Results and Problems in Cell Diff erentiation 59 Swathi Arur Editor Signaling- Mediated Control of Cell Division From Oogenesis to Oocyte-to-Embryo Development Results and Problems in Cell Differentiation Volume 59 Series editors JacekZ.Kubiak,RennesCX,France MalgorzataKloc,Houston,TX,USA More information about this series at http://www.springer.com/series/400 Swathi Arur Editor Signaling-Mediated Control of Cell Division From Oogenesis to Oocyte-to-Embryo Development Editor SwathiArur Dept.ofGenetics,Genes&Dev.Program UTMDAndersonCancerCenter Houston,Texas USA ISSN0080-1844 ISSN1861-0412 (electronic) ResultsandProblemsinCellDifferentiation ISBN978-3-319-44819-0 ISBN978-3-319-44820-6 (eBook) DOI10.1007/978-3-319-44820-6 LibraryofCongressControlNumber:2016961937 ©SpringerInternationalPublishingSwitzerland2017 Thisworkissubjecttocopyright.AllrightsarereservedbythePublisher,whetherthewholeorpartof the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilarmethodologynowknownorhereafterdeveloped. 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Printedonacid-freepaper ThisSpringerimprintispublishedbySpringerNature TheregisteredcompanyisSpringerInternationalPublishingAG Theregisteredcompanyaddressis:Gewerbestrasse11,6330Cham,Switzerland Preface Germcellssustainlifethroughgenerations.Germcellsaresetasidefromsomatic cellsintheembryoandgothroughthespecializedcelldivisionprocessofmeiosis toproducethegametes—theoocyteorthesperm.Theprocesswherebygermcells developintogametesisgovernedviaseveraldevelopmental,nutritional,andother environmental cues or signals. Unsurprisingly, due to a variety of causes, some- times these signals are spatially and/or temporally anomalous during organismal development, and such anomalies can manifest as birth defects in the progeny. Thus, elucidating how a multitude of molecular mediators integrate the various developmentalandenvironmentalsignalstocoordinategermcellformation,main- tenance,andfunctionremainsanactiveareaofinvestigation. Inbothinvertebrateandvertebrateanimals,environmentallyactivatedsignaling pathwaysregulateproductionofgameteswithnutritionalavailability.Muchwork has focused on understanding the mechanisms that regulate oocyte fitness and quality in humans and other vertebrate model organisms such as mice. However, in the mammalian female, germ cells enter and arrest in meiosis I during fetal development, and initiation of meiosis II—ovulation—occurs after birth and only when the progeny attains sexual maturity. In contrast, the invertebrate female germlinestemcellsproduceoocytescontinuouslythroughoutdevelopment.There- fore, understanding the cellular and molecular mechanisms that govern germline stem cell populations and meiosis I is relatively more tractable using invertebrate model organisms such as Caenorhabditis elegans and Drosophila melanogaster. Together,studiesusingbothvertebrateandinvertebratesarebeginningtoprovide insightsintothemechanismsthatensureoocytequalityandminimizeerrorsduring meiosisandmeioticmaturation.Inthisvolume,expertsworkingondiversemodel organismscometogethertodiscussthestate-of-the-artknowledgebaseontherole of signaling pathways in regulating germline stem cell biology and meiotic pro- gression of oocytes until fertilization and birth and identify exciting new avenues andquestionsforfutureresearch. WebeginwithadescriptionofepigeneticmechanismsthatregulateDrosophila germline stem cell gene expression. Rangan and coauthors elaborate the role of v vi Preface several histone variants and nucleosome remodeling complexes in maintaining germline stem cells. They further provide insights into the interplay between epigenetic and signaling mechanisms that drive differentiation into the meiotic program. The decision of a stem cell to differentiate or self-renew is of fundamental importancetoorganismaldevelopmentandtissuemaintenance.SinghandHansen discuss the signaling circuitry, including feedback loops between differentiated cellsandstemcells,whichenablesagermlinestemcelltomaintainafinebalance betweenself-renewal(enoughtomaintainapoolofstemcells)anddifferentiation (tomaintainoocytenumbers).Theyalsodiscussthesimilaritiesanduniqueaspects ofstemcellrenewalanddifferentiationinworms,flies,andmalemice. Oocytequalityisinfluencedsignificantlybynutritionalandotherenvironmental cuesorsignals. Laws and Drummond-Barbosa elaborate on the strong influence of diet and physiology on reproductive fitness. The authors critically review in vivo studies in model organisms (worms, flies, and mice) and discuss how diet-dependent signals can control the proliferation of germline stem cells and their maintenance andsubsequentmeioticprogressionandproductionofoocytes. I then provide a mechanistic view on how nutrition-induced signals regulate oogenic meiosis I progression via the ERK/MAPK pathway in C. elegans and signalingandsecondmessengerpathwaysthatregulateoocytemeioticmaturation in C. elegans, Drosophila and mammals. Through detailed discussions of several evolutionarily conserved signaling pathways, I synthesize common themes in the regulationofkeymeioticeventsduringoocytegrowthandmaturation. Meiosis-specific processes such as chromosomal pairing and recombination generate diversity in a species. Failure in the coordinated regulation of these meiotic processes also results in aneuploidy in the progeny. Smolikove and col- leaguesexaminetheinterplayofsignalingwithmeiosisIthatiscriticalfornormal oocyte development. They also examine the role of increasing maternal age on oocytequality. Oocytegrowth,development,andmaturationoccurunderamolecularenviron- ment of transcriptional quiescence. Transcription is not reinitiated until embryo- genesis. Thus, posttranscriptional and translational mechanisms are critical to normaloocytedevelopment.Subramaniamandcolleaguesdiscussthetranslational and posttranslational mechanisms that control the decision of stem cells to enter meiosis,oocytedevelopment,andmaturation. Mammalian oocytes undergo meiotic arrest intwo phases: meiotic Iarrest and meiotic II arrest. The second meiotic arrest is coordinated with embryo develop- ment by the activity of the cell division protein Cdc6. Kubiak and colleagues discuss mechanisms utilized by Cdc6 to exquisitely coordinate DNA replication after meiotic II arrest with that in the embryo. Yeste and colleagues weave in the importance of sperm- and oocyte-derived factors that regulate meiosis II comple- tion—after resumption from the meiotic II arrest—and prevent polyspermy, thereby ensuring a normal zygote. They discuss the role of lipid signaling in these processes and contemplate the impact of artificial oocyte activating factors Preface vii inclinicalsettingsdedicatedtohelpinghumanswithoocyteactivationdeficiency. Theyalsodiscussoptionsforbetterandmoreendogenousalternativestoartificial oocyteactivatingfactors. HoangandMillerfocusonthespecificmechanismsthatenablespermguidance in the female reproductive tract. They examine the role of pheromones and nutri- tionalsignalsthataffectthespermguidancemachineryandimpactspermmotility and fertility and discuss implications to human reproduction and oncologic treatments. Fassnacht and Ciosk analyze our current understanding on the critical reprogrammingmechanismsthatunderlietheprogression ofanoocytetoasingle totipotent embryo. They highlight the role of developmental reprogramming with implicationstovariedaspectsofhumandevelopmentandregenerativemedicine. The authors synthesize information derived from various different model sys- temstoprovidecriticalinsightsintotheprogressionoffemalegermlinestemcells throughmeioticmaturationanddevelopmentofahealthyembryo,highlightingthe impact on human health. Additionally, we discuss the critical gaps in knowledge and questions that remain to be addressed, understanding of which will influence humanreproduction,development,andregenerativemedicine. Houston,TX SwathiArur 2016 Contents 1 RoleofChromatinModificationsinDrosophilaGermlineStem CellDifferentiation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 PoojaFlora,AliciaMcCarthy,MaitreyiUpadhyay, andPrashanthRangan 2 RegulationoftheBalanceBetweenProliferation andDifferentiationinGermLineStemCells. . . . . . . . . . . . . . . . . 31 RamyaSinghandDaveHansen 3 ControlofGermlineStemCellLineagesbyDietandPhysiology. . . 67 KaitlinM.LawsandDanielaDrummond-Barbosa 4 Signaling-MediatedRegulationofMeioticProphaseI andTransitionDuringOogenesis. . . . . . . . . . . . . . . . . . . . . . . . . . 101 SwathiArur 5 ProphaseI:PreparingChromosomesforSegregation intheDevelopingOocyte. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125 RachelReichman,BenjaminAlleva,andSaritSmolikove 6 TranslationalControlofGermCellDecisions. . . . . . . . . . . . . . . . 175 KumariPushpa,GangaAnilKumar,andKuppuswamySubramaniam 7 RoleofCdc6DuringOogenesisandEarlyEmbryoDevelopment inMouseandXenopuslaevis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 201 EwaBorsuk,JoannaJachowicz,MalgorzataKloc,Jean-PierreTassan, andJacekZ.Kubiak 8 OocyteActivationandFertilisation:CrucialContributors fromtheSpermandOocyte. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 213 MarcYeste,CelineJones,SitiNornadhirahAmdani, andKevinCoward 9 SpermNavigationMechanismsintheFemaleReproductiveTract. . . 241 HieuD.HoangandMichaelA.Miller ix x Contents 10 CellFateMaintenanceandReprogrammingDuring theOocyte-to-EmbryoTransition. . . . . . . . . . . . . . . . . . . . . . . . . . 269 ChristinaFassnachtandRafalCiosk Index. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 287
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