{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,25]],"date-time":"2026-03-25T00:27:26Z","timestamp":1774398446335,"version":"3.50.1"},"reference-count":83,"publisher":"MDPI AG","issue":"12","license":[{"start":{"date-parts":[[2025,6,14]],"date-time":"2025-06-14T00:00:00Z","timestamp":1749859200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Project of Ministry of Agriculture and Rural Affairs of China","award":["19230558"],"award-info":[{"award-number":["19230558"]}]},{"name":"Project of Ministry of Agriculture and Rural Affairs of China","award":["19240887"],"award-info":[{"award-number":["19240887"]}]},{"name":"Project of Ministry of Agriculture and Rural Affairs of China","award":["6651122011"],"award-info":[{"award-number":["6651122011"]}]},{"name":"Project of Ministry of Agriculture and Rural Affairs of China","award":["SDAIT-27"],"award-info":[{"award-number":["SDAIT-27"]}]},{"name":"Start-up Fund for High-level Talents of Qingdao Agricultural University","award":["19230558"],"award-info":[{"award-number":["19230558"]}]},{"name":"Start-up Fund for High-level Talents of Qingdao Agricultural University","award":["19240887"],"award-info":[{"award-number":["19240887"]}]},{"name":"Start-up Fund for High-level Talents of Qingdao Agricultural University","award":["6651122011"],"award-info":[{"award-number":["6651122011"]}]},{"name":"Start-up Fund for High-level Talents of Qingdao Agricultural University","award":["SDAIT-27"],"award-info":[{"award-number":["SDAIT-27"]}]},{"name":"Donkey Innovation Team of Shandong Modern Agricultural Industry Technology System","award":["19230558"],"award-info":[{"award-number":["19230558"]}]},{"name":"Donkey Innovation Team of Shandong Modern Agricultural Industry Technology System","award":["19240887"],"award-info":[{"award-number":["19240887"]}]},{"name":"Donkey Innovation Team of Shandong Modern Agricultural Industry Technology System","award":["6651122011"],"award-info":[{"award-number":["6651122011"]}]},{"name":"Donkey Innovation Team of Shandong Modern Agricultural Industry Technology System","award":["SDAIT-27"],"award-info":[{"award-number":["SDAIT-27"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Donkeys (Equus asinus) hold significant agricultural value in China, particularly for their hides and meat, which possess notable medicinal and dietary importance. However, their reproductive efficiency remains suboptimal compared with other livestock. Ovarian function is a key determinant of fertility, yet the molecular mechanisms underlying donkey ovarian biology remain largely unexplored. To address this gap, we performed single-cell RNA sequencing of donkey ovaries, generating a high-resolution transcriptomic atlas comprising 17,423 cells. Cross-species comparative analysis revealed a high degree of evolutionary conservation in core ovarian cell types, including endothelial, epithelial, immune, and smooth muscle cells, among vertebrates. In contrast, granulosa and theca cells exhibited distinct transcriptional profiles across species, reflecting lineage-specific adaptations. Notably, we identified key genes with donkey-specific expression patterns, including NR3C1 in endothelial cells, LIPE in granulosa cells, and DHRS9 in theca interna cells. Furthermore, an in vitro cumulus\u2013oocyte complex model demonstrated the critical role of GATM in mammalian oocyte maturation. Collectively, these findings provide a comprehensive characterization of ovarian cell-type conservation and species-specific adaptations, offering key molecular insights into the mechanisms underlying cross-species differences in reproductive efficiency.<\/jats:p>","DOI":"10.3390\/ani15121761","type":"journal-article","created":{"date-parts":[[2025,6,16]],"date-time":"2025-06-16T04:06:24Z","timestamp":1750046784000},"page":"1761","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["The Transcriptomic Signature of Donkey Ovarian Tissue Revealed by Cross-Species Comparative Analysis at Single-Cell Resolution"],"prefix":"10.3390","volume":"15","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6645-269X","authenticated-orcid":false,"given":"Yu","family":"Tian","sequence":"first","affiliation":[{"name":"State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock (R2BGL), College of Life Sciences, Inner Mongolia University, Hohhot 010070, China"},{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yilin","family":"Niu","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xinhao","family":"Zhang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tao","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhe","family":"Tian","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaoyuan","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock (R2BGL), College of Life Sciences, Inner Mongolia University, Hohhot 010070, China"},{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiachen","family":"Guo","sequence":"additional","affiliation":[{"name":"College of Life Sciences, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4610-7933","authenticated-orcid":false,"given":"Wei","family":"Ge","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shuqin","family":"Liu","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yujiang","family":"Sun","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jianjun","family":"Li","sequence":"additional","affiliation":[{"name":"National Dezhou Donkey Original Breeding Farm, Binzhou 251903, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wei","family":"Shen","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7145-5702","authenticated-orcid":false,"given":"Junjie","family":"Wang","sequence":"additional","affiliation":[{"name":"College of Animal Science and Technology, Qingdao Agricultural University, Qingdao 266109, China"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Teng","family":"Zhang","sequence":"additional","affiliation":[{"name":"State Key Laboratory of Reproductive Regulation and Breeding of Grassland Livestock (R2BGL), College of Life Sciences, Inner Mongolia University, Hohhot 010070, China"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,6,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Wang, Y., Hua, X., Shi, X., and Wang, C. (2022). Origin, Evolution, and Research Development of Donkeys. Genes, 13.","DOI":"10.3390\/genes13111945"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1016\/j.meatsci.2014.11.001","article-title":"Nutritional properties and consumer evaluation of donkey bresaola and salami: Comparison with conventional products","volume":"101","author":"Marino","year":"2015","journal-title":"Meat Sci."},{"key":"ref_3","first-page":"2464","article-title":"Herbalogical study of Colla Corii Asini(Ejiao)","volume":"45","author":"Zhang","year":"2020","journal-title":"Zhongguo Zhong Yao Za Zhi"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"416","DOI":"10.1016\/j.foodres.2018.04.051","article-title":"Donkey milk as a supplement in infant formula: Benefits and technological challenges","volume":"109","author":"Souroullas","year":"2018","journal-title":"Food Res. Int."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"461","DOI":"10.1017\/S175173111600183X","article-title":"Reproductive characteristics of foal heat in female donkeys","volume":"11","author":"Carluccio","year":"2017","journal-title":"Animal"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1016\/j.ando.2010.02.021","article-title":"Human ovarian follicular development: From activation of resting follicles to preovulatory maturation","volume":"71","author":"Gougeon","year":"2010","journal-title":"Ann. D\u2019endocrinol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1016\/j.biocel.2005.01.016","article-title":"Ovarian theca cell","volume":"37","author":"Magoffin","year":"2005","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"65","DOI":"10.1016\/j.mce.2011.11.002","article-title":"Novel signaling mechanisms in the ovary during oocyte maturation and ovulation","volume":"356","author":"Conti","year":"2012","journal-title":"Mol. Cell. Endocrinol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Gong, X., Zhang, Y., Ai, J., and Li, K. (2022). Application of Single-Cell RNA Sequencing in Ovarian Development. Biomolecules, 13.","DOI":"10.3390\/biom13010047"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"4298195","DOI":"10.1155\/2018\/4298195","article-title":"Characterization of Follicular Atresia Responsive to BPA in Zebrafish by Morphometric Analysis of Follicular Stage Progression","volume":"2018","author":"Migliaccio","year":"2018","journal-title":"Int. J. Endocrinol."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Nicol, B., Estermann, M.A., Yao, H.H., and Mellouk, N. (2022). Becoming female: Ovarian differentiation from an evolutionary perspective. Front. Cell Dev. Biol., 10.","DOI":"10.3389\/fcell.2022.944776"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1786","DOI":"10.1093\/humrep\/dei002","article-title":"Human ovarian tissue from cortex surrounding benign cysts: A model to study ovarian tissue cryopreservation","volume":"20","author":"Schubert","year":"2005","journal-title":"Hum. Reprod."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1854","DOI":"10.1016\/j.scib.2022.08.027","article-title":"Deciphering the dynamics of the ovarian reserve in cynomolgus monkey through a quantitative morphometric study","volume":"67","author":"Tu","year":"2022","journal-title":"Sci. Bull."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3760","DOI":"10.7150\/thno.95197","article-title":"Sleep deprivation causes gut dysbiosis impacting on systemic metabolomics leading to premature ovarian insufficiency in adolescent mice","volume":"14","author":"Yan","year":"2024","journal-title":"Theranostics"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.anireprosci.2017.11.007","article-title":"Characterization of the ovarian preantral follicle populations and its correlation with age and nutritional status in Brazilian Northeastern donkeys (Equus assinus)","volume":"187","author":"Lopes","year":"2017","journal-title":"Anim. Reprod. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1046\/j.1439-0531.2003.00439.x","article-title":"Characteristics of ovarian follicle development in domestic animals","volume":"38","author":"Evans","year":"2003","journal-title":"Reprod. Domest. Anim."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"e22718","DOI":"10.1096\/fj.202201176RR","article-title":"A single-cell transcriptomic atlas characterizes cell types and their molecular features in yak ovarian cortex","volume":"37","author":"Pei","year":"2023","journal-title":"FASEB J."},{"key":"ref_18","doi-asserted-by":"crossref","unstructured":"Han, B., Tian, D., Li, X., Liu, S., Tian, F., Liu, D., Wang, S., and Zhao, K. (2024). Multiomics Analyses Provide New Insight into Genetic Variation of Reproductive Adaptability in Tibetan Sheep. Mol. Biol. Evol., 41.","DOI":"10.1093\/molbev\/msae058"},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Liu, C., Wu, T., Fan, F., Liu, Y., Wu, L., Junkin, M., Wang, Z., Yu, Y., Wang, W., and Wei, W. (2019). A portable and cost-effective microfluidic system for massively parallel single-cell transcriptome profiling. bioRxiv.","DOI":"10.1101\/818450"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1016\/j.devcel.2020.07.018","article-title":"Single-Cell RNA Sequencing of the Cynomolgus Macaque Testis Reveals Conserved Transcriptional Profiles during Mammalian Spermatogenesis","volume":"54","author":"Lau","year":"2020","journal-title":"Dev. Cell"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3164","DOI":"10.1038\/s41467-019-11036-9","article-title":"Single-cell reconstruction of follicular remodeling in the human adult ovary","volume":"10","author":"Fan","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"723","DOI":"10.1038\/s41586-022-04587-3","article-title":"Cell transcriptomic atlas of the non-human primate Macaca fascicularis","volume":"604","author":"Han","year":"2022","journal-title":"Nature"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1093\/nar\/gkac633","article-title":"Construction of a cross-species cell landscape at single-cell level","volume":"51","author":"Wang","year":"2023","journal-title":"Nucleic Acids Res."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Jiang, M., Xiao, Y., E, W., Ma, L., Wang, J., Chen, H., Gao, C., Liao, Y., Guo, Q., and Peng, J. (2021). Characterization of the Zebrafish Cell Landscape at Single-Cell Resolution. Front. Cell Dev. Biol., 9.","DOI":"10.3389\/fcell.2021.743421"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"4031","DOI":"10.1038\/s41596-021-00575-5","article-title":"Scaling up reproducible research for single-cell transcriptomics using MetaNeighbor","volume":"16","author":"Fischer","year":"2021","journal-title":"Nat. Protoc."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2247","DOI":"10.1038\/s41596-020-0336-2","article-title":"A scalable SCENIC workflow for single-cell gene regulatory network analysis","volume":"15","author":"Flerin","year":"2020","journal-title":"Nat. Protoc."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1436","DOI":"10.1016\/j.celrep.2018.10.045","article-title":"Revealing the Critical Regulators of Cell Identity in the Mouse Cell Atlas","volume":"25","author":"Suo","year":"2018","journal-title":"Cell Rep."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3763","DOI":"10.1038\/s41467-019-11738-0","article-title":"Metabolic landscape of the tumor microenvironment at single cell resolution","volume":"10","author":"Xiao","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1867","DOI":"10.1101\/gr.271205.120","article-title":"A graph neural network model to estimate cell-wise metabolic flux using single-cell RNA-seq data","volume":"31","author":"Alghamdi","year":"2021","journal-title":"Genome Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1038\/nmeth.4402","article-title":"Reversed graph embedding resolves complex single-cell trajectories","volume":"14","author":"Qiu","year":"2017","journal-title":"Nat. Methods"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Huynh-Thu, V.A., Irrthum, A., Wehenkel, L., and Geurts, P. (2010). Inferring regulatory networks from expression data using tree-based methods. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0012776"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1038\/s41467-021-21246-9","article-title":"Inference and analysis of cell-cell communication using CellChat","volume":"12","author":"Jin","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1038\/s41592-019-0667-5","article-title":"NicheNet: Modeling intercellular communication by linking ligands to target genes","volume":"17","author":"Browaeys","year":"2020","journal-title":"Nat. Methods"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1523","DOI":"10.1038\/s41467-019-09234-6","article-title":"Metascape provides a biologist-oriented resource for the analysis of systems-level datasets","volume":"10","author":"Zhou","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_35","first-page":"100141","article-title":"clusterProfiler 4.0: A universal enrichment tool for interpreting omics data","volume":"2","author":"Wu","year":"2021","journal-title":"Innovation"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"e240128","DOI":"10.1530\/REP-24-0128","article-title":"Expression profiling and function analysis identified new genes regulating cumulus expansion and apoptosis","volume":"168","author":"Zhang","year":"2024","journal-title":"Reproduction"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Kumar, S., Suleski, M., Craig, J.M., Kasprowicz, A.E., Sanderford, M., Li, M., Stecher, G., and Hedges, S.B. (2022). TimeTree 5: An Expanded Resource for Species Divergence Times. Mol. Biol. Evol., 39.","DOI":"10.1093\/molbev\/msac174"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e2413819","DOI":"10.1002\/advs.202413819","article-title":"Revealing the Transcriptional and Metabolic Characteristics of Sebocytes Based on the Donkey Cell Transcriptome Atlas","volume":"12","author":"Tian","year":"2025","journal-title":"Adv. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1016\/j.cell.2020.01.009","article-title":"Single-Cell Transcriptomic Atlas of Primate Ovarian Aging","volume":"180","author":"Wang","year":"2020","journal-title":"Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1038\/s41586-020-2157-4","article-title":"Construction of a human cell landscape at single-cell level","volume":"581","author":"Han","year":"2020","journal-title":"Nature"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1016\/j.yexcr.2017.06.003","article-title":"Endothelial cell-cell adhesion and signaling","volume":"358","author":"Cerutti","year":"2017","journal-title":"Exp. Cell Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/j.theriogenology.2014.09.019","article-title":"Individual bovine in vitro embryo production and cumulus cell transcriptomic analysis to distinguish cumulus-oocyte complexes with high or low developmental potential","volume":"83","author":"Bunel","year":"2015","journal-title":"Theriogenology"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"107987","DOI":"10.1016\/j.celrep.2020.107987","article-title":"Nicotinamide Mononucleotide Supplementation Reverses the Declining Quality of Maternally Aged Oocytes","volume":"32","author":"Miao","year":"2020","journal-title":"Cell Rep."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"10731","DOI":"10.1096\/fj.202000671R","article-title":"Trafficking of cholesterol from lipid droplets to mitochondria in bovine luteal cells: Acute control of progesterone synthesis","volume":"34","author":"Plewes","year":"2020","journal-title":"FASEB J."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"209","DOI":"10.1016\/j.yexcr.2015.11.024","article-title":"Lipid droplets and steroidogenic cells","volume":"340","author":"Shen","year":"2016","journal-title":"Exp. Cell Res"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.theriogenology.2023.04.009","article-title":"Oocyte-cumulus cells crosstalk: New comparative insights","volume":"205","author":"Martinez","year":"2023","journal-title":"Theriogenology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1210\/er.2017-00164","article-title":"Ovarian Follicular Theca Cell Recruitment, Differentiation, and Impact on Fertility: 2017 Update","volume":"39","author":"Richards","year":"2018","journal-title":"Endocr. Rev."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"3953","DOI":"10.1038\/s41467-020-17740-1","article-title":"Single-cell analysis uncovers fibroblast heterogeneity and criteria for fibroblast and mural cell identification and discrimination","volume":"11","author":"Muhl","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00401-018-1861-8","article-title":"The lysosomal function of progranulin, a guardian against neurodegeneration","volume":"136","author":"Paushter","year":"2018","journal-title":"Acta Neuropathol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"910","DOI":"10.1158\/0008-5472.CAN-20-0912","article-title":"A GRN Autocrine-Dependent FAM135B\/AKT\/mTOR Feedforward Loop Promotes Esophageal Squamous Cell Carcinoma Progression","volume":"81","author":"Dong","year":"2021","journal-title":"Cancer Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"103642","DOI":"10.1016\/j.jevs.2021.103642","article-title":"Donkey Industry in China: Current Aspects, Suggestions and Future Challenges","volume":"102","author":"Seyiti","year":"2021","journal-title":"J. Equine Vet. Sci."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Zhang, Z., Huang, B., Wang, Y., Zhu, M., Liu, G., and Wang, C. (2023). A survey report on the donkey original breeding farms in China: Current aspects and future prospective. Front. Vet. Sci., 10.","DOI":"10.3389\/fvets.2023.1126138"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"340","DOI":"10.5897\/AJB2021.17376","article-title":"Survival rate of donkey foals: Status quo and improvement methods","volume":"20","author":"Wang","year":"2021","journal-title":"Afr. J. Biotechnol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"103998","DOI":"10.1016\/j.jevs.2022.103998","article-title":"Pregnancy rates in Equids after Interspecific and Intraspecific Artificial Insemination","volume":"113","author":"Bocci","year":"2022","journal-title":"J. Equine Vet. Sci."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1711","DOI":"10.1038\/s41588-022-01197-7","article-title":"Deep learning of cross-species single-cell landscapes identifies conserved regulatory programs underlying cell types","volume":"54","author":"Li","year":"2022","journal-title":"Nat. Genet."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1093\/humupd\/dmv004","article-title":"Pathophysiological aspects of thyroid hormone disorders\/thyroid peroxidase autoantibodies and reproduction","volume":"21","author":"Vissenberg","year":"2015","journal-title":"Hum. Reprod. Update"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"bqab183","DOI":"10.1210\/endocr\/bqab183","article-title":"Mechanisms of OCT4 on 3,5,3\u2032-Tri-iodothyronine and FSH-induced Granulosa Cell Development in Female Mice","volume":"162","author":"Wang","year":"2021","journal-title":"Endocrinology"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.7150\/ijbs.69343","article-title":"HB-EGF induces mitochondrial dysfunction via estrogen hypersecretion in granulosa cells dependent on cAMP-PKA-JNK\/ERK-Ca(2+)-FOXO1 pathway","volume":"18","author":"Huang","year":"2022","journal-title":"Int. J. Biol. Sci."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"e3088","DOI":"10.1038\/cddis.2017.467","article-title":"miR-181a increases FoxO1 acetylation and promotes granulosa cell apoptosis via SIRT1 downregulation","volume":"8","author":"Zhang","year":"2017","journal-title":"Cell Death Dis."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Zhu, X., Li, W., Lu, M., Shang, J., Zhou, J., Lin, L., Liu, Y., Xing, J., Zhang, M., and Zhao, S. (2024). M(6)A demethylase FTO-stabilized exosomal circBRCA1 alleviates oxidative stress-induced granulosa cell damage via the miR-642a-5p\/FOXO1 axis. J. Nanobiotechnol., 22.","DOI":"10.1186\/s12951-024-02583-5"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"2593","DOI":"10.1242\/dev.006882","article-title":"Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells","volume":"134","author":"Sugiura","year":"2007","journal-title":"Development"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"314","DOI":"10.21037\/atm-22-393","article-title":"RAF1 mediates the FSH signaling pathway as a downstream molecule to stimulate estradiol synthesis and secretion in mouse ovarian granulosa cells","volume":"10","author":"Luo","year":"2022","journal-title":"Ann. Transl. Med."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"gaaa088","DOI":"10.1093\/molehr\/gaaa088","article-title":"Endoplasmic reticulum stress: A key regulator of the follicular microenvironment in the ovary","volume":"27","author":"Harada","year":"2021","journal-title":"Mol. Hum. Reprod."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1007\/s10456-005-9004-y","article-title":"Vascular morphogenesis in the primate ovary","volume":"8","author":"Fraser","year":"2005","journal-title":"Angiogenesis"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1038\/s41467-017-00405-x","article-title":"VEGF amplifies transcription through ETS1 acetylation to enable angiogenesis","volume":"8","author":"Chen","year":"2017","journal-title":"Nat. Commun."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1161\/CIRCRESAHA.121.319955","article-title":"Endothelial Loss of ETS1 Impairs Coronary Vascular Development and Leads to Ventricular Non-Compaction","volume":"131","author":"Wang","year":"2022","journal-title":"Circ. Res."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"762","DOI":"10.1016\/S0015-0282(01)02012-X","article-title":"Cyclic changes in expression of mRNA of vascular endothelial growth factor, its receptors Flt-1 and KDR\/Flk-1, and Ets-1 in human corpora lutea","volume":"76","author":"Endo","year":"2001","journal-title":"Fertil. Steril."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1161\/ATVBAHA.114.304525","article-title":"Endothelial glucocorticoid receptor suppresses atherogenesis--brief report","volume":"35","author":"Goodwin","year":"2015","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1007\/s10456-021-09773-x","article-title":"Loss of endothelial glucocorticoid receptor promotes angiogenesis via upregulation of Wnt\/beta-catenin pathway","volume":"24","author":"Liu","year":"2021","journal-title":"Angiogenesis"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1093\/humupd\/dmm040","article-title":"Oocyte-secreted factors: Regulators of cumulus cell function and oocyte quality","volume":"14","author":"Gilchrist","year":"2008","journal-title":"Hum. Reprod. Update"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1016\/j.cmet.2020.04.018","article-title":"Untangling Determinants of Enhanced Health and Lifespan through a Multi-omics Approach in Mice","volume":"32","author":"Aon","year":"2020","journal-title":"Cell Metab."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"gaab032","DOI":"10.1093\/molehr\/gaab032","article-title":"Lysophosphatidic acid improves oocyte quality during IVM by activating the ERK1\/2 pathway in cumulus cells and oocytes","volume":"27","author":"Ma","year":"2021","journal-title":"Mol. Hum. Reprod."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"3486","DOI":"10.18632\/aging.101660","article-title":"Phosphatidylcholine could protect the defect of zearalenone exposure on follicular development and oocyte maturation","volume":"10","author":"Lai","year":"2018","journal-title":"Aging"},{"key":"ref_74","doi-asserted-by":"crossref","unstructured":"Zhang, C.H., Liu, X.Y., and Wang, J. (2023). Essential Role of Granulosa Cell Glucose and Lipid Metabolism on Oocytes and the Potential Metabolic Imbalance in Polycystic Ovary Syndrome. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms242216247"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"e13481","DOI":"10.1111\/cpr.13481","article-title":"m(6) A promotes planarian regeneration","volume":"56","author":"Cui","year":"2023","journal-title":"Cell Prolif."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1255","DOI":"10.1007\/s10815-013-0068-0","article-title":"Plasticity of granulosa cells: On the crossroad of stemness and transdifferentiation potential","volume":"30","author":"Dzafic","year":"2013","journal-title":"J. Assist. Reprod. Genet."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1530\/REP-10-0094","article-title":"Theca: The forgotten cell of the ovarian follicle","volume":"140","author":"Young","year":"2010","journal-title":"Reproduction"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1186\/s13046-018-0850-z","article-title":"Hippo component YAP promotes focal adhesion and tumour aggressiveness via transcriptionally activating THBS1\/FAK signalling in breast cancer","volume":"37","author":"Shen","year":"2018","journal-title":"J. Exp. Clin. Cancer Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"444","DOI":"10.1210\/me.2005-0287","article-title":"Identification of the major oxidative 3\u03b1-hydroxysteroid dehydrogenase in human prostate that converts 5\u03b1-androstane-3alpha,17\u03b2-diol to 5\u03b1-dihydrotestosterone: A potential therapeutic target for androgen-dependent disease","volume":"20","author":"Bauman","year":"2006","journal-title":"Mol. Endocrinol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"4858","DOI":"10.1210\/jc.2005-0330","article-title":"Retinoids and retinol differentially regulate steroid biosynthesis in ovarian theca cells isolated from normal cycling women and women with polycystic ovary syndrome","volume":"90","author":"Wickenheisser","year":"2005","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.copsyc.2014.12.007","article-title":"Human estrus: Implications for relationship science","volume":"1","author":"Gangestad","year":"2015","journal-title":"Curr. Opin. Psychol."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s40738-020-00074-3","article-title":"Staging of the estrous cycle and induction of estrus in experimental rodents: An update","volume":"6","author":"Ajayi","year":"2020","journal-title":"Fertil. Res. Pract."},{"key":"ref_83","first-page":"200","article-title":"Initial and cyclic recruitment of ovarian follicles","volume":"21","author":"McGee","year":"2000","journal-title":"Endocr. Rev."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/12\/1761\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T17:52:09Z","timestamp":1760032329000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/15\/12\/1761"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6,14]]},"references-count":83,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2025,6]]}},"alternative-id":["ani15121761"],"URL":"https:\/\/doi.org\/10.3390\/ani15121761","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,6,14]]}}}