[PDF] Molecular mechanisms of cell polarity in a range of model systems

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Molecular andCellular Neuroscience

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Molecular mechanismsof cellpolarity ina rangeof modelsystems andin migrating neurons

Yves Jossin

Laboratory ofMammalian Development& CellBiology, Instituteof Neuroscience,Université Catholiquede Louvain,Brussels, Belgium

ARTICLE INFO

Keywords:

Development ofthe cerebralcortex

Cell polarity

Cell migration

Neuronal migration

Radial migration

Tangential migration

Polarity complexes

Actin cytoskeleton

Microtubule cytoskeleton

Rho familyGTPases

PI3K signalingABSTRACT

Cell polarityis definedas theasymmetric distributionof cellularcomponents alongan axis.Most cells,from the

simplest single-cellorganisms tohighly specializedmammalian cells,are polarizedand usesimilar mechanisms

to generateand maintainpolarity. Cellpolarity isimportant forcells tomigrate, formtissues, andcoordinate

activities. Duringdevelopment ofthe mammaliancerebral cortex,cell polarityis essentialfor neurogenesisand

for themigration ofnewborn butas-yet undifferentiatedneurons. Theseoriented migrationsinclude boththe

radial migrationof excitatoryprojection neuronsand thetangential migrationof inhibitoryinterneurons. Inthis

review, Iwill firstdescribe thedevelopment ofthe cerebralcortex, asrevealed atthe cellularlevel. Iwill then

define thecore molecularmechanisms -the Par/Crb/Scribpolarity complexes,small GTPases,the actinand

microtubule cytoskeletons,and phosphoinositides/PI3Kcsignaling -that arerequired forasymmetric celldivi-

sion, apico-basaland front-rearpolarity inmodel systems,including C eleganszygote,Drosophilaembryos and

cultured mammaliancells. AsI gothrough eachcore mechanismI willexplain whatis knownabout itsim- portance inradial andtangential migrationin thedeveloping mammaliancerebral cortex.1. Introduction Most animalcells arepolarized, withanisotropic distributionof membrane components,internal cytoskeletalstructures, organellesand signaling machinery.Polarity isessential forunicellular animalsto migrate andfind prey,and forindividual cellsin multicellularanimals to formtissues andcoordinate theiractivities. Differentiatedmature neurons arecommonly citedas anexample ofhighly polarizedmam- malian cells.However, beforereaching thisfinal asymmetricstate, immature neuronsundergo asuccession ofpolarized events.For in- stance, cellpolarity playsa crucialrole duringthe developmentof the cerebral cortexthat goesfrom athin neuroepithelialsheet toa complex structure withlayers composedof differenttypes ofneurons andglia

Kon etal., 2017

). Duringthis process,asymmetric divisionof neural stem cellsis importantto determinethe fateof thedaughter cellsby imposing adifferential inheritanceof fatedeterminants thatare asymmetrically distributedin thedividing mothercell. Theneuroe- pithelium exhibitsan apico-basalpolarity typicalof epitheliawith ad- hesive junctionsthat bindthe cellstogether andseparate theapical surface fromthe basolateraldomain. Afterthe lastcell division,new- born undifferentiatedneurons migrateaway fromtheir placeof birthto settle downin adistant area.During theiroriented migration,neurons

maintain afront-rear polarity.One prominentfeature isthe presenceof a longleading processfacing towardsthe directionof migration.This

process containsthe centrosome,working asthe microtubule-orga- nizing center(MTOC), andthe Golgiapparatus. Finally,mature neurons display axon-dendritepolarity withan axonat oneside ofthe celland neurites atthe otherside. Theapico-basal polarityof corticalneural stem cellsand theaxon-dendrite polarityof matureneurons donot change overtime. Onthe otherhand, thefront-rear polarityof mi- grating neuronsis dynamicand reactsto diversesignals fromthe en- vironment alongthe cell"spath. Currenttechniques allowscientists to investigate indetails thesecells. Neuronaloriented migrationcan be studied ina simplifiedcontrolled in vitroenvironment orin anin vivo- like organotypictissue cultureand recordedusing timelapse video- microscopy. Neuronalmigration andpositioning arecrucial forthe establishment offunctional neuralcircuitry. Notsurprisingly, defectsin establishing andmaintaining acorrect orientedneuronal migrationhas deleterious effectson theformation ofthe cerebralcortex andare as- sociated withhuman developmentalbrain disorders. Here wewill mainlyfocus onneuronal migrationand morespeci- fically theradial migrationof excitatoryneurons andthe tangential migration ofinhibitory interneurons.Fully differentiatedfunctional cortical neuronsare bornin agerminal zonelocated ata distancefrom their finaladult position.Intracellular molecularmechanisms comeinto

play tomake sureimmature neuronsgain andsustain acell polarity,https://doi.org/10.1016/j.mcn.2020.103503

Received 6February 2020;Received inrevised form20 April2020; Accepted23 May2020

E-mail address:yves.jossin@uclouvain.bec.

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