{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,4]],"date-time":"2026-10-04T01:38:23Z","timestamp":1791077903692,"version":"4.1.0"},"reference-count":52,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2009,10,1]],"date-time":"2009-10-01T00:00:00Z","timestamp":1254355200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2013,7,17]],"date-time":"2013-07-17T00:00:00Z","timestamp":1374019200000},"content-version":"vor","delay-in-days":1385,"URL":"https:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Developmental Biology"],"published-print":{"date-parts":[[2009,10]]},"DOI":"10.1016\/j.ydbio.2009.08.001","type":"journal-article","created":{"date-parts":[[2009,8,9]],"date-time":"2009-08-09T04:09:57Z","timestamp":1249790997000},"page":"458-467","source":"Crossref","is-referenced-by-count":83,"title":["Loss of inhibin alpha uncouples oocyte-granulosa cell dynamics and disrupts postnatal folliculogenesis"],"prefix":"10.1016","volume":"334","author":[{"given":"Michelle","family":"Myers","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brooke S.","family":"Middlebrook","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin M.","family":"Matzuk","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stephanie A.","family":"Pangas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.ydbio.2009.08.001_bib1","doi-asserted-by":"crossref","first-page":"3837","DOI":"10.1210\/en.2006-1590","article-title":"Effects of granulosa cell-specific deletion of Rb in Inha-alpha null female mice","volume":"148","author":"Andreu-Vieyra","year":"2007","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib2","doi-asserted-by":"crossref","first-page":"4951","DOI":"10.1210\/endo.136.11.7588229","article-title":"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","volume":"136","author":"Baarends","year":"1995","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib3","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.ydbio.2006.06.025","article-title":"Postnatal regulation of germ cells by activin: the establishment of the initial follicle pool","volume":"298","author":"Bristol-Gould","year":"2006","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib4","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1038\/78140","article-title":"Insertion of Inhbb into the Inhba locus rescues the Inhba-null phenotype and reveals new activin functions","volume":"25","author":"Brown","year":"2000","journal-title":"Nat. Genet."},{"key":"10.1016\/j.ydbio.2009.08.001_bib5","doi-asserted-by":"crossref","first-page":"2053","DOI":"10.1210\/me.2003-0038","article-title":"Cyclin D2 and p27 are tissue-specific regulators of tumorigenesis in inhibin alpha knockout mice","volume":"17","author":"Burns","year":"2003","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib6","doi-asserted-by":"crossref","first-page":"787","DOI":"10.1210\/er.2002-0003","article-title":"Genetic analysis of the mammalian transforming growth factor-beta superfamily","volume":"23","author":"Chang","year":"2002","journal-title":"Endocr. Rev."},{"key":"10.1016\/j.ydbio.2009.08.001_bib7","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1210\/mend.15.6.0650","article-title":"Inhibin and p27 interact to regulate gonadal tumorigenesis","volume":"15","author":"Cipriano","year":"2001","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib8","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1016\/j.ydbio.2007.11.026","article-title":"Activin signals via SMAD2\/3 between germ and somatic cells in the human fetal ovary and regulates kit ligand expression","volume":"314","author":"Coutts","year":"2008","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib9","doi-asserted-by":"crossref","first-page":"531","DOI":"10.1038\/383531a0","article-title":"Growth differentiation factor-9 is required during early ovarian folliculogenesis","volume":"383","author":"Dong","year":"1996","journal-title":"Nature"},{"key":"10.1016\/j.ydbio.2009.08.001_bib10","doi-asserted-by":"crossref","first-page":"1809","DOI":"10.1210\/mend.12.12.0206","article-title":"The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes","volume":"12","author":"Dube","year":"1998","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib11","doi-asserted-by":"crossref","first-page":"5789","DOI":"10.1210\/endo.140.12.7204","article-title":"Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary","volume":"140","author":"Durlinger","year":"1999","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib12","doi-asserted-by":"crossref","first-page":"1076","DOI":"10.1210\/endo.143.3.8691","article-title":"Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary","volume":"143","author":"Durlinger","year":"2002","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib13","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1530\/rep.0.1240601","article-title":"Regulation of ovarian function: the role of anti-Mullerian hormone","volume":"124","author":"Durlinger","year":"2002","journal-title":"Reproduction"},{"key":"10.1016\/j.ydbio.2009.08.001_bib14","doi-asserted-by":"crossref","first-page":"1018","DOI":"10.1210\/mend.13.6.0309","article-title":"Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary","volume":"13","author":"Elvin","year":"1999","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib15","doi-asserted-by":"crossref","first-page":"4382","DOI":"10.1210\/endo.136.10.7664658","article-title":"Regulation of inhibin\/activin subunit messenger ribonucleic acids (mRNAs) by activin A and expression of activin receptor mRNAs in cultured human granulosa-luteal cells","volume":"136","author":"Eramaa","year":"1995","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib16","doi-asserted-by":"crossref","first-page":"3811","DOI":"10.1242\/jcs.03105","article-title":"Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation","volume":"119","author":"Gilchrist","year":"2006","journal-title":"J. Cell. Sci."},{"key":"10.1016\/j.ydbio.2009.08.001_bib17","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1530\/jrf.0.0780119","article-title":"Effects of gonadotrophin deficiency on follicular development in hypogonadal (hpg) mice","volume":"78","author":"Halpin","year":"1986","journal-title":"J. Reprod. Fertil."},{"key":"10.1016\/j.ydbio.2009.08.001_bib18","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/S0303-7207(01)00469-5","article-title":"Gonadotropic control of ovarian follicular growth and development","volume":"179","author":"Hillier","year":"2001","journal-title":"Mol. Cell. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib19","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1016\/0303-7207(94)90278-X","article-title":"Follicular oestrogen synthesis: the \u2018two-cell, two-gonadotrophin\u2019 model revisited","volume":"100","author":"Hillier","year":"1994","journal-title":"Mol. Cell. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib20","first-page":"854","article-title":"Mullerian inhibiting substance messenger ribonucleic acid expression in granulosa and Sertoli cells coincides with their mitotic activity","volume":"131","author":"Hirobe","year":"1992","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib21","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1095\/biolreprod.102.007146","article-title":"Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep","volume":"67","author":"Juengel","year":"2002","journal-title":"Biol. Reprod."},{"key":"10.1016\/j.ydbio.2009.08.001_bib22","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1016\/j.anireprosci.2004.04.021","article-title":"Physiology of GDF9 and BMP15 signalling molecules","volume":"82-83","author":"Juengel","year":"2004","journal-title":"Anim. Reprod. Sci."},{"key":"10.1016\/j.ydbio.2009.08.001_bib23","doi-asserted-by":"crossref","first-page":"755","DOI":"10.1210\/jc.2002-021317","article-title":"Growth differentiation factor-9 induces Smad2 activation and inhibin B production in cultured human granulosa-luteal cells","volume":"88","author":"Kaivo-Oja","year":"2003","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"10.1016\/j.ydbio.2009.08.001_bib24","doi-asserted-by":"crossref","first-page":"4210","DOI":"10.1210\/endo.137.10.8828479","article-title":"Gonadotropins are essential modifier factors for gonadal tumor development in inhibin-deficient mice","volume":"137","author":"Kumar","year":"1996","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib25","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1038\/ng0297-201","article-title":"Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility","volume":"15","author":"Kumar","year":"1997","journal-title":"Nat. Genet."},{"key":"10.1016\/j.ydbio.2009.08.001_bib26","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1210\/mend.13.6.0297","article-title":"Transgenic models to study gonadotropin function: the role of follicle-stimulating hormone in gonadal growth and tumorigenesis","volume":"13","author":"Kumar","year":"1999","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib27","doi-asserted-by":"crossref","first-page":"675","DOI":"10.1093\/molehr\/gam055","article-title":"Prevention of cachexia-like syndrome development and reduction of tumor progression in inhibin-deficient mice following administration of a chimeric activin receptor type II-murine Fc protein","volume":"13","author":"Li","year":"2007","journal-title":"Mol. Hum. Reprod."},{"key":"10.1016\/j.ydbio.2009.08.001_bib28","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1242\/dev.02667","article-title":"Infertility caused by retardation of follicular development in mice with oocyte-specific expression of Foxo3a","volume":"134","author":"Liu","year":"2007","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2009.08.001_bib29","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1016\/j.ydbio.2003.10.030","article-title":"Expression of activin subunits and receptors in the developing human ovary: activin A promotes germ cell survival and proliferation before primordial follicle formation","volume":"266","author":"Martins da Silva","year":"2004","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib30","first-page":"s41","article-title":"Genetic dissection of mammalian fertility pathways","volume":"Suppl. 4","author":"Matzuk","year":"2002","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib31","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1038\/nm.f.1895","article-title":"The biology of infertility: research advances and clinical challenges","volume":"14","author":"Matzuk","year":"2008","journal-title":"Nat. Med."},{"key":"10.1016\/j.ydbio.2009.08.001_bib32","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1038\/360313a0","article-title":"Alpha-inhibin is a tumour-suppressor gene with gonadal specificity in mice","volume":"360","author":"Matzuk","year":"1992","journal-title":"Nature"},{"key":"10.1016\/j.ydbio.2009.08.001_bib33","doi-asserted-by":"crossref","first-page":"8817","DOI":"10.1073\/pnas.91.19.8817","article-title":"Development of cancer cachexia-like syndrome and adrenal tumors in inhibin-deficient mice","volume":"91","author":"Matzuk","year":"1994","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"10.1016\/j.ydbio.2009.08.001_bib34","first-page":"123","article-title":"Transgenic models to study the roles of inhibins and activins in reproduction, oncogenesis, and development","volume":"51","author":"Matzuk","year":"1996","journal-title":"Recent Prog. Horm. Res."},{"key":"10.1016\/j.ydbio.2009.08.001_bib35","doi-asserted-by":"crossref","first-page":"2178","DOI":"10.1126\/science.1071965","article-title":"Intercellular communication in the mammalian ovary: oocytes carry the conversation","volume":"296","author":"Matzuk","year":"2002","journal-title":"Science"},{"issue":"Suppl. 1","key":"10.1016\/j.ydbio.2009.08.001_bib36","doi-asserted-by":"crossref","first-page":"S25","DOI":"10.1186\/1297-9686-37-S1-S25","article-title":"Physiological effects of major genes affecting ovulation rate in sheep","volume":"37","author":"McNatty","year":"2005","journal-title":"Genet. Sel. Evol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib37","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1210\/endo.137.2.8593790","article-title":"Modulation of granulosa cell deoxyribonucleic acid synthesis and differentiation by activin","volume":"137","author":"Miro","year":"1996","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib38","doi-asserted-by":"crossref","unstructured":"Myers, M., Pangas, S.A., in press. Regulatory roles of transforming growth factor beta family members in folliculogenesis. WIREs Systems Biology and Medicine.","DOI":"10.1002\/wsbm.21"},{"key":"10.1016\/j.ydbio.2009.08.001_bib39","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.mce.2008.06.019","article-title":"Luteinizing hormone promotes gonadal tumorigenesis in inhibin-deficient mice","volume":"294","author":"Nagaraja","year":"2008","journal-title":"Mol. Cell. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib40","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.mce.2003.08.008","article-title":"Synergistic effects of activin and FSH on hyperphosphorylation of Rb and G1\/S transition in rat primary granulosa cells","volume":"210","author":"Ogawa","year":"2003","journal-title":"Mol. Cell. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib41","series-title":"The TGF-\u03b2 Family","first-page":"861","article-title":"The TGF-\u03b2 family in the reproductive tract","author":"Pangas","year":"2008"},{"key":"10.1016\/j.ydbio.2009.08.001_bib42","doi-asserted-by":"crossref","first-page":"2458","DOI":"10.1210\/me.2007-0146","article-title":"Intraovarian activins are required for female fertility","volume":"21","author":"Pangas","year":"2007","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib43","doi-asserted-by":"crossref","first-page":"9135","DOI":"10.1074\/jbc.M409486200","article-title":"Induction of cyclin D2 in rat granulosa cells requires FSH-dependent relief from FOXO1 repression coupled with positive signals from Smad","volume":"280","author":"Park","year":"2005","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.ydbio.2009.08.001_bib44","doi-asserted-by":"crossref","first-page":"622","DOI":"10.1002\/dvg.20258","article-title":"From primordial germ cell to primordial follicle: mammalian female germ cell development","volume":"44","author":"Pepling","year":"2006","journal-title":"Genesis"},{"key":"10.1016\/j.ydbio.2009.08.001_bib45","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1006\/dbio.2001.0269","article-title":"Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles","volume":"234","author":"Pepling","year":"2001","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib46","doi-asserted-by":"crossref","first-page":"559","DOI":"10.1530\/jrf.0.0450559","article-title":"Follicular growth: the basic event in the mouse and human ovary","volume":"45","author":"Peters","year":"1975","journal-title":"J. Reprod. Fertil."},{"key":"10.1016\/j.ydbio.2009.08.001_bib47","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1210\/en.2002-220618","article-title":"Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells","volume":"144","author":"Roh","year":"2003","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib48","doi-asserted-by":"crossref","first-page":"3540","DOI":"10.1210\/en.2009-0267","article-title":"Growth differentiation factor 9 (GDF9) enhances activin A-induced inhibin B production in human granulosa cells","volume":"150","author":"Shi","year":"2009","journal-title":"Endocrinology"},{"key":"10.1016\/j.ydbio.2009.08.001_bib49","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1186\/1477-7827-4-19","article-title":"Oocyte-granulosa cell interactions during mouse follicular development: regulation of kit ligand expression and its role in oocyte growth","volume":"4","author":"Thomas","year":"2006","journal-title":"Reprod. Biol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib50","doi-asserted-by":"crossref","first-page":"607","DOI":"10.1262\/jrd.18026","article-title":"Expression of inhibin\/activin subunits in the ovaries of fetal and neonatal mice","volume":"52","author":"Weng","year":"2006","journal-title":"J. Reprod. Dev."},{"key":"10.1016\/j.ydbio.2009.08.001_bib51","doi-asserted-by":"crossref","first-page":"1509","DOI":"10.1210\/me.2003-0399","article-title":"Interrelationship of growth differentiation factor 9 and inhibin in early folliculogenesis and ovarian tumorigenesis in mice","volume":"18","author":"Wu","year":"2004","journal-title":"Mol. Endocrinol."},{"key":"10.1016\/j.ydbio.2009.08.001_bib52","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1210\/mend.15.6.0662","article-title":"Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function","volume":"15","author":"Yan","year":"2001","journal-title":"Mol. Endocrinol."}],"updated-by":[{"DOI":"10.1016\/j.ydbio.2011.01.037","type":"erratum","label":"Erratum","source":"publisher","updated":{"date-parts":[[2011,4,1]],"date-time":"2011-04-01T00:00:00Z","timestamp":1301616000000}}],"container-title":["Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0012160609011105?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0012160609011105?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2019,5,21]],"date-time":"2019-05-21T18:45:49Z","timestamp":1558464349000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0012160609011105"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,10]]},"references-count":52,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2009,10]]}},"alternative-id":["S0012160609011105"],"URL":"https:\/\/doi.org\/10.1016\/j.ydbio.2009.08.001","relation":{},"ISSN":["0012-1606"],"issn-type":[{"value":"0012-1606","type":"print"}],"subject":[],"published":{"date-parts":[[2009,10]]}}}