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CURRENT TOPICS IN DEVELOPMENTAL BIOLOGY “Ameeting-groundforcriticalreviewanddiscussionofdevelopmentalprocesses” A.A.MosconaandAlbertoMonroy(Volume1,1966) SERIES EDITOR Paul M. Wassarman DepartmentofCell,DevelopmentalandRegenerativeBiology IcahnSchoolofMedicineatMountSinai NewYork,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 50HampshireStreet,5thFloor,Cambridge,MA02139,UnitedStates 525BStreet,Suite1650,SanDiego,CA92101,UnitedStates TheBoulevard,LangfordLane,Kidlington,OxfordOX51GB,UnitedKingdom 125LondonWall,London,EC2Y5AS,UnitedKingdom Firstedition2018 Copyright©2018ElsevierInc.Allrightsreserved. Nopartofthispublicationmaybereproducedortransmittedinanyformorbyanymeans, electronicormechanical,includingphotocopying,recording,oranyinformationstorageand retrievalsystem,withoutpermissioninwritingfromthepublisher.Detailsonhowtoseek permission,furtherinformationaboutthePublisher’spermissionspoliciesandour arrangementswithorganizationssuchastheCopyrightClearanceCenterandtheCopyright LicensingAgency,canbefoundatourwebsite:www.elsevier.com/permissions. Thisbookandtheindividualcontributionscontainedinitareprotectedundercopyrightby thePublisher(otherthanasmaybenotedherein). Notices Knowledgeandbestpracticeinthisfieldareconstantlychanging.Asnewresearchand experiencebroadenourunderstanding,changesinresearchmethods,professionalpractices, ormedicaltreatmentmaybecomenecessary. Practitionersandresearchersmustalwaysrelyontheirownexperienceandknowledgein evaluatingandusinganyinformation,methods,compounds,orexperimentsdescribed herein.Inusingsuchinformationormethodstheyshouldbemindfuloftheirownsafetyand thesafetyofothers,includingpartiesforwhomtheyhaveaprofessionalresponsibility. Tothefullestextentofthelaw,neitherthePublishernortheauthors,contributors,oreditors, assumeanyliabilityforanyinjuryand/ordamagetopersonsorpropertyasamatterof productsliability,negligenceorotherwise,orfromanyuseoroperationofanymethods, products,instructions,orideascontainedinthematerialherein. ISBN:978-0-12-809802-8 ISSN:0070-2153 ForinformationonallAcademicPresspublications visitourwebsiteathttps://www.elsevier.com/books-and-journals Publisher:ZoeKruze AcquisitionEditor:ZoeKruze EditorialProjectManager:ShellieBryant ProductionProjectManager:DennyMansingh CoverDesigner:GregHarris TypesetbySPiGlobal,India CONTRIBUTORS JosephineC.Adams SchoolofBiochemistry,UniversityofBristol,Bristol,UnitedKingdom MarcelBokhove DepartmentofBiosciencesandNutrition&CenterforInnovativeMedicine,Karolinska Institutet,Huddinge,Sweden DouglasW.DeSimone DepartmentofCellBiology,UniversityofVirginia,SchoolofMedicine,Charlottesville, VA,UnitedStates BetteJ.Dzamba DepartmentofCellBiology,UniversityofVirginia,SchoolofMedicine,Charlottesville, VA,UnitedStates StephenFrankenberg SchoolofBioSciences,UniversityofMelbourne,Parkville,VIC,Australia RichardJ.Goodyear SussexNeuroscience,SchoolofLifeSciences,UniversityofSussex,Brighton,United Kingdom SatishK.Gupta ReproductiveCellBiologyLaboratory,NationalInstituteofImmunology,NewDelhi, India DavidF.Holmes WellcomeTrustCentreforCell-MatrixResearch,FacultyofBiology,MedicineandHealth, ManchesterAcademicHealthScienceCentre,UniversityofManchester,Manchester, UnitedKingdom LucaJovine DepartmentofBiosciencesandNutrition&CenterforInnovativeMedicine,Karolinska Institutet,Huddinge,Sweden KarlE.Kadler WellcomeTrustCentreforCell-MatrixResearch,FacultyofBiology,MedicineandHealth, ManchesterAcademicHealthScienceCentre,UniversityofManchester,Manchester, UnitedKingdom EmilyE.Killingbeck DepartmentofGenomeSciences,UniversityofWashington,Seattle,WA,UnitedStates EvelineS.Litscher DepartmentofCell,Developmental,andRegenerativeBiology,IcahnSchoolofMedicineat MountSinai,NewYork,NY,UnitedStates YinhuiLu WellcomeTrustCentreforCell-MatrixResearch,FacultyofBiology,MedicineandHealth, ManchesterAcademicHealthScienceCentre,UniversityofManchester,Manchester, UnitedKingdom xi xii Contributors TsukasaMatsuda GraduateSchoolofBioagriculturalSciences,NagoyaUniversity,Nagoya,Japan RobertP.Mecham DepartmentofCellBiologyandPhysiology,WashingtonUniversitySchoolofMedicine, St.Louis,MO,UnitedStates JonathonM.Muncie CenterforBioengineeringandTissueRegeneration,UniversityofCalifornia;Graduate PrograminBioengineering,UniversityofCaliforniaSanFranciscoandUniversityof CaliforniaBerkeley,SanFrancisco,CA,UnitedStates ShunsukeNishio GraduateSchoolofBioagriculturalSciences,NagoyaUniversity,Nagoya,Japan HirokiOkumura FacultyofAgriculture,MeijoUniversity,Nagoya,Japan FrancescoRamirez DepartmentofPharmacologicalSciences,IcahnSchoolofMedicineatMountSinai, NewYork,NY,UnitedStates MarilynB.Renfree SchoolofBioSciences,UniversityofMelbourne,Parkville,VIC,Australia GuyP.Richardson SussexNeuroscience,SchoolofLifeSciences,UniversityofSussex,Brighton,United Kingdom ReiSekiguchi CellBiologySection,NationalInstituteofDentalandCraniofacialResearch,National InstitutesofHealth,Bethesda,MD,UnitedStates TobiasStarborg WellcomeTrustCentreforCell-MatrixResearch,FacultyofBiology,MedicineandHealth, ManchesterAcademicHealthScienceCentre,UniversityofManchester,Manchester, UnitedKingdom WillieJ.Swanson DepartmentofGenomeSciences,UniversityofWashington,Seattle,WA,UnitedStates PaulM.Wassarman DepartmentofCell,Developmental,andRegenerativeBiology,IcahnSchoolofMedicineat MountSinai,NewYork,NY,UnitedStates ValerieM.Weaver CenterforBioengineeringandTissueRegeneration;EliandEdytheBroadCenterof RegenerationMedicineandStemCellResearch,TheHelenDillerFamilyComprehensive CancerCenter,UniversityofCalifornia,SanFrancisco,CA,UnitedStates KennethM.Yamada CellBiologySection,NationalInstituteofDentalandCraniofacialResearch,National InstitutesofHealth,Bethesda,MD,UnitedStates PREFACE This volume of CTDB consists of 14 chapters, 7 on extracellular matrix (ECM)and7ontheegg’szonapellucida(ZP)contributedbyleadinginves- tigators in Australia, India, Japan, Sweden, the United Kingdom, and the United States. Research on ECM has a long andextensivehistory withnearly 100,000 primary papers and 20,000 reviews published on the subject during the past 70yearsorso(PubMed).ECMisacollectionofdiversemolecules,including proteins(e.g.,collagens,fibronectins,andlaminins),proteoglycans(e.g.,hep- arin, keratin, andchondroitin sulfates), and polysaccharides (e.g., hyaluronic acid),thatresideoutsideanimalcells.ECMservesmanyroles,suchasprovid- ing structural support for cells, tissues, and organs, and regulating numerous events, including gene expression, differentiation, morphogenesis, cellular adhesion, cellular migration, and intercellular communication. Similarly, nearly all animal eggs are surrounded by a unique, specialized ECM, called the ZP, that provides both structural support for eggs and follicle cells sur- rounding them and species-restricted receptors for binding of sperm during fertilization. InthisvolumeofCTDBcoverageofECMincludesthefollowingseven chapters: (Chapter 1) How the ECM functions as a highly complex entity that regulates tissue organization and cell behavior through dialogue with cellular constituents of tissues (J.M. Muncie and V.M. Weaver); (Chapter 2)Researchon matricellular proteinsof ECMinnonmammalian animals that provide access to early stages of embryonic development and limbandorganregeneration(J.C.Adams);(Chapter3)Mechanismsunder- lyingthegenerationofacollagenfibrilnetworkofdefinedarchitectureand mechanicalproperties(D.F.Holmes,Y.Lu,T.Starborg,andK.E.Kadler); (Chapter 4) Developmental and disease dynamics of basement membranes of nematodes, flies, and vertebrates (R. Sekiguchi and K.M. Yamada); (Chapter 5) How ECM composition and physical properties influence cell fate decisions associated with vascular tissue development and disease (R.P. Mecham and F. Ramirez); (Chapter 6) The structure, function, and development of the tectorial membrane and major events during its evolution(R.J.GoodyearandG.P.Richardson);(Chapter7)Howbiophys- ical features of ECM, such as stiffness and viscoelasticity, influence the sculpting of embryonic tissues and regulation of cell fates (B.J. Dzamba and D.W. DeSimone). xiii xiv Preface In this volume of CTDB coverage of the ZP includes the following seven chapters: Various aspects of the egg’s ZP in fish (Chapter 8, E.S. Litscher and P.M. Wassarman), birds (Chapter 9, S. Nishio, H. Okumura, and T. Matsuda), mice (Chapter 10, P.M. Wassarman and E.S. Litscher), marsupials and monotremes (Chapter 11, S. Frankenberg and M. Renfree), and human beings (Chapter 12, S.K. Gupta); (Chapter 13) The atomic structures of ZP module proteins of mammals and nonmammals in the context of sperm–egg interactions (M. Bokhove and L. Jovine); (Chapter 14) The structure and function of metazoan egg coatproteinswithemphasisonthepotentialroletheirevolutionhasplayed in creation and maintenance of species boundaries (E.E. Killingbeck and W.J. Swanson). WeareverygratefultoRichardGoodyearandGuyRichardsonforpro- viding a beautiful and relevant image for the cover of the volume. Finally, we thank all of the authors for their scholarly contributions to this volume and for their considerable efforts to complete their manuscripts on time in order to meet publisher’s deadlines. EVELINE S. LITSCHER PAUL M. WASSARMAN CHAPTER ONE The Physical and Biochemical Properties of the Extracellular Matrix Regulate Cell Fate Jonathon M. Muncie*,†, Valerie M. Weaver*,‡,1 *CenterforBioengineeringandTissueRegeneration,UniversityofCalifornia,SanFrancisco,CA, UnitedStates †GraduatePrograminBioengineering,UniversityofCaliforniaSanFranciscoandUniversityofCalifornia Berkeley,SanFrancisco,CA,UnitedStates ‡EliandEdytheBroadCenterofRegenerationMedicineandStemCellResearch,TheHelenDillerFamily ComprehensiveCancerCenter,UniversityofCalifornia,SanFrancisco,CA,UnitedStates 1Correspondingauthor:e-mailaddress:[email protected] Contents 1. Introduction 2 2. ECMComposition 4 2.1 Collagens 4 2.2 Proteoglycans 5 2.3 Glycoproteins 5 2.4 Elastin 6 2.5 TheDynamicNatureoftheECM 7 3. ECMRegulatesDevelopmentandModulatesStemCellFate 8 3.1 TheECMRegulatesDevelopment 8 3.2 ECM-DirectedCellMigrationinDevelopment 9 3.3 ECMasaCriticalComponentoftheStemCellNiche 10 4. Cell–ECMSignaling 10 4.1 ECM–IntegrinBinding 11 4.2 NonintegrinReceptors 12 5. ECM-DependentModulationofGrowthFactorandMorphogenFunction 13 5.1 ECM-TransformingGrowthFactorBetaSuperfamilyInteractions 13 5.2 ECM–GrowthFactorCollaboration 14 6. ECM-DependentSpatial–MechanicalRegulationofCellPhenotype 15 6.1 ControlofCellShape 15 6.2 ECMStiffnessandCellFate 17 6.3 ECMStiffnessModulatesMorphogenActivity 19 6.4 ECMStiffnessModulatesCellBehaviorbyRegulatingMechanosensitive IonChannels 19 6.5 ECMStiffnessModulatesYes-AssociatedProteinandTranscriptional CoactivatorWithPDZ-BindingMotif 20 CurrentTopicsinDevelopmentalBiology,Volume130 Copyright#2018ElsevierInc. 1 ISSN0070-2153 Allrightsreserved. https://doi.org/10.1016/bs.ctdb.2018.02.002 2 JonathonM.MuncieandValerieM.Weaver 7. SummaryandFutureDirections 21 Acknowledgments 24 References 24 Abstract The extracellular matrix is a complex network of hydrated macromolecular proteins andsugarsthat,inconcertwithboundsolublefactors,comprisetheacellularstromal microenvironment of tissues. Rather than merely providing structural information to cells, the extracellular matrix plays an instructive role in development and is critical forthemaintenanceoftissuehomeostasis.Inthischapter,wereviewthecomposition oftheextracellularmatrixandsummarizedataillustratingitsimportanceinembryogen- esis,tissue-specificdevelopment,andstemcelldifferentiation.Wediscusshowthebio- physical and biochemical properties of the extracellular matrix ligate specific transmembrane receptors to activate intracellular signaling that alter cell shape and cytoskeletaldynamicstomodulatecellgrowthandviability,anddirectcellmigration andcellfate.Wepresentexamplesdescribinghowtheextracellularmatrixfunctions as a highly complex physical and chemical entity that regulates tissue organization andcellbehaviorthroughadynamicandreciprocaldialoguewiththecellularconstit- uentsofthetissue.Wesuggestthattheextracellularmatrixnotonlytransmitscellular and tissue-level force to shape development and tune cellular activities that are key forcoordinatedtissuebehavior,butthatitisitselfremodeledsuchthatittemporally evolvestomaintaintheintegratedfunctionofthetissue.Accordingly,wearguethat perturbationsinextracellularmatrixcompositionandstructurecompromisekeydevel- opmentaleventsandtissuehomeostasis,andpromotedisease. 1. INTRODUCTION The extracellular matrix (ECM) is a complex network of proteins, polysaccharides, and water that comprise the acellular stromal microenvi- ronmentinalltissuesandorgans.Historically,theECMwasthoughttopro- videstructuralinformationrequiredtomaintainthephysicalintegrityofthe tissue.However,itisnowunderstoodthattheECMisabiologicallyactive component of all tissues that directs cell fate and influences tissue develop- ment and homeostasis (Fig. 1). As organisms develop, they continuously generate and reorganize their ECMtoprovidethenecessarystructuralframeworktosupportthegrowth and development of emerging tissues. The ECM in turn provides critical biochemicaland biophysical cues that guidecell fate, drive morphogenetic movements to sculpt the tissue, and induce tissue-specific differentiation. ECMandCellFate 3 Fig.1 Illustrationofthevariousphysicalandbiochemicalcuesintegratedbytheextra- cellularmatrix,whicharesimultaneouslysensedbycellsthroughparallelmechanisms andarecriticalfordeterminingcellfate,inducingtissue-specificdifferentiation,andpro- motingdevelopmentalmorphogenesis. The conceptof“dynamic reciprocity”which maintains thatthe evolving ECM dictates cell and tissue fate which feedback to modulate ECM composition and organization represents a critical concept in develop- mental biology (Bissell, Hall, & Parry, 1982; Paszek & Weaver, 2004). “Tensional homeostasis” incorporates the viscoelasticity of the ECM andcelltensionintothedynamicreciprocityparadigmtherebyproviding aunifiedworkinghypothesiswithwhichtounderstandhowtheevolving biochemical and biophysical properties of the ECM direct development and maintain tissue homeostasis. TheECMisalsoakeycomponentoftheadultstemcellnicheandrefers to the local microenvironment that sustains stem cell quiescence and facil- itates the maintenance of stem cells through regulated self-replication and retentionofmultipotency.TheECMphysicallybufferstemcellsthatreside withinthenichefromdifferentiationcuessequesterscriticalgrowthfactors and morphogens, and facilitates efficient nutrient exchange to sustain the long-term growth and survival and pluripotency of the stem cells.

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