{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T23:17:16Z","timestamp":1791933436754,"version":"4.3.4"},"reference-count":57,"publisher":"The Endocrine Society","issue":"4","license":[{"start":{"date-parts":[[2022,3,7]],"date-time":"2022-03-07T00:00:00Z","timestamp":1646611200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000925","name":"National Health and Medical Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000925","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2022,4,1]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Inhibins are members of the transforming growth factor-\u03b2 family, composed of a common \u03b1-subunit disulfide-linked to 1 of 2 \u03b2-subunits (\u03b2A in inhibin A or \u03b2B in inhibin B). Gonadal-derived inhibin A and B act in an endocrine manner to suppress the synthesis of follicle-stimulating hormone (FSH) by pituitary gonadotrope cells. Roles for inhibins beyond the pituitary, however, have proven difficult to delineate because deletion of the inhibin \u03b1-subunit gene (Inha) results in unconstrained expression of activin A and activin B (homodimers of inhibin \u03b2-subunits), which contribute to gonadal tumorigenesis and lethal cachectic wasting. Here, we generated mice with a single point mutation (Arg233Ala) in Inha that prevents proteolytic processing and the formation of bioactive inhibin. In vitro, this mutation blocked inhibin maturation and bioactivity, without perturbing activin production. Serum FSH levels were elevated 2- to 3-fold in InhaR233A\/R233A mice due to the loss of negative feedback from inhibins, but no pathological increase in circulating activins was observed. While inactivation of inhibin A and B had no discernible effect on male reproduction, female InhaR233A\/R233A mice had increased FSH-dependent follicle development and enhanced natural ovulation rates. Nevertheless, inhibin inactivation resulted in significant embryo-fetal resorptions and severe subfertility and was associated with disrupted maternal ovarian function. Intriguingly, heterozygous Inha+\/R233A females had significantly enhanced fecundity, relative to wild-type littermates. These studies have revealed novel effects of inhibins in the establishment and maintenance of pregnancy and demonstrated that partial inactivation of inhibin A\/B is an attractive approach for enhancing female fertility.<\/jats:p>","DOI":"10.1210\/endocr\/bqac025","type":"journal-article","created":{"date-parts":[[2022,3,7]],"date-time":"2022-03-07T21:15:27Z","timestamp":1646687727000},"source":"Crossref","is-referenced-by-count":19,"title":["Inhibin Inactivation in Female Mice Leads to Elevated FSH Levels, Ovarian Overstimulation, and Pregnancy Loss"],"prefix":"10.1210","volume":"163","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0627-2958","authenticated-orcid":false,"given":"Kelly L","family":"Walton","sequence":"first","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"},{"name":"School of Biomedical Sciences, The University of Queensland , Brisbane , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monica P","family":"Goney","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zoe","family":"Peppas","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica M","family":"Stringer","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Developmental Biology Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7848-1447","authenticated-orcid":false,"given":"Amy","family":"Winship","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Developmental Biology Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5111-8389","authenticated-orcid":false,"given":"Karla","family":"Hutt","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Developmental Biology Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Georgia","family":"Goodchild","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shreya","family":"Maskey","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karen L","family":"Chan","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emilie","family":"Br\u00fbl\u00e9","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Cell Biology, McGill University , Montreal , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel J","family":"Bernard","sequence":"additional","affiliation":[{"name":"Department of Anatomy and Cell Biology, McGill University , Montreal , Canada"},{"name":"Department of Pharmacology and Therapeutics, McGill University , Montreal , Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William A","family":"Stocker","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"},{"name":"Department of Chemistry and Biotechnology, Swinburne University of Technology , Hawthorn , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1059-3682","authenticated-orcid":false,"given":"Craig A","family":"Harrison","sequence":"additional","affiliation":[{"name":"Department of Physiology, Monash Biomedicine Discovery Institute, Monash University , Clayton , Australia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"80","published-online":{"date-parts":[[2022,3,7]]},"reference":[{"issue":"4","key":"2022071113594783300_CIT0001","first-page":"1401","article-title":"Measurement of dimeric inhibin B throughout the human menstrual cycle","volume":"81","author":"Groome","year":"1996","journal-title":"J Clin Endocrinol Metab."},{"issue":"2","key":"2022071113594783300_CIT0002","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1677\/joe.0.1190233","article-title":"Effects of 31 kDa bovine inhibin on FSH and LH in rat pituitary cells in vitro: antagonism of gonadotropein-releasing hormone agonists","volume":"119","author":"Farnworth","year":"1988","journal-title":"J Endocrinol."},{"issue":"1","key":"2022071113594783300_CIT0003","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.tem.2019.08.014","article-title":"Tale of two proteins: betaglycan, IGSF1, and the continuing search for the inhibin B receptor","volume":"31","author":"Bernard","year":"2020","journal-title":"Trends Endocrinol Metab."},{"issue":"9","key":"2022071113594783300_CIT0004","first-page":"3341","article-title":"Serum inhibin B levels reflect Sertoli cell function in normal men and men with testicular dysfunction","volume":"81","author":"Anawalt","year":"1996","journal-title":"J Clin Endocrinol Metab."},{"issue":"4","key":"2022071113594783300_CIT0005","first-page":"1321","article-title":"Inhibin-B: a likely candidate for the physiologically important form of inhibin in men","volume":"81","author":"Illingworth","year":"1996","journal-title":"J Clin Endocrinol Metab."},{"key":"2022071113594783300_CIT0006","first-page":"31","article-title":"The control of FSH secretion","volume":"288","author":"McNeilly","year":"1988","journal-title":"Acta Endocrinol Suppl."},{"issue":"8","key":"2022071113594783300_CIT0007","doi-asserted-by":"crossref","first-page":"2465","DOI":"10.1016\/j.fertnstert.2010.03.034","article-title":"Mechanisms of FSH synthesis: what we know, what we don\u2019t, and why you should care","volume":"93","author":"Bernard","year":"2010","journal-title":"Fertil Steril."},{"issue":"9","key":"2022071113594783300_CIT0008","doi-asserted-by":"crossref","first-page":"4432","DOI":"10.1210\/en.2007-0046","article-title":"Rising follicle-stimulating hormone levels with age accelerate female reproductive failure","volume":"148","author":"McTavish","year":"2007","journal-title":"Endocrinology."},{"key":"2022071113594783300_CIT0009","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1210\/rp.57.1.257","article-title":"Hormonal changes in the menopause transition","volume":"57","author":"Burger","year":"2002","journal-title":"Recent Prog Horm Res."},{"issue":"7","key":"2022071113594783300_CIT0010","first-page":"2742","article-title":"Decreased inhibin B secretion is associated with the monotropic FSH rise in older, ovulatory women: a study of serum and follicular fluid levels of dimeric inhibin A and B in spontaneous menstrual cycles","volume":"81","author":"Klein","year":"1996","journal-title":"J Clin Endocrinol Metab."},{"issue":"1","key":"2022071113594783300_CIT0011","first-page":"105","article-title":"Female reproductive aging is marked by decreased secretion of dimeric inhibin","volume":"84","author":"Welt","year":"1999","journal-title":"J Clin 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Endocrinol."},{"issue":"2","key":"2022071113594783300_CIT0033","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1002\/jor.21501","article-title":"Inhibin A enhances bone formation during distraction osteogenesis","volume":"30","author":"Perrien","year":"2012","journal-title":"J Orthop Res."},{"issue":"5","key":"2022071113594783300_CIT0034","doi-asserted-by":"crossref","first-page":"1848","DOI":"10.1210\/jc.2005-2423","article-title":"Bone turnover across the menopause transition: correlations with inhibins and follicle-stimulating hormone","volume":"91","author":"Perrien","year":"2006","journal-title":"J Clin Endocrinol Metab."},{"issue":"5","key":"2022071113594783300_CIT0035","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1071\/RD19131","article-title":"Morphometric, subcellular, in vitro fertilisation and embryonic developmental assessment of mouse oocytes produced by anti-inhibin serum or pregnant mare serum gonadotropein superovulation","volume":"32","author":"Wuri","year":"2020","journal-title":"Reprod Fertil Dev."},{"issue":"1","key":"2022071113594783300_CIT0036","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1016\/0378-4320(93)90122-8","article-title":"Inhibin as a fecundity vaccine","volume":"33","author":"Findlay","year":"1993","journal-title":"Anim Reprod Sci."},{"issue":"7","key":"2022071113594783300_CIT0037","doi-asserted-by":"crossref","first-page":"2799","DOI":"10.1210\/en.2015-1963","article-title":"A novel, more efficient approach to generate bioactive inhibins","volume":"157","author":"Walton","year":"2016","journal-title":"Endocrinology."},{"issue":"8","key":"2022071113594783300_CIT0038","doi-asserted-by":"crossref","DOI":"10.1210\/endocr\/bqaa099","article-title":"Engineering the ovarian hormones inhibin A and Inhibin B to enhance synthesis and activity","volume":"161","author":"Goney","year":"2020","journal-title":"Endocrinology."},{"issue":"4","key":"2022071113594783300_CIT0039","doi-asserted-by":"crossref","first-page":"886","DOI":"10.1095\/biolreprod62.4.886","article-title":"Development of time-resolved immunofluorometric assays for rat follicle-stimulating hormone and luteinizing hormone and application on sera of cycling rats","volume":"62","author":"van Casteren","year":"2000","journal-title":"Biol Reprod."},{"issue":"1-2","key":"2022071113594783300_CIT0040","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1016\/j.mce.2013.07.022","article-title":"Use of detergent-based buffers allows detection of precursor inhibin forms in an immunoassay format","volume":"381","author":"Walton","year":"2013","journal-title":"Mol Cell Endocrinol."},{"issue":"5","key":"2022071113594783300_CIT0041","doi-asserted-by":"crossref","first-page":"569","DOI":"10.1530\/rep.1.00095","article-title":"Methods for quantifying follicular 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Chem."},{"issue":"25","key":"2022071113594783300_CIT0046","doi-asserted-by":"crossref","first-page":"17011","DOI":"10.1074\/jbc.M601459200","article-title":"Identification of distinct inhibin and transforming growth factor beta-binding sites on betaglycan: functional separation of betaglycan co-receptor actions","volume":"281","author":"Wiater","year":"2006","journal-title":"J Biol Chem."},{"issue":"4","key":"2022071113594783300_CIT0047","doi-asserted-by":"crossref","first-page":"491","DOI":"10.1093\/biolre\/ioy015","article-title":"Reproductive failure in mice expressing transgenic follicle-stimulating hormone is not caused by loss of oocyte quality","volume":"98","author":"Upton","year":"2018","journal-title":"Biol Reprod."},{"issue":"3","key":"2022071113594783300_CIT0048","doi-asserted-by":"crossref","first-page":"849","DOI":"10.1210\/endo.136.3.7867593","article-title":"Activin promotes ovarian follicle development in 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(hFSH(24))","volume":"382","author":"Bousfield","year":"2014","journal-title":"Mol Cell Endocrinol."},{"key":"2022071113594783300_CIT0052","article-title":"Superovulation in pubertal heifers immunized against ovine inhibin purified by monoclonal antibody affinity chromatography","author":"Bindon","year":"1988, ,"},{"issue":"1","key":"2022071113594783300_CIT0053","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1530\/jrf.0.0900199","article-title":"Immunization against recombinant bovine inhibin \u03b1 subunit causes increased ovulation rates in gilts","volume":"90","author":"Brown","year":"1990","journal-title":"Reproduction."},{"issue":"1","key":"2022071113594783300_CIT0054","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1677\/joe.0.1200059","article-title":"Effects of immunization against recombinant bovine inhibin \u03b1 subunit on circulating concentrations of gonadotropeins in ewes","volume":"120","author":"Findlay","year":"1989","journal-title":"J Endocrinol."},{"issue":"1","key":"2022071113594783300_CIT0055","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1111\/rda.13854","article-title":"Improving ovulation in gilts using anti-inhibin serum treatment combined with fixed-time artificial insemination","volume":"56","author":"Jia","year":"2021","journal-title":"Reprod Domest Anim."},{"issue":"4","key":"2022071113594783300_CIT0056","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1262\/jrd.18028","article-title":"Immunization of goats against inhibin increased follicular development and ovulation rate","volume":"52","author":"Sasaki","year":"2006","journal-title":"J Reprod Dev."},{"issue":"Suppl. 1","key":"2022071113594783300_CIT0057","first-page":"62","article-title":"Increased ovulatory response of Suffolk ewes vaccinated against a synthetic fragment of porcine inhibin","volume":"38","author":"Schanbacher","year":"1988","journal-title":"Biol 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