{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,7]],"date-time":"2026-10-07T08:38:17Z","timestamp":1791362297119,"version":"4.3.1"},"reference-count":117,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2022,9,27]],"date-time":"2022-09-27T00:00:00Z","timestamp":1664236800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003725","name":"National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIP)","doi-asserted-by":"publisher","award":["NRF-2015R1A3A2033826"],"award-info":[{"award-number":["NRF-2015R1A3A2033826"]}],"id":[{"id":"10.13039\/501100003725","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The development of germ cells and other physiological events in the differentiated ovary of humans are highly conserved with several mammalian species, except for the differences in timing. However, comparative knowledge on this topic is very scarce with respect to humans and lower vertebrates, such as chickens. In chickens, female germ cells enter into meiosis around embryonic day (E) 15.5 and are arrested in meiotic prophase I as primary oocytes. The oocytes arrested in meiosis I are accumulated in germ-cell cysts; shortly after hatching, they are enclosed by flattened granulosa cells in order to form primordial follicles. In humans, the process of meiotic recombination in female germ cells begins in the 10\u201311th week of gestation, and primordial follicles are formed at around week 20. In this review, we comprehensively elucidate both the conservation and the species-specific differences between chickens and humans with respect to germ cell, oocyte, and follicle development. Importantly, we provide functional insights into a set of chicken oocyte enriched genes (from E16 to 1 week post-hatch) that show convergent and divergent expression patterns with respect to the human oocyte (from week 11 to 26).<\/jats:p>","DOI":"10.3390\/ijms231911412","type":"journal-article","created":{"date-parts":[[2022,9,28]],"date-time":"2022-09-28T01:51:49Z","timestamp":1664329909000},"page":"11412","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Female Germ Cell Development in Chickens and Humans: The Chicken Oocyte Enriched Genes Convergent and Divergent with the Human Oocyte"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9274-9921","authenticated-orcid":false,"given":"Deivendran","family":"Rengaraj","sequence":"first","affiliation":[{"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3413-3277","authenticated-orcid":false,"given":"Jae Yong","family":"Han","sequence":"additional","affiliation":[{"name":"Department of Agricultural Biotechnology, Research Institute of Agriculture and Life Sciences, Seoul National University, 1 Gwanak-ro, Gwanak-gu, Seoul 08826, Korea"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,9,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/bs.ctdb.2019.04.003","article-title":"The vertebrate Balbiani body, germ plasm, and oocyte polarity","volume":"135","author":"Mullins","year":"2019","journal-title":"Curr. Top. Dev. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Rengaraj, D., Lee, B.R., Lee, S.I., Seo, H.W., and Han, J.Y. (2011). Expression patterns and miRNA regulation of DNA methyltransferases in chicken primordial germ cells. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0019524"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/j.stem.2016.05.001","article-title":"Gametogenesis from pluripotent stem cells","volume":"18","author":"Saitou","year":"2016","journal-title":"Cell Stem Cell"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s40104-022-00712-4","article-title":"Single-cell RNA sequencing of mitotic-arrested prospermatogonia with DAZL::GFP chickens and revealing unique epigenetic reprogramming of chickens","volume":"13","author":"Choi","year":"2022","journal-title":"J. Anim. Sci. Biotechnol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"9910","DOI":"10.3390\/ijms16059910","article-title":"Effects of dietary vitamin E on fertility functions in poultry species","volume":"16","author":"Rengaraj","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1095\/biolreprod48.1.110","article-title":"Localization of 3 beta-hydroxysteroid dehydrogenase in the chicken ovarian follicle shifts from the theca layer to granulosa layer with follicular maturation","volume":"48","author":"Nitta","year":"1993","journal-title":"Biol. Reprod."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1677\/joe.0.1770045","article-title":"Ovarian follicle development in the laying hen is accompanied by divergent changes in inhibin A, inhibin B, activin A and follistatin production in granulosa and theca layers","volume":"177","author":"Lovell","year":"2003","journal-title":"J. Endocrinol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1007\/978-981-10-3975-1_5","article-title":"Avian egg and egg coat","volume":"1001","author":"Okumura","year":"2017","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"264","DOI":"10.1038\/s41586-020-3027-9","article-title":"Reconstitution of the oocyte transcriptional network with transcription factors","volume":"589","author":"Hamazaki","year":"2021","journal-title":"Nature"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"316","DOI":"10.1016\/j.devcel.2017.07.026","article-title":"Zygotic genome activation in vertebrates","volume":"42","author":"Jukam","year":"2017","journal-title":"Dev. Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.1007\/s00018-019-03360-6","article-title":"Zygotic genome activation in the chicken: A comparative review","volume":"77","author":"Rengaraj","year":"2020","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1016\/j.semcdb.2015.10.005","article-title":"Oocyte development, meiosis and aneuploidy","volume":"45","author":"MacLennan","year":"2015","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1395","DOI":"10.1016\/j.ygeno.2018.09.012","article-title":"Genome-wide differential expression of long noncoding RNAs and mRNAs in ovarian follicles of two different chicken breeds","volume":"111","author":"Peng","year":"2019","journal-title":"Genomics"},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Li, Q., Li, J., Li, C., Wu, X., Si, S.J., Yang, P.K., Li, W.T., Han, R.L., Li, G.X., and Liu, X.J. (2022). Transcriptome identification and characterization of long non-coding RNAs in the ovary of hens at four stages. Anim. Biotechnol., 1\u201312. Online ahead of print.","DOI":"10.1080\/10495398.2021.2024217"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"2741","DOI":"10.1242\/dev.127.12.2741","article-title":"Isolation of chicken vasa homolog gene and tracing the origin of primordial germ cells","volume":"127","author":"Tsunekawa","year":"2000","journal-title":"Development"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1530\/REP-14-0433","article-title":"Spatial and temporal action of chicken primordial germ cells during initial migration","volume":"149","author":"Kang","year":"2015","journal-title":"Reproduction"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1089\/scd.2015.0208","article-title":"DAZL expression explains origin and central formation of primordial germ cells in chickens","volume":"25","author":"Lee","year":"2016","journal-title":"Stem Cells Dev."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1387\/ijdb.170283jh","article-title":"The early development of germ cells in chicken","volume":"62","author":"Kim","year":"2018","journal-title":"Int. J. Dev. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/j.ydbio.2004.05.009","article-title":"Primordial germ cell migration in the chick and mouse embryo: The role of the chemokine SDF-1\/CXCL12","volume":"272","author":"Stebler","year":"2004","journal-title":"Dev. Biol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1530\/REP-09-0163","article-title":"Expression pattern of meiosis associated SYCP family members during germline development in chickens","volume":"138","author":"Zheng","year":"2009","journal-title":"Reproduction"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1002\/dvdy.22575","article-title":"The distribution of neuron-specific gene family member 1 in brain and germ cells: Implications for the regulation of germ-line development by brain","volume":"240","author":"Rengaraj","year":"2011","journal-title":"Dev. Dyn."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"650","DOI":"10.3382\/ps\/pex316","article-title":"The dynamic development of germ cells during chicken embryogenesis","volume":"97","author":"Yang","year":"2018","journal-title":"Poult. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1262\/jrd.2016-134","article-title":"Investigating right ovary degeneration in chick embryos by transcriptome sequencing","volume":"63","author":"Yu","year":"2017","journal-title":"J. Reprod. Dev."},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Smith, C.A., Roeszler, K.N., Bowles, J., Koopman, P., and Sinclair, A.H. (2008). Onset of meiosis in the chicken embryo; evidence of a role for retinoic acid. BMC Dev. Biol., 8.","DOI":"10.1186\/1471-213X-8-85"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1654","DOI":"10.1016\/j.csbj.2022.03.040","article-title":"Dissecting chicken germ cell dynamics by combining a germ cell tracing transgenic chicken model with single-cell RNA sequencing","volume":"20","author":"Rengaraj","year":"2022","journal-title":"Comput. Struct. Biotecnol. J."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1159\/000339133","article-title":"Chromosomal axis formation and meiotic progression in chicken oocytes: A quantitative analysis","volume":"137","author":"Pigozzi","year":"2012","journal-title":"Cytogenet. Genome Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1095\/biolreprod.112.101345","article-title":"Expression and knockdown analysis of glucose phosphate isomerase in chicken primordial germ cells","volume":"87","author":"Rengaraj","year":"2012","journal-title":"Biol. Reprod."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"91","DOI":"10.3389\/fendo.2019.00091","article-title":"Interaction of follicle-stimulating hormone and stem cell factor to promote primordial follicle assembly in the chicken","volume":"10","author":"Guo","year":"2019","journal-title":"Front. Endocrinol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1111\/j.1439-0531.2012.02087.x","article-title":"Follicle selection in the avian ovary","volume":"47","author":"Johnson","year":"2012","journal-title":"Reprod. Domest. Anim."},{"key":"ref_30","doi-asserted-by":"crossref","unstructured":"Nie, R.X., Zheng, X.T., Zhang, W.H., Zhang, B., Ling, Y., Zhang, H., and Wu, C.X. (2022). Morphological characteristics and transcriptome landscapes of chicken follicles during selective development. Animals, 12.","DOI":"10.3390\/ani12060713"},{"key":"ref_31","first-page":"99","article-title":"Nuclear events from fertilization to the early cleavage stages in the domestic fowl (Gallus domesticus)","volume":"150","author":"Perry","year":"1987","journal-title":"J. Anat."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1038\/nrg.2016.88","article-title":"Specification and epigenetic programming of the human germ line","volume":"17","author":"Tang","year":"2016","journal-title":"Nat. Rev. Genet."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1093\/molehr\/gaw069","article-title":"Progress towards human primordial germ cell specification in vitro","volume":"23","author":"Canovas","year":"2017","journal-title":"Mol. Hum. Reprod."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"4568","DOI":"10.1016\/j.celrep.2019.11.083","article-title":"Human primordial germ cells are specified from lineage-primed progenitors","volume":"29","author":"Chen","year":"2019","journal-title":"Cell Rep."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1282","DOI":"10.1038\/s41467-020-15042-0","article-title":"A critical role of PRDM14 in human primordial germ cell fate revealed by inducible degrons","volume":"11","author":"Sybirna","year":"2020","journal-title":"Nat. Commun."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1413","DOI":"10.1073\/pnas.89.4.1413","article-title":"A potentially critical Hpa-II site of the X-chromosome-linked PGK1 gene is unmethylated prior to the onset of meiosis of human oogenic cells","volume":"89","author":"Singersam","year":"1992","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Dalbies-Tran, R., Cadoret, V., Desmarchais, A., Elis, S., Maillard, V., Monget, P., Monniaux, D., Reynaud, K., Saint-Dizier, M., and Uzbekova, S. (2020). A comparative analysis of oocyte development in mammals. Cells, 9.","DOI":"10.3390\/cells9041002"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1093\/humupd\/dmm043","article-title":"Meiosis in oocytes: Predisposition to aneuploidy and its increased incidence with age","volume":"14","author":"Jones","year":"2008","journal-title":"Hum. Reprod. Update"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"836","DOI":"10.1126\/science.1183439","article-title":"PRDM9 is a major determinant of meiotic recombination hotspots in humans and mice","volume":"327","author":"Baudat","year":"2010","journal-title":"Science"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1002\/aja.1001220107","article-title":"The primary human oocyte: Some observations on the fine structure of Balbiani\u2019s vitelline body and the origin of the annulate lamellae","volume":"122","author":"Hertig","year":"1968","journal-title":"Am. J. Anat."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1073\/pnas.0609923104","article-title":"Mouse oocytes within germ cell cysts and primordial follicles contain a Balbiani body","volume":"104","author":"Pepling","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1093\/oxfordjournals.humrep.a137570","article-title":"Accelerated disappearance of ovarian follicles in mid-life: Implications for forecasting menopause","volume":"7","author":"Faddy","year":"1992","journal-title":"Hum. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"R15","DOI":"10.1530\/REP-19-0201","article-title":"Advances in human primordial follicle activation and premature ovarian insufficiency","volume":"159","author":"Ford","year":"2020","journal-title":"Reproduction"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1038\/s41419-019-1720-0","article-title":"BRCA2 deficiency is a potential driver for human primary ovarian insufficiency","volume":"10","author":"Miao","year":"2019","journal-title":"Cell Death Dis."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1071\/BI9810249","article-title":"Hormonal correlates of follicular development in the human-ovary","volume":"34","author":"Mcnatty","year":"1981","journal-title":"Aust. J. Biol. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1210\/edrv-17-2-121","article-title":"Regulation of ovarian follicular development in primates: Facts and hypotheses","volume":"17","author":"Gougeon","year":"1996","journal-title":"Endocr. Rev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1093\/biolre\/ioaa073","article-title":"In vitro ovarian follicle growth: A comprehensive analysis of key protocol variables","volume":"103","author":"Simon","year":"2020","journal-title":"Biol. Reprod."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"101191","DOI":"10.1016\/j.psj.2021.101191","article-title":"The morphological and histological study of chicken left ovary during growth and development among Hy-line brown layers of different ages","volume":"100","author":"Mfoundou","year":"2021","journal-title":"Poult. Sci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/0016-6480(87)90117-1","article-title":"The effect of age on egg-production in the domestic hen","volume":"65","author":"Joyner","year":"1987","journal-title":"Gen. Comp. Endocr."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1766","DOI":"10.5713\/ab.20.0791","article-title":"The effect of light on follicular development in laying hens","volume":"34","author":"Cheng","year":"2021","journal-title":"Anim. Biosci."},{"key":"ref_51","first-page":"949","article-title":"Follicle Diameters, Egg weight, and egg production performance in old laying hens injected with growth hormone and testosterone","volume":"18","author":"Mohammadi","year":"2016","journal-title":"J. Agr. Sci. Tech."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Amevor, F.K., Cui, Z.F., Du, X.X., Ning, Z.F., Shu, G., Jin, N.N., Deng, X., Tian, Y.F., Zhang, Z.C., and Kang, X.C. (2021). Combination of quercetin and vitamin E supplementation promotes yolk precursor synthesis and follicle development in aging breeder hens via liver-blood-ovary signal axis. Animals, 11.","DOI":"10.3390\/ani11071915"},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Wang, J.P., Jia, R., Gong, H.J., Celi, P., Zhuo, Y., Ding, X.M., Bai, S.P., Zeng, Q.F., Yin, H.D., and Xu, S.Y. (2021). The effect of oxidative stress on the chicken ovary: Involvement of microbiota and melatonin interventions. Antioxidants, 10.","DOI":"10.3390\/antiox10091422"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/S0378-5122(98)00069-3","article-title":"Ovarian follicular growth in humans: Ovarian ageing and population of growing follicles","volume":"30","author":"Gougeon","year":"1998","journal-title":"Maturitas"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"726","DOI":"10.7150\/ijbs.30369","article-title":"Autophagy in ovarian follicular development and atresia","volume":"15","author":"Zhou","year":"2019","journal-title":"Int. J. Biol. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"e13259","DOI":"10.1111\/acel.13259","article-title":"Ovarian stiffness increases with age in the mammalian ovary and depends on collagen and hyaluronan matrices","volume":"19","author":"Amargant","year":"2020","journal-title":"Aging Cell"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1093\/humupd\/dmm048","article-title":"Cellular and molecular aspects of ovarian follicle ageing","volume":"14","author":"Tatone","year":"2008","journal-title":"Hum. Reprod. Update"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1210\/er.2009-0006","article-title":"Ovarian aging: Mechanisms and clinical consequences","volume":"30","author":"Broekmans","year":"2009","journal-title":"Endocr. Rev."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/j.ogc.2011.05.002","article-title":"The timing of the age at which natural menopause occurs","volume":"38","author":"Gold","year":"2011","journal-title":"Obstet. Gynecol. Clin. N. Am."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1385\/ENDO:26:3:301","article-title":"Oogenesis in adult mammals, including humans: A review","volume":"26","author":"Bukovsky","year":"2005","journal-title":"Endocrine"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.devcel.2016.09.007","article-title":"The germ cell fate of cynomolgus monkeys is specified in the nascent amnion","volume":"39","author":"Sasaki","year":"2016","journal-title":"Dev. Cell"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"dev157453","DOI":"10.1242\/dev.157453","article-title":"The transcriptome of early chicken embryos reveals signaling pathways governing rapid asymmetric cellularization and lineage segregation","volume":"145","author":"Hwang","year":"2018","journal-title":"Development"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"858","DOI":"10.1016\/j.stem.2017.03.007","article-title":"Single-cell RNA-seq analysis maps development of human germline cells and gonadal niche interactions","volume":"20","author":"Li","year":"2017","journal-title":"Cell Stem Cell"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"2848","DOI":"10.1093\/humrep\/det297","article-title":"Length of human pregnancy and contributors to its natural variation","volume":"28","author":"Jukic","year":"2013","journal-title":"Hum. Reprod."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1002\/jmor.1050880104","article-title":"A series of normal stages in the development of the chick embryo","volume":"88","author":"Hamburger","year":"1951","journal-title":"J. Morphol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1002\/dvdy.24087","article-title":"Day-1 chick development","volume":"243","author":"Sheng","year":"2014","journal-title":"Dev. Dyn."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"W191","DOI":"10.1093\/nar\/gkz369","article-title":"g:Profiler: A web server for functional enrichment analysis and conversions of gene lists (2019 update)","volume":"47","author":"Raudvere","year":"2019","journal-title":"Nucleic Acids Res."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"3669","DOI":"10.1111\/j.1742-4658.2007.05900.x","article-title":"Human Cdc45 is a proliferation-associated antigen","volume":"274","author":"Pollok","year":"2007","journal-title":"FEBS J."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1083\/jcb.200109045","article-title":"Human Speedy: A novel cell cycle regulator that enhances proliferation through activation of Cdk2","volume":"157","author":"Porter","year":"2002","journal-title":"J. Cell Biol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"156","DOI":"10.1006\/geno.1999.5955","article-title":"Cloning, characterization, and localization of mouse and human SPO11","volume":"61","author":"Romanienko","year":"1999","journal-title":"Genomics"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"4391","DOI":"10.1128\/MCB.00002-10","article-title":"The expression profile of the major mouse SPO11 isoforms indicates that SPO11 beta introduces double strand breaks and suggests that SPO11 alpha has an additional role in prophase in both spermatocytes and oocytes","volume":"30","author":"Bellani","year":"2010","journal-title":"Mol. Cell Biol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1136\/jmedgenet-2019-106379","article-title":"Homozygous mutations in REC114 cause female infertility characterised by multiple pronuclei formation and early embryonic arrest","volume":"57","author":"Wang","year":"2020","journal-title":"J. Med. Genet."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"103097","DOI":"10.1016\/j.dnarep.2021.103097","article-title":"The meiosis-specific MEIOB-SPATA22 complex cooperates with RPA to form a compacted mixed MEIOB\/SPATA22\/RPA\/ssDNA complex","volume":"102","author":"Ribeiro","year":"2021","journal-title":"DNA Repair"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"507","DOI":"10.1111\/cge.14129","article-title":"Bi-allelic SPATA22 variants cause premature ovarian insufficiency and nonobstructive azoospermia due to meiotic arrest","volume":"101","author":"Yao","year":"2022","journal-title":"Clin. Genet."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"2316","DOI":"10.1093\/humrep\/deq180","article-title":"Dynamics of cohesin proteins REC8, STAG3, SMC1 beta and SMC3 are consistent with a role in sister chromatid cohesion during meiosis in human oocytes","volume":"25","author":"Brieno","year":"2010","journal-title":"Hum. Reprod."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"120099","DOI":"10.1098\/rsob.120099","article-title":"Structural analysis of the human SYCE2-TEX12 complex provides molecular insights into synaptonemal complex assembly","volume":"2","author":"Davies","year":"2012","journal-title":"Open Biol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1007\/s00412-019-00693-w","article-title":"Disassembly of the synaptonemal complex in chicken oocytes analyzed by super-resolution microscopy","volume":"128","author":"Sciurano","year":"2019","journal-title":"Chromosoma"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"112","DOI":"10.3389\/fgene.2012.00112","article-title":"Failure of homologous synapsis and sex-specific reproduction problems","volume":"3","author":"Kurahashi","year":"2012","journal-title":"Front. Genet."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1093\/molehr\/gah184","article-title":"RNA interference in meiosis I human oocytes: Towards an understanding of human aneuploidy","volume":"11","author":"Homer","year":"2005","journal-title":"Mol. Hum. Reprod."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"535","DOI":"10.1083\/jcb.200301105","article-title":"A novel human protein of the maternal centriole is required for the final stages of cytokinesis and entry into S phase","volume":"161","author":"Gromley","year":"2003","journal-title":"J. Cell Biol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1774","DOI":"10.1080\/15384101.2016.1264544","article-title":"Centriolin, a centriole-appendage protein, regulates peripheral spindle migration and asymmetric division in mouse meiotic oocytes","volume":"16","author":"Sun","year":"2017","journal-title":"Cell Cycle"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1093\/biolre\/ioab016","article-title":"Rbm46, a novel germ cell-specific factor, modulates meiotic progression and spermatogenesis","volume":"104","author":"Dai","year":"2021","journal-title":"Biol. Reprod."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.ydbio.2005.07.023","article-title":"The stem-loop binding protein regulates translation of histone mRNA during mammalian oogenesis","volume":"286","author":"Allard","year":"2005","journal-title":"Dev. Biol."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Zhou, J., Leu, N.A., Eckardt, S., McLaughlin, K.J., and Wang, P.J. (2014). STK31\/TDRD8, a germ cell-specific factor, is dispensable for reproduction in mice. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0089471"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"D605","DOI":"10.1093\/nar\/gkaa1074","article-title":"The STRING database in 2021: Customizable protein-protein networks, and functional characterization of user-uploaded gene\/measurement sets","volume":"49","author":"Szklarczyk","year":"2021","journal-title":"Nucleic Acids Res."},{"key":"ref_86","doi-asserted-by":"crossref","unstructured":"Ghafari, F., Gutierrez, C.G., and Hartshorne, G.M. (2007). Apoptosis in mouse fetal and neonatal oocytes during meiotic prophase one. BMC Dev. Biol., 7.","DOI":"10.1186\/1471-213X-7-87"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1501","DOI":"10.1098\/rstb.2009.0124","article-title":"Male germ cell apoptosis: Regulation and biology","volume":"365","author":"Shaha","year":"2010","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1006\/dbio.2001.0269","article-title":"Mouse ovarian germ cell cysts undergo programmed breakdown to form primordial follicles","volume":"234","author":"Pepling","year":"2001","journal-title":"Dev. Biol."},{"key":"ref_89","doi-asserted-by":"crossref","unstructured":"Higgins, J., Midgley, C., Bergh, A.M., Bell, S.M., Askham, J.M., Roberts, E., Binns, R.K., Sharif, S.M., Bennett, C., and Glover, D.M. (2010). Human ASPM participates in spindle organisation, spindle orientation and cytokinesis. BMC Cell Biol., 11.","DOI":"10.1186\/1471-2121-11-85"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1017","DOI":"10.1083\/jcb.200302129","article-title":"NuSAP, a novel microtubule-associated protein involved in mitotic spindle organization","volume":"162","author":"Raemaekers","year":"2003","journal-title":"J. Cell Biol."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"743","DOI":"10.1016\/j.cub.2006.03.056","article-title":"HURP is part of a ran-dependent complex involved in spindle formation","volume":"16","author":"Koffa","year":"2006","journal-title":"Curr. Biol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1186\/s13048-019-0578-1","article-title":"Identification of key biomarkers associated with development and prognosis in patients with ovarian carcinoma: Evidence from bioinformatic analysis","volume":"12","author":"Shen","year":"2019","journal-title":"J. Ovarian Res."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"457","DOI":"10.1186\/s12935-021-02155-9","article-title":"Pan-cancer analysis of the oncogenic role of discs large homolog associated protein 5 (DLGAP5) in human tumors","volume":"21","author":"Tang","year":"2021","journal-title":"Cancer Cell Int."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"631","DOI":"10.1083\/jcb.201606081","article-title":"GTSE1 tunes microtubule stability for chromosome alignment and segregation by inhibiting the microtubule depolymerase MCAK","volume":"215","author":"Bendre","year":"2016","journal-title":"J. Cell Biol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"873","DOI":"10.1083\/jcb.200505040","article-title":"Microtubule capture by CENP-E silences BubR1-dependent mitotic checkpoint signaling","volume":"170","author":"Mao","year":"2005","journal-title":"J. Cell Biol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1083\/jcb.200204048","article-title":"BubR1 is essential for kinetochore localization of other spindle checkpoint proteins and its phosphorylation requires Mad1","volume":"158","author":"Chen","year":"2002","journal-title":"J. Cell Biol."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"4042","DOI":"10.1083\/jcb.201907006","article-title":"CDK1-mediated CENP-C phosphorylation modulates CENP-A binding and mitotic kinetochore localization","volume":"218","author":"Watanabe","year":"2019","journal-title":"J. Cell Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"697","DOI":"10.1007\/s10059-009-0083-2","article-title":"Cancer-upregulated gene 2 (CUG2), a new component of centromere complex, is required for kinetochore function","volume":"27","author":"Kim","year":"2009","journal-title":"Mol. Cells"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"4552","DOI":"10.4161\/cc.9.22.13815","article-title":"Perturbation of Spc25 expression affects meiotic spindle organization, chromosome alignment and spindle assembly checkpoint in mouse oocytes","volume":"9","author":"Sun","year":"2010","journal-title":"Cell Cycle"},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1016\/j.biolcel.2003.09.008","article-title":"Aurora A, meiosis and mitosis","volume":"96","author":"Crane","year":"2004","journal-title":"Biol. Cell"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/j.tig.2017.03.005","article-title":"Specialize and divide (twice): Functions of three aurora kinase homologs in mammalian oocyte meiotic maturation","volume":"33","author":"Nguyen","year":"2017","journal-title":"Trends Genet."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"1007","DOI":"10.1016\/j.bbrc.2008.10.114","article-title":"Phosphorylation of CAP-G is required for its chromosomal DNA localization during mitosis","volume":"377","author":"Murphy","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1083\/jcb.200508154","article-title":"Repo-Man recruits PP1 gamma to chromatin and is essential for cell viability","volume":"172","author":"Andersen","year":"2006","journal-title":"J. Cell Biol."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"1133","DOI":"10.1038\/ncb1475","article-title":"Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis","volume":"8","author":"Vagnarelli","year":"2006","journal-title":"Nat. Cell Biol."},{"key":"ref_105","doi-asserted-by":"crossref","unstructured":"Han, Z., Li, L., Huang, Y., Zhao, H., and Luo, Y. (2021). PBK\/TOPK: A therapeutic target worthy of attention. Cells, 10.","DOI":"10.3390\/cells10020371"},{"key":"ref_106","doi-asserted-by":"crossref","unstructured":"Assou, S., Cerecedo, D., Tondeur, S., Pantesco, V., Hovatta, O., Klein, B., Hamamah, S., and De Vos, J. (2009). A gene expression signature shared by human mature oocytes and embryonic stem cells. BMC Genomics, 10.","DOI":"10.1186\/1471-2164-10-10"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"518","DOI":"10.1016\/j.fertnstert.2012.09.020","article-title":"Expression of survivin in human oocytes and preimplantation embryos","volume":"99","author":"Balakier","year":"2013","journal-title":"Fertil. Steril."},{"key":"ref_108","doi-asserted-by":"crossref","unstructured":"Rungaldier, S., Umlauf, E., Mairhofer, M., Salzer, U., Thiele, C., and Prohaska, R. (2017). Structure-function analysis of human stomatin: A mutation study. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0178646"},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1042\/BJ20111226","article-title":"Insights into the PX (phox-homology) domain and SNX (sorting nexin) protein families: Structures, functions and roles in disease","volume":"441","author":"Teasdale","year":"2012","journal-title":"Biochem. J."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1111\/tra.12148","article-title":"CNIH4 interacts with newly synthesized GPCR and controls their export from the endoplasmic reticulum","volume":"15","author":"Sauvageau","year":"2014","journal-title":"Traffic"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"12394","DOI":"10.1016\/S0021-9258(18)63872-4","article-title":"The human Rab genes encode a family of GTP-binding proteins related to yeast Ypt1 and Sec4 products involved in secretion","volume":"264","author":"Zahraoui","year":"1989","journal-title":"J. Biol. Chem."},{"key":"ref_112","doi-asserted-by":"crossref","unstructured":"Tsunedomi, R., Yoshimura, K., Kimura, Y., Nishiyama, M., Fujiwara, N., Matsukuma, S., Kanekiyo, S., Matsui, H., Shindo, Y., and Watanabe, Y. (2022). Elevated expression of RAB3B plays important roles in chemoresistance and metastatic potential of hepatoma cells. BMC Cancer, 22.","DOI":"10.1186\/s12885-022-09370-1"},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"989","DOI":"10.2174\/1381612826666200917145228","article-title":"Expression of Rab3b in human glioma: Influence on cell proliferation and apoptosis","volume":"27","author":"Luo","year":"2021","journal-title":"Curr. Pharm. Design"},{"key":"ref_114","first-page":"19","article-title":"Cloning, expression and characterization of human glutathione S-transferase Omega 2","volume":"16","author":"Wang","year":"2005","journal-title":"Int. J. Mol. Med."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"2217","DOI":"10.1242\/jeb.202.16.2217","article-title":"Expression of membrane transporters in cane toad Bufo marinus oocytes","volume":"202","author":"Markovich","year":"1999","journal-title":"J. Exp. Biol."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1016\/S0090-4295(01)01224-9","article-title":"Creatine kinase as an indicator of sperm quality and maturity in men with oligospermia","volume":"58","author":"Hallak","year":"2001","journal-title":"Urology"},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1530\/REP-08-0175","article-title":"Changes in the expression of interleukin-1beta and lipopolysaccharide-induced TNF factor in the oviduct of laying hens in response to artificial insemination","volume":"137","author":"Das","year":"2009","journal-title":"Reproduction"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/19\/11412\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:40:40Z","timestamp":1760143240000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/19\/11412"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,9,27]]},"references-count":117,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2022,10]]}},"alternative-id":["ijms231911412"],"URL":"https:\/\/doi.org\/10.3390\/ijms231911412","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,9,27]]}}}