Cellular adhesion in development and disease

520 Pages·2015·17.78 MB·English

by  Yap

CURRENT TOPICS IN
DEVELOPMENTAL BIOLOGY
“Ameeting-groundforcriticalreviewanddiscussionofdevelopmentalprocesses”
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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.