Results and Problems in Cell Diff erentiation 61 Jean-Pierre Tassan Jacek Z. Kubiak Editors Asymmetric Cell Division in Development, Diff erentiation and Cancer Results and Problems in Cell Differentiation Volume 61 Series editors JacekZ.Kubiak,RennesCX,France MalgorzataKloc,Houston,TX,USA More information about this series at http://www.springer.com/series/400 Jean-Pierre Tassan (cid:129) Jacek Z. Kubiak Editors Asymmetric Cell Division in Development, Differentiation and Cancer Editors Jean-PierreTassan JacekZ.Kubiak IGDR,UMR6290,CNRS InstofGenetics&DevofRennesIG Universite´deRennes1 CNRS/UniveRennes1UMR6290 Rennes,France RennesCedex,France ISSN0080-1844 ISSN1861-0412 (electronic) ResultsandProblemsinCellDifferentiation ISBN978-3-319-53149-6 ISBN978-3-319-53150-2 (eBook) DOI10.1007/978-3-319-53150-2 LibraryofCongressControlNumber:2017938011 ©SpringerInternationalPublishingAG2017 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 Contents 1 ModelingAsymmetricCellDivisioninCaulobactercrescentus UsingaBooleanLogicApproach. . . . . . . . . . . . . . . . . . . . . . . . . . 1 IsmaelSa´nchez-Osorio,CarlosA.Herna´ndez-Mart´ınez, andAgustinoMart´ınez-Antonio 2 SpatiotemporalModelsoftheAsymmetricDivisionCycle ofCaulobactercrescentus. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 23 KartikSubramanianandJohnJ.Tyson 3 IntrinsicandExtrinsicDeterminantsLinkingSpindlePoleFate, SpindlePolarity,andAsymmetricCellDivisionintheBudding YeastS.cerevisiae. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 49 MarcoGeymonatandMarisaSegal 4 WntSignalingPolarizesC.elegansAsymmetricCellDivisions DuringDevelopment. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 83 ArielleKoonyeeLamandBryanT.Phillips 5 AsymmetricCellDivisionintheOne-CellC.elegansEmbryo: MultipleStepstoGenerateCellSizeAsymmetry. . . . . . . . . . . . . . 115 AnnePacquelet 6 SizeMatters:HowC.elegansAsymmetricDivisionsRegulate Apoptosis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 141 JeromeTeuliereandGianGarriga 7 TheMidbodyanditsRemnantinCellPolarizationandAsymmetric CellDivision. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165 ChristianPohl 8 DrosophilamelanogasterNeuroblasts:AModelforAsymmetric StemCellDivisions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 183 EmmanuelGallaud,TriPham,andClemensCabernard v vi Contents 9 AsymmetricDivisionsinOogenesis. . . . . . . . . . . . . . . . . . . . . . . . . 211 SzczepanM.Bilinski,JacekZ.Kubiak,andMalgorzataKloc 10 AsymmetricLocalizationandDistributionofFactorsDetermining CellFateDuringEarlyDevelopmentofXenopuslaevis. . . . . . . . . 229 RadekSindelka,MonikaSidova,PavelAbaffy,andMikaelKubista 11 AsymmetriesinCellDivision,CellSize,andFurrowing intheXenopuslaevisEmbryo. . . . . . . . . . . . . . . . . . . . . . . . . . . . . 243 Jean-PierreTassan,MartinWühr,GuillaumeHatte,andJacekKubiak 12 AsymmetricandUnequalCellDivisionsinAscidianEmbryos. . . . 261 TakefumiNegishiandHirokiNishida 13 AsymmetriesandSymmetriesintheMouseOocyteandZygote. . . 285 AgatheChaigne,Marie-EmilieTerret,andMarie-He´le`neVerlhac 14 SymmetryDoesnotComeforFree:CellularMechanisms toAchieveaSymmetricCellDivision. . . . . . . . . . . . . . . . . . . . . . . 301 DamianDudkaandPatrickMeraldi 15 AComparativePerspectiveonWnt/β-CateninSignallinginCell FateDetermination. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323 ClareL.GarcinandShukryJ.Habib 16 ExtracellularRegulationoftheMitoticSpindleandFate DeterminantsDrivingAsymmetricCellDivision. . . . . . . . . . . . . . 351 PrestinaSmith,MarkAzzam,andLindsayHinck 17 RegulationofAsymmetricCellDivisioninMammalianNeural StemandCancerPrecursorCells. . . . . . . . . . . . . . . . . . . . . . . . . . 375 MathieuDaynacandClaudiaK.Petritsch 18 MolecularProgramsUnderlyingAsymmetricStemCellDivision andTheirDisruptioninMalignancy. . . . . . . . . . . . . . . . . . . . . . . . 401 SubhasMukherjeeandDanielJ.Brat Chapter 1 Modeling Asymmetric Cell Division Caulobacter crescentus in Using a Boolean Logic Approach IsmaelSa´nchez-Osorio,CarlosA.Herna´ndez-Mart´ınez, andAgustinoMart´ınez-Antonio Abstract Caulobactercrescentusisamodelorganismforthestudyofasymmetric division and cell type differentiation, as its cell division cycle generates a pair of daughtercellsthatdifferfromoneanotherintheirmorphologyandbehavior.One of these cells (called stalked) develops a structure that allows it to attach to solid surfacesandis theonlyonecapableofdividing,while theother(called swarmer) develops aflagellumthat allows it tomove inliquid mediaand divides only after differentiating into a stalked cell type. Although many genes, proteins, and other molecules involved in the asymmetric division exhibited by C. crescentus have beendiscoveredandcharacterizedforseveraldecades,itremainsasachallenging task to understand how cell properties arise from the high number of interactions betweenthesemolecularcomponents.Thischapterdescribesamodelingapproach basedontheBooleanlogicframeworkthatprovidesameansfortheintegrationof knowledgeandstudyoftheemergenceofasymmetricdivision.Thetextillustrates howthesimulationofsimplelogicmodelsgivesvaluableinsightintothedynamic behavior of the regulatory and signaling networks driving the emergence of the phenotypes exhibited by C. crescentus. These models provide useful tools for the characterizationandanalysisofothercomplexbiologicalnetworks. Abbreviation TF TranscriptionFactor I.Sa´nchez-Osorio(*)•C.A.Herna´ndez-Mart´ınez•A.Mart´ınez-Antonio DepartmentofGeneticEngineering,CenterforResearchandAdvancedStudiesofthe NationalPolytechnicInstitute,Irapuato,GuanajuatoCP36821,Me´xico e-mail:[email protected];[email protected] ©SpringerInternationalPublishingAG2017 1 J.-P.Tassan,J.Z.Kubiak(eds.),AsymmetricCellDivisioninDevelopment, DifferentiationandCancer,ResultsandProblemsinCellDifferentiation61, DOI10.1007/978-3-319-53150-2_1 2 I.Sa´nchez-Osorioetal. 1.1 Introduction Caulobacter crescentus is a Gram-negative bacterium that divides asymmetrically, generatingtwodaughtercellsthatdevelopdifferentappendagesatoneoftheirpoles at particular times during their division cycle. One newborn cell, called swarmer, developsaflagellumandachemotacticapparatus,whichenablesittomoveinliquid media following gradients of nutrient concentrations (Jensen 2006). The other daughter, in contrast, has a narrow extension of its cell body called stalk, which allowsthecelltoattachtosolidsurfaces.Thisistheonlycelltypecapableofdividing (WagnerandBrun2007).Afteracquiringenoughbiomass,stalkedcellsdivideand release motile swarmer cells that will remain in that state for a certain time period (Englandetal.2010).Eventually,theswarmercellslosetheirflagellaandacquirethe stalkedphenotype,generatingacyclicpatternofgrowthanddivision. In some sense, C. crescentus resembles the asymmetric cell division and cell typedifferentiationexhibitedbyeukaryotes.Becauseofthis,itisanorganismthat can be used as a biological model for the study of these phenomena in more complex organisms. As shown in Fig. 1.1, the cell cycle of C. crescentus can be Fig.1.1 AsymmetricdivisionandcellcycleofC.crescentus.Theformationoftheswarmerand stalkedcelltypesispresentedinthecontextofcelldivision.Thecellcycleisdividedindiscrete stagesanalogoustothoseofthecelldivisionofeukaryotes 1 ModelingAsymmetricCellDivisioninCaulobactercrescentusUsinga... 3 seenintermsofthreestagesanalogoustothoseoccurringduringmitosis,namely, G1,S,andG2/M.DuringtheG1phase,swarmercellsejecttheflagellum,synthe- size the holdfast and the stalk structure, and initiate the replication of their DNA (Jensen2006).IntheSphase,whenthesynthesisofDNAisoccurring,thenewly formed DNA strands get spooled toward a pole of the cell and fold into compact chromosomal microdomains (Jensen et al. 2001). From this pre-divisional com- partmentalization,bymechanismsthatarestillunclear,anewcellfatewillemerge on each of the daughter cells (Judd et al. 2003). Finally, at the G2/M phase, C. crescentus divides asymmetrically into swarmer and stalked cells, and the DNAofeachdaughterbecomesfullymethylated(ReisenauerandShapiro2002). From a molecular biology perspective, if we could determine the function of eachofthemoleculesinvolvedinthebehaviordisplayedbyC.crescentusduringits division cycle, then we could in principle understand how this phenotype arises fromthemolecularconstituentsofthecell.However,asmoregenes,geneproducts, and other molecules were discovered, it would remain a very challenging task to extractknowledgefromthatinformationandgrasptheresultofthesheernumberof their interactions. In consequence, it is necessary to have a way to unify that data intoacoherentpicture,sothatthiskind ofbiologicalphenomenoncan bestudied and understood in a more integrated manner. This integration would also require accountingforthetemporalvariationintheexpressionofallgenesinvolvedinthe developmentoftheobservedphenotypes,assuchdynamicsmaybedecisiveforthe emergence of cell cycle properties (Ryan and Shapiro 2003). Therefore, by no longer focusing on single genes and molecules, but on global system properties arising from dynamic interactions, it may be possible to achieve a better under- standing of how the asymmetric cell division of C. crescentus arises from its molecular cell components. This endeavor can be facilitated by the formal and preciselanguageofmathematics. In this chapter, we address the reconstruction, modeling, and analysis of the regulatory and signaling networks involved in the cell cycle and asymmetric division of C. crescentus, which we have studied in a previous work (Qui~nones- Valles et al. 2014). We introduce general modeling principles that provide a foundation for the construction, simulation, and verification of simple discrete models based on the Boolean modeling framework (Thomas 1978). We argue throughout the text that,despiteits limitations, thisis ausefultooltoexplore and studytheemergenceofasymmetricdivision,asitcapturessomeessentialdetailsof thedynamicinteractionsbetweenregulatorycomponentsthroughtheuseoflogical rules. These kinds of models have been successfully applied in the study of other biologicalphenomena,includingthephenotypictransitionbetweenlysisandlysog- eny in the lambda phage (Thieffry and Thomas 1995), cellular fate generation duringflowerdevelopmentinArabidopsisthaliana(Espinosa-Sotoetal.2004),and celldifferentiationinlymphocytes(Mendoza2006).