New markers for regulation of transcription and macromolecule metabolic process in porcine oocytes during in vitro maturation
Jazyk angličtina Země Řecko Médium print-electronic
Typ dokumentu časopisecké články
PubMed
32016446
PubMed Central
PMC7002967
DOI
10.3892/mmr.2020.10963
Knihovny.cz E-zdroje
- Klíčová slova
- pig, oocyte, rna, transcription, in vitro maturation,
- MeSH
- biologické markery MeSH
- buněčná diferenciace genetika MeSH
- energetický metabolismus * MeSH
- genetická transkripce MeSH
- genové regulační sítě MeSH
- imunohistochemie MeSH
- kultivované buňky MeSH
- metabolomika MeSH
- oocyty cytologie metabolismus MeSH
- oogeneze genetika MeSH
- ovarium metabolismus MeSH
- prasata MeSH
- stanovení celkové genové exprese MeSH
- transkriptom MeSH
- výpočetní biologie metody MeSH
- vývojová regulace genové exprese * MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- biologické markery MeSH
Oocyte maturation is essential for proper fertilization, embryo implantation and early development. While the physiological conditions of these processes are relatively well‑known, its exact molecular mechanisms remain widely undiscovered. Oocyte growth, differentiation and maturation are therefore the subject of scientific debate. Precious literature has indicated that the oocyte itself serves a regulatory role in the mechanisms underlying these processes. Hence, the present study performed expression microarrays to analyze the complete transcriptome of porcine oocytes during their in vitro maturation (IVM). Pig material was used for experimentation, as it possesses similarities to the reproductive processes and general genetic proximities of Sus scrofa to human. Oocytes, isolated from the ovaries of slaughtered animals were assessed via the Brilliant Cresyl Blue test and directed to IVM. A number of oocytes were left to be analyzed as the 'before IVM' group. Oocyte mRNA was isolated and used for microarray analysis, which was subsequently validated via RT‑qPCR. The current study particularly focused on genes belonging to 'positive regulation of transcription, DNA‑dependent', 'positive regulation of gene expression', 'positive regulation of macromolecule metabolic process' and 'positive regulation of transcription from RNA polymerase II promoter' ontologies. FOS, VEGFA, ESR1, AR, CCND2, EGR2, ENDRA, GJA1, INHBA, IHH, INSR, APP, WWTR1, SMARCA1, NFAT5, SMAD4, MAP3K1, EGR1, RORA, ECE1, NR5A1, KIT, IKZF2, MEF2C, SH3D19, MITF and PSMB4 were all determined to be significantly altered (fold change, >|2|; P<0.05) among these groups, with their downregulation being observed after IVM. Genes with the most altered expressions were analyzed and considered to be potential markers of maturation associated with transcription regulation and macromolecule metabolism process.
Department of Anatomy Poznan University of Medical Sciences Poznan 60‑781 Poland
Department of Histology and Embryology Poznan University of Medical Sciences Poznan 60‑781 Poland
Department of Toxicology Poznan University of Medical Sciences Poznan 60‑631 Poland
Veterinary Center Nicolaus Copernicus University in Torun Torun 87‑100 Poland
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Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction. 2001;122:829–838. doi: 10.1530/rep.0.1220829. PubMed DOI
Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci. 2004;82-83:431–446. doi: 10.1016/j.anireprosci.2004.05.017. PubMed DOI
Matzuk MM, Burns KH, Viveiros MM, Eppig JJ. Intercellular communication in the mammalian ovary: Oocytes carry the conversation. Science. 2002;296:2178–2180. doi: 10.1126/science.1071965. PubMed DOI
Rybska M, Knap S, Jankowski M, Jeseta M, Bukowska D, Antosik P, Nowicki M, Zabel M, Kempisty B, Jaśkowski JM. Cytoplasmic and nuclear maturation of oocytes in mammals-living in the shadow of cells developmental capability. Med J Cell Biol. 2018;6:13–17. doi: 10.2478/acb-2018-0003. DOI
Rybska M, Knap S, Stefańska K, Jankowski M, Gliszczyńska AC, Popis M, Jeseta M, Bukowska D, Antosik P, Kempisty B, Jaśkowski JM. Transforming growth factor (TGF)-is it a key protein in mammalian reproductive biology? Med J Cell Biol. 2018;6:125–130. doi: 10.2478/acb-2018-0020. DOI
Rybska M, Knap S, Jankowski M, Jeseta M, Bukowska D, Antosik P, Nowicki M, Zabel M, Kempisty B, Jaśkowski JM. Characteristic of factors influencing the proper course of folliculogenesis in mammals. Med J Cell Biol. 2018;6:33–38. doi: 10.2478/acb-2018-0006. DOI
Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K, Tesfaye D. Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genomics. 2011;12:57. doi: 10.1186/1471-2164-12-57. PubMed DOI PMC
Borys-Wójcik S, Kocherova I, Celichowski P, Popis M, Jeseta M, Bukowska D, Antosik P, Nowicki M, Kempisty B. Protein oligomerization is the biochemical process highly up-regulated in porcine oocytes before in vitro maturation (IVM) Med J Cell Biol. 2018;6:155–162. doi: 10.2478/acb-2018-0025. DOI
Budna J, Celichowski P, Bryja A, Jeseta M, Jankowski M, Bukowska D, Antosik P, Nowicki A, Brüssow KP, Bruska M, et al. Expression changes in fatty acid metabolic processrelated genes in porcine oocytes during in vitro maturation. Med J Cell Biol. 2018;6:48–54. doi: 10.2478/acb-2018-0009. DOI
Kranc W, Brązert M, Ożegowska K, Budna-Tukan J, Celichowski P, Jankowski M, Bryja A, Nawrocki MJ, Popis M, Jeseta M, et al. Response to abiotic and organic substances stimulation belongs to ontologic groups significantly up-regulated in porcine immature oocytes. Med J Cell Biol. 2018;6:91–100. doi: 10.2478/acb-2018-0015. DOI
Chermuła B, Brązert M, Jeseta M, Ożegowska K, Sujka-Kordowska P, Konwerska A, Bryja A, Kranc W, Jankowski M, Nawrocki MJ, et al. The unique mechanisms of cellular proliferation, migration and apoptosis are regulated through oocyte maturational development-A complete transcriptomic and histochemical study. Int J Mol Sci. 2018;20:E84. doi: 10.3390/ijms20010084. PubMed DOI PMC
Ożegowska K, Dyszkiewicz-Konwińska M, Celichowski P, Nawrocki MJ, Bryja A, Jankowski M, Kranc W, Brązert M, Knap S, Jeseta M, et al. Expression pattern of new genes regulating female sex differentiation and in vitro maturational status of oocytes in pigs. Theriogenology. 2018;121:122–133. doi: 10.1016/j.theriogenology.2018.08.019. PubMed DOI
Borys S, Brązert M, Jankowski M, Kocherova I, Ożegowska K, Celichowski P, Nawrocki MJ, Kranc W, Bryja A, Kulus M, et al. Enzyme linked receptor protein signaling pathway is one of the ontology groups that are highly up-regulated in porcine oocytes before in vitro maturation. J Biol Regul Homeost Agents. 2018;32:1089–1103. PubMed
Pujol M, López-Béjar M, Paramio MT. Developmental competence of heifer oocytes selected using the brilliant cresyl blue (BCB) test. Theriogenology. 2004;61:735–744. doi: 10.1016/S0093-691X(03)00250-4. PubMed DOI
Le Guienne B. Small atlas of bovine oocyte. Elevage et Insemination (France) 1998:24–30. [In French]
Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162:156–159. doi: 10.1016/0003-2697(87)90021-2. PubMed DOI
Nawrocki MJ, Celichowski P, Jankowski M, Kranc W, Bryja A, Borys-Wójcik S, Jeseta M, Antosik P, Bukowska D, Bruska M, et al. Ontology groups representing angiogenesis and blood vessels development are highly up-regulated during porcine oviductal epithelial cells long-term real-time proliferation-a primary cell culture approach. Med J Cell Biol. 2018;6:186–194. doi: 10.2478/acb-2018-0029. DOI
Budna J, Celichowski P, Karimi P, Kranc W, Bryja A, Ciesiółka S, Rybska M, Borys S, Jeseta M, Bukowska D, et al. Does porcine oocytes maturation in vitro is regulated by genes involved in transforming growth factor beta receptor signaling pathway? Adv Cell Biol. 2017;5:1–14. doi: 10.1515/acb-2017-0001. DOI
Curran T, Franza BR., Jr Fos and jun: The AP-1 connection. Cell. 1988;55:395–397. doi: 10.1016/0092-8674(88)90024-4. PubMed DOI
Angel P, Karin M. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim Biophys Acta. 1991;1072:129–157. PubMed
Rusovici R, LaVoie HA. Expression and distribution of AP-1 transcription factors in the porcine ovary. Biol Reprod. 2003;69:64–74. doi: 10.1095/biolreprod.102.013995. PubMed DOI
Johnson RS, Spiegelman BM, Papaioannou V. Pleiotropic effects of a null mutation in the c-fos proto-oncogene. Cell. 1992;71:577–586. doi: 10.1016/0092-8674(92)90592-Z. PubMed DOI
Müller R, Tremblay JM, Adamson ED, Verma IM. Tissue and cell type-specific expression of two human c-onc genes. Nature. 1983;304:454–456. doi: 10.1038/304454a0. PubMed DOI
Hattori MA, Kato Y, Fujihara N. Retinoic acid suppression of endothelial nitric oxide synthase in porcine oocyte. Can J Physiol Pharmacol. 2002;80:777–782. doi: 10.1139/y02-099. PubMed DOI
Blaha M, Nemcova L, Kepkova KV, Vodicka P, Prochazka R. Gene expression analysis of pig cumulus-oocyte complexes stimulated in vitro with follicle stimulating hormone or epidermal growth factor-like peptides. Reprod Biol Endocrinol. 2015;13:113. doi: 10.1186/s12958-015-0112-2. PubMed DOI PMC
Leung DW, Cachianes G, Kuang WJ, Goeddel DV, Ferrara N. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–1309. doi: 10.1126/science.2479986. PubMed DOI
Ferrara N, Henzel WJ. Pituitary follicular cells secrete a novel heparin-binding growth factor specific for vascular endothelial cells. Biochem Biophys Res Commun. 1989;161:851–858. doi: 10.1016/0006-291X(89)92678-8. PubMed DOI
Ferrara N, Davis-Smyth T. The biology of vascular endothelial growth factor. Endocr Rev. 1997;18:4–25. doi: 10.1210/edrv.18.1.0287. PubMed DOI
Sousa LM, Campos DB, Fonseca VU, Viau P, Kfoury JR, Jr, Oliveira CA, Binelli M, Buratini J, Jr, Papa PC. Vascular endothelial growth factor A (VEGFA) modulates bovine placenta steroidogenesis in vitro. Placenta. 2012;33:788–794. doi: 10.1016/j.placenta.2012.07.009. PubMed DOI
Shimizu T. Promotion of ovarian follicular development by injecting vascular endothelial growth factor (VEGF) and growth differentiation factor 9 (GDF-9) genes. J Reprod Dev. 2006;52:23–32. doi: 10.1262/jrd.17072. PubMed DOI
McFee RM, Rozell TG, Cupp AS. The balance of proangiogenic and antiangiogenic VEGFA isoforms regulate follicle development. Cell Tissue Res. 2012;349:635–647. doi: 10.1007/s00441-012-1330-y. PubMed DOI PMC
Bui TMT, Nguyễn KX, Karata A, Ferré P, Trần MT, Wakai T, Funahashi H. Presence of vascular endothelial growth factor during the first half of IVM improves the meiotic and developmental competence of porcine oocytes from small follicles. Reprod Fertil Dev. 2017;29:1902–1909. doi: 10.1071/RD16321. PubMed DOI
Ravindranath N, Little-Ihrig L, Phillips HS, Ferrara N, Zeleznik AJ. Vascular endothelial growth factor messenger ribonucleic acid expression in the primate ovary. Endocrinology. 1992;131:254–260. doi: 10.1210/endo.131.1.1612003. PubMed DOI
Yamamoto S, Konishi I, Tsuruta Y, Nanbu K, Mandai M, Kuroda H, Matsushita K, Hamid AA, Yura Y, Mori T. Expression of vascular endothelial growth factor (VEGF) during folliculogenesis and corpus luteum formation in the human ovary. Gynecol Endocrinol. 1997;11:371–381. doi: 10.3109/09513599709152564. PubMed DOI
Xu J, Xu M, Bernuci MP, Fisher TE, Shea LD, Woodruff TK, Zelinski MB, Stouffer RL. Primate follicular development and oocyte maturation in vitro. Adv Exp Med Biol. 2013;761:43–67. doi: 10.1007/978-1-4614-8214-7_5. PubMed DOI PMC
Silva CM, Matos MH, Rodrigues GQ, Faustino LR, Pinto LC, Chaves RN, Araújo VR, Campello CC, Figueiredo JR. In vitro survival and development of goat preantral follicles in two different oxygen tensions. Anim Reprod Sci. 2010;117:83–89. doi: 10.1016/j.anireprosci.2009.03.015. PubMed DOI
Walters KA, Simanainen U, Handelsman DJ. Molecular insights into androgen actions in male and female reproductive function from androgen receptor knockout models. Hum Reprod Update. 2010;16:543–558. doi: 10.1093/humupd/dmq003. PubMed DOI
Gleicher N, Weghofer A, Barad DH. The role of androgens in follicle maturation and ovulation induction: Friend or foe of infertility treatment? Reprod Biol Endocrinol. 2011;9:116. doi: 10.1186/1477-7827-9-116. PubMed DOI PMC
Lenie S, Smitz J. Functional AR signaling is evident in an in vitro mouse follicle culture bioassay that encompasses most stages of folliculogenesis. Biol Reprod. 2009;80:685–695. doi: 10.1095/biolreprod.107.067280. PubMed DOI
Li M, Ai JS, Xu BZ, Xiong B, Yin S, Lin SL, Hou Y, Chen DY, Schatten H, Sun QY. Testosterone potentially triggers meiotic resumption by activation of intra-oocyte SRC and MAPK in porcine oocytes. Biol Reprod. 2008;79:897–905. doi: 10.1095/biolreprod.108.069245. PubMed DOI
Van Nieuwerburgh F, Stoop D, Cabri P, Dhont M, Deforce D, De Sutter P. Shorter CAG repeats in the androgen receptor gene may enhance hyperandrogenicity in polycystic ovary syndrome. Gynecol Endocrinol. 2008;24:669–673. doi: 10.1080/09513590802342841. PubMed DOI
O'Donovan KJ, Tourtellotte WG, Millbrandt J, Baraban JM. The EGR family of transcription-regulatory factors: Progress at the interface of molecular and systems neuroscience. Trends Neurosci. 1999;22:167–173. doi: 10.1016/S0166-2236(98)01343-5. PubMed DOI
Shin H, Seol DW, Nam M, Song H, Lee DR, Lim HJ. Expression of Egr3 in mouse gonads and its localization and function in oocytes. Asian-Australas J Anim Sci. 2017;30:781–787. doi: 10.5713/ajas.16.0798. PubMed DOI PMC
Thiel G, Müller I, Rössler OG. Expression, signaling and function of Egr transcription factors in pancreatic β-cells and insulin-responsive tissues. Mol Cell Endocrinol. 2014;388:10–19. doi: 10.1016/j.mce.2014.03.001. PubMed DOI
Safford M, Collins S, Lutz MA, Allen A, Huang CT, Kowalski J, Blackford A, Horton MR, Drake C, Schwartz RH, Powell JD. Egr-2 and Egr-3 are negative regulators of T cell activation. Nat Immunol. 2005;6:472–480. doi: 10.1038/ni1193. PubMed DOI
Fang F, Ooka K, Bhattachyya S, Wei J, Wu M, Du P, Lin S, Del Galdo F, Feghali-Bostwick CA, Varga J. The early growth response gene Egr2 (alias Krox20) is a novel transcriptional target of transforming growth factor-β that is up-regulated in systemic sclerosis and mediates profibrotic responses. Am J Pathol. 2011;178:2077–2090. doi: 10.1016/j.ajpath.2011.01.035. PubMed DOI PMC
Nagarajan R, Svaren J, Le N, Araki T, Watson M, Milbrandt J. EGR2 mutations in inherited neuropathies dominant-negatively inhibit myelin gene expression. Neuron. 2001;30:355–368. doi: 10.1016/S0896-6273(01)00282-3. PubMed DOI
Hu TM, Chen CH, Chuang YA, Hsu SH, Cheng MC. Resequencing of early growth response 2 (EGR2) gene revealed a recurrent patient-specific mutation in schizophrenia. Psychiatry Res. 2015;228:958–960. doi: 10.1016/j.psychres.2015.05.035. PubMed DOI
Le N, Nagarajan R, Wang JY, Araki T, Schmidt RE, Milbrandt J. Analysis of congenital hypomyelinating Egr2Lo/Lo nerves identifies Sox2 as an inhibitor of schwann cell differentiation and myelination. Proc Natl Acad Sci USA. 2005;102:2596–2601. doi: 10.1073/pnas.0407836102. PubMed DOI PMC
Li X, Zhang Z, Yu M, Li L, Du G, Xiao W, Yang H. Involvement of miR-20a in promoting gastric cancer progression by targeting early growth response 2 (EGR2) Int J Mol Sci. 2013;14:16226–16239. doi: 10.3390/ijms140816226. PubMed DOI PMC
Barbeau DJ, La KT, Kim DS, Kerpedjieva SS, Shurin GV, Tamama K. Early growth response-2 signaling mediates immunomodulatory effects of human multipotential stromal cells. Stem Cells Dev. 2014;23:155–166. doi: 10.1089/scd.2013.0194. PubMed DOI PMC
Jin H, Won M, Shin E, Kim HM, Lee K, Bae J. EGR2 is a gonadotropin-induced survival factor that controls the expression of IER3 in ovarian granulosa cells. Biochem Biophys Res Commun. 2017;482:877–882. doi: 10.1016/j.bbrc.2016.11.127. PubMed DOI
Burger HG. Inhibin: Definition and nomenclature, including related substances. J Endocrinol. 1988;117:159–160. doi: 10.1677/joe.0.1170159. PubMed DOI
Seder CW, Hartojo W, Lin L, Silvers AL, Wang Z, Thomas DG, Giordano TJ, Chen G, Chang AC, Orringer MB, Beer DG. Upregulated INHBA expression may promote cell proliferation and is associated with poor survival in lung adenocarcinoma. Neoplasia. 2009;11:388–396. doi: 10.1593/neo.81582. PubMed DOI PMC
Howley BV, Hussey GS, Link LA, Howe PH. Translational regulation of inhibin βa by TGFβ via the RNA-binding protein hnRNP E1 enhances the invasiveness of epithelial-to- mesenchymal transitioned cells. Oncogene. 2016;35:1725–1735. doi: 10.1038/onc.2015.238. PubMed DOI PMC
Katayama Y, Oshima T, Sakamaki K, Aoyama T, Sato T, Masudo K, Shiozawa M, Yoshikawa T, Rino Y, Imada T, Masuda M. Clinical significance of INHBA gene expression in patients with gastric cancer who receive curative resection followed by adjuvant s-1 chemotherapy. In Vivo. 2017;31:565–571. doi: 10.21873/invivo.11095. PubMed DOI PMC
Donovan P, Dubey OA, Kallioinen S, Rogers KW, Muehlethaler K, Müller P, Rimoldi D, Constam DB. Paracrine activin-A signaling promotes melanoma growth and metastasis through immune evasion. J Invest Dermatol. 2017;137:2578–2587. doi: 10.1016/j.jid.2017.07.845. PubMed DOI
Locci M, Wu JE, Arumemi F, Mikulski Z, Dahlberg C, Miller AT, Crotty S. Activin A programs the differentiation of human TFH cells. Nat Immunol. 2016;17:976–984. doi: 10.1038/ni.3494. PubMed DOI PMC
McKenzie LJ, Pangas SA, Carson SA, Kovanci E, Cisneros P, Buster JE, Amato P, Matzuk MM. Human cumulus granulosa cell gene expression: A predictor of fertilization and embryo selection in women undergoing IVF. Hum Reprod. 2004;19:2869–2874. doi: 10.1093/humrep/deh535. PubMed DOI
Assidi M, Dufort I, Ali A, Hamel M, Algriany O, Dielemann S, Sirard MA. Identification of potential markers of oocyte competence expressed in bovine cumulus cells matured with follicle-stimulating hormone and/or phorbol myristate acetate in vitro. Biol Reprod. 2008;79:209–222. doi: 10.1095/biolreprod.108.067686. PubMed DOI
Bristol-Gould SK, Kreeger PK, Selkirk CG, Kilen SM, Cook RW, Kipp JL, Shea LD, Mayo KE, Woodruff TK. Postnatal regulation of germ cells by activin: The establishment of the initial follicle pool. Dev Biol. 2006;298:132–148. doi: 10.1016/j.ydbio.2006.06.025. PubMed DOI
Myers M, Middlebrook BS, Matzuk MM, Pangas SA. Loss of inhibin alpha uncouples oocyte-granulosa cell dynamics and disrupts postnatal folliculogenesis. Dev Biol. 2009;334:458–467. doi: 10.1016/j.ydbio.2009.08.001. PubMed DOI PMC
Maguire JJ, Davenport AP. Endothelin receptors and their antagonists. Semin Nephrol. 2015;35:125–136. doi: 10.1016/j.semnephrol.2015.02.002. PubMed DOI PMC
Asai R, Kurihara Y, Fujisawa K, Sato T, Kawamura Y, Kokubo H, Tonami K, Nishiyama K, Uchijima Y, Miyagawa-Tomita S, Kurihara H. Endothelin receptor type A expression defines a distinct cardiac subdomain within the heart field and is later implicated in chamber myocardium formation. Development. 2010;137:3823–3833. doi: 10.1242/dev.054015. PubMed DOI
Kawamura K, Ye Y, Liang CG, Kawamura N, Gelpke MS, Rauch R, Tanaka T, Hsueh AJ. Paracrine regulation of the resumption of oocyte meiosis by endothelin-1. Dev Biol. 2009;327:62–70. doi: 10.1016/j.ydbio.2008.11.033. PubMed DOI
Cui L, Shen J, Fang L, Mao X, Wang H, Ye Y. Endothelin-1 promotes human germinal vesicle-stage oocyte maturation by downregulating connexin-26 expression in cumulus cells. Mol Hum Reprod. 2018;24:27–36. doi: 10.1093/molehr/gax058. PubMed DOI
Cheng JC, Chang HM, Fang L, Sun YP, Leung PC. TGF-β1 up-regulates connexin43 expression: A potential mechanism for human trophoblast cell differentiation. J Cell Physiol. 2015;230:1558–1566. doi: 10.1002/jcp.24902. PubMed DOI
Salameh A, Haunschild J, Bräuchle P, Peim O, Seidel T, Reitmann M, Kostelka M, Bakhtiary F, Dhein S, Dähnert I. On the role of the gap junction protein Cx43 (GJA1) in human cardiac malformations with fallot-pathology. A study on paediatric cardiac specimen. PLoS One. 2014;9:e95344. doi: 10.1371/journal.pone.0095344. PubMed DOI PMC
Edry I, Sela-Abramovich S, Dekel N. Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle. Mol Cell Endocrinol. 2006;252:102–106. doi: 10.1016/j.mce.2006.03.009. PubMed DOI
Li SH, Lin MH, Hwu YM, Lu CH, Yeh LY, Chen YJ, Lee RK. Correlation of cumulus gene expression of GJA1, PRSS35, PTX3, and SERPINE2 with oocyte maturation, fertilization, and embryo development. Reprod Biol Endocrinol. 2015;13:93. doi: 10.1186/s12958-015-0091-3. PubMed DOI PMC
Hasegawa J, Yanaihara A, Iwasaki S, Mitsukawa K, Negishi M, Okai T. Reduction of connexin 43 in human cumulus cells yields good embryo competence during ICSI. J Assist Reprod Genet. 2007;24:463–466. doi: 10.1007/s10815-007-9155-4. PubMed DOI PMC
Wang HX, Tong D, El-Gehani F, Tekpetey FR, Kidder GM. Connexin expression and gap junctional coupling in human cumulus cells: Contribution to embryo quality. J Cell Mol Med. 2009;13:972–984. doi: 10.1111/j.1582-4934.2008.00373.x. PubMed DOI PMC
Amberger JS, Bocchini CA, Schiettecatte F, Scott AF, Hamosh A. OMIM.org: Online mendelian inheritance in man (OMIM®), an online catalog of human genes and genetic disorders. Nucleic Acids Res. 2015;43:D789–D798. doi: 10.1093/nar/gku1205. PubMed DOI PMC
Calatayud NE, Pask AJ, Shaw G, Richings NM, Osborn S, Renfree MB. Ontogeny of the oestrogen receptors ESR1 and ESR2 during gonadal development in the tammar wallaby, Macropus eugenii. Reproduction. 2010;139:599–611. doi: 10.1530/REP-09-0305. PubMed DOI
Jameson JL, DeGroot LJ, De Kretser DM, Giudice LC, Grossman AB, Melmed S, Potts JT Jr, Weir GC, editors. 7th. Elsevier; Philadelphia, PA: 2016. Endocrinology: Adult & Pediatric.
Labrie F, Luu-The V, Lin SX, Simard J, Labrie C. Role of 17β-hydroxysteroid dehydrogenases in sex steroid formation in peripheral intracrine tissues. Trends Endocrinol Metab. 2000;11:421–427. doi: 10.1016/S1043-2760(00)00342-8. PubMed DOI
Kuiper GG, Carlsson B, Grandien K, Enmark E, Häggblad J, Nilsson S, Gustafsson JA. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 1997;138:863–870. doi: 10.1210/endo.138.3.4979. PubMed DOI
Bondesson M, Hao R, Lin CY, Williams C, Gustafsson JÅ. Estrogen receptor signaling during vertebrate development. Biochim Biophys Acta. 2014;1849:142–151. doi: 10.1016/j.bbagrm.2014.06.005. PubMed DOI PMC
Paterni I, Granchi C, Katzenellenbogen JA, Minutolo F. Estrogen receptors alpha (ERα) and beta (ERβ): Subtype-selective ligands and clinical potential. Steroids. 2014;90:13–29. doi: 10.1016/j.steroids.2014.06.012. PubMed DOI PMC
Pelletier G, El-Alfy M. Immunocytochemical localization of estrogen receptors alpha and beta in the human reproductive organs. J Clin Endocrinol Metab. 2000;85:4835–4840. doi: 10.1210/jcem.85.12.7029. PubMed DOI
Nathan MR, Schmid P. A review of fulvestrant in breast cancer. Oncol Ther. 2017;5:17–29. doi: 10.1007/s40487-017-0046-2. PubMed DOI PMC
Artini PG, Tatone C, Sperduti S, D'Aurora M, Franchi S, Di Emidio G, Ciriminna R, Vento M, Di Pietro C, Stuppia L, et al. Cumulus cells surrounding oocytes with high developmental competence exhibit down-regulation of phosphoinositol 1, 3 kinase/protein kinase B (PI3K/AKT) signalling genes involved in proliferation and survival. Hum Reprod. 2017;32:2474–2484. doi: 10.1093/humrep/dex320. PubMed DOI PMC
Musgrove EA, Caldon CE, Barraclough J, Stone A, Sutherland RL. Cyclin D as a therapeutic target in cancer. Nat Rev Cancer. 2011;11:558–572. doi: 10.1038/nrc3090. PubMed DOI
Robker RL, Richards JS. Hormone-induced proliferation and differentiation of granulosa cells: A coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol. 1998;12:924–940. doi: 10.1210/mend.12.7.0138. PubMed DOI
Han Y, Xia G, Tsang BK. Regulation of cyclin D2 expression and degradation by follicle-stimulating hormone during rat granulosa cell proliferation in vitro. Biol Reprod. 2013;88:57. doi: 10.1095/biolreprod.112.105106. PubMed DOI
François CM, Petit F, Giton F, Gougeon A, Ravel C, Magre S, Cohen-Tannoudji J, Guigon CJ. A novel action of follicle-stimulating hormone in the ovary promotes estradiol production without inducing excessive follicular growth before puberty. Sci Rep. 2017;7:46222. doi: 10.1038/srep46222. PubMed DOI PMC