Expression of genes regulating cell division in porcine follicular granulosa cells

. 2023 Aug 07 ; 18 (1) : 12. [epub] 20230807

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37550786

Grantová podpora
2020/37/B/NZ5/03926 Narodowe Centrum Nauki

Odkazy

PubMed 37550786
PubMed Central PMC10408085
DOI 10.1186/s13008-023-00094-7
PII: 10.1186/s13008-023-00094-7
Knihovny.cz E-zdroje

BACKGROUND: Cell cycle regulation influences the proliferation of granulosa cells and affects many processes related to ovarian folliclular growth and ovulation. Abnormal regulation of the cell cycle can lead to many diseases within the ovary. The aim of this study was to describe the expression profile of genes within granulosa cells, which are related to the formation of the cytoskeleton, organization of cell organelles inside the cell, and regulation of cell division. Established in vitro primary cultures from porcine ovarian follicle granulosa cells were maintained for 48, 96, 144 h and evaluated via microarray expression analysis. RESULTS: Analyzed genes were assigned to 12 gene ontology groups "actin cytoskeleton organization", "actin filament organization", "actin filament-based process", "cell-matrix adhesion", "cell-substrate adhesion", "chromosome segregation", "chromosome separation", "cytoskeleton organization", "DNA integrity checkpoint", "DNA replication initiation", "organelle fision", "organelle organization". Among the genes with significantly changed expression, those whose role in processes within the ovary are selected for consideration. Genes with increased expression include (ITGA11, CNN1, CCl2, TPM2, ACTN1, VCAM-1, COL3A1, GSN, FRMD6, PLK2). Genes with reduced expression inlcude (KIF14, TACC3, ESPL1, CDC45, TTK, CDC20, CDK1, FBXO5, NEK2-NIMA, CCNE2). For the results obtained by microarray expressions, quantitative validation by RT-qPCR was performed. CONCLUSIONS: The results indicated expression profile of genes, which can be considered as new molecular markers of cellular processes involved in signaling, cell structure organization. The expression profile of selected genes brings new insight into regulation of physiological processes in porcine follicular granulosa cells during primary in vitro culture.

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Fletcher DA, Mullins RD. Cell mechanics and the cytoskeleton. Nature. 2010;463(7280):485. PubMed PMC

Hohmann T, Dehghani F. The cytoskeleton—a complex interacting meshwork. Cells. 2019;8(4):362. PubMed PMC

Jiang X, Qin Y, Kun L, Zhou Y. The significant role of the microfilament system in tumors. Front Oncol. 2021;17(11):333. PubMed PMC

Akamatsu M, Vasan R, Serwas D, Ferrin M, Rangamani P, Drubin DG. Principles of self-organization and load adaptation by the actin cytoskeleton during clathrin-mediated endocytosis. Elife. 2020;1:9. PubMed PMC

Barlan K, Gelfand VI. Microtubule-based transport and the distribution, tethering, and organization of organelles. Cold Spring Harb Perspect Biol. 2017 doi: 10.1101/cshperspect.a025817. PubMed DOI PMC

Forth S, Kapoor TM. The mechanics of microtubule networks in cell division. J Cell Biol. 2017;216(6):1525–1531. doi: 10.1083/jcb.201612064. PubMed DOI PMC

Wang L, Paudyal SC, Kang Y, Owa M, Liang F-X, Spektor A, et al. Regulators of tubulin polyglutamylation control nuclear shape and cilium disassembly by balancing microtubule and actin assembly. Cell Res. 2021 doi: 10.1038/s41422-021-00584-9. PubMed DOI PMC

Sanghvi-Shah R, Weber GF. Intermediate filaments at the junction of mechanotransduction, migration, and development. Front Cell Dev Biol. 2017;5(SEP):81. PubMed PMC

Ong MS, Deng S, Halim CE, Cai W, Tan TZ, Huang RYJ, et al. Cytoskeletal proteins in cancer and intracellular stress: a therapeutic perspective. Cancers (Basel) 2020 doi: 10.3390/cancers12010238. PubMed DOI PMC

Chamier-Gliszczyńska A, Kałuzna S, Stefańska K, Celichowski P, Antosik P, Bukowska D, et al. Analysis of expression of genes responsible for regulation of cellular proliferation and migration-Microarray approach based on porcine oocyte model. Med J Cell Biol. 2019;7(2):48–57.

Rybska M, Knap S, Jankowski M, Jeseta M, Bukowska D, Antosik P, et al. Characteristic of factors influencing the proper course of folliculogenesis in mammals. Med J Cell Biol. 2018 doi: 10.2478/acb-2018-0006. DOI

Irving-Rodgers HF, Rodgers RJ. Extracellular matrix of the developing ovarian follicle. Semin Reprod Med. 2006;24(4):195–203. PubMed

Jones MC, Zha J, Humphries MJ. Connections between the cell cycle, cell adhesion and the cytoskeleton. Philos Trans R Soc B. 2019 doi: 10.1098/rstb.2018.0227. PubMed DOI PMC

Carnegie JA, Tsang BK. The cytoskeleton and rat granulosa cell steroidogenesis: possible involvement of microtubules and microfilaments. Biol Reprod. 1988;38(1):100–108. PubMed

El Zowalaty AE, Li R, Zheng Y, Lydon JP, DeMayo FJ, Ye X. Deletion of RhoA in progesterone receptor-expressing cells leads to luteal insufficiency and infertility in female mice. Endocrinology. 2017;158(7):2168–2178. PubMed PMC

Shen WJ, Zaidi SK, Patel S, Cortez Y, Ueno M, Azhar R, et al. Ablation of vimentin results in defective steroidogenesis. Endocrinology. 2012;153(7):3249–3257. PubMed PMC

Nekrasova OE, Mendez MG, Chernoivanenko IS, Tyurin-Kuzmin PA, Kuczmarski ER, Gelfand VI, et al. Vimentin intermediate filaments modulate the motility of mitochondria. Mol Biol Cell. 2011;22(13):2282–2289. doi: 10.1091/mbc.e10-09-0766. PubMed DOI PMC

Miller WL. Steroid hormone synthesis in mitochondria. Mol Cell Endocrinol. 2013;379(1–2):62–73. PubMed

Duan X, Sun SC. Actin cytoskeleton dynamics in mammalian oocyte meiosis. Biol Reprod. 2019;100(1):15–24. PubMed

Pereira GR, Lorenzo PL, Carneiro GF, Ball BA, Pegoraro LMC, Pimentel CA, et al. Influence of equine growth hormone, insulin-like growth factor-I and its interaction with gonadotropins on in vitro maturation and cytoskeleton morphology in equine oocytes. Animal. 2013;7(9):1493–1499. PubMed

Li J, Qian WP, Sun QY. Cyclins regulating oocyte meiotic cell cycle progression†. Biol Reprod. 2019;101(5):878–881. PubMed PMC

Barnum KJ, O’Connell MJ. Cell cycle regulation by checkpoints. Methods Mol Bio. 2014;1170:29. PubMed PMC

Matthews HK, Bertoli C, de Bruin RAM. Cell cycle control in cancer. Nat Rev Mol Cell Biol. 2021 doi: 10.1038/s41580-021-00404-3. PubMed DOI

Bowen JA, Hunt JS. The role of integrins in reproduction. Proc Soc Exp Biol Med. 2000;223(4):331–343. PubMed

Weber GF, Bjerke MA, DeSimone DW. Integrins and cadherins join forces to form adhesive networks. J Cell Sci. 2011;124(8):1183–1193. PubMed PMC

Geiger B, Bershadsky A, Pankov R, Yamada KM. Transmembrane extracellular matrix-cytoskeleton crosstalk. Nat Rev Mol Cell Biol. 2001;2(11):793–805. PubMed

Théry M, Racine V, Pépin A, Piel M, Chen Y, Sibarita JB, et al. The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol. 2005;7(10):947–953. PubMed

D’Occhio MJ, Campanile G, Zicarelli L, Visintin JA, Baruselli PS. Adhesion molecules in gamete transport, fertilization, early embryonic development, and implantation—role in establishing a pregnancy in cattle: a review. Mol Reprod Dev. 2020;87(2):206–222. PubMed

Merc V, Frolikova M, Komrskova K. Role of integrins in sperm activation and fertilization. Int J Mol Sci. 2021;22(21):11809. PubMed PMC

Kossowska-Tomaszczuk K, De Geyter C. Cells with stem cell characteristics in somatic compartments of the ovary. Biomed Res Int. 2013 doi: 10.1155/2013/310859. PubMed DOI PMC

Józkowiak M, Hutchings G, Jankowski M, Kulcenty K, Mozdziak P, Kempisty B, et al. The stemness of human ovarian granulosa cells and the role of resveratrol in the differentiation of MSCs-A review based on cellular and molecular knowledge. Cells. 2020 doi: 10.3390/cells9061418. PubMed DOI PMC

Sordella R, Jiang W, Chen GC, Curto M, Settleman J. Modulation of Rho GTPase signaling regulates a switch between adipogenesis and myogenesis. Cell. 2003;113(2):147–158. PubMed

McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell. 2004;6(4):483–495. PubMed

Khan AU, Qu R, Fan T, Ouyang J, Dai J. A glance on the role of actin in osteogenic and adipogenic differentiation of mesenchymal stem cells. Stem Cell Res Ther. 2020;11(1):1–14. PubMed PMC

Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, et al. STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res. 2019;47(D1):D607–D613. PubMed PMC

Zhou Y, Zhou B, Pache L, Chang M, Khodabakhshi AH, Tanaseichuk O, et al. Metascape provides a biologist-oriented resource for the analysis of systems-level datasets. Nat Commun. 2019 doi: 10.1038/s41467-019-09234-6. PubMed DOI PMC

Moncrieff L, Mozdziak P, Jeseta M, Machatkova M, Kranc W, Kempisty B. Ovarian follicular cells—living in the shadow of stemness cellular competence. Med J Cell Biol. 2019;7(3):134–140.

Stefańska K, Sibiak R, Hutchings G, Dompe C, Moncrieff L, Janowicz K, et al. Evidence for existence of molecular stemness markers in porcine ovarian follicular granulosa cells. Med J Cell Biol. 2019;7(4):183–188.

Pollard TD. Actin and Actin-Binding Proteins. Cold Spring Harb Perspect Biol. 2016 doi: 10.1101/cshperspect.a018226. PubMed DOI PMC

Lappalainen P. Actin-binding proteins: the long road to understanding the dynamic landscape of cellular actin networks. Mol Biol Cell. 2016;27(16):2519–2522. doi: 10.1091/mbc.e15-10-0728. PubMed DOI PMC

Harris AR, Jreij P, Belardi B, Joffe AM, Bausch AR, Fletcher DA. Biased localization of actin binding proteins by actin filament conformation. Nat Commun. 2020;11(1):1–13. PubMed PMC

Yin LM, Schnoor M, Jun CD. Structural characteristics, binding partners and related diseases of the calponin homology (CH) domain. Front Cell Dev Biol. 2020 doi: 10.3389/fcell.2020.00342. PubMed DOI PMC

Harris AR, Belardi B, Jreij P, Wei K, Shams H, Bausch A, et al. Steric regulation of tandem calponin homology domain actin-binding affinity. Mol Biol Cell. 2019;30(26):3112. PubMed PMC

Wang Z, Li TE, Chen M, Pan JJ, Shen KW. miR-106b-5p contributes to the lung metastasis of breast cancer via targeting CNN1 and regulating Rho/ROCK1 pathway. Aging (Albany NY) 2020;12(2):1867–87. PubMed PMC

Liu R, Jin JP. Calponin isoforms CNN1, CNN2 and CNN3: Regulators for actin cytoskeleton functions in smooth muscle and non-muscle cells. Gene. 2016;585(1):143–153. PubMed PMC

Nagaraja AK, Middlebrook BS, Rajanahally S, Myers M, Li Q, Matzuk MM, et al. Defective gonadotropin-dependent ovarian folliculogenesis and granulosa cell gene expression in inhibin-deficient mice. Endocrinology. 2010;151(10):4994. PubMed PMC

Li L, Mo H, Zhang J, Zhou Y, Peng X, Luo X. The role of heat shock protein 90b1 in patients with polycystic ovary syndrome. PLoS One. 2016;11(4):e0152837. doi: 10.1371/journal.pone.0152837. PubMed DOI PMC

Yang X, Pang Y, Zhang J, Shi J, Zhang X, Zhang G, et al. High expression levels of ACTN1 and ACTN3 indicate unfavorable prognosis in acute myeloid leukemia. J Cancer. 2019;10(18):4286. PubMed PMC

Sasson R, Rimon E, Dantes A, Cohen T, Shinder V, Land-Bracha A, et al. Gonadotrophin-induced gene regulation in human granulosa cells obtained from IVF patients. Modulation of steroidogenic genes, cytoskeletal genes and genes coding for apoptotic signalling and protein kinases. Mol Hum Reprod. 2004;10(5):299–311. PubMed

Zhou Y, Deng X, Ma X, Zang N, Li H, Li G, et al. Cellular transcriptomics: gelsolin negatively regulates the expression of apoptosis-associated genes and inhibits apoptosis in hepatocarcinoma cells. Int J Clin Exp Pathol. 2015;8(11):13871. PubMed PMC

Jiang Y, Jiao B, Liao X, Xiao X, Liu X, Shen L. Analyses mutations in GSN, CST3, TTR, and ITM2B genes in Chinese patients with Alzheimer’s disease. Front Aging Neurosci. 2020;10(12):292. PubMed PMC

Asare-Werehene M, Nakka K, Reunov A, Chiu CT, Lee WT, Abedini MR, et al. The exosome-mediated autocrine and paracrine actions of plasma gelsolin in ovarian cancer chemoresistance. Oncogene. 2019;39(7):1600–16. PubMed PMC

Zhang W, Ou X, Wu X. Proteomics profiling of plasma exosomes in epithelial ovarian cancer: a potential role in the coagulation cascade, diagnosis and prognosis. Int J Oncol. 2019;54(5):1719–1733. doi: 10.3892/ijo.2019.4742/abstract. PubMed DOI PMC

Schiewek J, Schumacher U, Lange T, Joosse SA, Wikman H, Pantel K, et al. Clinical relevance of cytoskeleton associated proteins for ovarian cancer. J Cancer Res Clin Oncol. 2018;144(11):2195–2205. doi: 10.1007/s00432-018-2710-9. PubMed DOI PMC

Wigglesworth K, Lee KB, Emori C, Sugiura K, Eppig JJ. Transcriptomic diversification of developing cumulus and mural granulosa cells in mouse ovarian follicles. Biol Reprod. 2015;92(1):23–24. PubMed PMC

Delon I, Brown NH. Integrins and the actin cytoskeleton. Curr Opin Cell Biol. 2007;19(1):43–50. PubMed

Martino F, Perestrelo AR, Vinarský V, Pagliari S, Forte G. Cellular mechanotransduction: From tension to function. Front Physiol. 2018;9(JUL):824. PubMed PMC

Ji H, Long V, Briody V, Chien EK. Progesterone modulates integrin α2 (ITGA2) and α11 (ITGA11) in the pregnant cervix. Reprod Sci. 2011;18(2):156–163. PubMed

Li Z, Jia J, Gou J, Tong A, Liu X, Zhao X, et al. Mmu-miR-126a-3p plays a role in murine embryo implantation by regulating Itga11. Reprod Biomed Online. 2015;31(3):384–393. PubMed

Samborski A, Graf A, Krebs S, Kessler B, Bauersachs S. Deep sequencing of the porcine endometrial transcriptome on day 14 of pregnancy. Biol Reprod. 2013;88(4):1–13. PubMed

Yang S, Zhou X, Pei Y, Wang H, He K, Zhao A. Identification of differentially expressed genes in porcine ovaries at proestrus and estrus stages using RNA-seq technique. Biomed Res Int. 2018 doi: 10.1155/2018/9150723. PubMed DOI PMC

Grassot V, Da Silva A, Saliba J, Maftah A, Dupuy F, Petit JM. Highlights of glycosylation and adhesion related genes involved in myogenesis. BMC Genomics. 2014;15(1):1–17. doi: 10.1186/1471-2164-15-621. PubMed DOI PMC

Chan JP, Lin P-C, Zhou S, Duffy DM, Lydon JP, Ko CJ. Progesterone receptor serves the ovary as a trigger of ovulation and a terminator of inflammation in brief. Cell Reports. 2020;31:107496. doi: 10.1016/j.celrep.2020.03.060. PubMed DOI PMC

Nivet AL, Vigneault C, Blondin P, Sirard MA. Changes in granulosa cells’ gene expression associated with increased oocyte competence in bovine. Reproduction. 2013;145(6):555–565. PubMed

Nio-Kobayashi J, Kudo M, Sakuragi N, Kimura S, Iwanaga T, Colin DW. Regulated C-C motif ligand 2 (CCL2) in luteal cells contributes to macrophage infiltration into the human corpus luteum during luteolysis. Mol Hum Reprod. 2015;21(8):645–654. PubMed

Zhai B, Liu H, Li X, Dai L, Gao Y, Li C, et al. BMP15 prevents cumulus cell apoptosis through CCL2 and FBN1 in porcine ovaries. Cell Physiol Biochem. 2013;32(2):264–278. PubMed

Kong DH, Kim YK, Kim MR, Jang JH, Lee S. Emerging roles of vascular cell adhesion molecule-1 (VCAM-1) in immunological disorders and cancer. Int J Mol Sci. 2018 doi: 10.3390/ijms19041057. PubMed DOI PMC

Zhang D, Bi J, Liang Q, Wang S, Zhang L, Han F, et al. VCAM1 promotes tumor cell invasion and metastasis by inducing EMT and transendothelial migration in colorectal cancer. Front Oncol. 2020;10:1066. PubMed PMC

Sommaggio R, Máñez R, Costa C. TNF, pig CD86, and VCAM-1 identified as potential targets for intervention in xenotransplantation of pig chondrocytes. Cell Trans. 2009;18(12):1381–1393. PubMed

Kanmaz-Özer M, Vural P, Doru-Abbasolu S, Gedikbaşi A, Çil E, Karadaǧ B, et al. Polymorphisms of vascular cell adhesion molecule1 (VCAM1) in polycystic ovary syndrome determined by quantitative real-time polymerase chain reaction and melting curve analysis. Eur J Obstet Gynecol Reprod Biol. 2012;160(2):174–178. PubMed

Candelaria NR, Padmanabhan A, Stossi F, Cecilia Ljungberg M, Shelly KE, Pew BK, et al. VCAM1 is induced in ovarian theca and stromal cells in a mouse model of androgen excess. Endocrinology. 2019;160(6):1377–1393. PubMed PMC

Kulus J, Kulus M, Kranc W, Jopek K, Zdun M, Józkowiak M, et al. Transcriptomic profile of new gene markers encoding proteins responsible for structure of porcine ovarian granulosa cells. Biol. 2021;10(11):1214. PubMed PMC

Parkes WS, Amargant F, Zhou LT, Villanueva CE, Duncan FE, Pritchard MT. Hyaluronan and collagen are prominent extracellular matrix components in bovine and porcine ovaries. Genes (Basel) 2021;12(8):1186. PubMed PMC

Yao G, Kong Y, Yang G, Kong D, Xu Y, He J, et al. Lnc-GULP1–2:1 affects granulosa cell proliferation by regulating COL3A1 expression and localization. J Ovarian Res. 2021;14(1):1–10. doi: 10.1186/s13048-021-00769-1. PubMed DOI PMC

Kong Y, Yao G, He J, Yang G, Kong D, Sun Y. lncRNA LNC-GULP1-2:1 is involved in human granulosa cell proliferation by regulating COL3A1 gene. Fertil Steril. 2018;110(4):e320.

Engqvist H, Parris TZ, Kovács A, Nemes S, Werner Rönnerman E, De Lara S, et al. Immunohistochemical validation of COL3A1, GPR158 and PITHD1 as prognostic biomarkers in early-stage ovarian carcinomas. BMC Cancer. 2019;19(1):1–12. doi: 10.1186/s12885-019-6084-4. PubMed DOI PMC

Januchowski R, Świerczewska M, Sterzyńska K, Wojtowicz K, Nowicki M, Zabel M. Increased expression of several collagen genes is associated with drug resistance in ovarian cancer cell lines. J Cancer. 2016;7(10):1295–1310. PubMed PMC

Ma S, Charron J, Erikson RL. Role of Plk2 (Snk ) in mouse development and cell proliferation. Mol Cell Biol. 2003;23(19):6936–6943. doi: 10.1128/MCB.23.19.6936-6943.2003. PubMed DOI PMC

Li F, Jo M, Curry TE, Liu J. Hormonal induction of polo-like kinases (Plks) and impact of Plk2 on cell cycle progression in the rat ovary. PLoS ONE. 2012 doi: 10.1371/annotation/1a9779fe-f0ab-4937-a3ce-1bc7fb0268df. PubMed DOI PMC

Chen D, Yu W, Aitken L, Gunn-Moore F, Amadoro G. Willin/FRMD6: a multi-functional neuronal protein associated with Alzheimer’s disease. Cells. 2021;10(11):3024. PubMed PMC

Dos Santos EC, Lalonde-Larue A, Antoniazzi AQ, Barreta MH, Price CA, Dias Gonçalves PB, et al. YAP signaling in preovulatory granulosa cells is critical for the functioning of the EGF network during ovulation. Mol Cell Endocrinol. 2022;541:111524. PubMed

Plewes MR, Hou X, Zhang P, Liang A, Hua G, Wood JR, et al. Yes-associated protein 1 is required for proliferation and function of bovine granulosa cells in vitro. Biol Reprod. 2019;101(5):1001. PubMed PMC

Seo J, Kim J. Regulation of Hippo signaling by actin remodeling. BMB Rep. 2018;51(3):151. PubMed PMC

Yang Q, Yu B, Sun J. TTK, CDC25A, and ESPL1 as prognostic biomarkers for endometrial cancer. Biomed Res Int. 2020 doi: 10.1155/2020/4625123. PubMed DOI PMC

Jiang F, Kuang B, Que Y, Lin Z, Yuan L, Xiao W, et al. The clinical significance of transforming acidic coiled-coil protein 3 expression in non-small cell lung cancer. Oncol Rep. 2016;35(1):436–446. PubMed

Liu Y, Zhu K, Guan X, Xie S, Wang Y, Tong Y, et al. TTK is a potential therapeutic target for cisplatin-resistant ovarian cancer. J Ovarian Res. 2021;14(1):128. PubMed PMC

Gui T, Yao C, Jia B, Shen K. Identification and analysis of genes associated with epithelial ovarian cancer by integrated bioinformatics methods. PLoS ONE. 2021 doi: 10.1371/journal.pone.0253136. PubMed DOI PMC

Wissing ML, Kristensen SG, Andersen CY, Mikkelsen AL, Høst T, Borup R, et al. Identification of new ovulation-related genes in humans by comparing the transcriptome of granulosa cells before and after ovulation triggering in the same controlled ovarian stimulation cycle. Hum Reprod. 2014;29(5):997–1010. PubMed

Kulus M, Kranc W, Sujka-Kordowska P, Celichowski P, Konwerska A, Jankowski M, et al. Transcriptomic analysis of expression of genes regulating cell cycle progression in porcine ovarian granulosa cells during short-term in vitro primary culture. Histochem Cell Biol. 2020;153(6):397–412. doi: 10.1007/s00418-020-01860-2. PubMed DOI PMC

Du X, Li Q, Yang L, Zeng Q, Wang S, Li Q. Transcriptomic data analyses reveal that sow fertility-related lincRNA NORFA Is essential for the normal states and functions of granulosa cells. Front Cell Dev Biol. 2021;23(9):227. PubMed PMC

Yang F, Liu Q, Chen Y, Ye H, Wang H, Zeng S. Integrative proteomic and phosphoproteomic analyses of granulosa cells during follicular atresia in porcine. Front Cell Dev Biol. 2021;15(8):1722. PubMed PMC

Pan B, Liu C, Zhan X, Li J. Protegrin-1 regulates porcine granulosa cell proliferation via the EGFR-ERK1/2/p38 signaling pathway in vitro. Front Physiol. 2021;21(12):733. PubMed PMC

Zhou X, He Y, Li N, Bai G, Pan X, Zhang Z, et al. DNA methylation mediated RSPO2 to promote follicular development in mammals. Cell Death Dis. 2021;12(7):1–13. PubMed PMC

Donadeu FX, Schauer SN, Sontakke SD. Involvement of miRNAs in ovarian follicular and luteal development. J Endocrinol. 2012;215(3):323–34. PubMed

Wang L, Chen Y, Wu S, Tang J, Chen G, Li F. miR-135a suppresses granulosa cell growth by targeting Tgfbr1 and Ccnd2 during Folliculogenesis in mice. Cells. 2021;10(8):2104. PubMed PMC

Liu X, Gao Y, Lu Y, Zhang J, Li L, Yin F. Upregulation of NEK2 is associated with drug resistance in ovarian cancer. Oncol Rep. 2014;31(2):745–54. doi: 10.3892/or.2013.2910/abstract. PubMed DOI

Kokuryo T, Yokoyama Y, Yamaguchi J, Tsunoda N, Ebata T, Nagino M. NEK2 is an effective target for cancer therapy with potential to induce regression of multiple human malignancies. Anticancer Res. 2019;39(5):2251–8. PubMed

Liu Y, Pan B, Qu W, Cao Y, Li J, Zhao H. Systematic analysis of the expression and prognosis relevance of FBXO family reveals the significance of FBXO1 in human breast cancer. Cancer Cell Int. 2021;21(1):1–25. doi: 10.1186/s12935-021-01833-y. PubMed DOI PMC

Reimann JDR, Freed E, Hsu JY, Kramer ER, Peters JM, Jackson PK. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex. Cell. 2001;105(5):645–655. PubMed

Zhang L, Du X, Wei S, Li D, Li Q. A comprehensive transcriptomic view on the role of SMAD4 gene by RNAi-mediated knockdown in porcine follicular granulosa cells. Reproduction. 2016;152(1):81–9. PubMed

Zhao L, Xue S, Yao Z, Shi J, Chen B, Wu L, et al. Biallelic mutations in CDC20 cause female infertility characterized by abnormalities in oocyte maturation and early embryonic development. Protein Cell. 2020;11(12):921–7. doi: 10.1007/s13238-020-00756-0. PubMed DOI PMC

Lu CL, Yan ZQ, Song XL, Xu YY, Zheng XY, Li R, et al. Effect of exogenous gonadotropin on the transcriptome of human granulosa cells and follicular fluid hormone profiles. Reprod Biol Endocrinol. 2019 doi: 10.1186/s12958-019-0489-4. PubMed DOI PMC

Liu Y, Zhu K, Guan X, Xie S, Wang Y, Tong Y, et al. TTK is a potential therapeutic target for cisplatin-resistant ovarian cancer. J Ovarian Res. 2021;14(1):128. PubMed PMC

Gui T, Yao C, Jia B, Shen K. Identification and analysis of genes associated with epithelial ovarian cancer by integrated bioinformatics methods. PLoS ONE. 2021 doi: 10.1371/journal.pone.0253136. PubMed DOI PMC

Huo Q, Chen S, Li Z, Wang J, Li J, Xie N. Inhibiting of TACC3 promotes cell proliferation, cell invasion and the EMT pathway in breast cancer. Front Genet. 2021;3(12):649. PubMed PMC

Hou PF, Jiang T, Chen F, Shi PC, Li HQ, Bai J, et al. KIF4A facilitates cell proliferation via induction of p21-mediated cell cycle progression and promotes metastasis in colorectal cancer. Cell Death Dis. 2018;9(5):1–15. PubMed PMC

Chen X, Huo L, Ren L, Li Y, Sun Y, Li Y, et al. Polycystic ovary syndrome is associated with elevated periostin levels. Exp Clin Endocrinol Diabetes. 2019;127(9):571–7. PubMed

Hassani F, Oryan S, Eftekhari-Yazdi P, Bazrgar M, Moini A, Nasiri N, et al. Downregulation of extracellular matrix and cell adhesion molecules in cumulus cells of infertile polycystic ovary syndrome women with and without insulin resistance. Cell J. 2019;21(1):35–42. PubMed PMC

Henning NF, LeDuc RD, Even KA, Laronda MM. Proteomic analyses of decellularized porcine ovaries identified new matrisome proteins and spatial differences across and within ovarian compartments. Sci Rep. 2019 doi: 10.1038/s41598-019-56454-3. PubMed DOI PMC

Palani S, Ghosh S, Ivorra-Molla E, Clarke S, Suchenko A, Balasubramanian MK, et al. Calponin-homology domain mediated bending of membrane-associated actin filaments. Elife. 2021 doi: 10.7554/eLife.61078. PubMed DOI PMC

Trejter M, Hochol A, Tyczewska M, Ziolkowska A, Jopek K, Szyszka M, et al. Sex-related gene expression profiles in the adrenal cortex in the mature rat: microarray analysis with emphasis on genes involved in steroidogenesis. Int J Mol Med. 2015;35(3):702–14. PubMed PMC

Chamier-Gliszczyńska A, Brązert M, Sujka-Kordowska P, Popis M, Ożegowska K, Stefańska K, et al. Genes involved in angiogenesis and circulatory system development are differentially expressed in porcine epithelial oviductal cells during long-term primary in vitro culture—a transcriptomic study. Med J Cell Biol. 2018;6(4):163–173.

Nawrocki MJ, Celichowski P, Jankowski M, Kranc W, Bryja A, Borys-Wójcik S, 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(4):186–194.

Stefańska K, Chamier-Gliszczyńska A, Jankowski M, Celichowski P, Kulus M, Rojewska M, et al. Epithelium morphogenesis and oviduct development are regulated by significant increase of expression of genes after long-term in vitro primary culture—a microarray assays. Med J Cell Biol. 2018;6(4):195–204.

Kranc W, Brązert M, Ożegowska K, Budna-Tukan J, Celichowski P, Jankowski 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 doi: 10.2478/acb-2018-0015. DOI

Borys-Wójcik S, Kocherova I, Celichowski P, Popis M, Jeseta M, Bukowska D, et al. Protein oligomerization is the biochemical process highly up-regulated in porcine oocytes before in vitro maturation (IVM) Med J Cell Biol. 2018;6(4):155–162.

Budna J, Celichowski P, Bryja A, Jeseta M, Jankowski M, Bukowska D, et al. Expression changes in fatty acid metabolic processrelated genes in porcine oocytes during in vitro maturation. Med J Cell Biol. 2018;6(2):48–54.

Extract and Visualize the Results of Multivariate Data Analyses [R package factoextra version 1.0.7] | Semantic Scholar. https://www.semanticscholar.org/paper/Extract-and-Visualize-the-Results-of-Multivariate-Kassambara-Mundt/5cb503e3db8609405d9f286fadc2a8bb867e5b6e. Accessed 5 Mar 2023.

Golkar-Narenji A, Antosik P, Nolin S, Rucinski M, Jopek K, Zok A, et al. Gene ontology groups and signaling pathways regulating the process of avian satellite cell differentiation. Genes (Basel) 2022;13(2):242. PubMed PMC

Bader GD, Hogue CWV. An automated method for finding molecular complexes in large protein interaction networks. BMC Bioinformatics. 2003;4(1):1–27. doi: 10.1186/1471-2105-4-2. PubMed DOI PMC

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