Regulation of the ovarian reserve by members of the transforming growth factor beta family

Molecular Reproduction and Development

Volumn 79, Issue 10, 2012, Pages 666-679

  Pangas, Stephanie A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; FOLLISTATIN; GREMLIN; GROWTH DIFFERENTIATION FACTOR 9; INHIBIN; INHIBIN A; MUELLERIAN INHIBITING FACTOR; OSTEOGENIC PROTEIN 1; SMAD1 PROTEIN; SMAD5 PROTEIN; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3; UNCLASSIFIED DRUG;

ARTICLE; DEVELOPMENTAL STAGE; EMBRYO DEVELOPMENT; ENVIRONMENTAL FACTOR; GESTATION PERIOD; KNOCKOUT MOUSE; NONHUMAN; OOCYTE; OVARIAN RESERVE; OVARY DEVELOPMENT; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; OVARY INSUFFICIENCY; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; REGULATORY MECHANISM;

ANIMALS; FEMALE; HUMANS; MICE; MICE, KNOCKOUT; OVARIAN FOLLICLE; TRANSFORMING GROWTH FACTOR BETA;

MUS;

EID: 84867638397     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.22076     Document Type: Article

References (165)

1. Adhikari D, Liu K. 2009. Molecular mechanisms underlying the activation of mammalian primordial follicles. Endocr Rev 30:438-464.
2. Arango NA, Kobayashi A, Wang Y, Jamin SP, Lee HH, Orvis GD, Behringer RR. 2008. A mesenchymal perspective of Mullerian duct differentiation and regression in Amhr2-lacZ mice. Mol Reprod Dev 75:1154-1162.
3. Baarends WM, Uilenbroek JT, Kramer P, Hoogerbrugge JW, van Leeuwen EC, Themmen AP, Grootegoed JA. 1995. Anti-mullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology 136:4951-4962.
4. Baker T. 1963. A quantitative and cytological study of germ cells in human ovaries. Proc R Soc Lond B 158:417-433.
5. Balemans W, Van Hul W. 2002. Extracellular regulation of BMP signaling in vertebrates: A cocktail of modulators. Dev Biol 250:231-250.
6. Behringer RR, Finegold MJ, Cate RL. 1994. Müllerian-inhibiting substance function during mammalian sexual development. Cell 79:415-425.
7. Block E. 1952. Quantitative morphological investigations of the follicular system in women; variations at different ages. Acta Anat (Basel) 14:108-123.
8. Boerboom D, Paquet M, Hsieh M, Liu J, Jamin SP, Behringer RR, Sirois J, Taketo MM, Richards JS. 2005. Misregulated Wnt/beta-catenin signaling leads to ovarian granulosa cell tumor development. Cancer Res 65:9206-9215.
9. Bouilly J, Bachelot A, Broutin I, Touraine P, Binart N. 2011. Novel NOBOX loss-of-function mutations account for 6.2% of cases in a large primary ovarian insufficiency cohort. Hum Mutat 32:1108-1113.
10. Brown CW, Houston-Hawkins DE, Woodruff TK, Matzuk MM. 2000. Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions. Nat Genet 25:453-457.
11. Byskov AG, Hoyer PE, Yding Andersen C, Kristensen SG, Jespersen A, Mollgard K. 2011. No evidence for the presence of oogonia in the human ovary after their final clearance during the first two years of life. Hum Reprod 26:2129-2139.
12. Carlsson IB, Scott JE, Visser JA, Ritvos O, Themmen AP, Hovatta O. 2006. Anti-Mullerian hormone inhibits initiation of growth of human primordial ovarian follicles in vitro. Hum Reprod 21:2223-2227.
13. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. 2003. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 301:215-218.
14. Chang H, Matzuk MM. 2001. Smad5 is required for mouse primordial germ cell development. Mech Dev 104:61-67.
15. Chang H, Brown CW, Matzuk MM. 2002. Genetic analysis of the mammalian TGF-β superfamily. Endocr Rev 23:787-823.
16. Chang HL, Pieretti-Vanmarcke R, Nicolaou F, Li X, Wei X, MacLaughlin DT, Donahoe PK. 2011. Mullerian inhibiting substance inhibits invasion and migration of epithelial cancer cell lines. Gynecol Oncol 120:128-134.
17. Chen D, Zhao M, Mundy GR. 2004. Bone morphogenetic proteins. Growth Factors 22:233-241.
18. Childs AJ, Anderson RA. 2009. Activin A selectively represses expression of the membrane-bound isoform of Kit ligand in human fetal ovary. Fertil Steril 92:1416-1419.
19. Childs AJ, Kinnell HL, Collins CS, Hogg K, Bayne RA, Green SJ, McNeilly AS, Anderson RA. 2010. BMP signaling in the human fetal ovary is developmentally regulated and promotes primordial germ cell apoptosis. Stem Cells 28:1368-1378.
20. Coerver KA, Woodruff TK, Finegold MJ, Mather J, Bradley A, Matzuk MM. 1996. Activin signaling through activin receptor type II causes the cachexia-like symptoms in inhibin-deficient mice. Mol Endocrinol 10:534-543.
21. Coutts SM, Childs AJ, Fulton N, Collins C, Bayne RA, McNeilly AS, Anderson RA. 2008. Activin signals via SMAD2/3 between germ and somatic cells in the human fetal ovary and regulates kit ligand expression. Dev Biol 314:189-199.
22. Da Silva-Buttkus P, Marcelli G, Franks S, Stark J, Hardy K. 2009. Inferring biological mechanisms from spatial analysis: Prediction of a local inhibitor in the ovary. Proc Natl Acad Sci USA 106:456-461.
23. Davies M, Moore V, Willson K, Van Essen P, Priest K, Scott H, Haan E, Chan A. 2012. Reproductive technologies and the risk of birth defects. NEJM 336:1803-1813.
24. De Felici M, Lobascio AM, Klinger FG. 2008. Cell death in fetal oocytes: Many players for multiple pathways. Autophagy 4:240-242.
25. de Sousa Lopes SM, Roelen BA, Monteiro RM, Emmens R, Lin HY, Li E, Lawson KA, Mummery CL. 2004. BMP signaling mediated by ALK2 in the visceral endoderm is necessary for the generation of primordial germ cells in the mouse embryo. Genes Dev 18:1838-1849.
26. De Vos M, Devroey P, Fauser BC. 2010. Primary ovarian insufficiency. Lancet 376:911-921.
27. Derynck R, Chen RH, Ebner R, Filvaroff EH, Lawler S. 1994. An emerging complexity of receptors for transforming growth factor-beta. Princess Takamatsu Symp 24:264-275.
28. Diaz FJ, Wigglesworth K, Eppig JJ. 2007. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120:1330-1340.
29. Dickson MC, Martin JS, Cousins FM, Kulkarni AB, Karlsson S, Akhurst RJ. 1995. Defective haematopoiesis and vasculogenesis in transforming growth factor-beta 1 knock out mice. Development 121:1845-1854.
30. Dissen GA, Romero C, Hirshfield AN, Ojeda SR. 2001. Nerve growth factor is required for early follicular development in the mammalian ovary. Endocrinology 142:2078-2086.
31. Dole G, Nilsson EE, Skinner MK. 2008. Glial-derived neurotrophic factor promotes ovarian primordial follicle development and cell-cell interactions during folliculogenesis. Reproduction 135:671-682.
32. 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.
33. Dudley BM, Runyan C, Takeuchi Y, Schaible K, Molyneaux K. 2007. BMP signaling regulates PGC numbers and motility in organ culture. Mech Dev 124:68-77.
34. Durcova-Hills G, Capel B. 2008. Development of germ cells in the mouse. Curr Top Dev Biol 83:185-212.
35. 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.
36. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, Uilenbroek JT, Grootegoed JA, Themmen AP. 2002a. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 143:1076-1084.
37. Durlinger AL, Visser JA, Themmen AP. 2002b. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 124:601-609.
38. Edson MA, Nagaraja AK, Matzuk MM. 2009. The mammalian ovary from genesis to revelation. Endocr Rev 30:624-712.
39. Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM. 1999. Molecular characterization of the follicle defects in the growth differentiation factor-9-deficient ovary. Mol Endocrinol 13:1018-1034.
40. Elvin JA, Yan C, Matzuk MM. 2000. Oocyte-expressed TGF-β superfamily members in female fertility. Mol Cell Endocrinol 159:1-5.
41. Emery Thompson M, Jones JH, Pusey AE, Brewer-Marsden S, Goodall J, Marsden D, Matsuzawa T, Nishida T, Reynolds V, Sugiyama Y, Wrangham RW. 2007. Aging and fertility patterns in wild chimpanzees provide insights into the evolution of menopause. Curr Biol 17:2150-2156.
42. Ewen KA, Koopman P. 2010. Mouse germ cell development: from specification to sex determination. Mol Cell Endocrinol 323:76-93.
43. Faddy MJ. 2000. Follicle dynamics during ovarian ageing. Mol Cell Endocrinol 163:43-48.
44. Faddy MJ, Gosden RG, Gougeon A, Richardson SJ, Nelson JF. 1992. Accelerated disappearance of ovarian follicles in mid-life: Implications for forecasting menopause. Hum Reprod 7:1342-1346.
45. Fan HY, Liu Z, Paquet M, Wang J, Lydon JP, DeMayo FJ, Richards JS. 2009. Cell type-specific targeted mutations of Kras and Pten document proliferation arrest in granulosa cells versus oncogenic insult to ovarian surface epithelial cells. Cancer Res 69:6463-6472.
46. Fenwick MA, Mansour YT, Franks S, Hardy K. 2011. Identification and regulation of bone morphogenetic protein antagonists associated with preantral follicle development in the ovary. Endocrinology 15:3515-3526.
47. Flaws JA, Hirshfield AN, Hewitt JA, Babus JK, Furth PA. 2001. Effect of bcl-2 on the primordial follicle endowment in the mouse ovary. Biol Reprod 64:1153-1159.
48. Fulton N, Martins da Silva SJ, Bayne RA, Anderson RA. 2005. Germ cell proliferation and apoptosis in the developing human ovary. J Clin Endocrinol Metab 90:4664-4670.
49. Gazzerro E, Canalis E. 2006. Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord 7:51-65.
50. Gomperts M, Garcia-Castro M, Wylie C, Heasman J. 1994. Interactions between primordial germ cells play a role in their migration in mouse embryos. Development 120:135-141.
51. Gosden RG, Faddy MJ. 1998. Biological bases of premature ovarian failure. Reprod Fertil Dev 10:73-78.
52. Gougeon A. 1996. Ovarian follicular growth in humans: ovarian aging and populations of growing follicles. Endocr Rev 17:121-155.
53. Guo J, Wu G. 2012. The signaling and functions of heterodimeric bone morphogenetic proteins. Cytokine Growth Factor Rev 23:61-67.
54. Hammond SS, Matin A. 2009. Tools for the genetic analysis of germ cells. Genesis 47:617-627.
55. Hayashi K, Kobayashi T, Umino T, Goitsuka R, Matsui Y, Kitamura D. 2002. SMAD1 signaling is critical for initial commitment of germ cell lineage from mouse epiblast. Mech Dev 118:99-109.
56. Hill CS. 2009. Nucleocytoplasmic shuttling of Smad proteins. Cell Res 19:36-46.
57. Hutt KJ, McLaughlin EA, Holland MK. 2006. Kit ligand and c-Kit have diverse roles during mammalian oogenesis and folliculogenesis. Mol Hum Reprod 12:61-69.
58. Jagarlamudi K, Liu L, Adhikari D, Reddy P, Idahl A, Ottander U, Lundin E, Liu K. 2009. Oocyte-specific deletion of Pten in mice reveals a stage-specific function of PTEN/PI3K signaling in oocytes in controlling follicular activation. PLoS ONE 4:e6186.
59. Jamin SP, Arango NA, Mishina Y, Hanks MC, Behringer RR. 2002. Requirement of Bmpr1a for Mullerian duct regression during male sexual development. Nat Genet 7:7.
60. John GB, Gallardo TD, Shirley LJ, Castrillon DH. 2008. Foxo3 is a PI3K-dependent molecular switch controlling the initiation of oocyte growth. Dev Biol 321:197-204.
61. John GB, Shidler MJ, Besmer P, Castrillon DH. 2009. Kit signaling via PI3K promotes ovarian follicle maturation but is dispensable for primordial follicle activation. Dev Biol 331:292-299.
62. Jorgez CJ, Klysik M, Jamin SP, Behringer RR, Matzuk MM. 2004. Granulosa cell-specific inactivation of follistatin causes female fertility defects. Mol Endocrinol 18:953-967.
63. Josso N, Picard JY, Rey R, di Clemente N. 2006. Testicular anti-Mullerian hormone: History, genetics, regulation and clinical applications. Pediatr Endocrinol Rev 3:347-358.
64. Joyce IM, Clark AT, Pendola FL, Eppig JJ. 2000. Comparison of recombinant growth differentiation factor-9 and oocyte regulation of KIT ligand messenger ribonucleic acid expression in mouse ovarian follicles. Biol Reprod 63:1669-1675.
65. Kaartinen V, Voncken JW, Shuler C, Warburton D, Bu D, Heisterkamp N, Groffen J. 1995. Abnormal lung development and cleft palate in mice lacking TGF-beta 3 indicates defects of epithelial-mesenchymal interaction. Nat Genet 11:415-421.
66. Kezele P, Nilsson EE, Skinner MK. 2005. Keratinocyte growth factor acts as a mesenchymal factor that promotes ovarian primordial to primary follicle transition. Biol Reprod 73:967-973.
67. Khokha MK, Hsu D, Brunet LJ, Dionne MS, Harland RM. 2003. Gremlin is the BMP antagonist required for maintenance of Shh and Fgf signals during limb patterning. Nat Genet 34:303-307.
68. Kimura F, Sidis Y, Bonomi L, Xia Y, Schneyer A. 2010. The follistatin-288 isoform alone is sufficient for survival but not for normal fertility in mice. Endocrinology 151:1310-1319.
69. Kimura F, Bonomi LM, Schneyer AL. 2011. Follistatin regulates germ cell nest breakdown and primordial follicle formation. Endocrinology 152:697-706.
70. Kissel H, Timokhina I, Hardy MP, Rothschild G, Tajima Y, Soares V, Angeles M, Whitlow SR, Manova K, Besmer P. 2000. Point mutation in kit receptor tyrosine kinase reveals essential roles for kit signaling in spermatogenesis and oogenesis without affecting other kit responses. EMBO J 19:1312-1326.
71. Knight PG, Glister C. 2006. TGF-beta superfamily members and ovarian follicle development. Reproduction 132:191-206.
72. Kodaman PH. 2010. Early menopause: Primary ovarian insufficiency and surgical menopause. Semin Reprod Med 28:360-369.
73. Kulkarni AB, Huh CG, Becker D, Geiser A, Lyght M, Flanders KC, Roberts AB, Sporn MB, Ward JM, Karlsson S. 1993. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc Natl Acad Sci USA 90:770-774.
74. Kurilo LF. 1981. Oogenesis in antenatal development in man. Hum Genet 57:86-92.
75. La Marca A, Volpe A. 2006. Anti-Mullerian hormone (AMH) in female reproduction: Is measurement of circulating AMH a useful tool? Clin Endocrinol (Oxf) 64:603-610.
76. Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, Wright CV, Korving JP, Hogan BL. 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev 13:424-436.
77. Le Bouffant R, Guerquin MJ, Duquenne C, Frydman N, Coffigny H, Rouiller-Fabre V, Frydman R, Habert R, Livera G. 2010. Meiosis initiation in the human ovary requires intrinsic retinoic acid synthesis. Hum Reprod 25:2579-2590.
78. Ledger WL. 2010. Clinical utility of measurement of anti-mullerian hormone in reproductive endocrinology. J Clin Endocrinol Metab 95:5144-5154.
79. Lee WS, Yoon SJ, Yoon TK, Cha KY, Lee SH, Shimasaki S, Lee S, Lee KA. 2004. Effects of bone morphogenetic protein-7 (BMP-7) on primordial follicular growth in the mouse ovary. Mol Reprod Dev 69:159-163.
80. Li J, Kawamura K, Cheng Y, Liu S, Klein C, Duan EK, Hsueh AJ. 2010. Activation of dormant ovarian follicles to generate mature eggs. Proc Natl Acad Sci USA 107:10280-10284.
81. Liu L, Rajareddy S, Reddy P, Du C, Jagarlamudi K, Shen Y, Gunnarsson D, Selstam G, Boman K, Liu K. 2007. Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a. Development 134:199-209.
82. Liu CF, Liu C, Yao HH. 2010a. Building pathways for ovary organogenesis in the mouse embryo. Curr Top Dev Biol 90:263-290.
83. Liu CF, Parker K, Yao HH. 2010b. WNT4/beta-catenin pathway maintains female germ cell survival by inhibiting activin betaB in the mouse fetal ovary. PLoS ONE 5:e10382.
84. Loh JS, Maheshwari A. 2011. Anti-Mullerian hormone-Is it a crystal ball for predicting ovarian ageing? Hum Reprod 26:2925-2932.
85. Marino R, Misra M. 2011. Bone health in primary ovarian insufficiency. Semin Reprod Med 29:317-327.
86. Martins da Silva SJ, Bayne RA, Cambray N, Hartley PS, McNeilly AS, Anderson RA. 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.
87. Massagué J. 1998. TGF-beta signal transduction. Annu Rev Biochem 67:753-791.
88. Matzuk M, Finegold M, Su J, Hsueh A, Bradley A. 1992. α-Inhibin is a tumor-suppressor gene with gonadal specificity in mice. Nature 360:313-319.
89. Matzuk MM, Kumar TR, Vassalli A, Bickenbach JR, Roop DR, Jaenisch R, Bradley A. 1995a. Functional analysis of activins in mammalian development. Nature 374:354-356.
90. Matzuk MM, Lu H, Vogel H, Sellheyer K, Roop DR, Bradley A. 1995b. Multiple defects and perinatally death in mice deficient in follistatin. Nature 372:360-363.
91. McGee EA, Hsueh AJ. 2000. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 21:200-214.
92. McLaren A. 2000. Germ and somatic cell lineages in the developing gonad. Mol Cell Endocrinol 163:3-9.
93. Memon MA, Anway MD, Covert TR, Uzumcu M, Skinner MK. 2008. Transforming growth factor beta (TGFbeta1, TGFbeta2 and TGFbeta3) null-mutant phenotypes in embryonic gonadal development. Mol Cell Endocrinol 294:70-80.
94. Michos O, Panman L, Vintersten K, Beier K, Zeller R, Zuniga A. 2004. Gremlin-mediated BMP antagonism induces the epithelial-mesenchymal feedback signaling controlling metanephric kidney and limb organogenesis. Development 131:3401-3410.
95. Michos O, Goncalves A, Lopez-Rios J, Tiecke E, Naillat F, Beier K, Galli A, Vainio S, Zeller R. 2007. Reduction of BMP4 activity by gremlin 1 enables ureteric bud outgrowth and GDNF/WNT11 feedback signalling during kidney branching morphogenesis. Development 134:2397-2405.
96. Miyazawa K, Williams DA, Gotoh A, Nishimaki J, Broxmeyer HE, Toyama K. 1995. Membrane-bound Steel factor induces more persistent tyrosine kinase activation and longer life span of c-kit gene-encoded protein than its soluble form. Blood 85:641-649.
97. Molyneaux K, Wylie C. 2004. Primordial germ cell migration. Int J Dev Biol 48:537-544.
98. Monget P, Bobe J, Gougeon A, Fabre S, Monniaux D, Dalbies-Tran R. 2011. The ovarian reserve in mammals: A functional and evolutionary perspective. Mol Cell Endocrinol 356:2-12.
99. Mork L, Maatouk DM, McMahon JA, Guo JJ, Zhang P, McMahon AP, Capel B. 2012a. Temporal Differences in Granulosa Cell Specification in the Ovary Reflect Distinct Follicle Fates in Mice. Biol Reprod 86:1-9.
100. Mork L, Tang H, Batchvarov I, Capel B. 2012b. Mouse germ cell clusters form by aggregation as well as clonal divisions. Mech Dev 128:591-596.
101. Murabito JM, Yang Q, Fox C, Wilson PW, Cupples LA. 2005a. Heritability of age at natural menopause in the Framingham Heart Study. J Clin Endocrinol Metab 90:3427-3430.
102. Murabito JM, Yang Q, Fox CS, Cupples LA. 2005b. Genome-wide linkage analysis to age at natural menopause in a community-based sample: The Framingham Heart Study. Fertil Steril 84:1674-1679.
103. Myers M, Middlebrook BS, Matzuk MM, Pangas SA. 2009. Loss of inhibin alpha uncouples oocyte-granulosa cell dynamics and disrupts postnatal folliculogenesis. Dev Biol 334:458-467.
104. Myers M, Tripurani SK, Middlebrook B, Economides AN, Canalis E, Pangas SA. 2011. Loss of gremlin delays primordial follicle assembly but does not affect female fertility in mice. Biol Reprod 85:1175-1182.
105. Nelson SM, Anderson RA, Broekmans FJ, Raine-Fenning N, Fleming R, La Marca A. 2012. Anti-Mullerian hormone: clairvoyance or crystal clear? Hum Reprod 27:631-636.
106. Nilsson EE, Skinner MK. 2003. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 69:1265-1272.
107. Nilsson EE, Detzel C, Skinner MK. 2006. Platelet-derived growth factor modulates the primordial to primary follicle transition. Reproduction 131:1007-1015.
108. Nilsson EE, Schindler R, Savenkova MI, Skinner MK. 2011. Inhibitory actions of anti-Mullerian hormone (AMH) on ovarian primordial follicle assembly. PLoS ONE 6:e20087.
109. Otsuka F, 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.
110. Pangas SA. 2011. Bone morphogenetic protein signaling transcription factor (SMAD) function in granulosa cells. Mol Cell Endocrinol 356:40-47.
111. Pangas S, Matzuk MM. 2008. The TGF-B family in the reproductive tract. In: Derynck, R, Miyazono, K, editors. The TGF-beta family. Cold Spring Harbor: Cold Spring Harbor Laboratory Press. pp 861-888.
112. Pangas SA, Li X, Robertson EJ, Matzuk MM. 2006. Premature luteinization and cumulus cell defects in ovarian-specific Smad4 knockout mice. Mol Endocrinol 20:1406-1422.
113. Pangas SA, Jorgez CJ, Tran M, Agno J, Li X, Brown CW, Kumar TR, Matzuk MM. 2007. Intraovarian activins are required for female fertility. Mol Endocrinol 21:2458-2471.
114. Paredes A, Garcia-Rudaz C, Kerr B, Tapia V, Dissen GA, Costa ME, Cornea A, Ojeda SR. 2005. Loss of synaptonemal complex protein-1, a synaptonemal complex protein, contributes to the initiation of follicular assembly in the developing rat ovary. Endocrinology 146:5267-5277.
115. Pepling ME, Spradling AC. 1998. Female mouse germ cells form synchronously dividing cysts. Development 125:3323-3328.
116. Pepling ME, Spradling AC. 2001. Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles. Dev Biol 234:339-351.
117. Pepling ME, Sundman EA, Patterson NL, Gephardt GW, Medico L, Jr., Wilson KI. 2010. Differences in oocyte development and estradiol sensitivity among mouse strains. Reproduction 139:349-357.
118. Persani L, Rossetti R, Cacciatore C, Fabre S. 2011. Genetic defects of ovarian TGF-beta-like factors and premature ovarian failure. J Endocrinol Invest 34:244-251.
119. Peters H. 1979. Some aspects of early follicular development. In: Midgley A, Sadler W, editors. Ovarian follicular development and function. New York: Raven Press. pp 1-13.
120. Proetzel G, Pawlowski SA, Wiles MV, Yin M, Boivin GP, Howles PN, Ding J, Ferguson MW, Doetschman T. 1995. Transforming growth factor-beta 3 is required for secondary palate fusion. Nat Genet 11:409-414.
121. Qin Y, Shi Y, Zhao Y, Carson SA, Simpson JL, Chen ZJ. 2009. Mutation analysis of NOBOX homeodomain in Chinese women with premature ovarian failure. Fertil Steril 91:1507-1509.
122. Rajkovic A, Pangas SA, Ballow D, Suzumori N, Matzuk MM. 2004. NOBOX deficiency disrupts early folliculogenesis and oocyte-specific gene expression. Science 305:1157-1159.
123. Reddy P, Liu L, Adhikari D, Jagarlamudi K, Rajareddy S, Shen Y, Du C, Tang W, Hamalainen T, Peng SL, Lan ZJ, Cooney AJ, Huhtaniemi I, Liu K. 2008. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 319:611-613.
124. Richards JS, Pangas SA. 2010. The ovary: Basic biology and clinical implications. J Clin Invest 120:963-972.
125. Richardson BE, Lehmann R. 2010. Mechanisms guiding primordial germ cell migration: strategies from different organisms. Nat Rev Mol Cell Biol 11:37-49.
126. Robbins AM, Robbins MM, Gerald-Steklis N, Steklis HD. 2006. Age-related patterns of reproductive success among female mountain gorillas. Am J Phys Anthropol 131:511-521.
127. Rodrigues P, Limback D, McGinnis LK, Plancha CE, Albertini DF. 2009. Multiple mechanisms of germ cell loss in the perinatal mouse ovary. Reproduction 137:709-720.
128. Rosairo D, Kuyznierewicz I, Findlay J, Drummond A. 2008. Transforming growth factor-beta: Its role in ovarian follicle development. Reproduction 136:799-809.
129. Ross A, Munger S, Capel B. 2007. Bmp7 regulates germ cell proliferation in mouse fetal gonads. Sex Dev 1:127-137.
130. Sadeu JC, Adriaenssens T, Smitz J. 2008. Expression of growth differentiation factor 9, bone morphogenetic protein 15, and anti-Mullerian hormone in cultured mouse primary follicles. Reproduction 136:195-203.
131. Salmon NA, Handyside AH, Joyce IM. 2004. Oocyte regulation of anti-Mullerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev Biol 266:201-208.
132. Sanford LP, Ormsby I, Gittenberger-de Groot AC, Sariola H, Friedman R, Boivin GP, Cardell EL, Doetschman T. 1997. TGFbeta2 knockout mice have multiple developmental defects that are non-overlapping with other TGFbeta knockout phenotypes. Development 124:2659-2670.
133. Schneyer AL, Rzucidlo DA, Sluss PM, Crowley J, W F. 1994. Characterization of unique binding kinetics of follistatin and activin or inhibin in serum. Endocrinology 135:667-674.
134. Shimasaki S, Zachow RJ, Li D, Kim H, Iemura S-I, Ueno N, Sampath K, Chang RJ, Erickson GF. 1999. A functional bone morphogenetic protein system in the ovary. Proc Natl Acad Sci USA 96:7282-7287.
135. Shull MM, Ormsby I, Kier AB, Pawlowski S, Diebold RJ, Yin M, Allen R, Sidman C, Proetzel G, Calvin D, Annunziata N, Doetschman T. 1992. Targeted disruption of the mouse transforming growth factor-β1 gene results in multifocal inflammatory disease. Nature 359:693-699.
136. Sidis Y, Mukherjee A, Keutmann H, Delbaere A, Sadatsuki M, Schneyer A. 2006. Biological activity of follistatin isoforms and follistatin-like-3 is dependent on differential cell surface binding and specificity for activin, myostatin, and bone morphogenetic proteins. Endocrinology 147:3586-3597.
137. Snieder H, MacGregor AJ, Spector TD. 1998. Genes control the cessation of a woman's reproductive life: A twin study of hysterectomy and age at menopause. J Clin Endocrinol Metab 83:1875-1880.
138. Soyal SM, Amleh A, Dean J. 2000. FIGα, a germ cell-specific transcription factor required for ovarian follicle formation. Development 127:4645-4654.
139. Sugiura K, Su YQ, Eppig JJ. 2010. Does bone morphogenetic protein 6 (BMP6) affect female fertility in the mouse? Biol Reprod 83:997-1004.
140. Sun QY, Liu K, Kikuchi K. 2008. Oocyte-specific knockout: a novel in vivo approach for studying gene functions during folliculogenesis, oocyte maturation, fertilization, and embryogenesis. Biol Reprod 79:1014-1020.
141. Telfer E, Torrance C, Gosden RG. 1990. Morphological study of cultured preantral ovarian follicles of mice after transplantation under the kidney capsule. J Reprod Fertil 89:565-571.
142. Thompson TB, Lerch TF, Cook RW, Woodruff TK, Jardetzky TS. 2005. The structure of the follistatin:activin complex reveals antagonism of both type I and type II receptor binding. Dev Cell 9:535-543.
143. Tingen C, Kim A, Woodruff TK. 2009a. The primordial pool of follicles and nest breakdown in mammalian ovaries. Mol Hum Reprod 15:795-803.
144. Tingen CM, Bristol-Gould SK, Kiesewetter SE, Wellington JT, Shea L, Woodruff TK. 2009b. Prepubertal primordial follicle loss in mice is not due to classical apoptotic pathways. Biol Reprod 81:16-25.
145. van den Berg SM, Boomsma DI. 2007. The familial clustering of age at menarche in extended twin families. Behav Genet 37:661-667.
146. van Houten EL, Themmen AP, Visser JA. 2010. Anti-Mullerian hormone (AMH): Regulator and marker of ovarian function. Ann Endocrinol (Paris) 71:191-197.
147. Vassalli A, Matzuk MM, Gardner H, Lee K, Jaenisch R. 1994. Activin/inhibin βB subunit gene disruption leads to defects in eyelid development and female reproduction. Genes Dev 8:414-427.
148. Vogel G. 2012. Reproductive biology. Potential egg stem cells reignite debate. Science 335:1029-1030.
149. Wellons M. 2011. Cardiovascular disease and primary ovarian insufficiency. Semin Reprod Med 29:328-341.
150. White YA, Woods DC, Takai Y, Ishihara O, Seki H, Tilly JL. 2012. Oocyte formation by mitotically active germ cells purified from ovaries of reproductive-age women. Nat Med 18:413-421.
151. Wiater E, Vale W. 2008. Activins and Inhibins. In: Miyazono K, Derynk R, editors. The TGF-B Family. New York: Cold Spring Harbor Press. pp 79-120.
152. Wich SA, Utami-Atmoko SS, Setia TM, Rijksen HD, Schurmann C, van Hooff JA, van Schaik CP. 2004. Life history of wild Sumatran orangutans (Pongo abelii). J Hum Evol 47:385-398.
153. Wordinger RJ, Zode G, Clark AF. 2008. Focus on molecules: Gremlin. Exp Eye Res 87:78-79.
154. Yan C, Wang P, DeMayo J, DeMayo F, Elvin J, Carino C, Prasad S, Skinner S, Dunbar B, Dube J, Celeste A, Matzuk M. 2001. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 15:854-866.
155. Yao HH, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A, Capel B. 2004. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn 230:210-215.
156. Yao HH, Aardema J, Holthusen K. 2006. Sexually dimorphic regulation of inhibin beta B in establishing gonadal vasculature in mice. Biol Reprod 74:978-983.
157. Ying Y, Zhao GQ. 2001. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol 232:484-492.
158. Yuan QA, Simmons HH, Robinson MK, Russeva M, Marasco WA, Adams GP. 2006. Development of engineered antibodies specific for the Mullerian inhibiting substance type II receptor: A promising candidate for targeted therapy of ovarian cancer. Mol Cancer Ther 5:2096-2105.
159. Zhang H, Bradley A. 1996. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122:2977-2986.
160. Zhang H, Zheng W, Shen Y, Adhikari D, Ueno H, Liu K. 2012. Experimental evidence showing that no mitotically active female germline progenitors exist in postnatal mouse ovaries. Proc Natl Acad Sci USA 109:12580-12585.
161. Zhao GQ, Hogan BL. 1996. Evidence that mouse Bmp8a (Op2) and Bmp8b are duplicated genes that play a role in spermatogenesis and placental development. Mech Dev 57:159-168.
162. Zhao H, Qin Y, Kovanci E, Simpson JL, Chen ZJ, Rajkovic A. 2007. Analyses of GDF9 mutation in 100 Chinese women with premature ovarian failure. Fertil Steril 88:1474-1476.
163. Zhao H, Chen ZJ, Qin Y, Shi Y, Wang S, Choi Y, Simpson JL, Rajkovic A. 2008. Transcription factor FIGLA is mutated in patients with premature ovarian failure. Am J Hum Genet 82:1342-1348.
164. Zhu J, Lin SJ, Zou C, Makanji Y, Jardetzky TS, Woodruff TK. 2012. Inhibin alpha-subunit n terminus interacts with activin type IB receptor to disrupt activin signaling. J Biol Chem 287:8060-8070.
165. Zou K, Yuan Z, Yang Z, Luo H, Sun K, Zhou L, Xiang J, Shi L, Yu Q, Zhang Y, Hou R, Wu J. 2009. Production of offspring from a germline stem cell line derived from neonatal ovaries. Nat Cell Biol 11:631-636.