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In Early Development of the Rat Mrna for the Major Myelin Protein

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In Early Development of the Rat Mrna for the Major Myelin Protein DEVELOPMENTALDYNAMICS222:40–51(2001) InEarlyDevelopmentoftheRatmRNAfortheMajor MyelinProteinP0 IsExpressedinNonsensoryAreasof theEmbryonicInnerEar,Notochord,EntericNervous System,andOlfactoryEnsheathingCells MENG-JENLEE,1 ESTERCALLE,1 ANGELABRENNAN,1 SABRINAAHMED,1 ELENASVIDERSKAYA,2 1 1 KRISTJANR.JESSEN, ANDRHONAMIRSKY * 1DepartmentofAnatomyandDevelopmentalBiology,UniversityCollegeLondon,London,UnitedKingdom 2DepartmentofAnatomy,StGeorge’sHospitalMedicalSchool,London,UnitedKingdom ABSTRACT ThemyelinproteinP0 hasama- INTRODUCTION jorstructuralroleinSchwanncellmyelin,andthe TheP0 geneandthemechanismsthatcontrolithave expressionofP0 proteinandmRNAinthe beenofgreatinteresteversinceitwasrealizedthatP0 Schwanncelllineagehasbeenextensivelydocu- proteinwasbyfarthemostabundantproteinofmyelin mented.Weshowhere,usinginsituhybridization, inthePNS,andthatitsexpressionwassubjectto thattheP0 geneisalsoactivatedinanumberof dramaticregulationbysignalsfromneurons(Gieseet othertissuesduringembryonicdevelopment.P0 al.,1992;LemkeandAxel,1985;SommerandSuter, mRNAisfirstdetectablein10-day-oldembryos 1998).Inmammals,P0 appearedinitiallytobean (E10)andisatthistimeseenonlyincellsinthe exampleparexcellenceofacelltypespecificgene, cephalicneuralcrestandintheoticplacode/pit.P0 beingrestrictedtothoseSchwanncellsinducedtoform expressioncontinuesintheoticvesicleandatE12 myelinsheaths(Colmanetal.,2001).Ithasnowbe- P0 expressioninthisstructurelargelyoverlaps comeclearthattheP0 geneisactivated,albeitatrel- withexpressionofanothermyelingene,proteo- ativelylowlevels,priortomyelinationnotonlyinall lipidprotein.InthedevelopingearatE14,P0 ex- immatureSchwanncellsbutalsoinSchwanncellpre- pressioniscomplementarytoexpressionofserrate cursors(Burronietal.,1988;ChengandMudge,1996; andc-retmRNAs,whichlaterareexpressedinsen- Leeetal.,1997;MirskyandJessen,2001;Zhangetal., soryareasoftheinnerear,whileexpressionof 1995).P0 isalsoseenevenearlierinasubpopulationof bonemorphogeneticprotein(BMP)-4andP0, cellsinthetrunkneuralcrest,thetissuethatgivesrise thoughlargelycomplementary,showssmallareas toSchwanncellprecursors,whereitssignificancehas ofoverlap.P0 mRNAandproteinaredetectablein becomecontroversial(Bhattacharyyaetal.,1991; thenotochordfromE10toatleastE13.Inaddition Hagedornetal.,1999;Leeetal.,1997).Furthermore, thereissomeevidencefromimmunochemicalandim- toP0 expressioninasubpopulationoftrunkcrest cellsatE11/E12andinSchwanncellprecursors munohistochemicalstudiesthatP0 proteinisseenin populationsofneuronsintheCNS(Satoetal.,1999; thereafter,P0 mRNAisalsopresenttransiently inasubpopulationofcellsmigratingintheen- SatoandEndo,2000),andtransgenicmicegenerated tericneuralcrestpathway,butisdown-regu- withareportergenedrivenbya1.1-kbstretchofreg- ulatorysequencefromtheP0 geneshowtransgene latedinthesecellsatE14andthereafter.P0 is alsodetectedintheplacode-derivedolfactoryen- expressioninnumerousplacesincludingsomeperiph- sheathingcellsfromE13andismaintainedinthe eralneurons(Yamauchietal.,1999).Thus,ourpicture adult.Nosignalisseenincellsinthemelanocyte ofP0 geneexpressionduringmammalianembryonic developmentischanging.Itwillcertainlyturnoutto migrationpathwayorinTUJ1positiveneuronal bemorecomplexthanoriginallyenvisagedandmuchis cellsintissuesections.TheactivationoftheP 0 stillunclearabouttissuesandtimingofgeneactiva- geneinspecifictissuesoutsidethenervoussys- tion,letaloneaboutwhatmightbethefunctionofP temwasunexpected.Itremainstobedetermined 0 outsidethemyelinsheath.Withtheaimofprovidinga whetherthisisfunctionallysignificant,or whetheritisanevolutionaryrelic,perhapsre- flectingancestraluseofP0 asanadhesionmole- Grantsponsor:WellcomeTrust;Grantnumber:042257/Z/94/Z; cule. ©2001Wiley-Liss,Inc. Grantsponsor:EuropeanCommission;Grantnumber:ERBFM- BICT98-3106. *Correspondenceto:R.Mirsky,DepartmentofAnatomyandDevel- Keywords:neuralcrest;Schwanncells;oticpit; opmentalBiology,UniversityCollegeLondon,GowerStreet,London WC1E6BT,UK.E-mail:[email protected] oticvesicle;glia;serrate;BMP-4;c- Received26March2001;Accepted14May2001 ret Publishedonline20July2001;DOI10.1002/dvdy.1165 ©2001WILEY-LISS,INC. P0 IN RAT PERIPHERAL GLIAL LINEAGE 41 more comprehensive view of P0 expression during and the vagal crest migrating into the gut to form the mammalian embryonic development, we have, in the enteric nervous system. In enteric cells, P0 mRNA ex- present work, monitored P0 mRNA expression during pression was strikingly transient, resembling, on a embryonic rat development using whole embryos, tis- shorter time scale, the transient expression of P0 sue sections, and dissected organs. mRNA in the development of nonmyelin-forming P0 comprises approximately 50% of the total protein Schwann cells (Lee et al., 1997). Moreover, in the in Schwann cell myelin in peripheral nerves where it oesophageal part of the gut P0 mRNA expression was plays a major stabilizing role, acting via homophilic first detected a day after the first appearance of the interactions (Colman et al., 2001). The levels of mRNA early neuronal marker ␤3-tubulin, a finding with clear expressed in Schwann cell precursors and immature implications for questions concerning the lineage sta- Schwann cells prior to myelination represent constitu- tus of P0-positive cells in the neural crest. P0 was not tive basal expression levels of P0 that are many times detected in the dorsolateral crest melanocyte migration lower than the peak levels of P0 mRNA seen in those pathway, nor was it found in crest cells in the jaw Schwann cells that are induced to myelinate large di- region. These findings indicate that P0 expression is ameter axons (Lee et al., 1997; Trapp et al., 1988). low or absent from non-neural cells of the crest lineage. Conversely, in those cells that develop to form mature Lastly, in contrast to the general finding in the rat that non-myelinating Schwann cells, the basal P0 levels are basal P0 expression is down-regulated in mature non- down-regulated. This divergent regulation of basal P0 myelin-forming glia (Lee et al., 1997), we found that levels is reversible: if Schwann cells lose contact with olfactory ensheathing cells, which start expressing P0 axons, P0 levels in myelinating and nonmyelinating at E13, continue to do so in the adult. This is of interest cells fall and rise, respectively, as the cells de-differen- because P0 protein promotes axonal growth in vitro and tiate. Thus, denervated adult Schwann cells express olfactory ensheathing cells uniquely associate with ax- basal P0 mRNA levels comparable to those seen in ons that continue to regrow throughout life (Schneider- immature Schwann cells (Lee et al., 1997). Basal P0 Schaulies et al., 1990). mRNA levels in developing satellite cells in rat dorsal root ganglia (DRG) are also suppressed as these cells RESULTS mature (Lamperth et al., 1989; Lee et al., 1997). P0 at To determine the onset of P0 mRNA expression in the cell surface can take part in homophilic and het- embryogenesis, in situ hybridization using digoxygenin erophilic interactions with P0 and other adhesion mol- (DIG)-labelled mRNA probes was performed on whole ecules on the surface of neighbouring cells outside the mount preparations of rat embryos at E9–12. context of the myelin sheath, and in this way mediate cell–cell adhesion (Doyle et al., 1995; D’Urso et al., P0 Is First Detectable Within the Otic Vesicle 1990; Filbin et al., 1990; Schneider-Schaulies et al., and Developing Inner Ear 1990). While it is possible that basal P0 expression acts No signal was detectable at E9. At E10 (10 somite to promote cell adhesion, there is as yet no direct evi- stage), some cells in the otic placode/pit were strongly dence for this, and the significance of nonmyelin re- P0 positive, and by E11 intense expression of P0 was lated P0 expression in developing Schwann cells re- seen in most areas of the otic vesicle (Fig. 1A,B). By mains uncertain. E12 it was still widely expressed in the vesicle but Perhaps because of the highly restricted distribution showed a more variable distribution, being low in some of P0 to myelinated nerves in the adult, previous stud- areas, remaining extremely high in others, including ies did not pay much attention to whether P0 expres- the developing endolymphatic duct and the adjacent sion during development was limited to the peripheral dorsomedial area (Figs. 1C and 2A). To test whether nervous system (PNS). Even within the developing other myelin related genes might also be expressed in PNS, although it has been noted that P0 mRNA is the developing ear, we compared the expression of P0 expressed in a subpopulation of trunk neural crest with that of PLP/DM20, another myelin gene that has cells, P0 expression has not been examined in other been detected in glial cells early in development divisions of the rat neural crest and little is known (Spassky et al., 1998; Timsit et al., 1992). Using in situ about the relationship between P0 and other markers hybridization, PLP/DM20 labelling was clearly seen in of early crest differentiation. the otic vesicle at E11, and was, like P0 mRNA, located Since it would be useful to have a comprehensive mainly in the dorsal part of the vesicle (Fig. 2B). We picture of the expression pattern and developmental also examined the expression of a lacZ reporter con- regulation of this important gene, we have used in situ struct expressed under the control of PLP regulatory hybridization to detect P0 mRNA in the rat embryo sequences in a transgenic mouse line where labelling between E9 and birth. P0 gene activation was seen in has been reported in the otic vesicle at E10
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