{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,31]],"date-time":"2026-10-31T20:48:47Z","timestamp":1793479727136,"version":"4.5.0"},"reference-count":93,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,10,22]],"date-time":"2025-10-22T00:00:00Z","timestamp":1761091200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Vet. Sci."],"abstract":"<jats:p>\n                    The hypothalamic\u2013pituitary-ovarian (HPO) axis serves as the pivotal regulatory system governing reproduction in chickens. This study performed whole transcriptome sequencing on hypothalamus, pituitary, and ovarian tissues of Bian chickens to identify differentially expressed (DE) lncRNAs, miRNAs, and mRNAs (\n                    <jats:italic>p<\/jats:italic>\n                    \u202f&amp;lt;\u202f0.05, FC\u202f&amp;gt;\u202f2) between low- and high-laying groups. The hypothalamus exhibited 57 DE lncRNAs, 86 DE miRNAs, and 36 DE mRNAs; the pituitary showed the highest numbers with 206 DE lncRNAs, 234 DE miRNAs, and 528 DE mRNAs; while the ovary contained 111 lncRNAs, 230 miRNAs, and 62 mRNAs. GO functional enrichment analysis indicated that trans-target genes of hypothalamic and pituitary DE lncRNAs were enriched in cell proliferation Biological process (BP) terms (e.g., cell cycle, mitotic cell cycle). Hypothalamic miRNA targets clustered in metabolic regulation (cellular metabolic process), whereas pituitary miRNAs governed transport processes (nitrogen compound transport, intracellular transport). DE mRNAs showed BP terms enrichment in serotonin biosynthesis process, pituitary gland development, and DNA integration. KEGG pathway enrichment analysis revealed that lncRNA targets were significantly enriched in Progesterone-mediated oocyte maturation and Oocyte meiosis pathways in both hypothalamus and pituitary, with additional enrichment in Cell cycle and DNA replication. Notably, miRNA target genes showed conserved enrichment in metabolic regulation-related pathways (Metabolic pathways, Cysteine and methionine metabolism) across all three tissues. Key enriched pathways for DE mRNAs included Steroid biosynthesis, Cortisol synthesis and secretion, and Hippo signaling pathway. Finally, we constructed lncRNA-mRNA and miRNA-mRNA pairwise interaction networks, as well as ceRNA regulatory networks, through which we identified key regulatory networks targeting critical DE mRNAs, including\n                    <jats:italic>GATA4, SMAD3, FOXL2, INHBA, POU1F1, LHX3, SPP1, SNAP25, COLQ,<\/jats:italic>\n                    and\n                    <jats:italic>AMPH<\/jats:italic>\n                    . These results elucidate the multi-tissue molecular mechanisms underlying egg-laying performance in chickens, providing novel targets for improving poultry reproductive efficiency through marker-assisted breeding.\n                  <\/jats:p>","DOI":"10.3389\/fvets.2025.1687863","type":"journal-article","created":{"date-parts":[[2025,10,22]],"date-time":"2025-10-22T04:17:52Z","timestamp":1761106672000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Whole transcriptome sequencing reveals the functional regulation of chicken reproduction by lncRNAs, miRNAs, and mRNAs across the hypothalamus-pituitary-ovary axis"],"prefix":"10.3389","volume":"12","author":[{"given":"Peifeng","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chengzhu","family":"Chu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lijuan","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Genxi","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pengfei","family":"Wu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,10,22]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"1088","DOI":"10.24272\/j.issn.2095-8137.2024.037","article-title":"Single nucleus\/cell RNA-Seq of the chicken hypothalamic-pituitary-ovarian axis offers new insights into the molecular regulatory mechanisms of ovarian development","volume":"45","author":"Leng","year":"2024","journal-title":"Zool Res"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1016\/j.psj.2019.12.028","article-title":"Characterization of the Hypothalamo-pituitary-gonadal Axis in low and high egg producing Turkey hens","volume":"99","author":"Brady","year":"2020","journal-title":"Poult Sci"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1469","DOI":"10.1093\/humrep\/deab065","article-title":"Reduced Fsh and Lh action: implications for medically assisted reproduction","volume":"36","author":"Bosch","year":"2021","journal-title":"Hum Reprod"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"8229","DOI":"10.1038\/s41598-024-58064-0","article-title":"Mechanism of elevated Lh\/Fsh ratio in lean Pcos revisited: a path analysis","volume":"14","author":"Pratama","year":"2024","journal-title":"Sci Rep"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"105737","DOI":"10.1016\/j.rvsc.2025.105737","article-title":"Dose- and time-dependent effects of intravenous Irisin administration on Gnrh, Lh, Fsh, and estrogen in Kurdish ewes during the breeding season","volume":"193","author":"Shokrollahi","year":"2025","journal-title":"Res Vet Sci"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"5976","DOI":"10.1038\/s41598-020-62886-z","article-title":"Transcriptome analysis reveals differentially expressed genes associated with high rates of egg production in chicken hypothalamic-pituitary-ovarian Axis","volume":"10","author":"Mishra","year":"2020","journal-title":"Sci Rep"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"651491","DOI":"10.3389\/fphys.2021.651491","article-title":"Changes in the control of the hypothalamic-pituitary gonadal Axis across three differentially selected strains of laying hens (Gallus Gallus Domesticus)","volume":"12","author":"Hanlon","year":"2021","journal-title":"Front Physiol"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"e12590","DOI":"10.1111\/jne.12590","article-title":"Emerging insights into hypothalamic-pituitary-gonadal Axis regulation and interaction with stress Signalling","volume":"30","author":"Acevedo-Rodriguez","year":"2018","journal-title":"J Neuroendocrinol"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"103820","DOI":"10.1016\/j.psj.2024.103820","article-title":"Estrogen promotes gonadotropin-releasing hormone expression by regulating tachykinin 3 and Prodynorphin Systems in Chicken","volume":"103","author":"Wu","year":"2024","journal-title":"Poult Sci"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"591672","DOI":"10.3389\/fgene.2020.591672","article-title":"Novel regulatory factors in the hypothalamic-pituitary-ovarian Axis of hens at four developmental stages","volume":"11","author":"Li","year":"2020","journal-title":"Front Genet"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"103478","DOI":"10.1016\/j.psj.2024.103478","article-title":"Molecular mechanisms of hypothalamic-pituitary-ovarian\/thyroid Axis regulating age at first egg in geese","volume":"103","author":"He","year":"2024","journal-title":"Poult Sci"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"105837","DOI":"10.1016\/j.psj.2025.105837","article-title":"Dhcr7 expression, function and estrogen-induced promoter histone modification changes in chicken granulosa cells of pre-hierarchical follicles","volume":"104","author":"Li","year":"2025","journal-title":"Poult Sci"},{"key":"ref13","doi-asserted-by":"publisher","first-page":"141","DOI":"10.3390\/genes14010141","article-title":"Interacting networks of the hypothalamic-pituitary-ovarian Axis regulate layer hens performance","volume":"14","author":"Zhao","year":"2023","journal-title":"Genes (Basel)"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"157","DOI":"10.3390\/genes10020157","article-title":"Pituitary transcriptomic study reveals the differential regulation of Lncrnas and Mrnas related to prolificacy in different Fecb genotyping sheep","volume":"10","author":"Zheng","year":"2019","journal-title":"Genes"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"985","DOI":"10.3390\/cells11060985","article-title":"The novel competing endogenous Long noncoding Rna Sm2 regulates gonadotropin secretion in the Hu sheep anterior pituitary by targeting the oar-Mir-16b\/Tgf-\u0392\/Smad2 signaling pathway","volume":"11","author":"Wan","year":"2022","journal-title":"Cells"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"110969","DOI":"10.1016\/j.mce.2020.110969","article-title":"The role of Mir-7 as a potential switch in the mouse hypothalamus-pituitary-ovary Axis through regulation of gonadotropins","volume":"518","author":"He","year":"2020","journal-title":"Mol Cell Endocrinol"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"1583287","DOI":"10.3389\/fvets.2025.1583287","article-title":"Lnc Mstrg 4701.7 targets Mir-1786\/Rora to competitively regulate proliferation and apoptosis in chicken follicular granulosa cells","volume":"12","author":"Ma","year":"2025","journal-title":"Front Vet Sci"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"457","DOI":"10.3390\/cimb43020036","article-title":"A comprehensive analysis of northern versus liquid hybridization assays for Mrnas, small Rnas, and Mirnas using a non-radiolabeled approach","volume":"43","author":"Ahmad","year":"2021","journal-title":"Curr Issues Mol Biol"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"531","DOI":"10.1186\/s12864-024-10439-3","article-title":"Mfpinc: prediction of plant Ncrnas based on multi-source feature fusion","volume":"25","author":"Nie","year":"2024","journal-title":"BMC Genomics"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1038\/nrg2484","article-title":"Rna-Seq: a revolutionary tool for Transcriptomics","volume":"10","author":"Wang","year":"2009","journal-title":"Nat Rev Genet"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"135","DOI":"10.3389\/fgene.2020.00135","article-title":"Pituitary-derived circular Rnas expression and regulatory network prediction during the onset of puberty in landrace \u00d7 Yorkshire crossbred pigs","volume":"11","author":"Chen","year":"2020","journal-title":"Front Genet"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"147024","DOI":"10.1016\/j.ijbiomac.2025.147024","article-title":"Comprehensive transcriptomic analysis of the hypothalamic-pituitary-ovarian Axis reveals the role of Aurora kinase B in regulating follicular granulosa cell development and steroid hormone synthesis in Wuding chickens","volume":"322","author":"Fan","year":"2025","journal-title":"Int J Biol Macromol"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"1100","DOI":"10.1186\/s12864-024-11035-1","article-title":"Pituitary whole transcriptome analysis reveals key genes regulating reproduction in Hy-line Brown hens and the construction of their Cerna molecular regulatory network","volume":"25","author":"Li","year":"2024","journal-title":"BMC Genomics"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"i884","DOI":"10.1093\/bioinformatics\/bty560","article-title":"Fastp: an ultra-fast all-in-one Fastq preprocessor","volume":"34","author":"Chen","year":"2018","journal-title":"Bioinformatics"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with bowtie 2","volume":"9","author":"Langmead","year":"2012","journal-title":"Nat Methods"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1038\/nmeth.3317","article-title":"Hisat: a fast spliced aligner with low memory requirements","volume":"12","author":"Kim","year":"2015","journal-title":"Nat Methods"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"290","DOI":"10.1038\/nbt.3122","article-title":"Stringtie enables improved reconstruction of a transcriptome from Rna-Seq reads","volume":"33","author":"Pertea","year":"2015","journal-title":"Nat Biotechnol"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"e166","DOI":"10.1093\/nar\/gkt646","article-title":"Utilizing sequence intrinsic composition to classify protein-coding and Long non-coding transcripts","volume":"41","author":"Sun","year":"2013","journal-title":"Nucleic Acids Res"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"W12","DOI":"10.1093\/nar\/gkx428","article-title":"Cpc2: a fast and accurate coding potential calculator based on sequence intrinsic features","volume":"45","author":"Kang","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"R25","DOI":"10.1186\/gb-2009-10-3-r25","article-title":"Ultrafast and memory-efficient alignment of Short DNA sequences to the human genome","volume":"10","author":"Langmead","year":"2009","journal-title":"Genome Biol"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"37","DOI":"10.1093\/nar\/gkr688","article-title":"Mirdeep2 accurately identifies known and hundreds of novel Microrna genes in seven animal clades","volume":"40","author":"Friedl\u00e4nder","year":"2012","journal-title":"Nucleic Acids Res"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"550","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for Rna-Seq data with Deseq2","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"139","DOI":"10.1093\/bioinformatics\/btp616","article-title":"Edger: a bioconductor package for differential expression analysis of digital gene expression data","volume":"26","author":"Robinson","year":"2010","journal-title":"Bioinformatics"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2022\/1393392","article-title":"Advanced practical strategies to enhance table egg production","volume":"2022","author":"El-Sabrout","year":"2022","journal-title":"Scientifica (Cairo)"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"1","DOI":"10.31487\/j.JFNM.2020.03.02","article-title":"The role of chicken eggs in human nutrition","volume":"3","author":"Lei","year":"2021","journal-title":"J Food Nutr Metab"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.4236\/fns.2015.613127","article-title":"An updated review on chicken eggs: production, consumption, management aspects and nutritional benefits to human health","volume":"6","author":"Zaheer","year":"2015","journal-title":"Food Nutr Sci"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1111\/nure.12107","article-title":"Eggs: the Uncracked potential for improving maternal and young child nutrition among the world's poor","volume":"72","author":"Iannotti","year":"2014","journal-title":"Nutr Rev"},{"key":"ref38","article-title":"Eggs: harnessing their Power for the fight against hunger and malnutrition global forum on food security and nutrition (Fsn forum)","author":"Otekunrin","year":"2019"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"2208","DOI":"10.3382\/ps\/pew137","article-title":"Biology of stress in poultry with emphasis on glucocorticoids and the Heterophil to lymphocyte ratio","volume":"95","author":"Scanes","year":"2016","journal-title":"Poult Sci"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.aninu.2017.03.001","article-title":"Nutritional modulation of health, egg quality and environmental pollution of the layers","volume":"3","author":"Wang","year":"2017","journal-title":"Anim Nutr"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"89","DOI":"10.3390\/insects16010089","article-title":"Challenges of Dermanyssus Gallinae in poultry: biological insights, economic impact and management strategies","volume":"16","author":"S\u00e1rk\u00e1ny","year":"2025","journal-title":"Insects"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1111\/jpn.14032","article-title":"Abiotic stressors in poultry production: a comprehensive review","volume":"109","author":"Ncho","year":"2025","journal-title":"J Anim Physiol Anim Nutr (Berl)"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"1197","DOI":"10.1007\/s43032-019-00131-3","article-title":"Metabolic lateralization in the hypothalamus of male rats related to reproductive and satiety states","volume":"27","author":"Kiss","year":"2020","journal-title":"Reprod Sci"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"4694","DOI":"10.3390\/ijms25094694","article-title":"Single-cell transcriptional profile construction of rat pituitary glands before and after sexual maturation and identification of novel marker Spp1 in Gonadotropes","volume":"25","author":"Huang","year":"2024","journal-title":"Int J Mol Sci"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"362","DOI":"10.1038\/s41419-021-03634-7","article-title":"Adgra1 negatively regulates energy expenditure and thermogenesis through both sympathetic nervous system and hypothalamus-pituitary-thyroid Axis in male mice","volume":"12","author":"Zhang","year":"2021","journal-title":"Cell Death Dis"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"e12961","DOI":"10.1111\/jpi.12961","article-title":"Melatonin in energy control: circadian time-giver and homeostatic monitor","volume":"76","author":"Challet","year":"2024","journal-title":"J Pineal Res"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"35014","DOI":"10.1021\/acsomega.4c04998","article-title":"Pacs-1 interacts with Trpc3 and Esyt1 to mediate protein trafficking while promoting Soce and cooperatively regulating hormone secretion","volume":"9","author":"Trothen","year":"2024","journal-title":"ACS Omega"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"180","DOI":"10.1016\/j.fertnstert.2022.12.005","article-title":"Rerouting of follicle-stimulating hormone secretion and gonadal function","volume":"119","author":"Kumar","year":"2023","journal-title":"Fertil Steril"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"e22","DOI":"10.15190\/d.2014.14","article-title":"Insights into the nanobiology of growth hormone secretion","volume":"2","author":"Anderson","year":"2014","journal-title":"Discoveries (Craiova)"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"1541075","DOI":"10.3389\/fnins.2025.1541075","article-title":"Hypothalamus-pituitary-adrenal and gut-brain axes in biological interaction pathway of the depression","volume":"19","author":"Bertollo","year":"2025","journal-title":"Front Neurosci"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"1764","DOI":"10.1080\/15476286.2019.1657743","article-title":"Deep sequencing of small non-coding Rna highlights brain-specific expression patterns and Rna cleavage","volume":"16","author":"Haack","year":"2019","journal-title":"RNA Biol"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"8063","DOI":"10.3168\/jds.2018-14798","article-title":"Genomic heritability and genome-wide association analysis of anti-M\u00fcllerian hormone in Holstein dairy heifers","volume":"101","author":"Nawaz","year":"2018","journal-title":"J Dairy Sci"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"13","DOI":"10.7554\/eLife.92635","article-title":"Progesterone induces meiosis through two obligate co-receptors with Pla2 activity","volume":"13","author":"Nader","year":"2025","journal-title":"eLife"},{"key":"ref54","doi-asserted-by":"publisher","first-page":"37","DOI":"10.3389\/fendo.2015.00037","article-title":"Nuclear progestin receptor (Pgr) knockouts in zebrafish demonstrate role for Pgr in ovulation but not in rapid non-genomic steroid mediated meiosis resumption","volume":"6","author":"Zhu","year":"2015","journal-title":"Front Endocrinol (Lausanne)"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"654028","DOI":"10.3389\/fcell.2021.654028","article-title":"Mechanisms of oocyte maturation and related epigenetic regulation","volume":"9","author":"He","year":"2021","journal-title":"Front Cell Dev Biol"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1083\/jcb.136.4.919","article-title":"Cross-talk between adherens junctions and desmosomes depends on plakoglobin","volume":"136","author":"Lewis","year":"1997","journal-title":"J Cell Biol"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"660","DOI":"10.1016\/j.bbamem.2007.07.012","article-title":"Adherens and tight junctions: structure, function and connections to the actin cytoskeleton","volume":"1778","author":"Hartsock","year":"2008","journal-title":"Biochim Biophys Acta"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"289","DOI":"10.1016\/j.physbeh.2004.02.007","article-title":"Energy balance and reproduction","volume":"81","author":"Schneider","year":"2004","journal-title":"Physiol Behav"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"790","DOI":"10.1210\/me.2013-1413","article-title":"Minireview: metabolism of female reproduction: regulatory mechanisms and clinical implications","volume":"28","author":"Seli","year":"2014","journal-title":"Mol Endocrinol"},{"key":"ref60","doi-asserted-by":"publisher","first-page":"a016964","DOI":"10.1101\/cshperspect.a016964","article-title":"Reciprocal regulation of endocytosis and metabolism","volume":"6","author":"Antonescu","year":"2014","journal-title":"Cold Spring Harb Perspect Biol"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.ceb.2015.05.005","article-title":"Effects of endocytosis on receptor-mediated signaling","volume":"35","author":"Irannejad","year":"2015","journal-title":"Curr Opin Cell Biol"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"939","DOI":"10.14218\/jcth.2022.00067","article-title":"Reactive oxygen species and oxidative stress in the pathogenesis of Mafld","volume":"10","author":"Clare","year":"2022","journal-title":"J Clin Transl Hepatol"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"1469","DOI":"10.1002\/cbin.12065","article-title":"The role of peroxisome proliferator-activated receptor \u0393 in lipid metabolism and inflammation in atherosclerosis","volume":"47","author":"Yang","year":"2023","journal-title":"Cell Biol Int"},{"key":"ref64","doi-asserted-by":"publisher","first-page":"653","DOI":"10.3390\/antiox13060653","article-title":"Vitamin C alleviates the negative effects of heat stress on reproductive processes by regulating amino acid metabolism in granulosa cells","volume":"13","author":"Sammad","year":"2024","journal-title":"Antioxidants"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"849","DOI":"10.1016\/j.aninu.2021.02.006","article-title":"Effect of gestation dietary methionine-to-lysine ratio on methionine metabolism and antioxidant ability of high-prolific sows","volume":"7","author":"Xia","year":"2021","journal-title":"Anim Nutr"},{"key":"ref66","doi-asserted-by":"publisher","first-page":"1443","DOI":"10.3390\/antiox13121443","article-title":"Protective effects of L-cysteine against cisplatin-induced oxidative stress-mediated reproductive damage","volume":"13","author":"Chiang","year":"2024","journal-title":"Antioxidants (Basel)"},{"key":"ref67","doi-asserted-by":"publisher","first-page":"233","DOI":"10.1081\/erc-100107184","article-title":"Camp-induced apoptosis in granulosa cells is associated with up-regulation of P53 and Bax and down-regulation of clusterin","volume":"27","author":"Zwain","year":"2001","journal-title":"Endocr Res"},{"key":"ref68","doi-asserted-by":"publisher","first-page":"20","DOI":"10.3892\/mmr.2020.11658","article-title":"Role of the Sirt1\/P53 regulatory Axis in oxidative stress-mediated granulosa cell apoptosis","volume":"23","author":"Park","year":"2021","journal-title":"Mol Med Rep"},{"key":"ref69","doi-asserted-by":"publisher","first-page":"1291","DOI":"10.3390\/cells11081291","article-title":"Protective effect of follicle-stimulating hormone on DNA damage of chicken follicular granulosa cells by inhibiting Chk2\/P53","volume":"11","author":"Zhou","year":"2022","journal-title":"Cells"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"67","DOI":"10.1016\/j.cbd.2018.11.004","article-title":"Comparative Transcriptology reveals effects of circadian rhythm in the nervous system on precocious puberty of the female Chinese mitten crab","volume":"29","author":"Fu","year":"2019","journal-title":"Comp Biochem Physiol Part D Genomics Proteomics"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"21559","DOI":"10.1038\/srep21559","article-title":"Progestins Alter photo-transduction Cascade and circadian rhythm network in eyes of zebrafish (Danio Rerio)","volume":"6","author":"Zhao","year":"2016","journal-title":"Sci Rep"},{"key":"ref72","doi-asserted-by":"publisher","first-page":"166834","DOI":"10.1016\/j.scitotenv.2023.166834","article-title":"Ioxynil and diethylstilbestrol impair cardiac performance and shell growth in the mussel Mytilus coruscus","volume":"905","author":"Li","year":"2023","journal-title":"Sci Total Environ"},{"key":"ref73","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10695-020-00859-9","article-title":"Identification of reproduction-related genes and pathways in the Culter Alburnus H-P-G Axis and characterization of their expression differences in malformed and Normal Gynogenetic ovaries","volume":"47","author":"Jia","year":"2021","journal-title":"Fish Physiol Biochem"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"744","DOI":"10.3389\/fendo.2019.00744","article-title":"Integrated analysis of Mrna and Mirna expression profiles in the ovary of Oryctolagus Cuniculus in response to gonadotrophic stimulation","volume":"10","author":"Hu","year":"2019","journal-title":"Front Endocrinol (Lausanne)"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"1613","DOI":"10.1007\/s11011-024-01393-w","article-title":"Stress, hypothalamic-pituitary-adrenal Axis, hypothalamic-pituitary-gonadal Axis, and aggression","volume":"39","author":"Mbiydzenyuy","year":"2024","journal-title":"Metab Brain Dis"},{"key":"ref76","doi-asserted-by":"publisher","first-page":"1152","DOI":"10.1038\/cr.2015.114","article-title":"Ci antagonizes hippo signaling in the somatic cells of the ovary to drive germline stem cell differentiation","volume":"25","author":"Li","year":"2015","journal-title":"Cell Res"},{"key":"ref77","doi-asserted-by":"publisher","first-page":"471","DOI":"10.1016\/j.jgg.2011.09.009","article-title":"Hippo signaling: a hub of growth control, tumor suppression and pluripotency maintenance","volume":"38","author":"Yin","year":"2011","journal-title":"J Genet Genomics"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"397","DOI":"10.3390\/genes15040397","article-title":"The involvement of the microRNAs Mir-466c and Mir-340 in the palmitate-mediated dysregulation of gonadotropin-releasing hormone gene expression","volume":"15","author":"Nkechika","year":"2024","journal-title":"Genes (Basel)"},{"key":"ref79","doi-asserted-by":"publisher","first-page":"e70717","DOI":"10.1096\/fj.202401718RR","article-title":"Brain-specific Gata4 downregulation in Greywick female mice models the metabolic subtype of polycystic ovary syndrome","volume":"39","author":"Nawaito","year":"2025","journal-title":"FASEB J"},{"key":"ref80","doi-asserted-by":"publisher","first-page":"4923","DOI":"10.1038\/s41467-019-12895-y","article-title":"Hypothalamus-Hippocampus circuitry regulates impulsivity via melanin-concentrating hormone","volume":"10","author":"Noble","year":"2019","journal-title":"Nat Commun"},{"key":"ref81","doi-asserted-by":"publisher","first-page":"745","DOI":"10.1038\/s41574-021-00559-1","article-title":"Multifaceted actions of melanin-concentrating hormone on mammalian energy homeostasis","volume":"17","author":"Al-Massadi","year":"2021","journal-title":"Nat Rev Endocrinol"},{"key":"ref82","doi-asserted-by":"publisher","first-page":"170975","DOI":"10.1016\/j.peptides.2023.170975","article-title":"Melanin-concentrating hormone regulation by estradiol and progesterone in the Incerto-hypothalamic area","volume":"163","author":"Duarte","year":"2023","journal-title":"Peptides"},{"key":"ref83","doi-asserted-by":"publisher","first-page":"1849","DOI":"10.1210\/me.2004-0475","article-title":"Smad3 mediates activin-induced transcription of follicle-stimulating hormone beta-subunit gene","volume":"19","author":"Suszko","year":"2005","journal-title":"Mol Endocrinol"},{"key":"ref84","doi-asserted-by":"publisher","first-page":"7631","DOI":"10.1074\/jbc.M806676200","article-title":"Foxl2 and Smad3 coordinately regulate Follistatin gene transcription","volume":"284","author":"Blount","year":"2009","journal-title":"J Biol Chem"},{"key":"ref85","doi-asserted-by":"publisher","first-page":"5456","DOI":"10.1210\/en.2010-0605","article-title":"Activin a regulates porcine follicle-stimulating hormone Beta-subunit transcription via cooperative actions of Smads and Foxl2","volume":"151","author":"Lamba","year":"2010","journal-title":"Endocrinology"},{"key":"ref86","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1016\/j.mce.2013.03.021","article-title":"Granulosa cell tumor mutant Foxl2c134w suppresses Gdf-9 and Activin a-induced follistatin transcription in primary granulosa cells","volume":"372","author":"McTavish","year":"2013","journal-title":"Mol Cell Endocrinol"},{"key":"ref87","doi-asserted-by":"publisher","first-page":"1558","DOI":"10.1210\/me.2003-0470","article-title":"Activin inhibits pituitary prolactin expression and cell growth through Smads, Pit-1 and Menin","volume":"18","author":"Lacerte","year":"2004","journal-title":"Mol Endocrinol"},{"key":"ref88","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1095\/biolreprod.111.094904","article-title":"The forkhead transcription factor, Foxp3, is required for normal pituitary gonadotropin expression in mice","volume":"86","author":"Jung","year":"2012","journal-title":"Biol Reprod"},{"key":"ref89","doi-asserted-by":"publisher","first-page":"52","DOI":"10.1186\/s13062-024-00496-9","article-title":"Single-cell transcriptomic profiling unveils insights into ovarian fibrosis in obese mice","volume":"19","author":"Xiao","year":"2024","journal-title":"Biol Direct"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"266","DOI":"10.1007\/s00018-025-05797-4","article-title":"Sox3 facilitates granulosa cell proliferation and suppresses cell apoptosis through modulating Pi3k\/Akt pathway by targeting Spp1","volume":"82","author":"Cai","year":"2025","journal-title":"Cell Mol Life Sci"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"49","DOI":"10.1007\/s10815-023-02967-w","article-title":"In vitro evaluation of exocytosis-associated snare molecules in human granulosa cells in polycystic ovary syndrome","volume":"41","author":"Erol","year":"2024","journal-title":"J Assist Reprod Genet"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1124\/jpet.102.033746","article-title":"Wild-type and A328w mutant human Butyrylcholinesterase tetramers expressed in Chinese Hamster ovary cells have a 16-hour half-life in the circulation and protect mice from cocaine toxicity","volume":"302","author":"Duysen","year":"2002","journal-title":"J Pharmacol Exp Ther"},{"key":"ref93","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1093\/hmg\/4.2.265","article-title":"Primary structure of human Amphiphysin, the dominant autoantigen of paraneoplastic stiff-man syndrome, and mapping of its gene (Amph) to chromosome 7p13-P14","volume":"4","author":"Yamamoto","year":"1995","journal-title":"Hum Mol Genet"}],"container-title":["Frontiers in Veterinary Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2025.1687863\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,22]],"date-time":"2025-10-22T04:17:53Z","timestamp":1761106673000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fvets.2025.1687863\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,22]]},"references-count":93,"alternative-id":["10.3389\/fvets.2025.1687863"],"URL":"https:\/\/doi.org\/10.3389\/fvets.2025.1687863","relation":{},"ISSN":["2297-1769"],"issn-type":[{"value":"2297-1769","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,22]]},"article-number":"1687863"}}