Analysis of expression of genes responsible for regulation of cellular proliferation and migration – microarray approach based on porcine oocyte model

1Jamnongjit M, Hammes SR. Oocyte maturation: the coming of age of a germ cell. Semin Reprod Med. 2005;23:234–41; DOI:10.1055/s-2005-872451.10.1055/s-2005-87245116059829JamnongjitMHammesSROocyte maturation: the coming of age of a germ cellSemin Reprod Med2005232344110.1055/s-2005-872451148243016059829Open DOISearch in Google Scholar

2Mrazek M, Fulka J. Failure of oocyte maturation: Possible mechanisms for oocyte maturation arrest. Hum Reprod. 2003;18:2249–52; DOI:10.1093/humrep/deg434.10.1093/humrep/deg43414585868MrazekMFulkaJFailure of oocyte maturation: Possible mechanisms for oocyte maturation arrestHum Reprod20031822495210.1093/humrep/deg43414585868Open DOISearch in Google Scholar

3Hunt PA, Hassold TJ. Human female meiosis: what makes a good egg go bad? Trends Genet. 2008;24:86–93; DOI:10.1016/j.tig.2007.11.010.1819206310.1016/j.tig.2007.11.010HuntPAHassoldTJHuman female meiosis: what makes a good egg go bad?Trends Genet200824869310.1016/j.tig.2007.11.01018192063Search in Google Scholar

4Verlhac M-H, Terret M-E. Oocyte Maturation and Development. F1000Research. 2016;5:309; DOI:10.12688/f1000research.7892.1.10.12688/f1000research.7892.1VerlhacM-HTerretM-EOocyte Maturation and DevelopmentF1000Research2016530910.12688/f1000research.7892.1478690826998245Open DOISearch in Google Scholar

5Levran D, Farhi J, Nahum H, Glezerman M, Weissman A. Maturation arrest of human oocytes as a cause of infertility: Case report. Hum Reprod. 2002;17:1604–9; DOI:10.1093/humrep/17.6.1604.1204228510.1093/humrep/17.6.1604LevranDFarhiJNahumHGlezermanMWeissmanAMaturation arrest of human oocytes as a cause of infertility: Case reportHum Reprod2002171604910.1093/humrep/17.6.160412042285Search in Google Scholar

6Ming T, Nielsen H, Chen Z. Maturation arrest of human oocytes at germinal vesicle stage. J Hum Reprod Sci. 2010;3:153; DOI:10.4103/0974-1208.74161.10.4103/0974-1208.7416121234179MingTNielsenHChenZMaturation arrest of human oocytes at germinal vesicle stageJ Hum Reprod Sci2010315310.4103/0974-1208.74161301733421234179Open DOISearch in Google Scholar

7Rybska 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;6:13–7; DOI:10.2478/acb-2018-0003.10.2478/acb-2018-0003RybskaMKnapSJankowskiMJesetaMBukowskaDAntosikPNowickiMZabelMKempistyBJaśkowskiJMCytoplasmic and nuclear maturation of oocytes in mammals – living in the shadow of cells developmental capabilityMed J Cell Biol2018613710.2478/acb-2018-0003Open DOISearch in Google Scholar

8Gilchrist R., Ritter L., Armstrong D. Oocyte–somatic cell interactions during follicle development in mammals. Anim Reprod Sci. 2004;82–83:431–46; DOI:10.1016/j.anireprosci.2004.05.017.15271471GilchristR.RitterL.ArmstrongDOocyte–somatic cell interactions during follicle development in mammalsAnim Reprod Sci200482–834314610.1016/j.anireprosci.2004.05.01715271471Search in Google Scholar

9Li R, Norman RJ, Armstrong DT, Gilchrist RB. Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod. 2000;63:839–45.10.1095/biolreprod63.3.839LiRNormanRJArmstrongDTGilchristRBOocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cellsBiol Reprod2000638394510952929Open DOISearch in Google Scholar

10Macaulay AD, Gilbert I, Caballero J, Barreto R, Fournier E, Tossou P, Sirard M-A, Clarke HJ, Khandjian ÉW, Richard FJ, Hyttel P, Robert C. The Gametic Synapse: RNA Transfer to the Bovine Oocyte1. Biol Reprod. 2014;91:90; DOI:10.1095/biolreprod.114.119867.MacaulayADGilbertICaballeroJBarretoRFournierETossouPSirardM-AClarkeHJKhandjianÉW, Richard FJHyttelPRobertCThe Gametic Synapse: RNA Transfer to the Bovine Oocyte1Biol Reprod2014919010.1095/biolreprod.114.11986725143353Open DOISearch in Google Scholar

11Antosik P, Kempisty B, Jackowska M, Piotrowska H, Bukowska D, Wozna M, Lianeri M, Brussow K-P, Jaskowski JM. Assessment of transcript and protein levels contributing to cell cycle control and gap junction connections in morphologically variable groups of porcine cumulus-oocyte complexes. Vet Med (Praha). 2010;55:512–21.10.17221/2941-VETMEDAntosikPKempistyBJackowskaMPiotrowskaHBukowskaDWoznaMLianeriMBrussowK-PJaskowskiJMAssessment of transcript and protein levels contributing to cell cycle control and gap junction connections in morphologically variable groups of porcine cumulus-oocyte complexesVet Med (Praha)20105551221Open DOISearch in Google Scholar

12Chang CL, Wang H-S, Soong Y-K, Huang SY, Pai SY, Hsu SYT. Regulation of Oocyte and Cumulus Cell Interactions by Intermedin/Adrenomedullin 2. J Biol Chem. 2011;286:43193–203; DOI:10.1074/jbc.M111.297358.10.1074/jbc.M111.29735822009752ChangCLWangH-SSoongY-KHuangSYPaiSYHsuSYTRegulation of Oocyte and Cumulus Cell Interactions by Intermedin/Adrenomedullin 2J Biol Chem20112864319320310.1074/jbc.M111.297358323484922009752Open DOISearch in Google Scholar

13Huang DW, Sherman BT, Tan Q, Collins JR, Alvord WG, Roayaei J, Stephens R, Baseler MW, Lane HC, Lempicki RA. The DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene lists. Genome Biol. 2007;8:R183; DOI:10.1186/gb-2007-8-9-r183.10.1186/gb-2007-8-9-r183HuangDWShermanBTTanQCollinsJRAlvordWGRoayaeiJStephensRBaselerMWLaneHCLempickiRAThe DAVID Gene Functional Classification Tool: a novel biological module-centric algorithm to functionally analyze large gene listsGenome Biol20078R18310.1186/gb-2007-8-9-r183237502117784955Open DOISearch in Google Scholar

14Walter W, Sánchez-Cabo F, Ricote M. GOplot: An R package for visually combining expression data with functional analysis. Bioinformatics. 2015;31:2912–4; DOI:10.1093/bioinformatics/btv300.10.1093/bioinformatics/btv300WalterWSánchez-CaboFRicoteMGOplot: An R package for visually combining expression data with functional analysisBioinformatics2015312912410.1093/bioinformatics/btv30025964631Open DOISearch in Google Scholar

15von Mering C, Jensen LJ, Snel B, Hooper SD, Krupp M, Foglierini M, Jouffre N, Huynen MA, Bork P. STRING: known and predicted protein-protein associations, integrated and transferred across organisms. Nucleic Acids Res. 2004;33:D433–7; DOI:10.1093/nar/gki005.10.1093/nar/gki005vonMering CJensenLJSnelBHooperSDKruppMFoglieriniMJouffreNHuynenMABorkPSTRING: known and predicted protein-protein associations, integrated and transferred across organismsNucleic Acids Res200433D433710.1093/nar/gki00553995915608232Open DOISearch in Google Scholar

16Yokota Y, Mori S. Role of Id family proteins in growth control. J Cell Physiol. 2002;190:21–8; DOI:10.1002/jcp.10042.1180780710.1002/jcp.10042YokotaYMoriSRole of Id family proteins in growth controlJ Cell Physiol200219021810.1002/jcp.1004211807807Search in Google Scholar

17Massari ME, Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol. 2000;20:429–40.1061122110.1128/MCB.20.2.429-440.2000MassariMEMurreCHelix-loop-helix proteins: regulators of transcription in eucaryotic organismsMol Cell Biol200020429408509710611221Search in Google Scholar

18Lee SB, Frattini V, Bansal M, Castano AM, Sherman D, Hutchinson K, Bruce JN, Califano A, Liu G, Cardozo T, Iavarone A, Lasorella A. An ID2-dependent mechanism for VHL inactivation in cancer. Nature. 2016;529:172–7; DOI:10.1038/nature16475.10.1038/nature1647526735018LeeSBFrattiniVBansalMCastanoAMShermanDHutchinsonKBruceJNCalifanoALiuGCardozoTIavaroneALasorellaAAn ID2-dependent mechanism for VHL inactivation in cancerNature2016529172710.1038/nature16475538464726735018Open DOISearch in Google Scholar

19Roschger C, Cabrele C. The Id-protein family in developmental and cancer-associated pathways. Cell Commun Signal. 2017;15:7; DOI:10.1186/s12964-016-0161-y.10.1186/s12964-016-0161-y28122577RoschgerCCabreleCThe Id-protein family in developmental and cancer-associated pathwaysCell Commun Signal201715710.1186/s12964-016-0161-y526747428122577Open DOISearch in Google Scholar

20Trau HA, Brännström M, Curry TE, Duffy DM. Prostaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cells. Hum Reprod. 2016;31:dev320; DOI:10.1093/humrep/dev320.26740577TrauHABrännströmMCurryTEDuffyDMProstaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cellsHum Reprod20163110.1093/humrep/dev320471681026740577Search in Google Scholar

21Celichowski P, Nawrocki MJ, Dyszkiewicz-Konwińska M, Jankowski M, Budna J, Bryja A, Kranc W, Borys S, Knap S, Ciesiółka S, Jeseta M, Piasecka-Stryczyńska K, Khozmi R, Bukowska D, Antosik P, Brüssow KPKP, Bruska M, Nowicki M, Zabel M, Kempisty B. “Positive Regulation of RNA Metabolic Process” Ontology Group Highly Regulated in Porcine Oocytes Matured In Vitro : A Microarray Approach. Biomed Res Int. 2018;2018:1–10; DOI:10.1155/2018/2863068.CelichowskiPNawrockiMJDyszkiewicz-KonwińskaMJankowskiMBudnaJBryjaAKrancWBorysSKnapSCiesiółkaSJesetaMPiasecka-StryczyńskaKKhozmiRBukowskaDAntosikPBrüssowKPKPBruskaMNowickiMZabelMKempistyB.“Positive Regulation of RNA Metabolic Process” Ontology Group Highly Regulated in Porcine Oocytes Matured In Vitro : A Microarray ApproachBiomed Res Int2018201811010.1155/2018/2863068581892229546053Open DOISearch in Google Scholar

22Borys S, Brązert M, Jankowski M, Kocherova I, Ożegowska K, Celichowski P, Nawrocki MJ, Kranc W, Bryja A, Kulus M, Jeseta M, Pieńkowski W, Bręborowicz A, Bukowska D, Antosik P, Pawelczyk L, Skowroński MT, BRÜ SSOW KP, Bruska M, Zabel M, Nowicki M, Kempisty B. 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;32:21–35.BorysSBrązertMJankowskiMKocherovaIOżegowskaKCelichowskiPNawrockiMJKrancWBryjaAKulusMJesetaMPieńkowskiWBręborowiczABukowskaDAntosikPPawelczykLSkowrońskiMTBRÜSSOW KPBruskaMZabelMNowickiMKempistyBEnzyme linked receptor protein signaling pathway is one of the ontology groups that are highly up-regulated in porcine oocytes before in vitro maturationJ Biol Regul Homeost Agents2018322135Search in Google Scholar

23Chermuła B, Brązert M, Jeseta M, Ożegowska K, Sujka-Kordowska P, Konwerska A, Bryja A, Kranc W, Jankowski M, Nawrocki M, Kocherova I, Celichowski P, Borowiec B, Popis M, Budna-Tukan J, Antosik P, Bukowska D, Brussow K, Pawelczyk L, Bruska M, Zabel M, Nowicki M, Kempisty B. 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;20:84; DOI:10.3390/ijms20010084.10.3390/ijms20010084ChermułaBBrązertMJesetaMOżegowskaKSujka-KordowskaPKonwerskaABryjaAKrancWJankowskiMNawrockiMKocherovaICelichowskiPBorowiecBPopisMBudna-TukanJAntosikPBukowskaDBrussowKPawelczykLBruskaMZabelMNowickiMKempistyBThe Unique Mechanisms of Cellular Proliferation, Migration and Apoptosis are Regulated through Oocyte Maturational Development—A Complete Transcriptomic and Histochemical StudyInt J Mol Sci2018208410.3390/ijms20010084633754830587792Open DOISearch in Google Scholar

24Chaves RN, Duarte ABG, Rodrigues GQ, Celestino JJH, Silva GM, Lopes CAP, Almeida AP, Donato MAM, Peixoto CA, Moura AAA, Lobo CH, Locatelli Y, Mermillod P, Campello CC, Figueiredo JR. The Effects of Insulin and Follicle-Simulating Hormone (FSH) During In Vitro Development of Ovarian Goat Preantral Follicles and the Relative mRNA Expression for Insulin and FSH Receptors and Cytochrome P450 Aromatase in Cultured Follicles1. Biol Reprod. 2012;87:69; DOI:10.1095/biolreprod.112.099010.22811569ChavesRNDuarteABGRodriguesGQCelestinoJJHSilvaGMLopesCAPAlmeidaAPDonatoMAMPeixotoCAMouraAAALoboCHLocatelliYMermillodPCampelloCCFigueiredoJRThe Effects of Insulin and Follicle-Simulating Hormone (FSH) During In Vitro Development of Ovarian Goat Preantral Follicles and the Relative mRNA Expression for Insulin and FSH Receptors and Cytochrome P450 Aromatase in Cultured Follicles1Biol Reprod2012876910.1095/biolreprod.112.09901022811569Search in Google Scholar

25Jones RL, Pepling ME. KIT signaling regulates primordial follicle formation in the neonatal mouse ovary. Dev Biol. 2013;382:186–97; DOI:10.1016/j.ydbio.2013.06.030.2383137810.1016/j.ydbio.2013.06.030JonesRLPeplingMEKIT signaling regulates primordial follicle formation in the neonatal mouse ovaryDev Biol20133821869710.1016/j.ydbio.2013.06.03023831378Search in Google Scholar

26Cadoret V, Frapsauce C, Jarrier P, Maillard V, Bonnet A, Locatelli Y, Royère D, Monniaux D, Guérif F, Monget P. Molecular evidence that follicle development is accelerated in vitro compared to in vivo. Reproduction. 2017;153:493–508; DOI:10.1530/REP-16-0627.2815411110.1530/REP-16-0627CadoretVFrapsauceCJarrierPMaillardVBonnetALocatelliYRoyèreDMonniauxDGuérifFMongetPMolecular evidence that follicle development is accelerated in vitro compared to in vivoReproduction201715349350810.1530/REP-16-062728154111Search in Google Scholar

27Chermuła B, Brązert M, Jeseta M, Ożegowska K, Kocherova I, Jankowski M, Celichowski P, Sujka-Kordowska P, Konwerska A, Piotrowska-Kempisty H, Budna-Tukan J, Antosik P, Bukowska D, Machatkova M, Brussow KP, Skowroński MT, Pawelczyk L, Bruska M, Nowicki M, Kempisty B. Transcriptomic Pattern of Genes Regulating Protein Response and Status of Mitochondrial Activity Are Related to Oocyte Maturational Competence—A Transcriptomic Study. Int J Mol Sci. 2019;20:2238; DOI:10.3390/ijms20092238.10.3390/ijms20092238ChermułaBBrązertMJesetaMOżegowskaKKocherovaIJankowskiMCelichowskiPSujka-KordowskaPKonwerskaAPiotrowska-KempistyHBudna-TukanJAntosikPBukowskaDMachatkovaMBrussowKPSkowrońskiMTPawelczykLBruskaMNowickiMKempistyBTranscriptomic Pattern of Genes Regulating Protein Response and Status of Mitochondrial Activity Are Related to Oocyte Maturational Competence—A Transcriptomic StudyInt J Mol Sci201920223810.3390/ijms20092238653904831067669Open DOISearch in Google Scholar

28Ożegowska K, Dyszkiewicz-Konwińska M, Celichowski P, Nawrocki MJ, Bryja A, Jankowski M, Kranc W, Brązert M, Knap S, Jeseta M, Skowroński MT, Bukowska D, Antosik P, Brüssow KP, Bręborowicz A, Bruska M, Nowicki M, Pawelczyk L, Zabel M, Kempisty B. Expression pattern of new genes regulating female sex differentiation and in vitro maturational status of oocytes in pigs. Theriogenology. 2018;121:122–33; DOI:10.1016/j.theriogenology.2018.08.019.3014554210.1016/j.theriogenology.2018.08.019OżegowskaKDyszkiewicz-KonwińskaMCelichowskiPNawrockiMJBryjaAJankowskiMKrancWBrązertMKnapSJesetaMSkowrońskiMTBukowskaDAntosikPBrüssowKPBręborowiczABruskaMNowickiMPawelczykLZabelMKempistyBExpression pattern of new genes regulating female sex differentiation and in vitro maturational status of oocytes in pigsTheriogenology20181211223310.1016/j.theriogenology.2018.08.01930145542Search in Google Scholar

29Robker 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;12:924–40; DOI:10.1210/mend.12.7.0138.10.1210/mend.12.7.01389658398RobkerRLRichardsJSHormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1Mol Endocrinol1998129244010.1210/mend.12.7.01389658398Open DOISearch in Google Scholar

30Bridges PJ, Cho J, Ko C. Endothelins in regulating ovarian and oviductal function. Front Biosci (Schol Ed). 2011;3:145–55.21196365BridgesPJChoJKoCEndothelins in regulating ovarian and oviductal functionFront Biosci (Schol Ed)201131455510.2741/s140303047321196365Search in Google Scholar

31Kawamura K, Ye Y, Liang CG, Kawamura N, Gelpke MS, Rauch R, Tanaka T, Hsueh AJW. Paracrine regulation of the resumption of oocyte meiosis by endothelin-1. Dev Biol. 2009;327:62–70; DOI:10.1016/j.ydbio.2008.11.033.10.1016/j.ydbio.2008.11.03319111534KawamuraKYeYLiangCGKawamuraNGelpkeMSRauchRTanakaTHsuehAJWParacrine regulation of the resumption of oocyte meiosis by endothelin-1Dev Biol2009327627010.1016/j.ydbio.2008.11.03319111534Open DOISearch in Google Scholar

32Piotrowska H, Kempisty B, Sosinska P, Ciesiolka S, Bukowska D, Antosik P, Rybska M, Brussow KP, Nowicki M, Zabel M. The role of TGF superfamily gene expression in the regulation of folliculogenesis and oogenesis in mammals: a review. Vet Med (Praha). 2013;58:505–15.10.17221/7082-VETMEDPiotrowskaHKempistyBSosinskaPCiesiolkaSBukowskaDAntosikPRybskaMBrussowKPNowickiMZabelMThe role of TGF superfamily gene expression in the regulation of folliculogenesis and oogenesis in mammals: a reviewVet Med (Praha)20135850515Open DOISearch in Google Scholar