Animal Reproduction (AR)
Animal Reproduction (AR)
Conference Paper

The life and death of the dominant follicle

Christopher A Price, Anthony Estienne

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Much work has been conducted over the years to determine the major factors that control follicle growth, including the role of FSH, LH and IGF1. These factors permit the dominant follicle to grow while subordinate follicles regress. The dominant follicle enters a phase of growth, and then that growth slows as the follicle reaches maximum size. The dominant follicle remains morphologically larger for a few days in the static phase, before starting to regress with the loss of functional dominance. Few studies have addressed the factors that determine follicle fate during the static phase. In this review, we summarize the differences in gene expression between growing and non-growing (static or early regressing) dominant follicles, highlighting areas that require further study. Potential factors that may help survival of the dominant follicle include IGF1, estradiol and BMP4/BMP7, and intrafollicular factors that likely initiate regression and apoptosis include FGF18 and AMH acting through FASLG. It is also very likely that the influence of microRNAs, especially miR-21, play a role in determining the fate of the dominant follicle.


apoptosis, atresia, follicle, granulose.


Adams GP, Kot K, Smith CA, Ginther OJ. 1993. Selection of a dominant follicle and suppression of follicular growth in heifers. Anim Reprod Sci, 30:259-271.

Ali A, Lange A, Gilles M, Glatzel PS. 2001. Morphological and functional characteristics of the dominant follicle and corpus luteum in cattle and their influence on ovarian function. Theriogenology, 56:569-576.

Anttonen M, Färkkilä A, Tauriala H, Kauppinen M, MacLaughlin DT, Unkila-Kallio L, Bützow R, Heikinheimo M. 2011. Anti-Müllerian hormone inhibits growth of AMH type II receptor-positive human ovarian granulosa cell tumor cells by activating apoptosis. Lab Invest, 91:1605-1614.

Badinga L, Driancourt MA, Savio JD, Wolfenson D, Drost M, de la Sota RL, Thatcher WW. 1992. Endocrine and ovarian responses associated with the first-wave dominant follicle in cattle. Biol Reprod, 47:871-883.

Bao B, Garverick HA. 1998. Expression of steroidogenic enzyme and gonadotropin receptor genes in bovine follicles during ovarian follicular waves: a review. J Anim Sci, 76:1903-1921.

Berisha B, Sinowatz F, Schams D. 2004. Expression and localization of fibroblast growth factor (FGF) family members during the final growth of bovine ovarian follicles. Mol Reprod Dev, 67:162-171.

Besnard N, Pisselet C, Zapf J, Hornebeck W, Monniaux D, Monget P. 1996. Proteolytic activity is involved in changes in intrafollicular insulin-like growth factor-binding protein levels during growth and atresia of ovine ovarian follicles. Endocrinology, 137:1599-1607.

Bigelow KL, Fortune JE. 1998. Characteristics of prolonged dominant versus control follicles: follicle cell numbers, steroidogenic capabilities, and messenger ribonucleic acid for steroidogenic enzymes. Biol Reprod, 58:1241-1249.

Bodin L, Di Pasquale E, Fabre S, Bontoux M, Monget P, Persani L, Mulsant P. 2007. A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in lacaune sheep. Endocrinology, 148:393-400.

Buratini J Jr, Pinto MGL, Castilho AC, Amorim RL, Giometti IC, Portela VM, Nicola ES, Price CA. 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.

Burke CR, Cárdenas H, Mussard ML, Day ML. 2005. Histological and steroidogenic changes in dominant ovarian follicles during oestradiol-induced atresia in heifers. Reproduction, 129:611-620.

Campbell BK, Souza CJH, Skinner AJ, Webb R, Baird DT. 2006. ricoEnhanced response of granulosa and theca cells from sheep carriers of the FecB mutation in vitro to gonadotropins and bone morphogenic protein-2, -4, and -6. Endocrinology, 147:1608-1620.

Campbell BK, Clinton M, Webb R. 2012. The role of anti-Müllerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology, 153:4533-4543.

Carletti MZ, Fiedler SD, Christenson LK. 2010. MicroRNA 21 blocks apoptosis in mouse periovulatory granulosa cells. Biol Reprod, 83:286-295.

Chen Q, Yano T, Matsumi H, Osuga Y, Yano N, Xu J, Wada O, Koga K, Fujiwara T, Kugu K, Taketani Y. 2005. Cross-talk between Fas/Fas ligand system and nitric oxide in the pathway subserving granulosa cell apoptosis: a possible regulatory mechanism for ovarian follicle atresia. Endocrinology, 146:808-815.

Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. 1996. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature, 383:531-535.

Drummond AE, Findlay JK. 1999. The role of estrogen in folliculogenesis. Mol Cell Endocrinol, 151:57-64.

Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, Themmen AP. 1999. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology, 140:5789-5796.

Estienne A, Pierre A, di Clemente N, Picard J-Y, Jarrier P, Mansanet C, Monniaux D, Fabre S. 2015. Anti-Müllerian hormone regulation by the bone morphogenetic proteins in the sheep ovary: deciphering a direct regulatory pathway. Endocrinology, 156:301-313.

Fabre S, Pierre A, Mulsant P, Bodin L, Di Pasquale E, Persani L, Monget P, Monniaux D. 2006. Regulation of ovulation rate in mammals: contribution of sheep genetic models. Reprod Biol Endocrinol, 4:20. doi: 10.1186/1477-7827-4-20.

Fan S-J, Li H-B, Cui G, Kong X-L, Sun L-L, Zhao Y-Q, Li Y-H, Zhou J. 2016. miRNA-149* promotes cell proliferation and suppresses apoptosis by mediating JunB in T-cell acute lymphoblastic leukemia. Leuk Res, 41:62-70.

Fatehi AN, Van Den Hurk R, Colenbrander B, Daemen A, van Tol HTA, Monteiro RM, Roelen BAJ, Bevers MM. 2005. Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology, 63:872-889.

Galloway SM, McNatty KP, Cambridge LM, Laitinen MPE, Juengel JL, Jokiranta TS, McLaren RJ, Luiro K, Dodds KG, Montgomery GW, Beattie AE, Davis GH, Ritvos O. 2000. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet, 25:279-283.

Garcia-Guerra A, Kamalludin MH, Kirkpatrick BW, Wiltbank MC. 2018. Trio a novel bovine high-fecundity allele: II. Hormonal profile and follicular dynamics underlying the high ovulation rate. Biol Reprod, 98:335-349.

Gebremedhn S, Salilew-Wondim D, Ahmad I, Sahadevan S, Hossain MM, Hoelker M, Rings F, Neuhoff C, Tholen E, Looft C, Schellander K, Tesfaye D. 2015. MicroRNA expression profile in bovine granulosa cells of preovulatory dominant and subordinate follicles during the late follicular phase of the estrous cycle. PLoS One, 10:e0125912. doi: 10.1371/journal.pone.0125912.

Ginther OJ. 2016. The theory of follicle selection in cattle. Domest Anim Endocrinol, 57:85-99.

Ginther OJ, Siddiqui MAR, Baldrighi JM, Hoffman MM. 2016. Stimulation of regressing subordinate follicles of wave 2 with a gonadotropin product in heifers. Domest Anim Endocrinol, 55:46-50.

Girard A, Dufort I, Douville G, Sirard M-A. 2015. Global gene expression in granulosa cells of growing, plateau and atretic dominant follicles in cattle. Reprod Biol Endocrinol, 13:17. doi: 10.1186/s12958-015-0010-7.

Glister C, Kemp CF, Knight PG. 2004. Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction, 127:239-254.

Glister C, Richards SL, Knight PG. 2005. Bone morphogenetic proteins (BMP) -4, -6, and -7 potently suppress basal and luteinizing hormone-induced androgen production by bovine theca interna cells in primary culture: could ovarian hyperandrogenic dysfunction be caused by a defect in thecal BMP signaling? Endocrinology, 146:1883-1892.

Glister C, Satchell L, Knight PG. 2010. Changes in expression of bone morphogenetic proteins (BMPs), their receptors and inhibin co-receptor betaglycan during bovine antral follicle development: inhibin can antagonize the suppressive effect of BMPs on thecal androgen production. Reproduction, 140:699-712.

Glister C, Satchell L, Knight PG. 2011. Granulosal and thecal expression of bone morphogenetic protein- and activin-binding protein mRNA transcripts during bovine follicle development and factors modulating their expression in vitro. Reproduction, 142:581-591.

Gong JG, McBride D, Bramley TA, Webb R. 1993. Effects of recombinant bovine somatotrophin, insulin-like growth factor-I and insulin on the proliferation of bovine granulosa cells in vitro. J Endocrinol, 139:67-75.

Guerrero-Netro HM, Chorfi Y, Price CA. 2015. Effects of the mycotoxin deoxynivalenol on steroidogenesis and apoptosis in granulosa cells. Reproduction, 149:555-561.

Guerrero-Netro HM, Estienne A, Chorfi Y, Price CA. 2017. The mycotoxin metabolite deepoxy- deoxynivalenol increases apoptosis and decreases steroidogenesis in bovine ovarian theca cells. Biol Reprod, 97:746-757.

Han P, Guerrero-Netro H, Estienne A, Cao B, Price CA. 2017. Regulation and action of early growth response 1 in bovine granulosa cells. Reproduction, 154:547-557.

Hatzirodos N, Nigro J, Irving-Rodgers HF, Vashi AV, Hummitzsch K, Caterson B, Sullivan TR, Rodgers RJ. 2012. Glycomic analyses of ovarian follicles during development and atresia. Matrix Biol, 31:45-56.

Hatzirodos N, Irving-Rodgers HF, Hummitzsch K, Rodgers RJ. 2014. Transcriptome profiling of the theca interna from bovine ovarian follicles during atresia. PLoS One, 9:e99706. doi: 10.1371/journal.pone.0099706.

Heath DA, Pitman JL, McNatty KP. 2017. Molecular forms of ruminant BMP15 and GDF9 and putative interactions with receptors. Reproduction, 154:521-534.

Hu CL, Cowan RG, Harman RM, Porter DA, Quirk SM. 2001. Apoptosis of bovine granulosa cells after serum withdrawal is mediated by Fas antigen (CD95) and Fas ligand. Biol Reprod, 64:518-526.

Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB. 2005. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci, 118:5257-5268.

Ireland JJ, Roche JF. 1983. Development of nonovulatory antral follicles in heifers: changes in steroids in follicular fluid and receptors for gonadotropins. Endocrinology, 112:150-156.

Ireland JJ, Mihm M, Austin E, Diskin MG, Roche JF. 2000. Historical perspective of turnover of dominant follicles during the bovine estrous cycle: key concepts, studies, advancements, and terms. J Dairy Sci, 83:1648-1658.

Irving-Rodgers HF, van Wezel IL, Mussard ML, Kinder JE, Rodgers RJ. 2001. Atresia revisited: two basic patterns of atresia of bovine antral follicles. Reproduction, 122:761-775.

Jiang Z, Guerrero-Netro HM, Juengel JL, Price CA. 2013. Divergence of intracellular signaling pathways and early response genes of two closely related fibroblast growth factors, FGF8 and FGF18, in bovine ovarian granulosa cells. Mol Cell Endocrinol, 375:97-105.

Juengel JL, Reader KL, Bibby AH, Lun S, Ross I, Haydon LJ, McNatty KP. 2006. The role of bone morphogenetic proteins 2, 4, 6 and 7 during ovarian follicular development in sheep: contrast to rat. Reproduction, 131:501-513.

Knight PG, Glister C. 2006. TGF-β superfamily members and ovarian follicle development. Reproduction 132:191-206.

Ko JCH, Kastelic JP, Del Campo MR, Ginther OJ. 1991. Effects of a dominant follicle on ovarian follicular dynamics during the oestrous cycle in heifers. J Reprod Fertil, 91:511-519.

Li J, Hu L, Tian C, Lu F, Wu J, Liu L. 2015. microRNA-150 promotes cervical cancer cell growth and survival by targeting FOXO4. BMC Molecular Biology, 16:24. doi: 10.1186/s12867-015-0052-6.

Li Y, Chen D, Jin LU, Liu J, Li Y, Su Z, Qi Z, Shi MIN, Jiang Z, Yang S, Gui Y, Mao X, Wu X, Lai Y. 2016. Oncogenic microRNA-142-3p is associated with cellular migration, proliferation and apoptosis in renal cell carcinoma. Oncol Lett, 11:1235-1241.

Liang A, Salzano A, D'Esposito M, Comin A, Montillo M, Yang L, Campanile G, Gasparrini B. 2016. Anti-Mullerian hormone (AMH) concentration in follicular fluid and mRNA expression of AMH receptor type II and LH receptor in granulosa cells as predictive markers of good buffalo (Bubalus bubalis) donors. Theriogenology, 86:963-970.

Lin JY, Pitman-Crawford JL, Bibby AH, Hudson NL, McIntosh CJ, Juengel JL, McNatty KP. 2012. Effects of species differences on oocyte regulation of granulosa cell function. Reproduction, 144:557-567.

Lv L, Jimenez-Krassel F, Sen A, Bettegowda A, Mondal M, Folger JK, Lee KB, Ireland JJ, Smith GW. 2009. Evidence supporting a role for cocaine- and amphetamine-regulated transcript (CARTPT) in control of granulosa cell estradiol production associated with dominant follicle selection in cattle. Biol Reprod, 81:580-586.

Martinez-Royo A, Jurado JJ, Smulders JP, Martí JI, Alabart JL, Roche A, Fantova E, Bodin L, Mulsant P, Serrano M, Folch J, Calvo JH. 2008. A deletion in the bone morphogenetic protein 15 gene causes sterility and increased prolificacy in Rasa Aragonesa sheep. Anim Genet, 39:294-297.

Mazerbourg S, Monget P. 2018. Insulin-like growth factor binding proteins and IGFBP proteases: a dynamic system regulating the ovarian folliculogenesis. Front Endocrinol, 9:134. doi: 10.3389/fendo.2018.00134.

McNatty KP, Juengel JL, Reader KL, Lun S, Myllymaa S, Lawrence SB, Western A, Meerasahib MF, Mottershead DG, Groome NP, Ritvos O, Laitinen MP. 2005. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction, 129:481-487.

Mihm M, Good TEM, Ireland JLH, Ireland JJ, Knight PG, Roche JF. 1997. kuDecline in serum follicle-stimulating hormone concentrations alters key intrafollicular growth factors involved in selection of the dominant follicle in heifers. Biol Reprod, 57:1328-1337.

Mihm M, Baker PJ, Ireland JL, Smith GW, Coussens PM, Evans AC, Ireland JJ. 2006. Molecular evidence that growth of dominant follicles involves a reduction in follicle-stimulating hormone dependence

and an increase in luteinizing hormone dependence in cattle. Biol Reprod, 74:1051-1059.

Monniaux D, Pisselet C. 1992. Control of proliferation and differentiation of ovine granulosa cells by insulin-like growth factor-I and follicle-stimulating hormone in vitro. Biol Reprod, 46:109-119.

Monniaux D, Clemente Nd, Touzé J-L, Belville C, Rico C, Bontoux M, Picard J-Y, Fabre S. 2008. liIntrafollicular steroids and anti-Müllerian hormone during normal and cystic ovarian follicular development in the cow. Biol Reprod, 79:387-396.

Mottershead DG, Sugimura S, Al-Musawi SL, Li J-J, Richani D, White MA, Martin GA, Trotta AP, Ritter LJ, Shi J, Mueller TD, Harrison CA, Gilchrist RB. 2015. Cumulin, an oocyte-secreted heterodimer of the transforming growth factor-β family, is a potent activator of granulosa cells and improves oocyte quality. J Biol Chem, 290:24007-24020.

Mulsant P, Lecerf F, Fabre S, Schibler L, Monget P, Lanneluc I, Pisselet C, Riquet J, Monniaux D, Callebaut I, Cribiu E, Thimonier J, Teyssier J, Bodin L, Cognié Y, Chitour N, Elsen J-M. 2001. Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Mérino ewes. Proc Natl Sci USA, 98:5104-5109.

Nicol L, Bishop SC, Pong-Wong R, Bendixen C, Holm L-E, Rhind SM, McNeilly AS. 2009. Homozygosity for a single base-pair mutation in the oocyte-specific GDF9 gene results in sterility in Thoka sheep. Reproduction, 138:921-933.

Nivet A-L, Vigneault C, Blondin P, Sirard M-A. 2013. Changes in granulosa cells' gene expression associated with increased oocyte competence in bovine. Reproduction, 145:555-565.

Pierre A, Estienne A, Racine C, Picard J-Y, Fanchin R, Lahoz B, Alabart JL, Folch J, Jarrier P, Fabre S, Monniaux D, di Clemente N. 2016. The bone morphogenetic protein 15 up-regulates the anti-Müllerian hormone receptor expression in granulosa cells. J Clin Endocrinol Metab, 101:2602-2611.

Portela VM, Machado M, Buratini J, Jr., Zamberlam G, Amorim RL, Goncalves P, Price CA. 2010. Expression and function of fibroblast growth factor 18 in the ovarian follicle in cattle. Biol Reprod, 83:339-346.

Portela VM, Dirandeh E, Guerrero-Netro HM, Zamberlam G, Barreta MH, Goetten AF, Price CA. 2015. The role of fibroblast growth factor-18 in follicular atresia in cattle. Biol Reprod, 92:14. doi: 10.1095/biolreprod.114.121376.

Porter DA, Vickers SL, Cowan RG, Huber SC, Quirk SM. 2000. Expression and function of Fas antigen vary in bovine granulosa and theca cells during ovarian follicular development and atresia. Biol Reprod, 62:62-66.

Price CA, Webb R. 1988. Steroid control of gonadotropin secretion and ovarian function in heifers. Endocrinology, 122:2222-2231.

Price CA, Carrière PD, Bhatia B, Groome NP. 1995. Comparison of hormonal and histological changes during follicular growth, as measured by ultrasonography, in cattle. J Reprod Fertil, 103:63-68.

Quirk SM, Harman RM, Cowan RG. 2000. Regulation of Fas antigen (Fas, CD95)-mediated apoptosis of bovine granulosa cells by serum and growth factors. Biol Reprod, 63:1278-1284.

Quirk SM, Cowan RG, Harman RM. 2006. The susceptibility of granulosa cells to apoptosis is influenced by oestradiol and the cell cycle. J Endocrinol, 189:441-453.

Rajesh G, Mishra SR, Paul A, Punetha M, Vidyalakshmi GM, Narayanan K, Bag S, Bhure SK, Singh Chouhan V, Maurya VP, Singh G, Sarkar M. 2018. Transcriptional and translational abundance of Bone morphogenetic protein (BMP) 2, 4, 6, 7 and their receptors BMPR1A, 1B and BMPR2 in buffalo ovarian follicle and the role of BMP4 and BMP7 on estrogen production and survival of cultured granulosa cells. Res Vet Sci, 118:371-388.

Rico C, Médigue C, Fabre S, Jarrier P, Bontoux M, Clément F, Monniaux D. 2011. Regulation of anti-Müllerian hormone production in the cow: a multiscale study at endocrine, ovarian, follicular, and granulosa cell levels. Biol Reprod, 84:560-571.

Rivera GM, Fortune JE. 2001. Development of codominant follicles in cattle is associated with a follicle-stimulating hormone-dependent insulin-like growth factor binding protein-4 protease. Biol Reprod, 65:112-118.

Roberts AJ, Echternkamp SE. 2003. Insulin-like growth factor binding proteins in granulosa and thecal cells from bovine ovarian follicles at different stages of development1,2. J Anim Sci, 81:2826-2839.

Rosenfeld CS, Wagner JS, Roberts RM, Lubahn DB. 2001. Intraovarian actions of oestrogen. Reproduction, 122:215-226.

Salilew-Wondim D, Ahmad I, Gebremedhn S, Sahadevan S, Hossain MDM, Rings F, Hoelker M, Tholen E, Neuhoff C, Looft C, Schellander K, Tesfaye D. 2014. The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle. PLoS One, 9:e106795. doi: 10.1371/journal.pone. 0106795.

Sang W, Sun C, Zhang C, Zhang D, Wang Y, Xu L, Zhang Z, Wei X, Pan B, Yan D, Zhu F, Yan Z, Cao J, Loughran TP, Xu K. 2016. MicroRNA-150 negatively regulates the function of CD4+ T cells through AKT3/Bim signaling pathway. Cell Immunol, 306/307:35-40.

Schreiber NB, Spicer LJ. 2012. Effects of fibroblast growth factor 9 (FGF9) on steroidogenesis and gene expression and control of FGF9 mRNA in bovine granulosa cells. Endocrinology, 153:4491-4501.

Schütz LF, Schreiber NB, Gilliam JN, Cortinovis C, Totty ML, Caloni F, Evans JR, Spicer LJ. 2016. Changes in fibroblast growth factor 9 mRNA in granulosa and theca cells during ovarian follicular growth in dairy cattle. J Dairy Sci, 99:9143-9151.

Selvaraju S, Folger JK, Gupta PSP, Ireland JJ, Smith GW. 2013. Stage-specific expression and effect of bone morphogenetic protein 2 on bovine granulosa cell estradiol production: regulation by cocaine and amphetamine regulated transcript. Domest Anim

Endocrinol, 44:115-120.

Shimizu T, Magata F, Abe Y, Miyamoto A. 2012. Bone morphogenetic protein 4 (BMP-4) and BMP-7 induce vascular endothelial growth factor expression in bovine granulosa cells. Anim Sci J, 83:663-667.

Shimizu T. 2016. Molecular and cellular mechanisms for the regulation of ovarian follicular function in cows. J Reprod Dev, 62:323-329.

Siddiqui MAR, Baldrighi JM, Greene JM, Wolf CA, Ginther OJ. 2015. Spontaneous and experimental conversion of a regressing subordinate follicle of wave 1 to the dominant follicle of wave 2 in heifers. Theriogenology, 83:1352-1359.

Sontakke SD, Mohammed BT, McNeilly AS, Donadeu FX. 2014. Characterization of microRNAs differentially expressed during bovine follicle development. Reproduction, 148:271-283.

Souza CJ, MacDougall C, MacDougall C, Campbell BK, McNeilly AS, Baird DT. 2001. The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor type 1 B (BMPR1B) gene. J Endocrinol, 169:R1-R6.

Souza CJ, Campbell BK, McNeilly AS, Baird DT. 2002. Effect of bone morphogenetic protein 2 (BMP2) on oestradiol and inhibin A production by sheep granulosa cells, and localization of BMP receptors in the ovary by immunohistochemistry. Reproduction, 123:363-369.

Spicer LJ, Alpizar E, Echternkamp SE. 1993. Effects of insulin, insulin-like growth factor I, and gonadotropins on bovine granulosa cell proliferation, progesterone production, estradiol production, and(or) insulin-like growth factor I production in vitro. J Anim Sci, 71:1232-1241.

Spicer LJ, Aad PY, Allen DT, Mazerbourg S, Payne AH, Hsueh AJ. 2008. Growth differentiation factor 9 (GDF9) stimulates proliferation and inhibits steroidogenesis by bovine theca cells: influence of follicle size on responses to GDF9. Biol Reprod, 78:243-253.

Stock AE, Fortune JE. 1993. Ovarian follicular dominance in cattle: relationship between prolonged growth of the ovulatory follicle and endocrine parameters. Endocrinology, 132:1108-1114.

Webb R, Buratini J, Hernandez-Medrano JH, Gutierrez CG, Campbell BK. 2016. Follicle development and selection: past, present and future. Anim Reprod, 13:234-249.

Yamashita H, Murayama C, Takasugi R, Miyamoto A, Shimizu T. 2011. BMP-4 suppresses progesterone production by inhibiting histone H3 acetylation of StAR in bovine granulosa cells in vitro. Mol Cell Biochem, 348:183-190.

Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM. 2001. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol, 15:854-866.

Zamberlam G, Portela V, de Oliveira JF, Goncalves PB, Price CA. 2011. Regulation of inducible nitric oxide synthase expression in bovine ovarian granulosa cells. Mol Cell Endocrinol, 335:189-194.

Zielak-Steciwko AE, Evans ACO. 2016. Genomic portrait of ovarian follicle growth regulation in cattle. Reprod Biol, 16:197-202.

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