Cellular adhesion in development and disease PDF
Preview Cellular adhesion in development and disease
CURRENT TOPICS IN DEVELOPMENTAL BIOLOGY “Ameeting-groundforcriticalreviewanddiscussionofdevelopmentalprocesses” A.A.MosconaandAlbertoMonroy(Volume1,1966) SERIES EDITOR Paul M. Wassarman Department ofDevelopmental andRegenerative Biology IcahnSchool ofMedicine atMount Sinai New York, NY,USA CURRENT ADVISORY BOARD Blanche Capel Susan Mango Wolfgang Driever Philippe Soriano Denis Duboule Cliff Tabin Anne Ephrussi MagdalenaZernicka-Goetz FOUNDING EDITORS A.A. Moscona and Alberto Monroy FOUNDING ADVISORY BOARD Vincent G. Allfrey Dame Honor B.Fell Jean Brachet John C. Kendrew Seymour S. Cohen S.Spiegelman Bernard D.Davis Hewson W.Swift James D. Ebert E.N.Willmer Mac V. Edds, Jr. Etienne Wolff AcademicPressisanimprintofElsevier 225WymanStreet,Waltham,MA02451,USA 525BStreet,Suite1800,SanDiego,CA92101-4495,USA 125LondonWall,London,EC2Y5AS,UK TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UK Firstedition2015 Copyright©2015ElsevierInc.Allrightsreserved. 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ISBN:978-0-12-407758-4 ISSN:0070-2153 ForinformationonallAcademicPresspublications visitourwebsiteatstore.elsevier.com CONTRIBUTORS EliasH.Barriga CellandDevelopmentalBiologyDepartment,UniversityCollegeLondon,London, UnitedKingdom DeannaL.Benson FishbergDepartmentofNeuroscience,FriedmanBrainInstituteandtheGraduateSchoolof BiomedicalSciences,IcahnSchoolofMedicineatMountSinai,NewYork,USA NicholasH.Brown DepartmentofPhysiology,DevelopmentandNeuroscience,TheGurdonInstitute, UniversityofCambridge,Cambridge,UnitedKingdom AlexanderN.Combes InstituteforMolecularBioscience,TheUniversityofQueensland,St.Lucia,Brisbane, Queensland,Australia JamieA.Davies CentreforIntegrativePhysiology,UniversityofEdinburgh,Edinburgh,UnitedKingdom AndrewJ.Ewald DepartmentofCellBiology,CenterforCellDynamics,andDepartmentofOncology,Johns HopkinsUniversitySchoolofMedicine,Baltimore,Maryland,USA Franc¸oisFagotto DepartmentofBiology,McGillUniversity,Montre´al,Que´bec,Canada LaurenG.Friedman FishbergDepartmentofNeuroscience,FriedmanBrainInstituteandtheGraduate SchoolofBiomedicalSciences,IcahnSchoolofMedicineatMountSinai, NewYork,USA CaraJ.Gottardi CellularandMolecularBiology,andMedicine,NorthwesternUniversityFeinbergSchoolof Medicine,Chicago,Illinois,USA BenjaminM.Hogan InstituteforMolecularBioscience,TheUniversityofQueensland,Brisbane,Queensland, Australia GeorgeW.Huntley FishbergDepartmentofNeuroscience,FriedmanBrainInstituteandtheGraduateSchoolof BiomedicalSciences,IcahnSchoolofMedicineatMountSinai,NewYork,USA AnneKarineLagendijk InstituteforMolecularBioscience,TheUniversityofQueensland,Brisbane,Queensland, Australia xi xii Contributors TerryLechler DepartmentofDermatology,andDepartmentofCellBiology,DukeUniversityMedical Center,Durham,NorthCarolina,USA MelissaH.Little MurdochChildren’sResearchInstitute,RoyalChildren’sHospital,Melbourne,Victoria, Australia AidanP.Maartens DepartmentofPhysiology,DevelopmentandNeuroscience,TheGurdonInstitute, UniversityofCambridge,Cambridge,UnitedKingdom MeghanT.Maher DepartmentofBiology,WashingtonUniversityinSt.Louis,St.Louis,Missouri,USA KenjiMandai DivisionofPathogeneticSignaling,KobeUniversityGraduateSchoolofMedicine,and CREST,JapanScienceandTechnologyAgency,Kobe,Japan RobertoMayor CellandDevelopmentalBiologyDepartment,UniversityCollegeLondon,London,United Kingdom PierreD.McCrea DepartmentofGenetics,UniversityofTexasMDAndersonCancerCenter;Programin Genes&Development,GraduateSchoolinBiomedicalSciences,Houston,Texas,USA MasahiroMori CREST,JapanScienceandTechnologyAgency;DivisionofNeurophysiology,Department ofPhysiologyandCellBiology,KobeUniversityGraduateSchoolofMedicine,andFaculty ofHealthSciences,KobeUniversityGraduateSchoolofHealthSciences,Kobe,Japan NicolasPlachta EuropeanMolecularBiologyLaboratory(EMBL)Australia,AustralianRegenerative MedicineInstitute,MonashUniversity,Clayton,Victoria,Australia RashmiPriya DivisionofCellBiologyandMolecularMedicine,InstituteforMolecularBioscience, TheUniversityofQueensland,Brisbane,Queensland,Australia YoshiyukiRikitake CREST,JapanScienceandTechnologyAgency;DivisionofSignalTransduction, DepartmentofBiochemistryandMolecularBiology,andDivisionofCardiovascular Medicine,DepartmentofInternalMedicine,KobeUniversityGraduateSchoolofMedicine, Kobe,Japan KatjaRo€per MRC-LaboratoryofMolecularBiology,CambridgeBiomedicalCampus,Cambridge, UnitedKingdom PierreSavagner IRCM,InstitutdeRechercheenCance´rologiedeMontpellier,INSERMU896,Institut re´gionalduCancerUniversite´ Montpellier1,Montpellier,France Contributors xiii EliahR.Shamir DepartmentofCellBiology,CenterforCellDynamics,andDepartmentofOncology,Johns HopkinsUniversitySchoolofMedicine,Baltimore,Maryland,USA KaelynD.Sumigray DepartmentofDermatology,andDepartmentofCellBiology,DukeUniversityMedical Center,Durham,NorthCarolina,USA YoshimiTakai DivisionofPathogeneticSignaling,KobeUniversityGraduateSchoolofMedicine,and CREST,JapanScienceandTechnologyAgency,Kobe,Japan MelanieD.White EuropeanMolecularBiologyLaboratory(EMBL)Australia,AustralianRegenerative MedicineInstitute,MonashUniversity,Clayton,Victoria,Australia AlphaS.Yap DivisionofCellBiologyandMolecularMedicine,InstituteforMolecularBioscience, TheUniversityofQueensland,Brisbane,Queensland,Australia PREFACE Cell adhesion is a fundamental determinant of development in metazoan organisms.Foroveracentury—fromtheearlyobservationsofHVWilson, throughtheseminalstudiesofTownesandHoltfreter,andsince—wehave endeavoredtounderstandhowadhesionhelpsmakemulticellularorganisms morethan justthesum oftheir parts.Wenow knowthatphysical interac- tions between cells and their environment (other cells and components of the extracellular matrix) influence critical parameters of development, includingtissuecohesion,cellularpatterning,differentiation,andpopulation control.Thesediversefunctionaleffectsreflectthecomplexwaysinwhich distinct adhesion systems interact with cellular processes such as signaling, thecytoskeleton,andmembranetrafficking.Inthisvolume,weaimtosur- vey recent developments in understanding how the cellular and molecular mechanismsofadhesiondeterminethedevelopmentoforganismsandtheir constituent organs. The early chapters in this volume endeavor to define some of the key processes that allow adhesion to influence development. Melanie White andNicolasPlachtareviewhowadhesioncooperateswiththecytoskeleton to drive the earliest cellular events in the preimplantation mouse embryo: compaction, change in cell shape, polarity, and cell fate. Franc¸ois Fagotto thenaddressesoneofthelong-standingproblemsindevelopmentalbiology: understanding how boundaries are formed in the embryo. Building on the long-standing realization that boundaries reflect physical differences betweenpopulationsofcells,Fagottooutlineshowdifferentcell–celladhe- sion systems may cooperate with the cytoskeleton to segregate cell populations at boundaries. Wethenhaveaseriesofchaptersthatfocusonthemechanismsbywhich cadherin cell adhesion molecules influence animal development. Here, a majoradvancehascomefromtherealizationthatcadherinscooperatewith thecontractileapparatus,thatis,theactomyosincytoskeleton.Accordingly, RashmiPriyaandAlphaYapdiscussthemolecularandcellularmechanisms that allow cadherin adhesion systems to physically interact with, and also regulate, the actomyosin cytoskeleton. Katja Ro€per then addresses how cooperation between cell–cell adhesion and contractility determines mor- phogenesisintheearlyDrosophilaembryo.Intheirchapter,PierreMcCrea, Meghan Maher, and Cara Gottardi broaden the discussion to review how xv xvi Preface cadherinsandtheirassociatedproteinssignaltothenucleus,aparadigmthat underlies canonical Wnt signaling and also impinges on other fundamental developmental pathways, such as the Hippo signaling pathway. Of course, cadherins are not the only adhesion systems that influence development. Another large family of cell–cell adhesion molecules are thenectinsandnectin-likeproteins.KenjiMandai,YoshimiTakai,andtheir colleagues discuss the fundamental cell biology of nectins and review how thesemoleculesaffectthedevelopmentofmanyorgansinthebody.Aidan MaartensandNicholasBrownthenoutlinedevelopmentsinunderstanding howintegrincell–matrixadhesionmoleculescontributetoDrosophiladevel- opment, including notable developments in how integrins influence cell fate, cell migration, and cell polarity. The two subsequent chapters focus on developmental processes that integrateadhesion,signaling,andthecytoskeleton.PierreSavagnerdiscusses the concept of epithelial-to-mesenchymal transition, providing a historical and conceptual framework for this complex phenomenon, with its often controversialmechanisticunderpinnings.EliasBarrigaandRobertoMayor then take the example of neural crest migration to consider how adhesive events generate collective patterns of cell migration. Finally, we examine how cell adhesion influences the development of individual organs. Anne Lagendijk and Benjamin Hogan review how cell signaling and cell–cell adhesion cooperate during vascular development. EliahShamirandAndrewEwaldfocusonhowindividualandcollectivecell migrationareregulatedbycell–celladhesiontodriveepithelialmorphogen- esisofthemammarygland.KaelynSumigrayandTerryLechlerreviewhow multiple junctions (adherens, tight, and desmosomes) contribute to devel- opment of the epidermis as a fundamental biological barrier in the body. Lauren Friedman, Deanna Benson, and George Huntley consider the role thatcadherinsplayinthenervoussystem,withaparticularfocusonunder- standing their role in synapse formation and the generation of synaptic networks, the bases of neural activity. And in the final chapter of this vol- ume,AlexanderCombes, JamieDavies,and Melissa Littlediscuss howcell adhesion drives self-organization in the embryonic kidney, providing insights relevant to tissue engineering and regenerative medicine. Wehopethatthecontributionsinthisvolumeillustratesomeofthedif- ferentperspectivesthatarenowbeingusedtounderstandhowcelladhesion contributes to development. A final perspective lies in the relationship between development and disease. Many of the cellular mechanisms and biological processes that we consider are also implicated in disease. Thus, Preface xvii we also sought, where possible, to highlight how basic biology illuminates ourunderstandingofdiseaseandviceversa.Wehopethatthesereviewswill then be a useful guide to students of fundamental biology and pathology. Andwewillbewellpleasediftheypromptfurtherresearchattheinterface between these disciplines. ALPHA S. YAP CHAPTER ONE How Adhesion Forms the Early Mammalian Embryo Melanie D. White, Nicolas Plachta1 EuropeanMolecularBiologyLaboratory(EMBL)Australia,AustralianRegenerativeMedicineInstitute, MonashUniversity,Clayton,Victoria,Australia 1Correspondingauthor:e-mailaddress:[email protected] Contents 1. TheMousePreimplantationEmbryoasaModelofAdhesioninMammalian Development 1 1.1 Adhesionmoleculesinthepreimplantationmouseembryo 3 2. AdhesionRegulatesCellShape 5 3. AdhesionControlsCellPolarity 7 4. AdhesionDeterminesCellFate 7 5. EmergingTechnologiestoStudyAdhesion 9 6. QuestionsfortheFuture 11 References 13 Abstract Theearlymouseembryoisanexcellentsystemtostudyhowasmallgroupofinitially rounded cells start to change shape and establish the first forms of adhesion-based cell–cellinteractionsinmammalsinvivo.Inadditiontoitscriticalroleinthestructural integrityoftheembryo,wediscussherehowadhesionisimportanttoregulatecellpolar- ityandcellfate.Recentevidencesuggeststhatadherensjunctionsparticipateinsignaling pathwaysbylocalizingkeyproteinstosubcellularmicrodomains.E-cadherinhasbeen identifiedasthemainplayerrequiredfortheestablishmentofadhesionbutothermech- anismsinvolvingadditionalproteinsorphysicalforcesactingintheembryomayalsocon- tribute. Application of new technologies that enable high-resolution quantitative imagingofadhesionproteindynamicsandmeasurementsofbiomechanicalforceswill provideagreaterunderstandingofhowadhesionpatternstheearlymammalianembryo. 1. THE MOUSE PREIMPLANTATION EMBRYO AS A MODEL OF ADHESION IN MAMMALIAN DEVELOPMENT Mostresearchon adhesionhasbeen performedoncells intissuecul- ture due to their availability and ease of manipulation. However, it is only CurrentTopicsinDevelopmentalBiology,Volume112 #2015ElsevierInc. 1 ISSN0070-2153 Allrightsreserved. http://dx.doi.org/10.1016/bs.ctdb.2014.11.022 2 MelanieD.WhiteandNicolasPlachta duringtruecellulardifferentiationwithinanembryothatthecontributionof adhesiontodevelopmentcanbeexamineddirectly.Themousepreimplan- tation embryo provides an ideal system to study adhesion mechanisms that are based exclusively on cell–cell interactions. A glycoprotein membrane, thezonapellucida,enclosesthepreimplantationembryosocell–celladhesion can bestudiedin thecomplete absenceof extracellular matrix interactions. Preimplantationdevelopmentnaturallyoccurswithintheoviduct,butit can be recapitulated in vitro without adversely affecting the developmental potential of embryos (Summers & Biggers, 2003). Mouse embryos can be easily removed from the maternal oviducts and cultured in simple media conditions. Under these ex utero conditions, the embryos develop almost as rapidly as they do in utero and if transferred back to the uterus they can implant and continue developing to produce viable offspring. During the first 2 days of development, the fertilized mouse egg undergoes three cleavage divisions to produce an 8-cell embryo (Fig. 1A). At this stage, the cells are round and visibly indistinguishable. The first major cell morphological changes begin as the 8-cell embryo undergoes compaction. Concomitant with a rise in intercellular adhesion, the cells flatten their membranes against each other, maximizing contact and forming a highly packed mass. This process of increased adhesion and embryo compaction occurs ubiquitously during preimplantation Figure 1 Imaging preimplantation development in the mouse embryo. (A) DIC images showing development of mouse embryo from 1-cell to blastocyst stage. (B)MicroinjectionofmRNAorDNAintothepronucleusallowsvisualizationofproteins ofinterestthroughoutpreimplantationdevelopment.Intheexampleshown,themem- braneislabeledwithmCherryandthenucleusislabeledwithH2B-GFP.ICM,innercell mass;TE,trophectoderm.
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