Browse > Article
http://dx.doi.org/10.5653/cerm.2012.39.3.95

Regulation and 3 dimensional culture of tertiary follicle growth  

Cheon, Yong-Pil (Division of Developmental Biology and Physiology, School of Biosciences and Chemistry, Sungshin Women's University)
Publication Information
Clinical and Experimental Reproductive Medicine / v.39, no.3, 2012 , pp. 95-106 More about this Journal
Abstract
It has been revealed that multiple cohorts of tertiary follicles develop during some animal estrous cycle and the human menstrual cycle. To reach developmental competence, oocytes need the support of somatic cells. During embryogenesis, the primordial germ cells appear, travel to the gonadal rudiments, and form follicles. The female germ cells develop within the somatic cells of the ovary, granulosa cells, and theca cells. How the oocyte and follicle cells support each other has been seriously studied. The latest technologies in genes and proteins and genetic engineering have allowed us to collect a great deal of information about folliculogenesis. For example, a few web pages (http://www.ncbi.nlm. nih.gov; http://mrg.genetics.washington.edu) provide access to databases of genomes, sequences of transcriptomes, and various tools for analyzing and discovering genes important in ovarian development. Formation of the antrum (tertiary follicle) is the final phase of folliculogenesis and the transition from intraovarian to extraovian regulation. This final step coordinates with the hypothalamic-pituitary-ovarian axis. On the other hand, currently, follicle physiology is under intense investigation, as little is known about how to overcome women's ovarian problems or how to develop competent oocytes from in vitro follicle culture or transplantation. In this review, some of the known roles of hormones and some of the genes involved in tertiary follicle growth and the general characteristics of tertiary follicles are summarized. In addition, in vitro culture of tertiary follicles is also discussed as a study model and an assisted reproductive technology model.
Keywords
Tertiary follicle; Growth; Folliculogenesis; In vitro follicle culture;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Touraine P, Beau I, Gougeon A, Meduri G, Desroches A, Pichard C, et al. New natural inactivating mutations of the follicle-stimulating hormone receptor: correlations between receptor function and phenotype. Mol Endocrinol 1999;13:1844-54.
2 Aguirre C, Jayes FC, Veldhuis JD. Luteinizing hormone (LH) drives diverse intracellular calcium second messenger signals in isolated porcine ovarian thecal cells: preferential recruitment of intracellular Ca2+ oscillatory cells by higher concentrations of LH. Endocrinology 2000;141:2220-8.
3 Filicori M, Cognigni GE, Samara A, Melappioni S, Perri T, Cantelli B, et al. The use of LH activity to drive folliculogenesis: exploring uncharted territories in ovulation induction. Hum Reprod Update 2002;8:543-57.
4 Kumar TR. Functional analysis of LHbeta knockout mice. Mol Cell Endocrinol 2007;269:81-4.
5 Zhang FP, Poutanen M, Wilbertz J, Huhtaniemi I. Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Mol Endocrinol 2001;15:172-83.
6 Medigovic I, Ristic N, Trifunovic S, Manojlovic-Stojanoski M, Milosevic V, Zikic D, et al. Genistein affects ovarian folliculogenesis: A stereological study. Microsc Res 2012 Aug 28 [Epub]. http:// dx.doi.org/10.1002/jemt.22117.
7 Korach KS, Emmen JM, Walker VR, Hewitt SC, Yates M, Hall JM, et al. Update on animal models developed for analyses of estrogen receptor biological activity. J Steroid Biochem Mol Biol 2003;86:387-91.
8 Lee S, Kang DW, Hudgins-Spivey S, Krust A, Lee EY, Koo Y, et al. Theca-specific estrogen receptor-alpha knockout mice lose fertility prematurely. Endocrinology 2009;150:3855-62.
9 Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P, Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 2000;127:4277-91.
10 Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci U S A 1998;95:6965-70.
11 Ito Y, Fisher CR, Conte FA, Grumbach MM, Simpson ER. Molecular basis of aromatase deficiency in an adult female with sexual infantilism and polycystic ovaries. Proc Natl Acad Sci U S A 1993;90:11673-7.
12 Shozu M, Akasofu K, Harada T, Kubota Y. A new cause of female pseudohermaphroditism: placental aromatase deficiency. J Clin Endocrinol Metab 1991;72:560-6.
13 Sharara FI, Nieman LK. Identification and cellular localization of growth hormone receptor gene expression in the human ovary. J Clin Endocrinol Metab 1994;79:670-2.
14 Zaczek D, Hammond J, Suen L, Wandji S, Service D, Bartke A, et al. Impact of growth hormone resistance on female reproductive function: new insights from growth hormone receptor knockout mice. Biol Reprod 2002;67:1115-24.
15 Ryan NK, Woodhouse CM, Van der Hoek KH, Gilchrist RB, Armstrong DT, Norman RJ. Expression of leptin and its receptor in the murine ovary: possible role in the regulation of oocyte maturation. Biol Reprod 2002;66:1548-54.
16 Chehab FF, Lim ME, Lu R. Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin. Nat Genet 1996;12:318-20.
17 Barkan D, Jia H, Dantes A, Vardimon L, Amsterdam A, Rubinstein M. Leptin modulates the glucocorticoid-induced ovarian steroidogenesis. Endocrinology 1999;140:1731-8.
18 Findlay JK. An update on the roles of inhibin, activin, and follistatin as local regulators of folliculogenesis. Biol Reprod 1993;48:15-23.
19 Zachow RJ, Magoffin DA. Direct intraovarian effects of leptin: impairment of the synergistic action of insulin-like growth factor-I on follicle-stimulating hormone-dependent estradiol-17 beta production by rat ovarian granulosa cells. Endocrinology 1997;138:847-50.
20 Sierra-Honigmann MR, Nath AK, Murakami C, Garcia-Cardena G, Papapetropoulos A, Sessa WC, et al. Biological action of leptin as an angiogenic factor. Science 1998;281:1683-6.
21 Hillier SG, Yong EL, Illingworth PJ, Baird DT, Schwall RH, Mason AJ. Effect of recombinant activin on androgen synthesis in cultured human thecal cells. J Clin Endocrinol Metab 1991;72:1206-11.
22 Matzuk MM, Kumar TR, Bradley A. Different phenotypes for mice deficient in either activins or activin receptor type II. Nature 1995;374:356-60.
23 Matzuk MM, Finegold MJ, Mishina Y, Bradley A, Behringer RR. Synergistic effects of inhibins and mullerian-inhibiting substance on testicular tumorigenesis. Mol Endocrinol 1995;9:1337-45.
24 Campbell BK, Baird DT. Inhibin A is a follicle stimulating hormoneresponsive marker of granulosa cell differentiation, which has both autocrine and paracrine actions in sheep. J Endocrinol 2001;169:333-45.
25 Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction 2006;132:191-206.
26 Schneyer AL, Fujiwara T, Fox J, Welt CK, Adams J, Messerlian GM, et al. Dynamic changes in the intrafollicular inhibin/activin/follistatin axis during human follicular development: relationship to circulating hormone concentrations. J Clin Endocrinol Metab 2000;85:3319-30.
27 Sadatsuki M, Tsutsumi O, Yamada R, Muramatsu M, Taketani Y. Local regulatory effects of activin A and follistatin on meiotic maturation of rat oocytes. Biochem Biophys Res Commun 1993; 196:388-95.
28 Schwall RH, Mason AJ, Wilcox JN, Bassett SG, Zeleznik AJ. Localization of inhibin/activin subunit mRNAs within the primate ovary. Mol Endocrinol 1990;4:75-9.
29 Arai KY, Kishi H, Onodera S, Jin W, Watanabe G, Suzuki AK, et al. Cyclic changes in messenger RNAs encoding inhibin/activin subunits in the ovary of the golden hamster (Mesocricetus auratus). J Endocrinol 2005;185:561-75.
30 Alak BM, Coskun S, Friedman CI, Kennard EA, Kim MH, Seifer DB. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil Steril 1998;70:1126-30.
31 Silva CC, Knight PG. Modulatory actions of activin-A and follistatin on the developmental competence of in vitro-matured bovine oocytes. Biol Reprod 1998;58:558-65.
32 Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002;124:601-9.
33 Sirotkin AV. Growth factors controlling ovarian functions. J Cell Physiol 2011;226:2222-5.
34 Wandji SA, Wood TL, Crawford J, Levison SW, Hammond JM. Expression of mouse ovarian insulin growth factor system components during follicular development and atresia. Endocrinology 1998;139:5205-14.
35 Zhou Y, Kato H, Asanoma K, Kondo H, Arima T, Kato K, et al. Identification of FOXC1 as a TGF-beta1 responsive gene and its involvement in negative regulation of cell growth. Genomics 2002;80:465-72.
36 Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature 1997;385:525-9.
37 Mattiske D, Kume T, Hogan BL. The mouse forkhead gene Foxc1 is required for primordial germ cell migration and antral follicle development. Dev Biol 2006;290:447-58.
38 Juneja SC, Barr KJ, Enders GC, Kidder GM. Defects in the germ line and gonads of mice lacking connexin43. Biol Reprod 1999;60:1263-70.
39 Kidder GM, Mhawi AA. Gap junctions and ovarian folliculogenesis. Reproduction 2002;123:613-20.
40 Otsuka F, Moore RK, Shimasaki S. Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J Biol Chem 2001;276:32889-95.
41 Wrathall JH, Knight PG. Effects of inhibin-related peptides and oestradiol on androstenedione and progesterone secretion by bovine theca cells in vitro. J Endocrinol 1995;145:491-500.
42 Souza CJ, Campbell BK, McNeilly AS, Baird DT. 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 2002;123:363-9.
43 Otsuka F. Multiple endocrine regulation by bone morphogenetic protein system. Endocr J 2010;57:3-14.
44 Erickson GF, Shimasaki S. The role of the oocyte in folliculogenesis. Trends Endocrinol Metab 2000;11:193-8.
45 Lee WS, Otsuka F, Moore RK, Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod 2001;65:994-9.
46 Nilsson EE, Doraiswamy V, Skinner MK. Transforming growth factor- beta isoform expression during bovine ovarian antral follicle development. Mol Reprod Dev 2003;66:237-46.
47 Pierre A, Pisselet C, Dupont J, Mandon-Pepin B, Monniaux D, Monget P, et al. Molecular basis of bone morphogenetic protein-4 inhibitory action on progesterone secretion by ovine granulosa cells. J Mol Endocrinol 2004;33:805-17.
48 Pierre A, Pisselet C, Dupont J, Bontoux M, Monget P. Bone morphogenetic protein 5 expression in the rat ovary: biological effects on granulosa cell proliferation and steroidogenesis. Biol Reprod 2005;73:1102-8.
49 Pangas SA, Jorgez CJ, Matzuk MM. Growth differentiation factor 9 regulates expression of the bone morphogenetic protein antagonist gremlin. J Biol Chem 2004;279:32281-6.
50 Dunkel L, Tilly JL, Shikone T, Nishimori K, Hsueh AJ. Follicle-stimulating hormone receptor expression in the rat ovary: increases during prepubertal development and regulation by the opposing actions of transforming growth factors beta and alpha. Biol Reprod 1994;50:940-8.
51 Drummond AE, Dyson M, Thean E, Groome NP, Robertson DM, Findlay JK. Temporal and hormonal regulation of inhibin protein and subunit mRNA expression by post-natal and immature rat ovaries. J Endocrinol 2000;166:339-54.
52 Fournet N, Weitsman SR, Zachow RJ, Magoffin DA. Transforming growth factor-beta inhibits ovarian 17 alpha-hydroxylase activity by a direct noncompetitive mechanism. Endocrinology 1996; 137:166-74.
53 Uzumcu M, Pan Z, Chu Y, Kuhn PE, Zachow R. Immunolocalization of the hepatocyte growth factor (HGF) system in the rat ovary and the anti-apoptotic effect of HGF in rat ovarian granulosa cells in vitro. Reproduction 2006;132:291-9.
54 Ota T, Choi KB, Gilks CB, Leung PC, Auersperg N. Cell type- and stage-specific changes in HOXA7 protein expression in human ovarian folliculogenesis: possible role of GDF-9. Differentiation 2006;74:1-10.
55 Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellve AR, et al. Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996;10:903-18.
56 Sicinski P, Donaher JL, Geng Y, Parker SB, Gardner H, Park MY, et al. Cyclin D2 is an FSH-responsive gene involved in gonadal cell proliferation and oncogenesis. Nature 1996;384:470-4.
57 Duggavathi R, Murphy BD. Development. Ovulation signals. Science 2009;324:890-1.
58 Sato E, Ishibashi T, Koide SS. Prevention of spontaneous degeneration of mouse oocytes in culture by ovarian glycosaminoglycans. Biol Reprod 1987;37:371-6.
59 Wang H, Jiang JY, Zhu C, Peng C, Tsang BK. Role and regulation of nodal/activin receptor-like kinase 7 signaling pathway in the control of ovarian follicular atresia. Mol Endocrinol 2006;20:2469-82.
60 Matsumoto K, Nakayama T, Sakai H, Tanemura K, Osuga H, Sato E, et al. Neuronal apoptosis inhibitory protein (NAIP) may enhance the survival of granulosa cells thus indirectly affecting oocyte survival. Mol Reprod Dev 1999;54:103-11.
61 Kezele P, Nilsson EE, Skinner MK. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod 2005;73:967-73.
62 Parrott JA, Skinner MK. Thecal cell-granulosa cell interactions involve a positive feedback loop among keratinocyte growth factor, hepatocyte growth factor, and Kit ligand during ovarian follicular development. Endocrinology 1998;139:2240-5.
63 Erickson GF, Shimasaki S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol 2003;1:9.
64 Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 2002;99:2890-4.
65 Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001;122:829-38.
66 Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 2004;82-83:431-46.
67 Vitt UA, Hsueh AJ. Stage-dependent role of growth differentiation factor-9 in ovarian follicle development. Mol Cell Endocrinol 2001;183:171-7.
68 Nilsson EE, Skinner MK. Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol Reprod 2002;67:1018-24.
69 Vitt UA, Hayashi M, Klein C, Hsueh AJ. 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 2000;62:370-7.
70 Yamamoto N, Christenson LK, McAllister JM, Strauss JF 3rd. Growth differentiation factor-9 inhibits 3'5'-adenosine monophosphatestimulated steroidogenesis in human granulosa and theca cells. J Clin Endocrinol Metab 2002;87:2849-56.
71 Elvin JA, Clark AT, Wang P, Wolfman NM, Matzuk MM. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol 1999;13:1035-48.
72 Otsuka F, Yao Z, Lee T, Yamamoto S, Erickson GF, Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 2000;275:39523-8.
73 Glister C, Richards SL, Knight PG. 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 2005;146:1883-92.
74 Otsuka F, Moore RK, Iemura S, Ueno N, Shimasaki S. Follistatin inhibits the function of the oocyte-derived factor BMP-15. Biochem Biophys Res Commun 2001;289:961-6.
75 Glister C, Kemp CF, Knight PG. 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 2004;127:239-54.
76 Di Pasquale E, Beck-Peccoz P, Persani L. Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am J Hum Genet 2004;75:106-11.
77 Moore RK, Otsuka F, Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem 2003;278:304-10.
78 Yi SE, LaPolt PS, Yoon BS, Chen JY, Lu JK, Lyons KM. The type I BMP receptor BmprIB is essential for female reproductive function. Proc Natl Acad Sci U S A 2001;98:7994-9.
79 Chang CL, Wang HS, Soong YK, Huang SY, Pai SY, Hsu SY. Regulation of oocyte and cumulus cell interactions by intermedin/adrenomedullin J Biol Chem 2011;286:43193-203.
80 Ackert CL, Gittens JE, O'Brien MJ, Eppig JJ, Kidder GM. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 2001;233:258-70.
81 Burghardt RC, Matheson RL. Gap junction amplification in rat ovarian granulosa cells. I. A direct response to follicle-stimulating hormone. Dev Biol 1982;94:206-15.
82 Granot I, Dekel N. Developmental expression and regulation of the gap junction protein and transcript in rat ovaries. Mol Reprod Dev 1997;47:231-9.
83 Sommersberg B, Bulling A, Salzer U, Frohlich U, Garfield RE, Amsterdam A, et al. Gap junction communication and connexin 43 gene expression in a rat granulosa cell line: regulation by folliclestimulating hormone. Biol Reprod 2000;63:1661-8.
84 Granot I, Dekel N. Phosphorylation and expression of connexin-43 ovarian gap junction protein are regulated by luteinizing hormone. J Biol Chem 1994;269:30502-9.hormone. J Biol Chem 1994;269:30502-9.
85 Granot I, Bechor E, Barash A, Dekel N. Connexin43 in rat oocytes: developmental modulation of its phosphorylation. Biol Reprod 2002;66:568-73.
86 Grondahl ML, Andersen CY, Bogstad J, Borgbo T, Boujida VH, Borup R. Specific genes are selectively expressed between cumulus and granulosa cells from individual human pre-ovulatory follicles. Mol Hum Reprod 2012 Aug 24 [Epub]. http://dx.doi.org/1093/molehr/gas035.
87 Eppig JJ, Schroeder AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod 1989;41:268-76.
88 Eppig JJ, O'Brien MJ. Development in vitro of mouse oocytes from primordial follicles. Biol Reprod 1996;54:197-207.
89 Oktem O, Oktay K. The role of extracellular matrix and activin-A in in vitro growth and survival of murine preantral follicles. Reprod Sci 2007;14:358-66.
90 Hovatta O, Silye R, Abir R, Krausz T, Winston RM. Extracellular matrix improves survival of both stored and fresh human primordial and primary ovarian follicles in long-term culture. Hum Reprod 1997;12:1032-6.
91 Desai N, Abdelhafez F, Calabro A, Falcone T. Three dimensional culture of fresh and vitrified mouse pre-antral follicles in a hyaluronan- based hydrogel: a preliminary investigation of a novel biomaterial for in vitro follicle maturation. Reprod Biol Endocrinol 2012;10:29.
92 Nation A, Selwood L. The production of mature oocytes from adult ovaries following primary follicle culture in a marsupial. Reproduction 2009;138:247-55.
93 Mousset-Simeon N, Jouannet P, Le Cointre L, Coussieu C, Poirot C. Comparison of three in vitro culture systems for maturation ofearly preantral mouse ovarian follicles. Zygote 2005;13:167-75.
94 Kreeger PK, Deck JW, Woodruff TK, Shea LD. The in vitro regulation of ovarian follicle development using alginate-extracellular matrix gels. Biomaterials 2006;27:714-23.
95 Lee S. Role of estrogen receptor alpha (ER$\alpha$) in the folliculogenesis [dissertation]. Seoul (KR): Sungshin Women's University; 2010.
96 Visser JA, Themmen AP. Anti-Mullerian hormone and folliculogenesis. Mol Cell Endocrinol 2005;234:81-6.
97 Faddy MJ, Gosden RG. A mathematical model of follicle dynamics in the human ovary. Hum Reprod 1995;10:770-5.
98 Faddy MJ, Gosden RG. A model conforming the decline in follicle numbers to the age of menopause in women. Hum Reprod 1996;11:1484-6.
99 Peters H. The development of the mouse ovary from birth to maturity. Acta Endocrinol (Copenh) 1969;62:98-116.
100 Burns KH, Matzuk MM. The application of gene ablation and related technologies to the study of ovarian function. In: Leung PC, Adashi EY, editors. The ovary. 2nd ed. London: Elsevier; 2004.p. 411-32.
101 Pepling ME, Spradling AC. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 2001;234:339-51.
102 Gougeon A. Regulation of ovarian follicular development in primates: facts and hypotheses. Endocr Rev 1996;17:121-55.
103 Chun SY, Eisenhauer KM, Minami S, Billig H, Perlas E, Hsueh AJ. Hormonal regulation of apoptosis in early antral follicles: folliclestimulating hormone as a major survival factor. Endocrinology 1996;137:1447-56.
104 Hansen KR, Knowlton NS, Thyer AC, Charleston JS, Soules MR, Klein NA. A new model of reproductive aging: the decline in ovarian non-growing follicle number from birth to menopause. Hum Reprod 2008;23:699-708.
105 Baerwald AR, Adams GP, Pierson RA. Ovarian antral folliculogenesis during the human menstrual cycle: a review. Hum Reprod Update 2012;18:73-91.
106 Rajkovic A, Rangas S, Matzuk MM. Follicular development: mouse, sheep, and human models. In: Knobil E, Neill JD, editors. Knobil and Neill's physiology of reproduction. 3rd ed. New York: Elsvier; 2006. p. 383-423.
107 Dorrington JH, Moon YS, Armstrong DT. Estradiol-17beta biosynthesis in cultured granulosa cells from hypophysectomized immature rats; stimulation by follicle-stimulating hormone. Endocrinology 1975;97:1328-31.
108 Matzuk MM, Finegold MJ, Su JG, Hsueh AJ, Bradley A. Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice. Nature 1992;360:313-9.
109 Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 2001;121:647-53.
110 Sato E, Kimura N, Yokoo M, Miyake Y, Ikeda JE. Morphodynamics of ovarian follicles during oogenesis in mice. Microsc Res Tech 2006;69:427-35.
111 Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, et al. Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 2002;16:1154-67.
112 Matzuk MM. Revelations of ovarian follicle biology from gene knockout mice. Mol Cell Endocrinol 2000;163:61-6.
113 Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, et al. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 2003;130:2253-61.
114 Thomas FH, Ethier JF, Shimasaki S, Vanderhyden BC. Follicle-stimulating hormone regulates oocyte growth by modulation of expression of oocyte and granulosa cell factors. Endocrinology 2005;146:941-9.
115 Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997;15:201-4.
116 Kumar TR, Low MJ, Matzuk MM. Genetic rescue of follicle-stimulating hormone beta-deficient mice. Endocrinology 1998;139:3289-95.
117 Yang Y, Balla A, Danilovich N, Sairam MR. Developmental and molecular aberrations associated with deterioration of oogenesis during complete or partial follicle-stimulating hormone receptor deficiency in mice. Biol Reprod 2003;69:1294-302.
118 Burns KH, Yan C, Kumar TR, Matzuk MM. Analysis of ovarian gene expression in follicle-stimulating hormone beta knockout mice. Endocrinology 2001;142:2742-51.
119 Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellve AR, et al. Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996;10:903-18.
120 Zhou J, Kumar TR, Matzuk MM, Bondy C. Insulin-like growth factor I regulates gonadotropin responsiveness in the murine ovary. Mol Endocrinol 1997;11:1924-33.
121 Layman LC. Mutations in the follicle-stimulating hormone-beta (FSH beta) and FSH receptor genes in mice and humans. Semin Reprod Med 2000;18:5-10.