Cell type-specific localization of Ephs pairing with ephrin-B2 in the rat postnatal pituitary gland

Sox2 -expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and dense cell clusters in the parenchyma. In relation to the mechanism of regulation of niches, juxtacrine signaling via ephrin and its receptor...

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Published inCell and tissue research Vol. 370; no. 1; pp. 99 - 112
Main Authors Yoshida, Saishu, Kato, Takako, Kanno, Naoko, Nishimura, Naoto, Nishihara, Hiroto, Horiguchi, Kotaro, Kato, Yukio
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer Berlin Heidelberg 01.10.2017
Springer
Springer Nature B.V
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Abstract Sox2 -expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and dense cell clusters in the parenchyma. In relation to the mechanism of regulation of niches, juxtacrine signaling via ephrin and its receptor Eph is known to play important roles in various niches. The ephrin and Eph families are divided into two subclasses to create ephrin/Eph signaling in co-operation with confined partners. Recently, we reported that ephrin-B2 localizes specifically to both pituitary niches. However, the Ephs interacting with ephrin-B2 in these pituitary niches have not yet been identified. Therefore, the present study aims to identify the Ephs interacting with ephrin-B2 and the cells that produce them in the rat pituitary gland. In situ hybridization and immunohistochemistry demonstrated cell type-specific localization of candidate interacting partners for ephrin-B2, including EphA4 in cells located in the posterior lobe, EphB1 in gonadotropes, EphB2 in corticotropes, EphB3 in stem/progenitor cells and EphB4 in endothelial cells in the adult pituitary gland. In particular, double-immunohistochemistry showed cis -interactions between EphB3 and ephrin-B2 in the apical cell membranes of stem/progenitor cell niches throughout life and trans -interactions between EphB2 produced by corticotropes and ephrin-B2 located in the basolateral cell membranes of stem/progenitor cells in the early postnatal pituitary gland. These data indicate that ephrin-B2 plays a role in pituitary stem/progenitor cell niches by selective interaction with EphB3 in cis and EphB2 in trans .
AbstractList Sox2-expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and dense cell clusters in the parenchyma. In relation to the mechanism of regulation of niches, juxtacrine signaling via ephrin and its receptor Eph is known to play important roles in various niches. The ephrin and Eph families are divided into two subclasses to create ephrin/Eph signaling in co-operation with confined partners. Recently, we reported that ephrin-B2 localizes specifically to both pituitary niches. However, the Ephs interacting with ephrin-B2 in these pituitary niches have not yet been identified. Therefore, the present study aims to identify the Ephs interacting with ephrin-B2 and the cells that produce them in the rat pituitary gland. In situ hybridization and immunohistochemistry demonstrated cell type-specific localization of candidate interacting partners for ephrin-B2, including EphA4 in cells located in the posterior lobe, EphB1 in gonadotropes, EphB2 in corticotropes, EphB3 in stem/progenitor cells and EphB4 in endothelial cells in the adult pituitary gland. In particular, double-immunohistochemistry showed cis-interactions between EphB3 and ephrin-B2 in the apical cell membranes of stem/progenitor cell niches throughout life and trans-interactions between EphB2 produced by corticotropes and ephrin-B2 located in the basolateral cell membranes of stem/progenitor cells in the early postnatal pituitary gland. These data indicate that ephrin-B2 plays a role in pituitary stem/progenitor cell niches by selective interaction with EphB3 in cis and EphB2 in trans.
Sox2-expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and dense cell clusters in the parenchyma. In relation to the mechanism of regulation of niches, juxtacrine signaling via ephrin and its receptor Eph is known to play important roles in various niches. The ephrin and Eph families are divided into two subclasses to create ephrin/Eph signaling in co-operation with confined partners. Recently, we reported that ephrin-B2 localizes specifically to both pituitary niches. However, the Ephs interacting with ephrin-B2 in these pituitary niches have not yet been identified. Therefore, the present study aims to identify the Ephs interacting with ephrin-B2 and the cells that produce them in the rat pituitary gland. In situ hybridization and immunohistochemistry demonstrated cell type-specific localization of candidate interacting partners for ephrin-B2, including EphA4 in cells located in the posterior lobe, EphB1 in gonadotropes, EphB2 in corticotropes, EphB3 in stem/progenitor cells and EphB4 in endothelial cells in the adult pituitary gland. In particular, double-immunohistochemistry showed cis-interactions between EphB3 and ephrin-B2 in the apical cell membranes of stem/progenitor cell niches throughout life and trans-interactions between EphB2 produced by corticotropes and ephrin-B2 located in the basolateral cell membranes of stem/progenitor cells in the early postnatal pituitary gland. These data indicate that ephrin-B2 plays a role in pituitary stem/progenitor cell niches by selective interaction with EphB3 in cis and EphB2 in trans.Sox2-expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and dense cell clusters in the parenchyma. In relation to the mechanism of regulation of niches, juxtacrine signaling via ephrin and its receptor Eph is known to play important roles in various niches. The ephrin and Eph families are divided into two subclasses to create ephrin/Eph signaling in co-operation with confined partners. Recently, we reported that ephrin-B2 localizes specifically to both pituitary niches. However, the Ephs interacting with ephrin-B2 in these pituitary niches have not yet been identified. Therefore, the present study aims to identify the Ephs interacting with ephrin-B2 and the cells that produce them in the rat pituitary gland. In situ hybridization and immunohistochemistry demonstrated cell type-specific localization of candidate interacting partners for ephrin-B2, including EphA4 in cells located in the posterior lobe, EphB1 in gonadotropes, EphB2 in corticotropes, EphB3 in stem/progenitor cells and EphB4 in endothelial cells in the adult pituitary gland. In particular, double-immunohistochemistry showed cis-interactions between EphB3 and ephrin-B2 in the apical cell membranes of stem/progenitor cell niches throughout life and trans-interactions between EphB2 produced by corticotropes and ephrin-B2 located in the basolateral cell membranes of stem/progenitor cells in the early postnatal pituitary gland. These data indicate that ephrin-B2 plays a role in pituitary stem/progenitor cell niches by selective interaction with EphB3 in cis and EphB2 in trans.
Sox2 -expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and dense cell clusters in the parenchyma. In relation to the mechanism of regulation of niches, juxtacrine signaling via ephrin and its receptor Eph is known to play important roles in various niches. The ephrin and Eph families are divided into two subclasses to create ephrin/Eph signaling in co-operation with confined partners. Recently, we reported that ephrin-B2 localizes specifically to both pituitary niches. However, the Ephs interacting with ephrin-B2 in these pituitary niches have not yet been identified. Therefore, the present study aims to identify the Ephs interacting with ephrin-B2 and the cells that produce them in the rat pituitary gland. In situ hybridization and immunohistochemistry demonstrated cell type-specific localization of candidate interacting partners for ephrin-B2, including EphA4 in cells located in the posterior lobe, EphB1 in gonadotropes, EphB2 in corticotropes, EphB3 in stem/progenitor cells and EphB4 in endothelial cells in the adult pituitary gland. In particular, double-immunohistochemistry showed cis -interactions between EphB3 and ephrin-B2 in the apical cell membranes of stem/progenitor cell niches throughout life and trans -interactions between EphB2 produced by corticotropes and ephrin-B2 located in the basolateral cell membranes of stem/progenitor cells in the early postnatal pituitary gland. These data indicate that ephrin-B2 plays a role in pituitary stem/progenitor cell niches by selective interaction with EphB3 in cis and EphB2 in trans .
Audience Academic
Author Kanno, Naoko
Kato, Yukio
Nishihara, Hiroto
Horiguchi, Kotaro
Nishimura, Naoto
Kato, Takako
Yoshida, Saishu
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  givenname: Saishu
  surname: Yoshida
  fullname: Yoshida, Saishu
  organization: Division of Life Science, Graduate School of Agriculture, Meiji University, Institute of Reproduction and Endocrinology, Meiji University
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  givenname: Takako
  surname: Kato
  fullname: Kato, Takako
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  surname: Kanno
  fullname: Kanno, Naoko
  organization: Division of Life Science, Graduate School of Agriculture, Meiji University
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  surname: Nishimura
  fullname: Nishimura, Naoto
  organization: Division of Life Science, Graduate School of Agriculture, Meiji University
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  givenname: Hiroto
  surname: Nishihara
  fullname: Nishihara, Hiroto
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  givenname: Yukio
  surname: Kato
  fullname: Kato, Yukio
  email: yukato@meiji.ac.jp
  organization: Division of Life Science, Graduate School of Agriculture, Meiji University, Institute of Reproduction and Endocrinology, Meiji University, Department of Life Science, School of Agriculture, Meiji University
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28660300$$D View this record in MEDLINE/PubMed
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Issue 1
Keywords Niche
Rat pituitary
Ephrin-B2
Stem/progenitor cells
EphB3
Language English
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PublicationCentury 2000
PublicationDate 20171000
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  year: 2017
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PublicationDecade 2010
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PublicationTitle Cell and tissue research
PublicationTitleAbbrev Cell Tissue Res
PublicationTitleAlternate Cell Tissue Res
PublicationYear 2017
Publisher Springer Berlin Heidelberg
Springer
Springer Nature B.V
Publisher_xml – name: Springer Berlin Heidelberg
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References KonstantinovaINikolovaGOhara-ImaizumiMMedaPKuceraTZarbalisKWurstWNagamatsuSLammertEEphA-Ephrin-A-mediated beta cell communication regulates insulin secretion from pancreatic isletsCell20071293593701:CAS:528:DC%2BD2sXlsVWls7k%3D10.1016/j.cell.2007.02.04417448994
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KrupkeOABurkeRDEph-Ephrin signaling and focal adhesion kinase regulate actomyosin-dependent apical constriction of ciliary band cellsDevelopment2014141107510841:CAS:528:DC%2BC2cXmtVGkt78%3D10.1242/dev.10012324550115
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HardingMJMcGrawHFNechiporukAThe roles and regulation of multicellular rosette structures during morphogenesisDevelopment2014141254925581:CAS:528:DC%2BC2cXht1GgurjK10.1242/dev.101444249617964067956
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ZhuXGleibermanASRosenfeldMGMolecular physiology of pituitary development: signaling and transcriptional networksPhysiol Rev2007879339631:CAS:528:DC%2BD2sXptFGls7c%3D10.1152/physrev.00006.200617615393
FauquierTRizzotiKDattaniMLovell-BadgeRRobinsonICSOX2-expressing progenitor cells generate all of the major cell types in the adult mouse pituitary glandProc Natl Acad Sci U S A2008105290729121:CAS:528:DC%2BD1cXjtVSisrs%3D10.1073/pnas.0707886105182870782268558
GremeauxLFuQChenJVankelecomHActivated phenotype of the pituitary stem/progenitor cell compartment during the early-postnatal maturation phase of the glandStem Cells Dev2012218018131:CAS:528:DC%2BC38Xjs1Clsb4%3D10.1089/scd.2011.049621970375
VankelecomHChenJPituitary stem cells: where do we stand?Mol Cell Endocrinol20143852171:CAS:528:DC%2BC3sXhsVylt7vO10.1016/j.mce.2013.08.01823994027
FujiwaraKDavaadashBKikuchiMTakigamiSYashiroTEstrogen suppresses retinaldehyde dehydrogenase 1 expression in the anterior pituitary glands of female ratsEndocr J20085591961:CAS:528:DC%2BD1cXmtFGqu74%3D10.1507/endocrj.K07-10118202528
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HafnerCMeyerSHagenIBeckerBRoeschALandthalerMVogtTEphrin-B reverse signaling induces expression of wound healing associated genes in IEC-6 intestinal epithelial cellsWorld J Gastroenterol200511451145181:CAS:528:DC%2BD2MXhtVensL3O10.3748/wjg.v11.i29.4511160526804398700
ChenJGremeauxLFuQLiekensDVan LaereSVankelecomHPituitary progenitor cells tracked down by side population dissectionStem Cells200927118211951:CAS:528:DC%2BD1MXnsF2rsb4%3D10.1002/stem.5119418455
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KatoHKuwakoKSuzukiMTanakaSGene expression patterns of pro-opiomelanocortin-processing enzymes PC1 and PC2 during postnatal development of rat corticotrophsJ Histochem Cytochem2004529439571:CAS:528:DC%2BD2cXls1alu7w%3D10.1369/jhc.4A6276.200415208361
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IshiiMNakajimaTOgawaKComplementary expression of EphB receptors and ephrin-B ligand in the pyloric and duodenal epithelium of adult miceHistochem Cell Biol20111363453561:CAS:528:DC%2BC3MXhtVGju7fJ10.1007/s00418-011-0849-421818578
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TanakaSKurosumiKA certain step of proteolytic processing of proopiomelanocortin occurs during the transition between two distinct stages of secretory granule maturation in rat anterior pituitary corticotrophsEndocrinology19921317797861:CAS:528:DyaK38Xls1Ciuro%3D1322282
MeyerSHafnerCGubaMFlegelSGeisslerEKBeckerBKoehlGEOrsoELandthalerMVogtTEphrin-B2 overexpression enhances integrin-mediated ECM-attachment and migration of B16 melanoma cellsInt J Oncol200527119712061:CAS:528:DC%2BD2MXht1amtrjK16211213
ZagliaTDi BonaAChioatoTBassoCAusoniSMongilloMOptimized protocol for immunostaining of experimental GFP-expressing and human heartsHistochem Cell Biol20161464074191:CAS:528:DC%2BC28XhtVSksb3M10.1007/s00418-016-1456-127311322
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YoshidaSNishimuraNUeharuHKannoNHiguchiMHoriguchiKKatoTKatoYIsolation of adult pituitary stem/progenitor cell clusters located in the parenchyma of the rat anterior lobeStem Cell Res2016173183291:CAS:528:DC%2BC28XhsV2jsr7N10.1016/j.scr.2016.08.01627596959
BatlleEHendersonJTBeghtelHvan den BornMMSanchoEHulsGMeeldijkJRobertsonJvan de WeteringMPawsonTCleversHBeta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinBCell20021112512631:CAS:528:DC%2BD38Xotlahsrk%3D10.1016/S0092-8674(02)01015-212408869
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RD Ward (2646_CR51) 2005; 19
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29143864 - Cell Tissue Res. 2017 Nov 16
References_xml – reference: DavisSWCastinettiFCarvalhoLREllsworthBSPotokMALyonsRHBrinkmeierMLRaetzmanLTCarninciPMortensenAHHayashizakiYArnholdIJMendoncaBBBrueTCamperSAMolecular mechanisms of pituitary organogenesis: in search of novel regulatory genesMol Cell Endocrinol20103234191:CAS:528:DC%2BC3cXmtFWrt7Y%3D10.1016/j.mce.2009.12.01220025935
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Snippet Sox2 -expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and...
Sox2-expressing stem/progenitor cells in the anterior lobe of the pituitary gland form two types of micro-environments (niches): the marginal cell layer and...
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SubjectTerms adults
Animals
Biomedical and Life Sciences
Biomedicine
Cell membranes
Endothelial cells
Endothelial Cells - cytology
Endothelial Cells - metabolism
EphA4 protein
Ephrin-B2 - analysis
Ephrin-B2 - metabolism
Human Genetics
Immunohistochemistry
in situ hybridization
Localization
Molecular Medicine
niches
Parenchyma
Pituitary (anterior)
Pituitary gland
Pituitary Gland - cytology
Pituitary Gland - growth & development
Pituitary Gland - metabolism
Pituitary Gland - ultrastructure
Pituitary hormones
Progenitor cells
Protein Interaction Maps
Proteomics
rats
Rats - growth & development
Rats - metabolism
Rats, Wistar
Receptor, EphB3 - analysis
Receptor, EphB3 - metabolism
Receptors, Eph Family - analysis
Receptors, Eph Family - metabolism
Regular Article
Rodents
Stem cells
Stem Cells - cytology
Stem Cells - metabolism
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Title Cell type-specific localization of Ephs pairing with ephrin-B2 in the rat postnatal pituitary gland
URI https://link.springer.com/article/10.1007/s00441-017-2646-4
https://www.ncbi.nlm.nih.gov/pubmed/28660300
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