{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,21]],"date-time":"2026-09-21T21:08:11Z","timestamp":1790024891660,"version":"4.0.1"},"reference-count":80,"publisher":"Oxford University Press (OUP)","issue":"6","license":[{"start":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T00:00:00Z","timestamp":1747353600000},"content-version":"unspecified","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["T32 HD087166, T32 DK071212, R01 HD108722"],"award-info":[{"award-number":["T32 HD087166, T32 DK071212, R01 HD108722"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["rep.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2025,5,16]]},"abstract":"<jats:p>The Hippo signaling pathway, so named for its massive overgrowth mutant phenotypes, has become one of the most exciting signaling pathways to emerge in the field of reproductive biology. While disruption of Hippo is associated with tumorigenesis in many organs and tissues, relatively less is understood about the normal roles of Hippo signaling in the reproductive organs. Here, we highlight the recent literature illuminating the roles of Hippo pathway members in mouse and human reproduction. We place special emphasis on the inputs and outputs of Hippo signaling during preimplantation development, where Hippo signaling has been extensively studied in both mouse and human. We note a common emerging theme is the critical and highly conserved role of Hippo signaling in epithelia of the reproductive organs. We also discuss human reproductive disorders, whose etiology may be related to dysregulation of Hippo signaling, and possible therapies that have been proposed to correct this dysregulation. Finally, we describe the edge of our knowledge, which currently limits our understanding of Hippo signaling in reproductive health and disease.<\/jats:p>","DOI":"10.1530\/rep-25-0016","type":"journal-article","created":{"date-parts":[[2025,5,16]],"date-time":"2025-05-16T15:28:37Z","timestamp":1747409317000},"update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-11","source":"Crossref","is-referenced-by-count":10,"title":["Hippo signaling in mammalian reproduction"],"prefix":"10.1093","volume":"169","author":[{"given":"Robin E","family":"Kruger","sequence":"first","affiliation":[{"name":"Cell and Molecular Biology Graduate Program, Michigan State University, East Lansing, Michigan, USA"},{"name":"Reproductive and Developmental Sciences Training Program, Michigan State University, East Lansing, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Farina","family":"Aziz","sequence":"additional","affiliation":[{"name":"Cell and Molecular Biology Graduate Program, Michigan State University, East Lansing, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3755-8262","authenticated-orcid":true,"given":"Amy","family":"Ralston","sequence":"additional","affiliation":[{"name":"Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, Michigan, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","reference":[{"key":"bib1","series-title":"Biol Reprod","first-page":"102","article-title":"Multiple mechanisms cooperate to constitutively exclude the transcriptional Co-activator YAP from the nucleus during murine Oogenesis1","volume":"94","author":"Abbassi L","year":"2016","unstructured":"Abbassi L\n, \nMalki S\n, \nCockburn K\n, et al.\n 2016 Multiple mechanisms cooperate to constitutively exclude the transcriptional Co-activator YAP from the nucleus during murine Oogenesis1. 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(https:\/\/doi.org\/10.1016\/j.ajog.2015.08.042)"},{"key":"bib14","series-title":"Elife","article-title":"HIPPO signaling resolves embryonic cell fate conflicts during establishment of pluripotency in vivo","volume":"7","author":"Frum T","year":"2018","unstructured":"Frum T\n, \nMurphy TM\n & \nRalston A\n\n 2018 HIPPO signaling resolves embryonic cell fate conflicts during establishment of pluripotency in vivo. Elife 7 e42298. (https:\/\/doi.org\/10.7554\/eLife.42298)"},{"key":"bib15","series-title":"Development","first-page":"1","article-title":"TEAD4, YAP1 and WWTR1 prevent the premature onset of pluripotency prior to the 16-cell stage","volume":"146","author":"Frum T","year":"2019","unstructured":"Frum T\n, \nWatts JL\n & \nRalston A\n\n 2019 TEAD4, YAP1 and WWTR1 prevent the premature onset of pluripotency prior to the 16-cell stage. Development 146 1\u20137. (https:\/\/doi.org\/10.1242\/dev.179861)"},{"key":"bib16","series-title":"Endocr Relat Cancer","first-page":"297","article-title":"YAP regulates cell proliferation, migration, and steroidogenesis in adult granulosa cell tumors","volume":"21","author":"Fu D","year":"2014","unstructured":"Fu D\n, \nLv X\n, \nHua G\n, et al.\n 2014 YAP regulates cell proliferation, migration, and steroidogenesis in adult granulosa cell tumors. Endocr Relat Cancer 21 297\u2013310. (https:\/\/doi.org\/10.1530\/ERC-13-0339)"},{"key":"bib17","series-title":"Development","article-title":"A conserved role of the Hippo signalling pathway in initiation of the first lineage specification event across mammals","volume":"150","author":"Gerri C","year":"2023","unstructured":"Gerri C\n, \nMcCarthy A\n, \nScott GM\n, et al.\n 2023 A conserved role of the Hippo signalling pathway in initiation of the first lineage specification event across mammals. Development 150 dev201112. (https:\/\/doi.org\/10.1242\/dev.201112)"},{"key":"bib18","series-title":"Cell Commun Signal","first-page":"72","article-title":"The granulosa cell response to luteinizing hormone is partly mediated by YAP1-dependent induction of amphiregulin","volume":"20","author":"Godin P","year":"2022","unstructured":"Godin P\n, \nTsoi MF\n, \nMorin M\n, et al.\n 2022 The granulosa cell response to luteinizing hormone is partly mediated by YAP1-dependent induction of amphiregulin. Cell Commun Signal 20 72. (https:\/\/doi.org\/10.1186\/s12964-022-00843-1)"},{"key":"bib19","series-title":"Hum Reprod","first-page":"1705","article-title":"Dynamics of PI3K and Hippo signaling pathways during in vitro human follicle activation","volume":"33","author":"Grosbois J","year":"2018","unstructured":"Grosbois J\n & \nDemeestere I\n\n 2018 Dynamics of PI3K and Hippo signaling pathways during in vitro human follicle activation. Hum Reprod 33 1705\u20131714. (https:\/\/doi.org\/10.1093\/humrep\/dey250)"},{"key":"bib20","series-title":"Cell","first-page":"457","article-title":"The Drosophila Mst ortholog, Hippo, restricts growth and cell proliferation and promotes apoptosis","volume":"114","author":"Harvey KF","year":"2003","unstructured":"Harvey KF\n, \nPfleger CM\n & \nHariharan IK\n\n 2003 The Drosophila Mst ortholog, Hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114 457\u2013467. (https:\/\/doi.org\/10.1016\/S0092-8674(03)00557-9)"},{"key":"bib21","series-title":"Nat Rev Genet","first-page":"27","article-title":"Mechanisms of early placental development in mouse and humans","volume":"21","author":"Hemberger M","year":"2020","unstructured":"Hemberger M\n, \nHanna CW\n & \nDean W\n\n 2020 Mechanisms of early placental development in mouse and humans. Nat Rev Genet 21 27\u201343. (https:\/\/doi.org\/10.1038\/s41576-019-0169-4)"},{"key":"bib22","series-title":"Curr Biol","first-page":"1181","article-title":"Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos","volume":"23","author":"Hirate Y","year":"2013","unstructured":"Hirate Y\n, \nHirahara S\n, \nInoue K\n, et al.\n 2013 Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. Curr Biol 23 1181\u20131194. (https:\/\/doi.org\/10.1016\/j.cub.2013.05.014)"},{"key":"bib23","series-title":"Science","first-page":"1074","article-title":"TAZ, a transcriptional modulator of mesenchymal stem cell differentiation","volume":"309","author":"Hong J-H","year":"2005","unstructured":"Hong J-H\n, \nHwang ES\n, \nMcManus MT\n, et al.\n 2005 TAZ, a transcriptional modulator of mesenchymal stem cell differentiation. Science 309 1074\u20131078. (https:\/\/doi.org\/10.1126\/science.1110955)"},{"key":"bib24","series-title":"Proc Natl Acad Sci U S A","first-page":"1631","article-title":"Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1","volume":"104","author":"Hossain Z","year":"2007","unstructured":"Hossain Z\n, \nAli SM\n, \nKo HL\n, et al.\n 2007 Glomerulocystic kidney disease in mice with a targeted inactivation of Wwtr1. Proc Natl Acad Sci U S A 104 1631\u20131636. (https:\/\/doi.org\/10.1073\/pnas.0605266104)"},{"key":"bib25","series-title":"Fertil Steril","first-page":"458","article-title":"Hippo signaling disruption and ovarian follicle activation in infertile patients","volume":"114","author":"Hsueh AJW","year":"2020","unstructured":"Hsueh AJW\n & \nKawamura K\n\n 2020 Hippo signaling disruption and ovarian follicle activation in infertile patients. Fertil Steril 114 458\u2013464. (https:\/\/doi.org\/10.1016\/j.fertnstert.2020.07.031)"},{"key":"bib26","series-title":"Endocr Rev","first-page":"1","article-title":"Intraovarian control of early folliculogenesis","volume":"36","author":"Hsueh AJW","year":"2015","unstructured":"Hsueh AJW\n, \nKawamura K\n, \nCheng Y\n, et al.\n 2015 Intraovarian control of early folliculogenesis. Endocr Rev 36 1\u201324. (https:\/\/doi.org\/10.1210\/er.2014-1020)"},{"key":"bib27","series-title":"J Cell Physiol","first-page":"1578","article-title":"Hippo pathway functions as a downstream effector of AKT signaling to regulate the activation of primordial follicles in mice","volume":"234","author":"Hu L-L","year":"2019","unstructured":"Hu L-L\n, \nSu T\n, \nLuo R-C\n, et al.\n 2019 Hippo pathway functions as a downstream effector of AKT signaling to regulate the activation of primordial follicles in mice. J Cell Physiol 234 1578\u20131587. (https:\/\/doi.org\/10.1002\/jcp.27024)"},{"key":"bib28","series-title":"Mol Ther Nucleic Acids","first-page":"143","article-title":"miR21 modulates the Hippo signaling pathway via interference with PP2A B\u03b2 to inhibit trophoblast invasion and cause preeclampsia","volume":"30","author":"Hu M","year":"2022","unstructured":"Hu M\n, \nZheng Y\n, \nLiao J\n, et al.\n 2022 miR21 modulates the Hippo signaling pathway via interference with PP2A B\u03b2 to inhibit trophoblast invasion and cause preeclampsia. Mol Ther Nucleic Acids 30 143\u2013161. (https:\/\/doi.org\/10.1016\/j.omtn.2022.09.006)"},{"key":"bib29","series-title":"Mol Hum Reprod","first-page":"698","article-title":"The polycystic ovary syndrome-associated gene Yap1 is regulated by gonadotropins and sex steroid hormones in hyperandrogenism-induced oligo-ovulation in mouse","volume":"23","author":"Ji S-Y","year":"2017","unstructured":"Ji S-Y\n, \nLiu X-M\n, \nLi B-T\n, et al.\n 2017 The polycystic ovary syndrome-associated gene Yap1 is regulated by gonadotropins and sex steroid hormones in hyperandrogenism-induced oligo-ovulation in mouse. Mol Hum Reprod 23 698\u2013707. (https:\/\/doi.org\/10.1093\/molehr\/gax046)"},{"key":"bib30","series-title":"Medicine","article-title":"Promoter methylation of yes-associated protein (YAP1) gene in polycystic ovary syndrome","volume":"96","author":"Jiang L-L","year":"2017","unstructured":"Jiang L-L\n, \nXie J-K\n, \nCui J-Q\n, et al.\n 2017 Promoter methylation of yes-associated protein (YAP1) gene in polycystic ovary syndrome. Medicine 96 e5768. (https:\/\/doi.org\/10.1097\/MD.0000000000005768)"},{"key":"bib31","series-title":"Proc Natl Acad Sci U S A","first-page":"17474","article-title":"Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment","volume":"110","author":"Kawamura K","year":"2013","unstructured":"Kawamura K\n, \nCheng Y\n, \nSuzuki N\n, et al.\n 2013 Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc Natl Acad Sci U S A 110 17474\u201317479. (https:\/\/doi.org\/10.1073\/pnas.1312830110)"},{"key":"bib32","series-title":"Cell Rep","first-page":"270","article-title":"Transcriptional Co-repressor function of the Hippo pathway transducers YAP and TAZ","volume":"11","author":"Kim M","year":"2015","unstructured":"Kim M\n, \nKim T\n, \nJohnson RL\n, et al.\n 2015 Transcriptional Co-repressor function of the Hippo pathway transducers YAP and TAZ. Cell Rep 11 270\u2013282. 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(https:\/\/doi.org\/10.1096\/fj.201900179RR)"},{"key":"bib41","series-title":"Sci Bull","first-page":"1281","article-title":"Reprogramming of ovarian granulosa cells by YAP1 leads to development of high-grade cancer with mesenchymal lineage and serous features","volume":"65","author":"Lv X","year":"2020","unstructured":"Lv X\n, \nHe C\n, \nHuang C\n, et al.\n 2020 Reprogramming of ovarian granulosa cells by YAP1 leads to development of high-grade cancer with mesenchymal lineage and serous features. Sci Bull 65 1281\u20131296. (https:\/\/doi.org\/10.1016\/j.scib.2020.03.040)"},{"key":"bib42","series-title":"J Assist Reprod Genet","first-page":"1763","article-title":"Hippo signaling in the ovary and polycystic ovarian syndrome","volume":"35","author":"Maas K","year":"2018","unstructured":"Maas K\n, \nMirabal S\n, \nPenzias A\n, et al.\n 2018 Hippo signaling in the ovary and polycystic ovarian syndrome. J Assist Reprod Genet 35 1763\u20131771. (https:\/\/doi.org\/10.1007\/s10815-018-1235-0)"},{"key":"bib43","series-title":"Proc Natl Acad Sci U S A","first-page":"13562","article-title":"Pivotal role of the transcriptional co-activator YAP in trophoblast stemness of the developing human placenta","volume":"117","author":"Meinhardt G","year":"2020","unstructured":"Meinhardt G\n, \nHaider S\n, \nKunihs V\n, et al.\n 2020 Pivotal role of the transcriptional co-activator YAP in trophoblast stemness of the developing human placenta. Proc Natl Acad Sci U S A 117 13562\u201313570. (https:\/\/doi.org\/10.1073\/pnas.2002630117)"},{"key":"bib44","series-title":"Annu Rev Genet","first-page":"65","article-title":"The Hippo signaling network and its biological functions","volume":"52","author":"Misra JR","year":"2018","unstructured":"Misra JR\n & \nIrvine KD\n\n 2018 The Hippo signaling network and its biological functions. Annu Rev Genet 52 65\u201387. (https:\/\/doi.org\/10.1146\/annurev-genet-120417-031621)"},{"key":"bib45","series-title":"Mol Hum Reprod","article-title":"Inhibition of YAP\/TAZ-TEAD activity induces cytotrophoblast differentiation into syncytiotrophoblast in human trophoblast","volume":"28","author":"Mizutani T","year":"2022","unstructured":"Mizutani T\n, \nOrisaka M\n, \nMiyazaki Y\n, et al.\n 2022 Inhibition of YAP\/TAZ-TEAD activity induces cytotrophoblast differentiation into syncytiotrophoblast in human trophoblast. Mol Hum Reprod 28 gaac032. (https:\/\/doi.org\/10.1093\/molehr\/gaac032)"},{"key":"bib46","series-title":"Reproduction","article-title":"YAP1 and WWTR1 are required for murine pregnancy initiation","volume":"169","author":"Moldovan GE","year":"2024","unstructured":"Moldovan GE\n, \nMassri N\n, \nVegter EL\n, et al.\n 2024 YAP1 and WWTR1 are required for murine pregnancy initiation. Reproduction 169 e240355. 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