Coordinated regulation of follicle development by germ and somatic cells
Mario Binelli A B and Bruce D. Murphy B C
+ Author Affiliations
- Author Affiliations
A College of Veterinary Medicine and Animal Science, University of São Paulo, Pirassununga, SP 13635-900, Brazil.
B Centre de Recherche en Reproduction Animale, Université de Montréal, CP 5000, St-Hyacinthe, QC J2S 7C6, Canada.
C Corresponding author. Email: bruce.d.murphy@umontreal.ca
Reproduction, Fertility and Development 22(1) 1-12 https://doi.org/10.1071/RD09218
Published: 8 December 2009
Abstract
The continuum of folliculogenesis begins in the fetal ovary with the differentiation of the oogonia and their isolation within the primordial follicles. Primordial follicle activation is an enigmatic process, whereby some follicles enter the growing pool to become primary follicles, thereby embarking on an irreversible progression towards ovulation or atresia. This process is under the coordinated regulation of factors from the oocyte itself, as well as from the somatic cells of the ovary, in particular the theca and granulosa cells, which are structural components of the follicle. These two influences provide the principal stimuli for the growth of the follicle to the late preantral or early antral stage of development. The endocrine effects of the gonadotrophins FSH and LH are essential to the continued progression of the follicle and most atresia can be attributed to the failure to receive or process the gonadotrophin signals. The peri-ovulatory state has received intensive investigation recently, demonstrating a coordinated role for gonadotrophins, steroids, epidermal growth factor family proteins and prostaglandins. Thus, a complex programme of coordinated interaction of governing elements from both germ and somatic cell sources is required for successful follicle development.
Additional keywords: antrum, folliculogenesis, growth factor, oocyte, ovulation.
Acknowledgements
The authors thank Vickie Roussel for preparation the figures and Dr Valerio Portela for valuable discussions on the topics in this review. M.B. was supported by CAPES and FAPESP. Studies from the laboratory of B.D.M. were supported by the Canadian Institutes of Health Research.
References
Adams, G. P. , Matteri, R. L. , and Ginther, O. J. (1992a). Effect of progesterone on ovarian follicles, emergence of follicular waves and circulating follicle-stimulating hormone in heifers. J. Reprod. Fertil. 96, 627–640.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ahtiainen, P. , Rulli, S. , Pakarainen, T. , Zhang, F. P. , Poutanen, M. , and Huhtaniemi, I. (2007). Phenotypic characterisation of mice with exaggerated and missing LH/hCG action. Mol. Cell. Endocrinol. 260–262, 255–263.
| Crossref | GoogleScholarGoogle Scholar |
Baker, J. , Hardy, M. P. , Zhou, J. , Bondy, C. , Lupu, F. , Bellve, A. R. , and Efstratiadis, A. (1996). Effects of an Igf1 gene null mutation on mouse reproduction. Mol. Endocrinol. 10, 903–918.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ballow, D. J. , Xin, Y. , Choi, Y. , Pangas, S. A. , and Rajkovic, A. (2006). Sohlh2 is a germ cell-specific bHLH transcription factor. Gene Expr. Patterns 6, 1014–1018.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Berisha, B. , Sinowatz, F. , and 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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Bristol-Gould, S. K. , Kreeger, P. K. , Selkirk, C. G. , Kilen, S. M. , Mayo, K. E. , Shea, L. D. , and Woodruff, T. K. (2006). Fate of the initial follicle pool: empirical and mathematical evidence supporting its sufficiency for adult fertility. Dev. Biol. 298, 149–154.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Buratini, J. , Glapinski, V. F. , Giometti, I. C. , Teixeira, A. B. , Costa, I. B. , Avellar, M. C. , Barros, C. M. , and Price, C. A. (2005). Expression of fibroblast growth factor-8 and its cognate receptors, fibroblast growth factor receptor (FGFR)-3c and -4, in fetal bovine preantral follicles. Mol. Reprod. Dev. 70, 255–261.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Campbell, B. K. , Souza, C. J. H. , Skinner, A. J. , Webb, R. , and Baird, D. T. (2006). Enhanced 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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Choi, Y. , and Rajkovic, A. (2006). Genetics of early mammalian folliculogenesis. Cell. Mol. Life Sci. 63, 579–590.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Choi, Y. , Ballow, D. J. , Xin, Y. , and Rajkovic, A. (2008a). Lim homeobox gene, lhx8, is essential for mouse oocyte differentiation and survival. Biol. Reprod. 79, 442–449.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Choi, Y. , Yuan, D. , and Rajkovic, A. (2008b). Germ cell-specific transcriptional regulator sohlh2 is essential for early mouse folliculogenesis and oocyte-specific gene expression. Biol. Reprod. 79, 1176–1182.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Clarke, H. G. , Hope, S. A. , Byers, S. , and Rodgers, R. J. (2006). Formation of ovarian follicular fluid may be due to the osmotic potential of large glycosaminoglycans and proteoglycans. Reproduction 132, 119–131.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Conneely, O. M. , Lydon, J. P. , De Mayo, F. , and O’Malley, B. W. (2000). Reproductive functions of the progesterone receptor. J. Soc. Gynecol. Invest. 7(Suppl. 1), S25–S32.
| Crossref | GoogleScholarGoogle Scholar | CAS |
Conti, M. , Hsieh, M. , Park, J. Y. , and Su, Y. Q. (2006). Role of the epidermal growth factor network in ovarian follicles. Mol. Endocrinol. 20, 715–723.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Cortvrindt, R. , and Smitz, J. (2001). In vitro follicle growth: achievements in mammalian species. Reprod. Domest. Anim. 36, 3–9.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Deroo, B. J. , Rodriguez, K. F. , Couse, J. F. , Hamilton, K. J. , Collins, J. B. , Grissom, S. F. , and Korach, K. S. (2009). Estrogen receptor beta is required for optimal cAMP production in mouse granulosa cells. Mol. Endocrinol. 23, 955–965.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Drummond, A. E. (2005). TGFbeta signalling in the development of ovarian function. Cell Tissue Res. 322, 107–115.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Duggavathi, R. , and Murphy, B. D. (2009). Ovulation signals. Science 324, 890–891.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Duggavathi, R. , Volle, D. H. , Mataki, C. , Antal, M. C. , Messaddeq, N. , Auwerx, J. , Murphy, B. D. , and Schoonjans, K. (2008). Liver receptor homolog 1 is essential for ovulation. Genes Dev. 22, 1871–1876.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Dupont, S. , Krust, A. , Gansmuller, A. , Dierich, A. , Chambon, P. , and Mark, M. (2000). Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127, 4277–4291.
| CAS | PubMed |
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-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 143, 1076–1084.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Eggan, K. , Jurga, S. , Gosden, R. , Min, I. M. , and Wagers, A. J. (2006). Ovulated oocytes in adult mice derive from non-circulating germ cells. Nature 441, 1109–1114.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Eppig, J. , and O’Brien, M. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod. 54, 197–207.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Faddy, M. , and Gosden, R. (2007). Numbers of ovarian follicles and testing germ line renewal in the postnatal ovary: facts and fallacies. Cell Cycle 6, 1951–1952.
| CAS | PubMed |
Fan, H.-Y. , Liu, Z. , Shimada, M. , Sterneck, E. , Johnson, P. F. , Hedrick, S. M. , and Richards, J. S. (2009). MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324, 938–941.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Fatehi, A. N. , van den Hurk, R. , Colenbrander, B. , Daemen, A. J. J. M. , van Tol, H. T. A. , Monteiro, R. M. , Roelen, B. A. J. , and Bevers, M. M. (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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Findlay, J. K. , Drummond, A. E. , Dyson, M. , Baillie, A. J. , Robertson, D. M. , and Ethier, J. F. (2001). Production and actions of inhibin and activin during folliculogenesis in the rat. Mol. Cell. Endocrinol. 180, 139–144.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Fortune, J. E. , Rivera, G. M. , Evans, A. C. O. , and Turzillo, A. M. (2001). Differentiation of dominant versus subordinate follicles in cattle. Biol. Reprod. 65, 648–654.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Fowler, P. A. , Flannigan, S. , Mathers, A. , Gillanders, K. , and Lea, R. G. , et al. (2009). Gene expression analysis of human fetal ovarian primordial follicle formation. J. Clin. Endocrinol. Metab. 94, 1427–1435.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Fulton, N. , Martins da Silva, S. J. , Bayne, R. A. , and Anderson, R. A. (2005). Germ cell proliferation and apoptosis in the developing human ovary. J. Clin. Endocrinol. Metab. 90, 4664–4670.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Gilchrist, R. B. , Ritter, L. J. , Myllymaa, S. , Kaivo-Oja, N. , Dragovic, R. A. , Hickey, T. E. , Ritvos, O. , and Mottershead, D. G. (2006). Molecular basis of oocyte–paracrine signalling that promotes granulosa cell proliferation. J. Cell Sci. 119, 3811–3821.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Gilchrist, R. B. , Lane, M. , and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–177.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ginther, O. J. , Bergfelt, D. R. , Kulick, L. J. , and Kot, K. (1999). Selection of the dominant follicle in cattle: establishment of follicle deviation in less than 8 hours through depression of FSH concentrations. Theriogenology 52, 1079–1093.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ginther, O. J. , Beg, M. A. , Bergfelt, D. R. , Donadeu, F. X. , and Kot, K. (2001). Follicle selection in monovular species. Biol. Reprod. 65, 638–647.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ginther, O. , Bergfelt, D. , Beg, M. , and Kot, K. (2002). Role of low circulating FSH concentrations in controlling the interval to emergence of the subsequent follicular wave in cattle. Reproduction 124, 475–482.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Glister, C. , Kemp, C. F. , and Knight, P. G. (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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Gong, J. , Campbell, B. , Bramley, T. , Gutierrez, C. , Peters, A. , and Webb, R. (1996). Suppression in the secretion of follicle-stimulating hormone and luteinizing hormone, and ovarian follicle development in heifers continuously infused with a gonadotropin-releasing hormone agonist. Biol. Reprod. 55, 68–74.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Grinwich, D. L. , Kennedy, T. G. , and Armstrong, D. T. (1972). Dissociation of ovulatory and steroidogenic actions of luteinizing hormone in rabbits with indomethacin, an inhibitor of prostaglandin biosynthesis. Prostaglandins 1, 89–96.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Gueripel, X. , Brun, V. , and Gougeon, A. (2006). Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol. Reprod. 75, 836–843.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Hewitt, S. C. , Harrell, J. C. , and Korach, K. S. (2005). Lessons in estrogen biology from knockout and transgenic animals. Annu. Rev. Physiol. 67, 285–308.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Hillier, S. G. (2001). Gonadotropic control of ovarian follicular growth and development. Mol. Cell. Endocrinol. 179, 39–46.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Hirshfield, A. N. (1992). Heterogeneity of cell populations that contribute to the formation of primordial follicles in rats. Biol. Reprod. 47, 466–472.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Huang, H. F. , He, R. H. , Sun, C. C. , Zhang, Y. , Meng, Q. X. , and Ma, Y. Y. (2006). Function of aquaporins in female and male reproductive systems. Hum. Reprod. Update 12, 785–795.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Hunzicker-Dunn, M. , and Maizels, E. T. (2006). FSH signaling pathways in immature granulosa cells that regulate target gene expression: branching out from protein kinase A. Cell. Signal. 18, 1351–1359.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Hussein, T. S. , Froiland, D. A. , Amato, F. , Thompson, J. G. , and Gilchrist, R. B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257–5268.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ireland, J. L. H. , Scheetz, D. , Jimenez-Krassel, F. , Themmen, A. P. N. , Ward, F. , Lonergan, P. , Smith, G. W. , Perez, G. I. , Evans, A. C. O. , and Ireland, J. J. (2008). Antral follicle count reliably predicts number of morphologically healthy oocytes and follicles in ovaries of young adult cattle. Biol. Reprod. 79, 1219–1225.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ireland, J. J. , Zielak-Steciwko, A. E. , Jimenez-Krassel, F. , Folger, J. , and Bettegowda, A. , et al. (2009). Variation in the ovarian reserve is linked to alterations in intrafollicular estradiol production and ovarian biomarkers of follicular differentiation and oocyte quality in cattle. Biol. Reprod. 80, 954–964.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Irving-Rodgers, H. F. , Catanzariti, K. D. , Aspden, W. J. , D’Occhio, M. J. , and Rodgers, R. J. (2006). Remodeling of extracellular matrix at ovulation of the bovine ovarian follicle. Mol. Reprod. Dev. 73, 1292–1302.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Itoh, T. , Kacchi, M. , Abe, H. , Sendai, Y. , and Hoshi, H. (2002). Growth, antrum formation, and estradiol production of bovine preantral follicles cultured in a serum-free medium. Biol. Reprod. 67, 1099–1105.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Jimenez-Krassel, F. , Folger, J. K. , Ireland, J. L. H. , Smith, G. W. , Hou, X. , Davis, J. S. , Lonergan, P. , Evans, A. C. O. , and Ireland, J. J. (2009). Evidence that high variation in ovarian reserves of healthy young adults has a negative impact on the corpus luteum and endometrium during estrous cycles in cattle. Biol. Reprod. 80, 1272–1281.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Jo, M. , Komar, C. M. , and Fortune, J. E. (2002). Gonadotropin surge induces two separate increases in messenger RNA for progesterone receptor in bovine preovulatory follicles. Biol. Reprod. 67, 1981–1988.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Johnson, J. , Canning, J. , Kaneko, T. , Pru, J. K. , and Tilly, J. L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–150.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Johnson, J. , Bagley, J. , Skaznik-Wikiel, M. , Lee, H.-J. , and Adams, G. B. , et al. (2005). Oocyte generation in adult mammalian ovaries by putative germ cells in bone marrow and peripheral blood. Cell 122, 303–315.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Joshi, S. , Davies, H. , Sims, L. P. , Levy, S. E. , and Dean, J. (2007). Ovarian gene expression in the absence of FIGLA, an oocyte-specific transcription factor. BMC Dev. Biol. 7, 67.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Juengel, J. L. , Sawyer, H. R. , Smith, P. R. , Quirke, L. D. , Heath, D. A. , Lun, S. , Wakefield, S. J. , and McNatty, K. P. (2002). Origins of follicular cells and ontogeny of steroidogenesis in ovine fetal ovaries. Mol. Cell. Endocrinol. 191, 1–10.
| Crossref | GoogleScholarGoogle Scholar | CAS |
Kasa-Vubu, J. , Dahl, G. , Evans, N. , Thrun, L. , Moenter, S. , Padmanabhan, V. , and Karsch, F. (1992). Progesterone blocks the estradiol-induced gonadotropin discharge in the ewe by inhibiting the surge of gonadotropin-releasing hormone. Endocrinology 131, 208–212.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Kerr, J. B. , Duckett, R. , Myers, M. , Britt, K. L. , Mladenovska, T. , and Findlay, J. K. (2006). Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132, 95–109.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Kidder, G. M. , and Mhawi, A. A. (2002). Gap junctions and ovarian folliculogenesis. Reproduction 123, 613–620.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Kocer, A. , Reichmann, J. , Best, D. , and Adams, I. R. (2009). Germ cell sex determination in mammals. Mol. Hum. Reprod. 15, 205–213.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Latham, K. E. , Wigglesworth, K. , McMenamin, M. , and Eppig, J. J. (2004). Stage-dependent effects of oocytes and growth differentiation factor 9 on mouse granulosa cell development: advance programming and subsequent control of the transition from preantral secondary follicles to early antral tertiary follicles. Biol. Reprod. 70, 1253–1262.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Liang, L. , Soyal, S. M. , and Dean, J. (1997). FIGalpha, a germ cell specific transcription factor involved in the coordinate expression of the zona pellucida genes. Development 124, 4939–4947.
| CAS | PubMed |
Martins da Silva, S. J. , Bayne, R. A. , Cambray, N. , Hartley, P. S. , McNeilly, A. S. , and Anderson, R. A. (2004). Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation. Dev. Biol. 266, 334–345.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Mayo, K. , Jameson, L. , and Woodruff, T. K. (2007). Eggs in the nest. Endocrinology 148, 3577–3579.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
McNatty, K. P. , Hudson, N. L. , Whiting, L. , Reader, K. L. , Lun, S. , Western, A. , Heath, D. A. , and Juengel, J. L. (2007a). The effects of immunizing sheep with different BMP15 or GDF9 peptide sequences on ovarian follicular activity and ovulation rate. Biol. Reprod. 76, 552–560.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
McNatty, K. P. , Reader, K. , Smith, P. , Heath, D. A. , and Juengel, J. L. (2007b). Control of ovarian follicular development to the gonadotrophin-dependent phase: a 2006 perspective. Soc. Reprod. Fertil. Suppl. 64, 55–68.
| CAS | PubMed |
Moenter, S. M. , Caraty, A. , and Karsch, F. J. (1990). The estradiol-induced surge of gonadotropin-releasing hormone in the ewe. Endocrinology 127, 1375–1384.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Motta, P. M. , Nottola, S. A. , and Makabe, S. (1997). Natural history of the female germ cell from its origin to full maturation through prenatal ovarian development. Eur. J. Obstet. Gynecol. Reprod. Biol. 75, 5–10.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
O’Shaughnessy, P. J. , McLelland, D. , and McBride, M. W. (1997). Regulation of luteinizing hormone-receptor and follicle-stimulating hormone-receptor messenger ribonucleic acid levels during development in the neonatal mouse ovary. Biol. Reprod. 57, 602–608.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Okada-Ban, M. , Thiery, J. P. , and Jouanneau, J. (2000). Fibroblast growth factor-2. Int. J. Biochem. Cell Biol. 32, 263–267.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pan, H. , O’Brien, M. J. , Wigglesworth, K. , Eppig, J. J. , and Schultz, R. M. (2005). Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev. Biol. 286, 493–506.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pangas, S. A. , and Matzuk, M. M. (2005). The art and artifact of GDF9 activity: cumulus expansion and the cumulus expansion-enabling factor. Biol. Reprod. 73, 582–585.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Panigone, S. , Hsieh, M. , Fu, M. , Persani, L. , and Conti, M. (2008). Luteinizing hormone signaling in preovulatory follicles involves early activation of the epidermal growth factor receptor pathway. Mol. Endocrinol. 22, 924–936.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Park, J. Y. , Su, Y. Q. , Ariga, M. , Law, E. , Jin, S. L. , and Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–684.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pepling, M. E. (2006). From primordial germ cell to primordial follicle: mammalian female germ cell development. Genesis 44, 622–632.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pepling, M. E. , and Spradling, A. C. (1998). Female mouse germ cells form synchronously dividing cysts. Development 125, 3323–3328.
| CAS | PubMed |
Pepling, M. E. , and Spradling, A. C. (2001). Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev. Biol. 234, 339–351.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pescador, N. , Stocco, D. M. , and Murphy, B. D. (1999). Growth factor modulation of steroidogenic acute regulatory protein and luteinization in the pig ovary. Biol. Reprod. 60, 1453–1461.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Pisarska, M. D. , Bae, J. , Klein, C. , and Hsueh, A. J. (2004). Forkhead l2 is expressed in the ovary and represses the promoter activity of the steroidogenic acute regulatory gene. Endocrinology 145, 3424–3433.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Quirk, S. M. , Cowan, R. G. , Harman, R. M. , Hu, C. L. , and Porter, D. A. (2004). Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J. Anim. Sci. 82(E-Suppl.), E40–E52.
| PubMed |
Rajkovic, A. , Pangas, S. A. , Ballow, D. , Suzumori, N. , and Matzuk, M. M. (2004). NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305, 1157–1159.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Richards, J. S. (2005). Ovulation: new factors that prepare the oocyte for fertilization. Mol. Cell. Endocrinol. 234, 75–79.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Richards, J. S. (2007). Genetics of ovulation. Semin. Reprod. Med. 25, 235–242.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Robker, R. L. , Russell, D. L. , Yoshioka, S. , Sharma, S. C. , Lydon, J. P. , O’Malley, B. W. , Espey, L. L. , and Richards, J. S. (2000). Ovulation: a multi-gene, multi-step process. Steroids 65, 559–570.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Ruiz-Cortes, Z. T. , Kimmins, S. , Monaco, L. , Burns, K. H. , Sassone-Corsi, P. , and Murphy, B. D. (2005). Estrogen mediates phosphorylation of histone H3 in ovarian follicle and mammary epithelial tumor cells via the mitotic kinase, Aurora B. Mol. Endocrinol. 19, 2991–3000.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Salvador, L. M. , Park, Y. , Cottom, J. , Maizels, E. T. , and Jones, J. C. , et al. (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, 40 146–40 155.
| Crossref | GoogleScholarGoogle Scholar | CAS |
Sanchez, 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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Sawyer, H. R. , Smith, P. , Heath, D. A. , Juengel, J. L. , Wakefield, S. J. , and McNatty, K. P. (2002). Formation of ovarian follicles during fetal development in sheep. Biol. Reprod. 66, 1134–1150.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Schmidt, D. , Ovitt, C. E. , Anlag, K. , Fehsenfeld, S. , Gredsted, L. , Treier, A. C. , and Treier, M. (2004). The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance. Development 131, 933–942.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Silva, J. R. , Figueiredo, J. R. , and van den Hurk, R. (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71, 1193–1208.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Skinner, M. K. , Schmidt, M. , Savenkova, M. I. , Sadler-Riggleman, I. , and Nilsson, E. E. (2008). Regulation of granulosa and theca cell transcriptomes during ovarian antral follicle development. Mol. Reprod. Dev. 75, 1457–1472.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Slot, K. A. , Kastelijn, J. , Bachelot, A. , Kelly, P. A. , Binart, N. , and Teerds, K. J. (2006). Reduced recruitment and survival of primordial and growing follicles in GH receptor-deficient mice. Reproduction 131, 525–532.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Smitz, J. , and Cortvrindt, R. (2002). The earliest stages of folliculogenesis in vitro. Reproduction 123, 185–202.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Su, Y. Q. , Sugiura, K. , and Eppig, J. J. (2009). Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin. Reprod. Med. 27, 32–42.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Thomas, F. , and Vanderhyden, B. (2006). Oocyte–granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth. Reprod. Biol. Endocrinol. 4, 19.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Tong, D. , Gittens, J. E. , Kidder, G. M. , and Bai, D. (2006). Patch-clamp study reveals that the importance of connexin43-mediated gap junctional communication for ovarian folliculogenesis is strain specific in the mouse. Am. J. Physiol. Cell Physiol. 290, C290–C297.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Trombly, D. J. , Woodruff, T. K. , and Mayo, K. E. (2009). Suppression of Notch signaling in the neonatal mouse ovary decreases primordial follicle formation. Endocrinology 150, 1014–1024.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Tsafriri, A. , and Motola, S. (2007). Are steroids dispensable for meiotic resumption in mammals? Trends Endocrinol. Metab. 18, 321–327.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Vaccari, S. , Weeks Ii, J. L. , Hsieh, M. , Menniti, F. S. , and Conti, M. (2009). Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol. Reprod. ,
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Valve, E. , Penttila, T. L. , Paranko, J. , and Harkonen, P. (1997). FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem. Biophys. Res. Commun. 232, 173–177.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
van Wezel, I. L. , and Rodgers, R. J. (1996). Morphological characterization of bovine primordial follicles and their environment in vivo. Biol. Reprod. 55, 1003–1011.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
van Wezel, I. L. , Krupa, M. , and Rodgers, R. J. (1999). Development of the membrana granulosa of bovine antral follicles: structure, location of mitosis and pyknosis, and immunolocalization of involucrin and vimentin. Reprod. Fertil. Dev. 11, 37–48.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Vanderhyden, B. C. , Caron, P. J. , Buccione, R. , and Eppig, J. J. (1990). Developmental pattern of the secretion of cumulus expansion-enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev. Biol. 140, 307–317.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Wandji, S. , Srsen, V. , Voss, A. , Eppig, J. , and Fortune, J. (1996). Initiation in vitro of growth of bovine primordial follicles. Biol. Reprod. 55, 942–948.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Wartenberg, H. , Hilscher, B. , and Hilscher, W. (1998). Germ cell kinetics during early ovarian differentiation: an analysis of the oogonial cell cycle and the subsequent changes in oocyte development during the onset of meiosis in the rat. Microsc. Res. Tech. 40, 377–397.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Webb, R. , and Campbell, B. K. (2007). Development of the dominant follicle: mechanisms of selection and maintenance of oocyte quality. Soc. Reprod. Fertil. Suppl. 64, 141–163.
| CAS | PubMed |
Webb, R. , Garnsworthy, P. C. , Gong, J. G. , and Armstrong, D. G. (2004). Control of follicular growth: local interactions and nutritional influences. J. Anim. Sci. 82(E-Suppl.), E63–E74.
| PubMed |
West-Farrell, E. R. , Xu, M. , Gomberg, M. A. , Chow, Y. H. , Woodruff, T. K. , and Shea, L. D. (2009). The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol. Reprod. 80, 432–439.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Yang, M. Y. , and Fortune, J. E. (2008). The capacity of primordial follicles in fetal bovine ovaries to initiate growth in vitro develops during mid-gestation and is associated with meiotic arrest of oocytes. Biol. Reprod. 78, 1153–1161.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
Zou, K. , Yuan, Z. , Yang, Z. , Luo, H. , and Sun, K. , et al. (2009). Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat. Cell Biol. 11, 631–636.
| Crossref | GoogleScholarGoogle Scholar | CAS | PubMed |
