{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T03:34:44Z","timestamp":1760240084075,"version":"build-2065373602"},"reference-count":66,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2019,3,6]],"date-time":"2019-03-06T00:00:00Z","timestamp":1551830400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ministry of Future Planning and Technology and Ministry of Education, Republic of Korea","award":["2016R1E1A1A01943455"],"award-info":[{"award-number":["2016R1E1A1A01943455"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The in vitro maturation of oocytes is frequently used as an assisted reproductive technique (ART), and has been successfully established in humans and rodents. To overcome the limitations of ART, novel procedures for the in vitro maturation of early follicles are emerging. During the follicle isolation procedure, the unintended rupture of each follicle leads to a release of extra oocytes. Such oocytes, which are obtained during follicle isolation from marmosets, can be used for early maturation studies. Marmoset (Callithrix jacchus), which is classified as a new-world monkey, is a novel model that has been employed in reproductive biomedical research, as its reproductive physiology is similar to that of humans in several aspects. The ovaries of female marmosets were collected, and the excess oocytes present during follicle isolation were retrieved without pre-gonadotropin induction. Each oocyte was matured in vitro for 48 h in the presence of various concentrations of human chorionic gonadotropin (hCG) and epidermal growth factor (EGF), and the maturity of oocytes and optimal maturation conditions were evaluated. Each oocyte was individually reverse-transcribed, and the expression of mRNAs and microRNAs (miRs) were analyzed. Concentrations of hCG significantly affected the maturation rate of oocytes [the number of metaphase II (MII) oocytes]. The expression of BMP15 and ZP1 was highest when the oocytes were matured using 100 IU\/L of hCG without pre-treatment with gonadotropins, and that of Cja-mir-27a was highest when cultured with follicle stimulating hormone. These results suggest that these up-regulated miRs affect the maturation of oocytes. Interactions with other protein networks were analyzed, and a strong association of BMP15 and ZP1 with sperm binding receptor (ACR), anti-M\u00fcllerian hormone (AMH), and AMH receptor was demonstrated, which is related to the proliferation of granulosa cells. Collectively, on the basis of these results, the authors propose optimal maturation conditions of excess oocytes of marmoset without in vivo gonadotropin treatment, and demonstrated the roles of miRs in early oocyte maturation at the single-cell level in marmosets.<\/jats:p>","DOI":"10.3390\/ijms20051133","type":"journal-article","created":{"date-parts":[[2019,3,7]],"date-time":"2019-03-07T10:52:22Z","timestamp":1551955942000},"page":"1133","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Expression of Transcripts in Marmoset Oocytes Retrieved during Follicle Isolation Without Gonadotropin Induction"],"prefix":"10.3390","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0671-519X","authenticated-orcid":false,"given":"Yoon Young","family":"Kim","sequence":"first","affiliation":[{"name":"Department of Obstetrics and Gynecology, Seoul National University Hospital, Seoul National University College of Medicine, 28 Yonkeun-dong, Chongno-gu, Seoul 110-744, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Byeong-Cheol","family":"Kang","sequence":"additional","affiliation":[{"name":"Biomedical Research Institute, Seoul National University Hospital, Seoul 03080, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jun Won","family":"Yun","sequence":"additional","affiliation":[{"name":"Department of Biotechnology, The Catholic University, Bucheon 14662, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jae Hun","family":"Ahn","sequence":"additional","affiliation":[{"name":"Biomedical Research Institute, Seoul National University Hospital, Seoul 03080, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8684-2126","authenticated-orcid":false,"given":"Yong Jin","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Korea University Guro Hospital, Seoul 08308, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hoon","family":"Kim","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Seoul National University Hospital, Seoul National University College of Medicine, 28 Yonkeun-dong, Chongno-gu, Seoul 110-744, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zev","family":"Rosenwaks","sequence":"additional","affiliation":[{"name":"Center for Reproductive Medicine, Weill Cornell Medical College, New York, NY 10021, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6423-854X","authenticated-orcid":false,"given":"Seung-Yup","family":"Ku","sequence":"additional","affiliation":[{"name":"Department of Obstetrics and Gynecology, Seoul National University Hospital, Seoul National University College of Medicine, 28 Yonkeun-dong, Chongno-gu, Seoul 110-744, Korea"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,3,6]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"S84","DOI":"10.1016\/j.theriogenology.2007.03.016","article-title":"Isolation of genes associated with developmental competency of bovine oocytes","volume":"68","author":"Pfeffer","year":"2007","journal-title":"Theriogenology"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1095\/biolreprod14.4.502","article-title":"The distribution of collagenous connective tissue in rat ovarian follicles","volume":"14","author":"Espey","year":"1976","journal-title":"Biol. Reprod."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1095\/biolreprod14.3.233","article-title":"Factors which influence ovulatory regradation of rabbit ovarian follicles","volume":"14","author":"Espey","year":"1976","journal-title":"Biol. Reprod."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1007\/s13770-016-0006-1","article-title":"Effects of Estradiol on the Paracrine Regulator Expression of In Vitro Maturated Murine Ovarian Follicles","volume":"14","author":"Kim","year":"2017","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1177\/1933719112468948","article-title":"Effects of urinary and recombinant gonadotropins on in vitro maturation outcomes of mouse preantral follicles","volume":"20","author":"Park","year":"2013","journal-title":"Reprod. Sci."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1530\/rep.0.1220487","article-title":"Effect of ascorbic acid on health and morphology of bovine preantral follicles during long-term culture","volume":"122","author":"Thomas","year":"2001","journal-title":"Reproduction"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1007\/s13770-017-0051-4","article-title":"Differential MicroRNA Expression Profile of Human Embryonic Stem Cell-Derived Cardiac Lineage Cells","volume":"14","author":"Kim","year":"2017","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"844","DOI":"10.3389\/fmicb.2018.00844","article-title":"The Marmoset as an Animal Model of Influenza: Infection With A(H1N1)pdm09 and Highly Pathogenic A(H5N1) Viruses via the Conventional or Tracheal Spray Route","volume":"9","author":"Nakajima","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"811","DOI":"10.1016\/j.theriogenology.2012.03.029","article-title":"Minimally invasive transabdominal collection of preimplantation embryos from the common marmoset monkey (Callithrix jacchus)","volume":"78","author":"Hanazawa","year":"2012","journal-title":"Theriogenology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"673","DOI":"10.1016\/S0092-8674(03)00428-8","article-title":"MicroRNA pathways in flies and worms: Growth, death, fat, stress, and timing","volume":"113","author":"Ambros","year":"2003","journal-title":"Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"R925","DOI":"10.1016\/j.cub.2003.11.017","article-title":"microRNAs: Runts of the genome assert themselves","volume":"13","author":"Lai","year":"2003","journal-title":"Curr. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.1038\/nature07299","article-title":"MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation","volume":"455","author":"Tay","year":"2008","journal-title":"Nature"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1478","DOI":"10.1038\/ng.250","article-title":"Embryonic stem cell-specific microRNAs regulate the G1-S transition and promote rapid proliferation","volume":"40","author":"Wang","year":"2008","journal-title":"Nat. Genet."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1093\/molehr\/gas015","article-title":"Analysis of microRNAs and their precursors in bovine early embryonic development","volume":"18","author":"Mondou","year":"2012","journal-title":"Mol. Hum. Reprod."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"15144","DOI":"10.1073\/pnas.0705917104","article-title":"MicroRNA regulation of cyclooxygenase-2 during embryo implantation","volume":"104","author":"Chakrabarty","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"2374","DOI":"10.1016\/j.fertnstert.2009.01.069","article-title":"Aberration of blastocyst microRNA expression is associated with human infertility","volume":"93","author":"McCallie","year":"2010","journal-title":"Fertil. Steril."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"3050","DOI":"10.1093\/humrep\/det338","article-title":"MicroRNAs transfected into granulosa cells may regulate oocyte meiotic competence during in vitro maturation of mouse follicles","volume":"28","author":"Kim","year":"2013","journal-title":"Hum. Reprod."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1177\/1933719110377663","article-title":"MicroRNA expression profiles are altered by gonadotropins and vitamin C status during in vitro follicular growth","volume":"17","author":"Kim","year":"2010","journal-title":"Reprod. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1007\/s13770-016-0009-y","article-title":"The expression profile of angiotensin system on thawed murine ovaries","volume":"13","author":"Kim","year":"2016","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1089\/ten.teb.2016.0156","article-title":"Potential Use of Antiapoptotic Proteins and Noncoding RNAs for Efficient In Vitro Follicular Maturation and Ovarian Bioengineering","volume":"23","author":"Kim","year":"2017","journal-title":"Tissue Eng. Part B Rev."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"877","DOI":"10.1095\/biolreprod.106.056499","article-title":"A restricted role for sperm-borne microRNAs in mammalian fertilization","volume":"75","author":"Amanai","year":"2006","journal-title":"Biol. Reprod."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1111\/dgd.12109","article-title":"Common marmoset as a new model animal for neuroscience research and genome editing technology","volume":"56","author":"Kishi","year":"2014","journal-title":"Dev. Growth Differ."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"16894","DOI":"10.1038\/srep16894","article-title":"Resequencing of the common marmoset genome improves genome assemblies and gene-coding sequence analysis","volume":"5","author":"Sato","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1093\/molbev\/msp284","article-title":"Evolution of an X-linked primate-specific micro RNA cluster","volume":"27","author":"Li","year":"2010","journal-title":"Mol. Biol. Evol."},{"key":"ref_25","first-page":"4243","article-title":"Vitamin D in human reproduction: The more, the better? An evidence-based critical appraisal","volume":"21","author":"Lagana","year":"2017","journal-title":"Eur. Rev. Med. Pharmacol. Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1515\/hmbci-2015-0051","article-title":"Is there a role for vitamin D in human reproduction?","volume":"25","author":"Nandi","year":"2016","journal-title":"Horm. Mol. Biol. Clin. Investig."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"4987436","DOI":"10.1155\/2016\/4987436","article-title":"How to Achieve High-Quality Oocytes? The Key Role of Myo-Inositol and Melatonin","volume":"2016","author":"Vitale","year":"2016","journal-title":"Int. J. Endocrinol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.1007\/s12325-018-0810-1","article-title":"Polycystic Ovary Syndrome: Implication for Drug Metabolism on Assisted Reproductive Techniques-A Literature Review","volume":"35","author":"Sathyapalan","year":"2018","journal-title":"Adv. Ther."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1095\/biolreprod.110.088674","article-title":"In vitro oocyte maturation and preantral follicle culture from the luteal-phase baboon ovary produce mature oocytes","volume":"84","author":"Xu","year":"2011","journal-title":"Biol. Reprod."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1124\/dmd.116.070367","article-title":"A New Marmoset P450 4F12 Enzyme Expressed in Small Intestines and Livers Efficiently Metabolizes Antihistaminic Drug Ebastine","volume":"44","author":"Uehara","year":"2016","journal-title":"Drug Metab. Dispos."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"567","DOI":"10.1093\/intimm\/dxv031","article-title":"Common marmoset CD117+ hematopoietic cells possess multipotency","volume":"27","author":"Shimada","year":"2015","journal-title":"Int. Immunol."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Sadakane, O., Watakabe, A., Ohtsuka, M., Takaji, M., Sasaki, T., Kasai, M., Isa, T., Kato, G., Nabekura, J., and Mizukami, H. (2015). In Vivo Two-Photon Imaging of Dendritic Spines in Marmoset Neocortex. eNeuro, 2.","DOI":"10.1523\/ENEURO.0019-15.2015"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1007\/s10329-015-0500-4","article-title":"Sphere-formation culture of testicular germ cells in the common marmoset, a small New World monkey","volume":"57","author":"Lin","year":"2016","journal-title":"Primates"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"29122","DOI":"10.1038\/srep29122","article-title":"The transcriptomes of novel marmoset monkey embryonic stem cell lines reflect distinct genomic features","volume":"6","author":"Debowski","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1002\/mrd.22971","article-title":"Oocyte-activating capacity of fresh and frozen-thawed spermatids in the common marmoset (Callithrix jacchus)","volume":"85","author":"Ogonuki","year":"2018","journal-title":"Mol. Reprod. Dev."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1234","DOI":"10.1095\/biolreprod52.6.1234","article-title":"Meiotic competence of marmoset monkey oocytes is related to follicle size and oocyte-somatic cell associations","volume":"52","author":"Gilchrist","year":"1995","journal-title":"Biol. Reprod."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1016\/j.theriogenology.2007.07.009","article-title":"Effects of ovarian stimulation, with and without human chorionic gonadotrophin, on oocyte meiotic and developmental competence in the marmoset monkey (Callithrix jacchus)","volume":"68","author":"Grupen","year":"2007","journal-title":"Theriogenology"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1254","DOI":"10.1016\/j.theriogenology.2015.01.012","article-title":"Critical estradiol dose optimization for oocyte in vitro maturation in the common marmoset","volume":"83","author":"Tkachenko","year":"2015","journal-title":"Theriogenology"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1007\/s13770-016-9091-4","article-title":"Use of nonhuman primates for the development of bioengineered female reproductive organs","volume":"13","author":"Yun","year":"2016","journal-title":"Tissue Eng. Regen. Med."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"3100","DOI":"10.1002\/term.2214","article-title":"Induction of multiple ovulation via modulation of angiotensin II receptors in in vitro ovarian follicle culture models","volume":"11","author":"Kim","year":"2017","journal-title":"J. Tissue Eng. Regen. Med."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"888","DOI":"10.1136\/jim-2015-000001","article-title":"Gonadotropin ratio affects the in vitro growth of rhesus ovarian preantral follicles","volume":"64","author":"Kim","year":"2016","journal-title":"J. Investig. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"18","DOI":"10.1095\/biolreprod.115.133900","article-title":"In Vitro Maturation of Mouse Oocytes Increases the Level of Kif11\/Eg5 on Meiosis II Spindles","volume":"95","author":"Kovacovicova","year":"2016","journal-title":"Biol. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1946","DOI":"10.1093\/humrep\/dep104","article-title":"Assessment of a new in vitro maturation system for mouse and human cumulus-enclosed oocytes: Three-dimensional prematuration culture in the presence of a phosphodiesterase 3-inhibitor","volume":"24","author":"Vanhoutte","year":"2009","journal-title":"Hum. Reprod."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2047","DOI":"10.1093\/humrep\/deq148","article-title":"Epidermal growth factor effects on marmoset monkey (Callithrix jacchus) oocyte in vitro maturation, IVF and embryo development are altered by gonadotrophin concentration during oocyte maturation","volume":"25","author":"Tkachenko","year":"2010","journal-title":"Hum. Reprod."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"240","DOI":"10.1093\/humrep\/dei283","article-title":"Meiotic abnormalities in in vitro-matured marmoset monkey (Callithrix jacchus) oocytes: Development of a non-human primate model to investigate causal factors","volume":"21","author":"Delimitreva","year":"2006","journal-title":"Hum. Reprod."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1016\/j.theriogenology.2017.10.023","article-title":"Quality of common marmoset (Callithrix jacchus) oocytes collected after ovarian stimulation","volume":"106","author":"Kanda","year":"2018","journal-title":"Theriogenology"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"4341","DOI":"10.1073\/pnas.83.12.4341","article-title":"Oocyte-specific gene expression: Molecular characterization of a cDNA coding for ZP-3, the sperm receptor of the mouse zona pellucida","volume":"83","author":"Ringuette","year":"1986","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1016\/0012-1606(87)90192-8","article-title":"Oocyte-specific expression and developmental regulation of ZP3, the sperm receptor of the mouse zona pellucida","volume":"121","author":"Philpott","year":"1987","journal-title":"Dev. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1111\/j.1749-0774.2006.00019.x","article-title":"Mouse zona pellucida dynamically changes its elasticity during oocyte maturation, fertilization and early embryo development","volume":"19","author":"Murayama","year":"2006","journal-title":"Hum. Cell"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1042\/bst0040896","article-title":"Structure and composition of the zona pellucida of the mouse oocyte","volume":"4","author":"Newport","year":"1976","journal-title":"Biochem. Soc. Trans."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1002\/(SICI)1098-2795(199703)46:3<344::AID-MRD13>3.0.CO;2-Z","article-title":"Identification of bovine zona pellucida glycoproteins","volume":"46","author":"Topper","year":"1997","journal-title":"Mol. Reprod. Dev."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.1071\/RD9951209","article-title":"Nucleotide sequence of cDNA encoding bonnet monkey (Macaca radiata) zona pellucida glycoprotein-ZP3","volume":"7","author":"Kolluri","year":"1995","journal-title":"Reprod. Fertil. Dev."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"532","DOI":"10.1095\/biolreprod57.3.532","article-title":"Sequence of complementary deoxyribonucleic acid encoding bonnet monkey (Macaca radiata) zona pellucida glycoprotein-ZP1 and its high-level expression in Escherichia coli","volume":"57","author":"Gupta","year":"1997","journal-title":"Biol. Reprod."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1093\/molehr\/gah074","article-title":"Localization and synthesis of zona pellucida proteins in the marmoset monkey (Callithrix jacchus) ovary","volume":"10","author":"Bogner","year":"2004","journal-title":"Mol. Hum. Reprod."},{"key":"ref_55","first-page":"35","article-title":"The expression and localization of zona pellucida glycoproteins and mRNA in cynomolgus monkeys (Macaca fascicularis)","volume":"50","author":"Martinez","year":"1996","journal-title":"J. Reprod. Fertil. Suppl."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1439-0272.2011.01188.x","article-title":"Quantification of ZP1, ZP2 and ZP3 mRNA of marmoset monkey (Callithrix jacchus) oocytes from periantral and antral follicles","volume":"44","author":"Konrad","year":"2012","journal-title":"Andrologia"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1540","DOI":"10.1126\/science.1080372","article-title":"Vertebrate microRNA genes","volume":"299","author":"Lim","year":"2003","journal-title":"Science"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1016\/j.ando.2010.02.020","article-title":"Oocyte-somatic cell communication and microRNA function in the ovary","volume":"71","author":"Hawkins","year":"2010","journal-title":"Ann. Endocrinol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1167","DOI":"10.1093\/biolre\/iox044","article-title":"MicroRNA-21 plays a pivotal role in the oocyte-secreted factor-induced suppression of cumulus cell apoptosis","volume":"96","author":"Han","year":"2017","journal-title":"Biol. Reprod."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.mod.2016.12.004","article-title":"MicroRNA-224 delays oocyte maturation through targeting Ptx3 in cumulus cells","volume":"143","author":"Li","year":"2017","journal-title":"Mech. Dev."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"C268","DOI":"10.1152\/ajpcell.00065.2017","article-title":"MicroRNA-574 suppresses oocyte maturation via targeting hyaluronan synthase 2 in porcine cumulus cells","volume":"314","author":"Pan","year":"2018","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"E525","DOI":"10.1152\/ajpendo.00480.2014","article-title":"MicroRNA-378 regulates oocyte maturation via the suppression of aromatase in porcine cumulus cells","volume":"308","author":"Pan","year":"2015","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"16","DOI":"10.1016\/j.anireprosci.2011.12.021","article-title":"MicroRNA expression profile in bovine cumulus-oocyte complexes: Possible role of let-7 and miR-106a in the development of bovine oocytes","volume":"130","author":"Miles","year":"2012","journal-title":"Anim. Reprod. Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"304","DOI":"10.14348\/molcells.2015.2122","article-title":"Expression and preliminary functional profiling of the let-7 family during porcine ovary follicle atresia","volume":"38","author":"Cao","year":"2015","journal-title":"Mol. Cells"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1016\/j.repbio.2017.09.005","article-title":"MicroRNA-27a-3p affects estradiol and androgen imbalance by targeting Creb1 in the granulosa cells in mouse polycytic ovary syndrome model","volume":"17","author":"Wang","year":"2017","journal-title":"Reprod. Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"297","DOI":"10.1210\/en.2017-00219","article-title":"Functional Characterization of MicroRNA-27a-3p Expression in Human Polycystic Ovary Syndrome","volume":"159","author":"Wang","year":"2018","journal-title":"Endocrinology"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/5\/1133\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T12:36:34Z","timestamp":1760186194000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/20\/5\/1133"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,3,6]]},"references-count":66,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2019,3]]}},"alternative-id":["ijms20051133"],"URL":"https:\/\/doi.org\/10.3390\/ijms20051133","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2019,3,6]]}}}