. and Skinner M.K. (2001).Basic fibroblast growth factor induces primordial follicle development and  initiates folliculogenesis. Mol. Cell. Endocrinol. 175, 123-130.
NilssonE.E., Kezele P. and Skinner M.K. (2002). Leukemia inhibitory factor (LIF) promotes the primordial to primary follicle transition in rat ovaries. Mol. Cell. Endocrinol. 188, 65-73.
Nilsson E.E. and Skinner M.K. (2004). Kit ligand and basic fibroblast growth factor interactions in the induction of ovarian primordial to primary follicle transition. Mol. Cell. Endocrinol. 214, 19-25.
Orisaka M., Orisaka S., Jiang J.Y., Craig J., Wang Y., Kotsuji F. and Tsang B.K. (2006). Growth differentiation factor 9 is antiapoptotic duringfollicular development from preantral to early antral stage. Mol.Endocrinol. 20, 2456-2468.
Otsuka F., Yao Z., Lee T., Yamamoto S., Erickson G.F. and Shimasaki S. (2000).TBone morphogenetic protein-15T. Identification of target cells and biological functions. J. Biol. Chem. 275, 39523-39528.
Otsuka F. and Shimasaki S. (2002). A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. USA. 99, 8060-8065.
ParrottJ.A. and Skinner M.K. (1999).TKit-ligand / stem cell factor induces primordial follicle development and initiates folliculogenesis. Endocrinology. 140, 4262-4271.
Picton H.M., Tsonis C.G. and Mc Neilly A.S. (1990a). FSH causes a time-dependent stimulation of preovulatory follicle growth in the absence of pulsatile LH secretion in ewes chronically treated with gonadotrophin-releasing hormone releasing hormone. J. Endocrinol. 126, 297-307.
Picton H.M., Tsonis C.G. and Mc Neilly A.S. (1990b). The antagonistic effect of exogenous LH pulses on FSH stimulated preovulatory follicle growth in ewes chronically treated with GnRH agonist. J. Endocrinol. 127, 273-283.
Picton H.M. and Mc Neilly A.S. (1991). The effect of basal and pulsatile LH release on FSH-stimulates follicle growth in ewes chronically treated with gonadotrophin releasing hormone agonist. J. Endocrinol. 128, 449-456.
PhillippsT.R., Kokay I.C., Grattan D.R. and Hurst P.R. (2011). X-linked inhibitor of apoptosis protein and active caspase-3 expression patterns in antral follicles in the sheep ovary. Reproduction. 142, 855-867.
SadighiM., Bodensteiner K.J., Beattie A.E. and Galloway S.M. (2002). Genetic mapping of ovine growth differentiation factor 9 (GDF9) to sheep chromosome 5. Anim. Genet. 33, 244-245.
Samoto T.,  Maruo T., Ladines-Llave C.A., Matsuo H., Deguchi J., Barnea E.R. and Mochizuki M. (1993). Insulin receptor expression in follicular and stromal compartments of the human  ovary over the course of follicular growth, regression and atresia. Endocrinol. J. 40, 715-726.
Scaramuzzi R.J., Adams N.R., Baird D.T., Campbell B.K., Downing J.A., Findlay J.K., Henderson K.M., Martin G.B., Mc Natty K.P. and Mc Neilly A.S. (1993). A model for  follicle selection and the  determination of  ovulation rate in the  ewe . Reprod. Fertil. Dev. 5, 459-478.
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.
Shimizu T., Miyahayashi Y., Yokoo M., Hoshino Y., Sasada H. and Sato E. (2004). Molecular cloning of porcine growth differentiation factor 9 (TGDFT-9) cDNA and its role in early folliculogenesis: direct TovarianTinjection of TGDFT-9 gene fragments promotes early folliculogenesis. Reproduction. 128, 537-543.
Sidis TY., Fujiwara T., Leykin L., Isaacson K., Toth T. and Schneyer A.L. (1998). Characterization of inhibin / activin subunit, activin receptor  and follistatin messenger ribonucleic acid in human and mouse oocytes: evidence for activin's paracrine signaling from granulosa cells to oocytes. Biol. Reprod. 59, 807-812.
Sunderland S.J., Crowe M.A., Boland M.P., Roche J.F. and Ireland J.J. (1994). Selection, dominance and atresia of follicles during the oestrus cycle of heifers. J. Reprod. Fertil. 101, 547-555.
Tang K.,  Yang W.C., Li X T.,  Wu C.J., Sang L. and Yang L.G. (2012). GDF-9 and bFGF enhance the effect of FSH on the survival,  activation and growth of cattle primordial follicles. Anim. Reprod. Sci. 131, 129-134.
Tisdall D.J., Fidler A.E., Smith P., Quirke L.D., Stent V.C., Heath D.A. and Mc Natty K.P. (1999).Stem cell factorand c-kit gene expression and protein localization in the  sheep ovary during fetal development. J. Reprod. Fertil. 116, 277-291.
Van Eijk M., Mandelbaum J., Salat Baroux J., Belaisch Allart J., Plachot M., Junca A. and Mummery C. (1996). Expression of leukaemia inhibitory factor receptor subunits LIFR beta and gp130 in human oocytes and preimplantation embryos. Mol. Hum. Reprod. 2, 355-360.
Van Wezel I.L., Umapathysivam K., Tilley W.D. and Rodgers R.J. (1995). Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Mol. Cell. Endocrinol. 115, 133-140.
Vitt U.A., Hayashi M., Klein C. and Hsueh A.J. (2000). Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol. Reprod. 62, 370-377.
VittU.A., Mazerbourg S., Klein C. and Hsueh A.J. (2002). Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol. Reprod. 67, 473-480.
Wandji S.A., Pelletier G. and Sirard M.A. (1992a). Ontogeny and cellular localization of 125I-labelled insulin-like growth factor-1, 125I-labelled follicle-stimulating hormone, andPP125I-labelled human chorionic gonadotropin binding sites in ovaries from bovine fetuses and neonatal calves. Biol. Reprod. 47, 814-822.
Wandji S.A., Pelletier G. and Sirard M.A. (1992b). Ontogeny and cellular localization of 125I labeled basic fibroblast growth factor and 125I-labeled epidermal growth factor binding sites in ovaries from bovine fetuses and neonatal calves. Biol. Reprod. 47, 807-813.
Wandji S.A., Srsen V., Voss A.K. Eppig J.J. and Fortune J.E. (1996). Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod. 55, 942-948.
Webb R. and England B.G. (1982). Identification of ovulatory follicle in ewe: associated changes in follicular size, thecal and granulosa cell luteinizing hormone receptors, antral fluid steroids, and circulating hormones during the preovulatory period.Endocrinology. 110, 873-881.
Webb R., Campbell B.K., Garverick H.A., Gong J.G., Gutierrez C.G. and Armstrong D.G. (1999). Molecular mechanisms regulating follicular recruitment and selection. J. Reprod. Fertil. Suppl. 54, 33-48.
Weenen C., Laven J.S., Von Bergh A.R., Cranfield M., Groome N.P., Visser J.A., Kramer P., Fauser B.C. and Themmen A.P. (2004). Anti-müllerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol. Hum. Reprod. 10, 77-83.
Yamamoto S., Konishi I., Nanbu K., Komatsu T., Mandai M., Kuroda H., Matsushita K. and Mori T. (1997). Immunohistochemical localization of basic fibroblast growth factor (bFGF) during folliculogenesis in the human ovary. Gynecol. Endocrinol. 11, 223-230.
Yoshida H., Takakura N., Kataoka H., Kunisada T., Okamura H. and Nishikawa S.I. (1997). Stepwise requirement of c-kit tyrosine kinase in mouse ovarian follicle development.Dev. Biol. 184, 122-137.
Yuan J., Shaham S., Ledoux S., Ellis H.M. and Horvitz H.R. (1993). The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell. 75, 641-652.