{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,4]],"date-time":"2026-06-04T02:11:23Z","timestamp":1780539083830,"version":"3.54.1"},"reference-count":87,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,12,28]],"date-time":"2024-12-28T00:00:00Z","timestamp":1735344000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"},{"start":{"date-parts":[[2024,12,28]],"date-time":"2024-12-28T00:00:00Z","timestamp":1735344000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0"}],"funder":[{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["IOS-1456942"],"award-info":[{"award-number":["IOS-1456942"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["DMS-1916376"],"award-info":[{"award-number":["DMS-1916376"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100006094","name":"University of Delaware","doi-asserted-by":"publisher","award":["CANR Unique Strengths"],"award-info":[{"award-number":["CANR Unique Strengths"]}],"id":[{"id":"10.13039\/100006094","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100005825","name":"National Institute of Food and Agriculture","doi-asserted-by":"publisher","award":["2023-67011-40333"],"award-info":[{"award-number":["2023-67011-40333"]}],"id":[{"id":"10.13039\/100005825","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100021422","name":"Delaware-CTR ACCEL Program","doi-asserted-by":"publisher","award":["U54-GM104941"],"award-info":[{"award-number":["U54-GM104941"]}],"id":[{"id":"10.13039\/100021422","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100004587","name":"Instituto de Salud Carlos III","doi-asserted-by":"publisher","award":["PI22\/00877"],"award-info":[{"award-number":["PI22\/00877"]}],"id":[{"id":"10.13039\/501100004587","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100002369","name":"University of Delaware Research Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100002369","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100013429","name":"Delaware IDeA Network of Biomedical Research Excellence","doi-asserted-by":"publisher","award":["P20 GM103446"],"award-info":[{"award-number":["P20 GM103446"]}],"id":[{"id":"10.13039\/100013429","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/s41598-024-80003-2","type":"journal-article","created":{"date-parts":[[2024,12,28]],"date-time":"2024-12-28T01:22:23Z","timestamp":1735348943000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Cross-species regulatory network analysis identifies FOXO1 as a driver of ovarian follicular recruitment"],"prefix":"10.1038","volume":"14","author":[{"given":"Ashley E.","family":"Kramer","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alberto","family":"Berral-Gonz\u00e1lez","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kathryn M.","family":"Ellwood","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shanshan","family":"Ding","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Javier","family":"De Las Rivas","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aditya","family":"Dutta","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2024,12,28]]},"reference":[{"key":"80003_CR1","unstructured":"Ciccone, N., Sharp, P., Wilson, P. & Dunn, I. Expression of neuroendocrine genes within the hypothalamic-pituitary-ovarian axis of end of lay broiler breeder hens. (2003)."},{"key":"80003_CR2","doi-asserted-by":"publisher","first-page":"30","DOI":"10.3382\/ps.2010-01118","volume":"90","author":"A Wolc","year":"2011","unstructured":"Wolc, A., Arango, J., Settar, P., OSullivan, N. P. & Dekkers, J. C. Evaluation of egg production in layers using random regression models. Poult Sci 90, 30\u201334. https:\/\/doi.org\/10.3382\/ps.2010-01118 (2011).","journal-title":"Poult Sci"},{"key":"80003_CR3","doi-asserted-by":"publisher","unstructured":"Bain, M. M., Nys, Y. & Dunn, I. C. Increasing persistency in lay and stabilising egg quality in longer laying cycles. What are the challenges? Br Poult Sci 57, 330\u2013338, https:\/\/doi.org\/10.1080\/00071668.2016.1161727 (2016).","DOI":"10.1080\/00071668.2016.1161727"},{"key":"80003_CR4","doi-asserted-by":"publisher","first-page":"771","DOI":"10.3382\/japr\/pfz043","volume":"28","author":"M Kidd","year":"2019","unstructured":"Kidd, M. & Anderson, K. Laying hens in the US market: An appraisal of trends from the beginning of the 20th century to present. Journal of Applied Poultry Research 28, 771\u2013784 (2019).","journal-title":"Journal of Applied Poultry Research"},{"key":"80003_CR5","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1093\/ps\/86.1.30","volume":"86","author":"PT Luo","year":"2007","unstructured":"Luo, P. T., Yang, R. Q. & Yang, N. Estimation of genetic parameters for cumulative egg numbers in a broiler dam line by using a random regression model. Poult Sci 86, 30\u201336. https:\/\/doi.org\/10.1093\/ps\/86.1.30 (2007).","journal-title":"Poult Sci"},{"key":"80003_CR6","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1080\/00071669208417478","volume":"33","author":"SS Palmer","year":"1992","unstructured":"Palmer, S. S. & Bahr, J. M. Follicle stimulating hormone increases serum oestradiol-17 beta concentrations, number of growing follicles and yolk deposition in aging hens (Gallus gallus domesticus) with decreased egg production. Br Poult Sci 33, 403\u2013414. https:\/\/doi.org\/10.1080\/00071669208417478 (1992).","journal-title":"Br Poult Sci"},{"key":"80003_CR7","doi-asserted-by":"publisher","first-page":"2185","DOI":"10.1016\/j.psj.2019.11.040","volume":"99","author":"EY Hao","year":"2020","unstructured":"Hao, E. Y. et al. Melatonin regulates the ovarian function and enhances follicle growth in aging laying hens via activating the mammalian target of rapamycin pathway. Poult Sci 99, 2185\u20132195. https:\/\/doi.org\/10.1016\/j.psj.2019.11.040 (2020).","journal-title":"Poult Sci"},{"key":"80003_CR8","doi-asserted-by":"publisher","first-page":"2005","DOI":"10.3382\/ps.0722005","volume":"72","author":"K Lillpers","year":"1993","unstructured":"Lillpers, K. & Wilhelmson, M. Age-dependent changes in oviposition pattern and egg production traits in the domestic hen. Poult Sci 72, 2005\u20132011. https:\/\/doi.org\/10.3382\/ps.0722005 (1993).","journal-title":"Poult Sci"},{"key":"80003_CR9","doi-asserted-by":"publisher","unstructured":"Vollenhoven, B. & Hunt, S. Ovarian ageing and the impact on female fertility. F1000Res 7, https:\/\/doi.org\/10.12688\/f1000research.16509.1 (2018).","DOI":"10.12688\/f1000research.16509.1"},{"key":"80003_CR10","doi-asserted-by":"publisher","first-page":"105","DOI":"10.5935\/1518-0557.20210026","volume":"26","author":"ARE Moghadam","year":"2022","unstructured":"Moghadam, A. R. E., Moghadam, M. T., Hemadi, M. & Saki, G. Oocyte quality and aging. JBRA Assist Reprod 26, 105\u2013122. https:\/\/doi.org\/10.5935\/1518-0557.20210026 (2022).","journal-title":"JBRA Assist Reprod"},{"key":"80003_CR11","doi-asserted-by":"publisher","first-page":"1437","DOI":"10.3382\/ps.0381437","volume":"38","author":"AH Smith","year":"1959","unstructured":"Smith, A. H. Follicular permeability and yolk formation. Poultry Science 38, 1437\u20131446 (1959).","journal-title":"Poultry Science"},{"key":"80003_CR12","doi-asserted-by":"publisher","first-page":"385","DOI":"10.3923\/ijps.2006.385.389","volume":"5","author":"M Oguike","year":"2006","unstructured":"Oguike, M., Igboeli, G. & Ibe, S. Effect of Induced-moult on the Number Small Ovarian Follicles and Egg Production of Old Layers. Int. J. Poult. Sci 5, 385\u2013389 (2006).","journal-title":"Int. J. Poult. Sci"},{"key":"80003_CR13","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1080\/00071669508417809","volume":"36","author":"H Su","year":"1995","unstructured":"Su, H., Silversides, F. G. & Villeneuve, P. Ovarian morphology and follicular development in sex-linked imperfect albino (s(al)-s) and nonalbino hens before or after a forced moult. Br Poult Sci 36, 645\u2013653. https:\/\/doi.org\/10.1080\/00071669508417809 (1995).","journal-title":"Br Poult Sci"},{"key":"80003_CR14","doi-asserted-by":"publisher","first-page":"897","DOI":"10.3382\/ps.0720897","volume":"72","author":"PJ Sharp","year":"1993","unstructured":"Sharp, P. J. Photoperiodic control of reproduction in the domestic hen. Poult Sci 72, 897\u2013905. https:\/\/doi.org\/10.3382\/ps.0720897 (1993).","journal-title":"Poult Sci"},{"key":"80003_CR15","doi-asserted-by":"publisher","first-page":"2355","DOI":"10.3382\/ps.0652355","volume":"65","author":"R Silver","year":"1986","unstructured":"Silver, R. Circadian and interval timing mechanisms in the ovulatory cycle of the hen. Poult Sci 65, 2355\u20132362. https:\/\/doi.org\/10.3382\/ps.0652355 (1986).","journal-title":"Poult Sci"},{"key":"80003_CR16","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1159\/000014628","volume":"9","author":"AL Johnson","year":"2000","unstructured":"Johnson, A. L. Granulosa cell apoptosis: conservation of cell signaling in an avian ovarian model system. Biol Signals Recept 9, 96\u2013101. https:\/\/doi.org\/10.1159\/000014628 (2000).","journal-title":"Biol Signals Recept"},{"key":"80003_CR17","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1530\/jrf.0.0500179","volume":"50","author":"AB Gilbert","year":"1977","unstructured":"Gilbert, A. B., Evans, A. J., Perry, M. M. & Davidson, M. H. A method for separating the granulosa cells, the basal lamina and the theca of the preovulatory ovarian follicle of the domestic fowl (Gallus domesticus). J Reprod Fertil 50, 179\u2013181. https:\/\/doi.org\/10.1530\/jrf.0.0500179 (1977).","journal-title":"J Reprod Fertil"},{"key":"80003_CR18","doi-asserted-by":"publisher","unstructured":"Kramer, A. E., Ellwood, K. M., Brannick, E. M. & Dutta, A. Separation of Avian Preovulatory Follicle Granulosa and Theca Cell Layers for Downstream Applications. J Vis Exp (212), https:\/\/doi.org\/10.3791\/67344 (2024).","DOI":"10.3791\/67344"},{"key":"80003_CR19","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1016\/j.psj.2019.12.028","volume":"99","author":"K Brady","year":"2020","unstructured":"Brady, K., Porter, T. E., Liu, H. C. & Long, J. A. Characterization of the hypothalamo-pituitary-gonadal axis in low and high egg producing turkey hens. Poult Sci 99, 1163\u20131173. https:\/\/doi.org\/10.1016\/j.psj.2019.12.028 (2020).","journal-title":"Poult Sci"},{"key":"80003_CR20","doi-asserted-by":"publisher","DOI":"10.1016\/j.psj.2022.102319","volume":"102","author":"C Li","year":"2023","unstructured":"Li, C. et al. The adiponectin receptor agonist, AdipoRon, promotes reproductive hormone secretion and gonadal development via the hypothalamic-pituitary-gonadal axis in chickens. Poult Sci 102, 102319. https:\/\/doi.org\/10.1016\/j.psj.2022.102319 (2023).","journal-title":"Poult Sci"},{"key":"80003_CR21","doi-asserted-by":"publisher","unstructured":"Zhao, J. et al. Interacting Networks of the Hypothalamic-Pituitary-Ovarian Axis Regulate Layer Hens Performance. Genes (Basel) 14, https:\/\/doi.org\/10.3390\/genes14010141 (2023).","DOI":"10.3390\/genes14010141"},{"key":"80003_CR22","doi-asserted-by":"publisher","first-page":"96","DOI":"10.1016\/j.ygcen.2018.10.011","volume":"270","author":"Q Chen","year":"2019","unstructured":"Chen, Q. et al. Expression dynamics of gonadotropin-releasing hormone-I and its mutual regulation with luteinizing hormone in chicken ovary and follicles. Gen Comp Endocrinol 270, 96\u2013102. https:\/\/doi.org\/10.1016\/j.ygcen.2018.10.011 (2019).","journal-title":"Gen Comp Endocrinol"},{"key":"80003_CR23","doi-asserted-by":"publisher","first-page":"212","DOI":"10.1002\/mrd.21288","volume":"78","author":"FJ Diaz","year":"2011","unstructured":"Diaz, F. J., Anthony, K. & Halfhill, A. N. Early avian follicular development is characterized by changes in transcripts involved in steroidogenesis, paracrine signaling and transcription. Mol Reprod Dev 78, 212\u2013223. https:\/\/doi.org\/10.1002\/mrd.21288 (2011).","journal-title":"Mol Reprod Dev"},{"key":"80003_CR24","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.ygcen.2017.03.013","volume":"247","author":"J Wang","year":"2017","unstructured":"Wang, J. & Gong, Y. Transcription of CYP19A1 is directly regulated by SF-1 in the theca cells of ovary follicles in chicken. Gen Comp Endocrinol 247, 1\u20137. https:\/\/doi.org\/10.1016\/j.ygcen.2017.03.013 (2017).","journal-title":"Gen Comp Endocrinol"},{"key":"80003_CR25","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0146028","volume":"10","author":"G Zhu","year":"2015","unstructured":"Zhu, G., Mao, Y., Zhou, W. & Jiang, Y. Dynamic Changes in the Follicular Transcriptome and Promoter DNA Methylation Pattern of Steroidogenic Genes in Chicken Follicles throughout the Ovulation Cycle. PLoS One 10, e0146028. https:\/\/doi.org\/10.1371\/journal.pone.0146028 (2015).","journal-title":"PLoS One"},{"key":"80003_CR26","doi-asserted-by":"publisher","first-page":"5462","DOI":"10.1038\/s41598-019-41132-1","volume":"9","author":"G Zhu","year":"2019","unstructured":"Zhu, G. et al. Transcriptomic Diversification of Granulosa Cells during Follicular Development in Chicken. Sci Rep 9, 5462. https:\/\/doi.org\/10.1038\/s41598-019-41132-1 (2019).","journal-title":"Sci Rep"},{"key":"80003_CR27","doi-asserted-by":"publisher","unstructured":"Heidarzadehpilehrood, R. et al. A Review on CYP11A1, CYP17A1, and CYP19A1 Polymorphism Studies: Candidate Susceptibility Genes for Polycystic Ovary Syndrome (PCOS) and Infertility. Genes (Basel) 13, https:\/\/doi.org\/10.3390\/genes13020302 (2022).","DOI":"10.3390\/genes13020302"},{"key":"80003_CR28","doi-asserted-by":"publisher","first-page":"638","DOI":"10.1016\/j.ccr.2014.03.017","volume":"25","author":"A Aytes","year":"2014","unstructured":"Aytes, A. et al. Cross-species regulatory network analysis identifies a synergistic interaction between FOXM1 and CENPF that drives prostate cancer malignancy. Cancer Cell 25, 638\u2013651. https:\/\/doi.org\/10.1016\/j.ccr.2014.03.017 (2014).","journal-title":"Cancer Cell"},{"key":"80003_CR29","doi-asserted-by":"publisher","first-page":"377","DOI":"10.1038\/msb.2010.31","volume":"6","author":"C Lefebvre","year":"2010","unstructured":"Lefebvre, C. et al. A human B-cell interactome identifies MYB and FOXM1 as master regulators of proliferation in germinal centers. Mol Syst Biol 6, 377. https:\/\/doi.org\/10.1038\/msb.2010.31 (2010).","journal-title":"Mol Syst Biol"},{"key":"80003_CR30","doi-asserted-by":"publisher","first-page":"2233","DOI":"10.1093\/bioinformatics\/btw216","volume":"32","author":"A Lachmann","year":"2016","unstructured":"Lachmann, A., Giorgi, F. M., Lopez, G. & Califano, A. ARACNe-AP: gene network reverse engineering through adaptive partitioning inference of mutual information. Bioinformatics 32, 2233\u20132235. https:\/\/doi.org\/10.1093\/bioinformatics\/btw216 (2016).","journal-title":"Bioinformatics"},{"key":"80003_CR31","doi-asserted-by":"publisher","unstructured":"Margolin, A. A. et al. ARACNE: an algorithm for the reconstruction of gene regulatory networks in a mammalian cellular context. BMC Bioinformatics 7 Suppl 1, S7, https:\/\/doi.org\/10.1186\/1471-2105-7-S1-S7 (2006).","DOI":"10.1186\/1471-2105-7-S1-S7"},{"key":"80003_CR32","doi-asserted-by":"publisher","first-page":"486","DOI":"10.1186\/s12864-020-06855-w","volume":"21","author":"Q Chen","year":"2020","unstructured":"Chen, Q. et al. Transcriptomic and proteomic analyses of ovarian follicles reveal the role of VLDLR in chicken follicle selection. BMC Genomics 21, 486. https:\/\/doi.org\/10.1186\/s12864-020-06855-w (2020).","journal-title":"BMC Genomics"},{"key":"80003_CR33","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.theriogenology.2021.04.002","volume":"169","author":"A Hrabia","year":"2021","unstructured":"Hrabia, A., Wolak, D. & Sechman, A. Response of the matrix metalloproteinase system of the chicken ovary to prolactin treatment. Theriogenology 169, 21\u201328. https:\/\/doi.org\/10.1016\/j.theriogenology.2021.04.002 (2021).","journal-title":"Theriogenology"},{"key":"80003_CR34","doi-asserted-by":"publisher","unstructured":"Huang, X. et al. Ovarian Transcriptomic Analysis of Ninghai Indigenous Chickens at Different Egg-Laying Periods. Genes (Basel) 13, https:\/\/doi.org\/10.3390\/genes13040595 (2022).","DOI":"10.3390\/genes13040595"},{"key":"80003_CR35","doi-asserted-by":"publisher","unstructured":"Li, J. et al. Identification of the Key microRNAs and miRNA-mRNA Interaction Networks during the Ovarian Development of Hens. Animals (Basel) 10, https:\/\/doi.org\/10.3390\/ani10091680 (2020).","DOI":"10.3390\/ani10091680"},{"key":"80003_CR36","doi-asserted-by":"publisher","first-page":"491","DOI":"10.3389\/fgene.2018.00491","volume":"9","author":"W Wang","year":"2018","unstructured":"Wang, W. et al. Dynamic Changes in the Global MicroRNAome and Transcriptome Identify Key Nodes Associated With Ovarian Development in Chickens. Front Genet 9, 491. https:\/\/doi.org\/10.3389\/fgene.2018.00491 (2018).","journal-title":"Front Genet"},{"key":"80003_CR37","doi-asserted-by":"publisher","first-page":"3144","DOI":"10.1080\/10495398.2022.2136680","volume":"34","author":"C Yu","year":"2023","unstructured":"Yu, C. et al. Whole transcriptome analysis reveals the key genes and noncoding RNAs related to follicular atresia in broilers. Anim Biotechnol 34, 3144\u20133153. https:\/\/doi.org\/10.1080\/10495398.2022.2136680 (2023).","journal-title":"Anim Biotechnol"},{"key":"80003_CR38","doi-asserted-by":"publisher","unstructured":"Guo, R., Chen, F. & Shi, Z. Suppression of Notch Signaling Stimulates Progesterone Synthesis by Enhancing the Expression of NR5A2 and NR2F2 in Porcine Granulosa Cells. Genes (Basel) 11, https:\/\/doi.org\/10.3390\/genes11020120 (2020).","DOI":"10.3390\/genes11020120"},{"key":"80003_CR39","doi-asserted-by":"publisher","first-page":"82","DOI":"10.1186\/s40104-023-00884-7","volume":"14","author":"L Huang","year":"2023","unstructured":"Huang, L. et al. CLOCK inhibits the proliferation of porcine ovarian granulosa cells by targeting ASB9. J Anim Sci Biotechnol 14, 82. https:\/\/doi.org\/10.1186\/s40104-023-00884-7 (2023).","journal-title":"J Anim Sci Biotechnol"},{"key":"80003_CR40","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1016\/j.aninu.2023.05.012","volume":"14","author":"DM Dansou","year":"2023","unstructured":"Dansou, D. M. et al. Carotenoid enrichment in eggs: From biochemistry perspective. Anim Nutr 14, 315\u2013333. https:\/\/doi.org\/10.1016\/j.aninu.2023.05.012 (2023).","journal-title":"Anim Nutr"},{"key":"80003_CR41","doi-asserted-by":"publisher","unstructured":"Yang, L. et al. Dynamic Expression Profile of Follicles at Different Stages in High- and Low-Production Laying Hens. Genes (Basel) 15, https:\/\/doi.org\/10.3390\/genes15010040 (2023).","DOI":"10.3390\/genes15010040"},{"key":"80003_CR42","doi-asserted-by":"publisher","DOI":"10.1016\/j.anireprosci.2020.106604","volume":"221","author":"Q Han","year":"2020","unstructured":"Han, Q. et al. Effects of FOXO1 on the proliferation and cell cycle-, apoptosis- and steroidogenesis-related genes expression in sheep granulosa cells. Anim Reprod Sci 221, 106604. https:\/\/doi.org\/10.1016\/j.anireprosci.2020.106604 (2020).","journal-title":"Anim Reprod Sci"},{"key":"80003_CR43","doi-asserted-by":"publisher","first-page":"116","DOI":"10.1016\/j.mce.2016.06.020","volume":"434","author":"MK Herndon","year":"2016","unstructured":"Herndon, M. K., Law, N. C., Donaubauer, E. M., Kyriss, B. & Hunzicker-Dunn, M. Forkhead box O member FOXO1 regulates the majority of follicle-stimulating hormone responsive genes in ovarian granulosa cells. Mol Cell Endocrinol 434, 116\u2013126. https:\/\/doi.org\/10.1016\/j.mce.2016.06.020 (2016).","journal-title":"Mol Cell Endocrinol"},{"key":"80003_CR44","doi-asserted-by":"publisher","first-page":"108","DOI":"10.1016\/j.theriogenology.2022.02.004","volume":"183","author":"C Kong","year":"2022","unstructured":"Kong, C. et al. Signaling pathways of Periplaneta americana peptide resist H(2)O(2)-induced apoptosis in pig-ovary granulosa cells through FoxO1. Theriogenology 183, 108\u2013119. https:\/\/doi.org\/10.1016\/j.theriogenology.2022.02.004 (2022).","journal-title":"Theriogenology"},{"key":"80003_CR45","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1530\/rep.0.1260133","volume":"126","author":"SY Lin","year":"2003","unstructured":"Lin, S. Y., Morrison, J. R., Phillips, D. J. & de Kretser, D. M. Regulation of ovarian function by the TGF-beta superfamily and follistatin. Reproduction 126, 133\u2013148. https:\/\/doi.org\/10.1530\/rep.0.1260133 (2003).","journal-title":"Reproduction"},{"key":"80003_CR46","doi-asserted-by":"publisher","first-page":"836","DOI":"10.1126\/science.2106159","volume":"247","author":"T Nakamura","year":"1990","unstructured":"Nakamura, T. et al. Activin-binding protein from rat ovary is follistatin. Science 247, 836\u2013838. https:\/\/doi.org\/10.1126\/science.2106159 (1990).","journal-title":"Science"},{"key":"80003_CR47","doi-asserted-by":"publisher","first-page":"5984","DOI":"10.1038\/s41598-024-55993-8","volume":"14","author":"S Ling","year":"2024","unstructured":"Ling, S. et al. Epidemiologic and genetic associations of female reproductive disorders with depression or dysthymia: a Mendelian randomization study. Sci Rep 14, 5984. https:\/\/doi.org\/10.1038\/s41598-024-55993-8 (2024).","journal-title":"Sci Rep"},{"key":"80003_CR48","doi-asserted-by":"publisher","first-page":"11682","DOI":"10.1096\/fj.201900662R","volume":"33","author":"MB Rabaglino","year":"2019","unstructured":"Rabaglino, M. B. & Conrad, K. P. Evidence for shared molecular pathways of dysregulated decidualization in preeclampsia and endometrial disorders revealed by microarray data integration. FASEB J 33, 11682\u201311695. https:\/\/doi.org\/10.1096\/fj.201900662R (2019).","journal-title":"FASEB J"},{"key":"80003_CR49","doi-asserted-by":"publisher","DOI":"10.1016\/j.psj.2023.102745","volume":"102","author":"K Bai","year":"2023","unstructured":"Bai, K. et al. Melatonin alleviates ovarian function damage and oxidative stress induced by dexamethasone in the laying hens through FOXO1 signaling pathway. Poult Sci 102, 102745. https:\/\/doi.org\/10.1016\/j.psj.2023.102745 (2023).","journal-title":"Poult Sci"},{"key":"80003_CR50","doi-asserted-by":"publisher","first-page":"2685310","DOI":"10.1155\/2020\/2685310","volume":"2020","author":"L Zhou","year":"2020","unstructured":"Zhou, L. et al. Oxidized Oils and Oxidized Proteins Induce Apoptosis in Granulosa Cells by Increasing Oxidative Stress in Ovaries of Laying Hens. Oxid Med Cell Longev 2020, 2685310. https:\/\/doi.org\/10.1155\/2020\/2685310 (2020).","journal-title":"Oxid Med Cell Longev"},{"key":"80003_CR51","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2022.762228","volume":"10","author":"S Zhou","year":"2022","unstructured":"Zhou, S., Zhao, A., Wu, Y., Mi, Y. & Zhang, C. Protective Effect of Grape Seed Proanthocyanidins on Oxidative Damage of Chicken Follicular Granulosa Cells by Inhibiting FoxO1-Mediated Autophagy. Front Cell Dev Biol 10, 762228. https:\/\/doi.org\/10.3389\/fcell.2022.762228 (2022).","journal-title":"Front Cell Dev Biol"},{"key":"80003_CR52","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1210\/me.2012-1296","volume":"27","author":"Z Liu","year":"2013","unstructured":"Liu, Z., Castrillon, D. H., Zhou, W. & Richards, J. S. FOXO1\/3 depletion in granulosa cells alters follicle growth, death and regulation of pituitary FSH. Mol Endocrinol 27, 238\u2013252. https:\/\/doi.org\/10.1210\/me.2012-1296 (2013).","journal-title":"Mol Endocrinol"},{"key":"80003_CR53","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1016\/j.mce.2013.09.034","volume":"385","author":"VG Thackray","year":"2014","unstructured":"Thackray, V. G. Fox tales: regulation of gonadotropin gene expression by forkhead transcription factors. Mol Cell Endocrinol 385, 62\u201370. https:\/\/doi.org\/10.1016\/j.mce.2013.09.034 (2014).","journal-title":"Mol Cell Endocrinol"},{"key":"80003_CR54","doi-asserted-by":"publisher","DOI":"10.1016\/j.mce.2022.111675","volume":"552","author":"M Yang","year":"2022","unstructured":"Yang, M. et al. Corticosterone triggers anti-proliferative and apoptotic effects, and downregulates the ACVR1-SMAD1-ID3 cascade in chicken ovarian prehierarchical, but not preovulatory granulosa cells. Mol Cell Endocrinol 552, 111675. https:\/\/doi.org\/10.1016\/j.mce.2022.111675 (2022).","journal-title":"Mol Cell Endocrinol"},{"key":"80003_CR55","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.854312","volume":"13","author":"TT Luu","year":"2022","unstructured":"Luu, T. T. et al. FOXO1 and FOXO3 Cooperatively Regulate Innate Lymphoid Cell Development. Front Immunol 13, 854312. https:\/\/doi.org\/10.3389\/fimmu.2022.854312 (2022).","journal-title":"Front Immunol"},{"key":"80003_CR56","doi-asserted-by":"publisher","unstructured":"Zhang, S. et al. PAX3-FOXO1 coordinates enhancer architecture, eRNA transcription, and RNA polymerase pause release at select gene targets. Mol Cell 82, 4428\u20134442 e4427, https:\/\/doi.org\/10.1016\/j.molcel.2022.10.025 (2022).","DOI":"10.1016\/j.molcel.2022.10.025"},{"key":"80003_CR57","doi-asserted-by":"publisher","first-page":"2691","DOI":"10.1007\/s00018-009-0045-z","volume":"66","author":"JT Dong","year":"2009","unstructured":"Dong, J. T. & Chen, C. Essential role of KLF5 transcription factor in cell proliferation and differentiation and its implications for human diseases. Cell Mol Life Sci 66, 2691\u20132706. https:\/\/doi.org\/10.1007\/s00018-009-0045-z (2009).","journal-title":"Cell Mol Life Sci"},{"key":"80003_CR58","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1161\/CIRCRESAHA.120.316738","volume":"128","author":"ID Kyriazis","year":"2021","unstructured":"Kyriazis, I. D. et al. KLF5 Is Induced by FOXO1 and Causes Oxidative Stress and Diabetic Cardiomyopathy. Circ Res 128, 335\u2013357. https:\/\/doi.org\/10.1161\/CIRCRESAHA.120.316738 (2021).","journal-title":"Circ Res"},{"key":"80003_CR59","doi-asserted-by":"publisher","unstructured":"Liu, L. et al. Identification of a KLF5-dependent program and drug development for skeletal muscle atrophy. Proc Natl Acad Sci U S A 118, https:\/\/doi.org\/10.1073\/pnas.2102895118 (2021).","DOI":"10.1073\/pnas.2102895118"},{"key":"80003_CR60","doi-asserted-by":"publisher","first-page":"6902906","DOI":"10.1155\/2019\/6902906","volume":"2019","author":"C Cui","year":"2019","unstructured":"Cui, C. et al. FOXO3 Is Expressed in Ovarian Tissues and Acts as an Apoptosis Initiator in Granulosa Cells of Chickens. Biomed Res Int 2019, 6902906. https:\/\/doi.org\/10.1155\/2019\/6902906 (2019).","journal-title":"Biomed Res Int"},{"key":"80003_CR61","doi-asserted-by":"publisher","DOI":"10.1038\/cddis.2014.400","volume":"5","author":"M Shen","year":"2014","unstructured":"Shen, M. et al. Involvement of FoxO1 in the effects of follicle-stimulating hormone on inhibition of apoptosis in mouse granulosa cells. Cell Death Dis 5, e1475. https:\/\/doi.org\/10.1038\/cddis.2014.400 (2014).","journal-title":"Cell Death Dis"},{"key":"80003_CR62","doi-asserted-by":"publisher","first-page":"R103","DOI":"10.1530\/JME-14-0220","volume":"53","author":"A Makker","year":"2014","unstructured":"Makker, A., Goel, M. M. & Mahdi, A. A. PI3K\/PTEN\/Akt and TSC\/mTOR signaling pathways, ovarian dysfunction, and infertility: an update. J Mol Endocrinol 53, R103-118. https:\/\/doi.org\/10.1530\/JME-14-0220 (2014).","journal-title":"J Mol Endocrinol"},{"key":"80003_CR63","doi-asserted-by":"publisher","first-page":"649","DOI":"10.1210\/me.2008-0412","volume":"23","author":"Z Liu","year":"2009","unstructured":"Liu, Z. et al. FSH and FOXO1 regulate genes in the sterol\/steroid and lipid biosynthetic pathways in granulosa cells. Mol Endocrinol 23, 649\u2013661. https:\/\/doi.org\/10.1210\/me.2008-0412 (2009).","journal-title":"Mol Endocrinol"},{"key":"80003_CR64","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1007\/978-1-4419-1599-3_17","volume":"665","author":"JJ Brosens","year":"2009","unstructured":"Brosens, J. J., Wilson, M. S. & Lam, E. W. FOXO transcription factors: from cell fate decisions to regulation of human female reproduction. Adv Exp Med Biol 665, 227\u2013241. https:\/\/doi.org\/10.1007\/978-1-4419-1599-3_17 (2009).","journal-title":"Adv Exp Med Biol"},{"key":"80003_CR65","doi-asserted-by":"publisher","unstructured":"Koch, S. Regulation of Wnt Signaling by FOX Transcription Factors in Cancer. Cancers (Basel) 13, https:\/\/doi.org\/10.3390\/cancers13143446 (2021).","DOI":"10.3390\/cancers13143446"},{"key":"80003_CR66","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1186\/s13046-019-1174-3","volume":"38","author":"J Ling","year":"2019","unstructured":"Ling, J. et al. FOXO1-regulated lncRNA LINC01197 inhibits pancreatic adenocarcinoma cell proliferation by restraining Wnt\/beta-catenin signaling. J Exp Clin Cancer Res 38, 179. https:\/\/doi.org\/10.1186\/s13046-019-1174-3 (2019).","journal-title":"J Exp Clin Cancer Res"},{"key":"80003_CR67","doi-asserted-by":"publisher","first-page":"3731","DOI":"10.1242\/dev.024653","volume":"135","author":"NL Manuylov","year":"2008","unstructured":"Manuylov, N. L., Smagulova, F. O., Leach, L. & Tevosian, S. G. Ovarian development in mice requires the GATA4-FOG2 transcription complex. Development 135, 3731\u20133743. https:\/\/doi.org\/10.1242\/dev.024653 (2008).","journal-title":"Development"},{"key":"80003_CR68","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1159\/000350687","volume":"7","author":"B Nicol","year":"2013","unstructured":"Nicol, B. et al. Follistatin is an early player in rainbow trout ovarian differentiation and is both colocalized with aromatase and regulated by the wnt pathway. Sex Dev 7, 267\u2013276. https:\/\/doi.org\/10.1159\/000350687 (2013).","journal-title":"Sex Dev"},{"key":"80003_CR69","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1095\/biolreprod59.2.271","volume":"59","author":"AJ Davis","year":"1998","unstructured":"Davis, A. J. & Johnson, P. A. Expression pattern of messenger ribonucleic acid for follistatin and the inhibin\/activin subunits during follicular and testicular development in gallus domesticus. Biol Reprod 59, 271\u2013277. https:\/\/doi.org\/10.1095\/biolreprod59.2.271 (1998).","journal-title":"Biol Reprod"},{"key":"80003_CR70","doi-asserted-by":"publisher","unstructured":"Chen, R. et al. Immuno-Neutralization of Follistatin Bioactivity Enhances the Developmental Potential of Ovarian Pre-hierarchical Follicles in Yangzhou Geese. Animals (Basel) 12, https:\/\/doi.org\/10.3390\/ani12172275 (2022).","DOI":"10.3390\/ani12172275"},{"key":"80003_CR71","doi-asserted-by":"publisher","first-page":"7802","DOI":"10.1128\/MCB.02179-06","volume":"27","author":"D Sinner","year":"2007","unstructured":"Sinner, D. et al. Sox17 and Sox4 differentially regulate beta-catenin\/T-cell factor activity and proliferation of colon carcinoma cells. Mol Cell Biol 27, 7802\u20137815. https:\/\/doi.org\/10.1128\/MCB.02179-06 (2007).","journal-title":"Mol Cell Biol"},{"key":"80003_CR72","doi-asserted-by":"publisher","first-page":"65","DOI":"10.1016\/j.semcancer.2019.08.008","volume":"67","author":"DS Tan","year":"2020","unstructured":"Tan, D. S., Holzner, M., Weng, M., Srivastava, Y. & Jauch, R. SOX17 in cellular reprogramming and cancer. Semin Cancer Biol 67, 65\u201373. https:\/\/doi.org\/10.1016\/j.semcancer.2019.08.008 (2020).","journal-title":"Semin Cancer Biol"},{"key":"80003_CR73","doi-asserted-by":"publisher","first-page":"3031","DOI":"10.1210\/en.2007-0044","volume":"148","author":"N Nakao","year":"2007","unstructured":"Nakao, N. et al. Circadian clock gene regulation of steroidogenic acute regulatory protein gene expression in preovulatory ovarian follicles. Endocrinology 148, 3031\u20133038. https:\/\/doi.org\/10.1210\/en.2007-0044 (2007).","journal-title":"Endocrinology"},{"key":"80003_CR74","doi-asserted-by":"publisher","first-page":"14295","DOI":"10.1073\/pnas.1209249111","volume":"111","author":"Y Liu","year":"2014","unstructured":"Liu, Y. et al. Loss of BMAL1 in ovarian steroidogenic cells results in implantation failure in female mice. Proc Natl Acad Sci U S A 111, 14295\u201314300. https:\/\/doi.org\/10.1073\/pnas.1209249111 (2014).","journal-title":"Proc Natl Acad Sci U S A"},{"key":"80003_CR75","doi-asserted-by":"publisher","DOI":"10.1016\/j.psj.2023.103159","volume":"102","author":"R Chen","year":"2023","unstructured":"Chen, R. et al. Circadian clock gene BMAL1 regulates STAR expression in goose ovarian preovulatory granulosa cells. Poult Sci 102, 103159. https:\/\/doi.org\/10.1016\/j.psj.2023.103159 (2023).","journal-title":"Poult Sci"},{"key":"80003_CR76","doi-asserted-by":"publisher","first-page":"10","DOI":"10.3109\/07420528.2010.530363","volume":"28","author":"SA Tischkau","year":"2011","unstructured":"Tischkau, S. A., Howell, R. E., Hickok, J. R., Krager, S. L. & Bahr, J. M. The luteinizing hormone surge regulates circadian clock gene expression in the chicken ovary. Chronobiol Int 28, 10\u201320. https:\/\/doi.org\/10.3109\/07420528.2010.530363 (2011).","journal-title":"Chronobiol Int"},{"key":"80003_CR77","doi-asserted-by":"publisher","DOI":"10.1016\/j.psj.2024.104547","author":"AE Kramer","year":"2024","unstructured":"Kramer, A. E. et al. Transcriptomic data reveals MYC as an upstream regulator in laying hen follicular recruitment. Poultry Science.  https:\/\/doi.org\/10.1016\/j.psj.2024.104547 (2024).","journal-title":"Poultry Science"},{"key":"80003_CR78","doi-asserted-by":"publisher","unstructured":"Papachristodoulou, A. et al. Metformin Overcomes the Consequences of NKX3.1 Loss to Suppress Prostate Cancer Progression. Eur Urol 85 (4), 361\u2013372, https:\/\/doi.org\/10.1016\/j.eururo.2023.07.016 (2024).","DOI":"10.1016\/j.eururo.2023.07.016"},{"key":"80003_CR79","doi-asserted-by":"publisher","first-page":"2015","DOI":"10.1101\/pdb.top084970","volume":"951\u2013969","author":"KR Kukurba","year":"2015","unstructured":"Kukurba, K. R. & Montgomery, S. B. RNA Sequencing and Analysis. Cold Spring Harb Protoc 951\u2013969, 2015. https:\/\/doi.org\/10.1101\/pdb.top084970 (2015).","journal-title":"Cold Spring Harb Protoc"},{"key":"80003_CR80","doi-asserted-by":"publisher","first-page":"16853","DOI":"10.1038\/s41598-018-35203-y","volume":"8","author":"N Sah","year":"2018","unstructured":"Sah, N. et al. RNA sequencing-based analysis of the laying hen uterus revealed the novel genes and biological pathways involved in the eggshell biomineralization. Sci Rep 8, 16853. https:\/\/doi.org\/10.1038\/s41598-018-35203-y (2018).","journal-title":"Sci Rep"},{"key":"80003_CR81","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1038\/nrg2484","volume":"10","author":"Z Wang","year":"2009","unstructured":"Wang, Z., Gerstein, M. & Snyder, M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10, 57\u201363. https:\/\/doi.org\/10.1038\/nrg2484 (2009).","journal-title":"Nat Rev Genet"},{"issue":"Suppl 4","key":"80003_CR82","doi-asserted-by":"publisher","first-page":"283","DOI":"10.1111\/j.1439-0531.2012.02087.x","volume":"47","author":"PA Johnson","year":"2012","unstructured":"Johnson, P. A. Follicle selection in the avian ovary. Reprod Domest Anim 47(Suppl 4), 283\u2013287. https:\/\/doi.org\/10.1111\/j.1439-0531.2012.02087.x (2012).","journal-title":"Reprod Domest Anim"},{"key":"80003_CR83","doi-asserted-by":"publisher","unstructured":"Griffin, A. T., Vlahos, L. J., Chiuzan, C. & Califano, A. NaRnEA: An Information Theoretic Framework for Gene Set Analysis. Entropy (Basel) 25, https:\/\/doi.org\/10.3390\/e25030542 (2023).","DOI":"10.3390\/e25030542"},{"key":"80003_CR84","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","volume":"26","author":"MD Robinson","year":"2010","unstructured":"Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139\u2013140. https:\/\/doi.org\/10.1093\/bioinformatics\/btp616 (2010).","journal-title":"Bioinformatics"},{"key":"80003_CR85","doi-asserted-by":"publisher","first-page":"838","DOI":"10.1038\/ng.3593","volume":"48","author":"MJ Alvarez","year":"2016","unstructured":"Alvarez, M. J. et al. Functional characterization of somatic mutations in cancer using network-based inference of protein activity. Nat Genet 48, 838\u2013847. https:\/\/doi.org\/10.1038\/ng.3593 (2016).","journal-title":"Nat Genet"},{"key":"80003_CR86","doi-asserted-by":"publisher","first-page":"93","DOI":"10.1093\/bioinformatics\/btg382","volume":"20","author":"JJ Goeman","year":"2004","unstructured":"Goeman, J. J., van de Geer, S. A., de Kort, F. & van Houwelingen, H. C. A global test for groups of genes: testing association with a clinical outcome. Bioinformatics 20, 93\u201399. https:\/\/doi.org\/10.1093\/bioinformatics\/btg382 (2004).","journal-title":"Bioinformatics"},{"key":"80003_CR87","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.1038\/nprot.2008.73","volume":"3","author":"TD Schmittgen","year":"2008","unstructured":"Schmittgen, T. D. & Livak, K. J. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3, 1101\u20131108. https:\/\/doi.org\/10.1038\/nprot.2008.73 (2008).","journal-title":"Nat Protoc"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-80003-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-80003-2","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-80003-2.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,12,28]],"date-time":"2024-12-28T14:03:22Z","timestamp":1735394602000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-024-80003-2"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,28]]},"references-count":87,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["80003"],"URL":"https:\/\/doi.org\/10.1038\/s41598-024-80003-2","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,28]]},"assertion":[{"value":"28 June 2024","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"14 November 2024","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"28 December 2024","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"All animal research reported in this manuscript are as per ARRIVE guidelines.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical approval"}}],"article-number":"30787"}}