138
Views
1
CrossRef citations to date
0
Altmetric
Review

Emerging role for leucine-rich repeat-containing G-protein-coupled receptors LGR5 and LGR4 in cancer stem cells

, &
Pages 171-180 | Published online: 24 Mar 2014

References

  • QuintanaEShackletonMSabelMSFullenDRJohnsonTMMorrisonSJEfficient tumour formation by single human melanoma cellsNature2008456722259359819052619
  • RoeschAFukunaga-KalabisMSchmidtECA temporarily distinct subpopulation of slow-cycling melanoma cells is required for continuous tumor growthCell2010141458359420478252
  • ReyaTMorrisonSJClarkeMFWeissmanILStem cells, cancer, and cancer stem cellsNature2001414685910511111689955
  • LaksDRVisnyeiKKornblumHIBrain tumor stem cells as therapeutic targets in models of gliomaYonsei Med J201051563364020635435
  • AndersonARWeaverAMCummingsPTQuarantaVTumor morphology and phenotypic evolution driven by selective pressure from the microenvironmentCell2006127590591517129778
  • GreavesMMaleyCCClonal evolution in cancerNature2012481738130631322258609
  • LapidotTSirardCVormoorJA cell initiating human acute myeloid leukaemia after transplantation into SCID miceNature199436764646456487509044
  • HuntlyBJGillilandDGLeukaemia stem cells and the evolution of cancer-stem-cell researchNat Rev Cancer20055431132115803157
  • BonnetDDickJEHuman acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cellNat Med1997377307379212098
  • WangJCLapidotTCashmanJDHigh level engraftment of NOD/SCID mice by primitive normal and leukemic hematopoietic cells from patients with chronic myeloid leukemia in chronic phaseBlood1998917240624149516140
  • SirardCLapidotTVormoorJNormal and leukemic SCID-repopulating cells (SRC) coexist in the bone marrow and peripheral blood from CML patients in chronic phase, whereas leukemic SRC are detected in blast crisisBlood1996874153915488608245
  • HuffCAMatsuiWMultiple myeloma cancer stem cellsJ Clin Oncol200826172895290018539970
  • JonesRJGockeCDKasamonYLCirculating clonotypic B cells in classic Hodgkin lymphomaBlood2009113235920592619188663
  • VisvaderJELindemanGJCancer stem cells in solid tumours: accumulating evidence and unresolved questionsNat Rev Cancer200881075576818784658
  • KlonischTWiechecEHombach-KlonischSCancer stem cell markers in common cancers – therapeutic implicationsTrends Mol Med2008141045046018775674
  • KimJOrkinSEmbryonic stem cell-specific signatures in cancer: insights into genomic regulatory networks and implications for medicineGenome Med20113117522126538
  • DorsamRTGutkindJSG-protein-coupled receptors and cancerNat Rev Cancer200772799417251915
  • HsuSYLiangSGHsuehAJCharacterization of two LGR genes homologous to gonadotropin and thyrotropin receptors with extracellular leucine-rich repeats and a G protein-coupled, seven-transmembrane regionMol Endocrinol19981212183018459849958
  • de LauWBarkerNLowTYLGR5 homologues associate with Wnt receptors and mediate R-spondin signallingNature2011476736029329721727895
  • PengWCde LauWFornerisFStructure of stem cell growth factor R-spondin 1 in complex with the ectodomain of its receptor LGR5Cell Rep2013361885189223809763
  • BarkerNvan EsJHKuipersJIdentification of stem cells in small intestine and colon by marker gene LGR5Nature200744971651003100717934449
  • BakerMStem cells by any other nameNature2007449716138917898732
  • BarkerNHuchMKujalaPLGR5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitroCell Stem Cell201061253620085740
  • JaksVBarkerNKasperMLGR5 marks cycling, yet long-lived, hair follicle stem cellsNat Genet200840111291129918849992
  • BarkerNRookmaakerMBKujalaPLGR5(+ve) stem/progenitor cells contribute to nephron formation during kidney developmentCell Rep20122354055222999937
  • PlaksVBrenotALawsonDALGR5-expressing cells are sufficient and necessary for postnatal mammary gland organogenesisCell Rep201331707823352663
  • SatoTVriesRGSnippertHJSingle LGR5 stem cells build crypt-villus structures in vitro without a mesenchymal nicheNature2009459724426226519329995
  • SatoTvan EsJHSnippertHJPaneth cells constitute the niche for LGR5 stem cells in intestinal cryptsNature2011469733041541821113151
  • MendiveFLaurentPVan SchooreGSkarnesWPochetRVassartGDefective postnatal development of the male reproductive tract in LGR4 knockout miceDev Biol2006290242143416406039
  • KatoSMatsubaraMMatsuoTLeucine-rich repeat-containing G protein-coupled receptor-4 (LGR4, Gpr48) is essential for renal development in miceNephron Exp Nephrol20061042e63e7516785743
  • KatoSMohriYMatsuoTEye-open at birth phenotype with reduced keratinocyte motility in LGR4 null miceFEBS Lett2007581244685469017850793
  • SongHLuoJLuoWInactivation of G-protein-coupled receptor 48 (Gpr48/LGR4) impairs definitive erythropoiesis at midgestation through down-regulation of the ATF4 signaling pathwayJ Biol Chem200828352366873669718955481
  • MohriYKatoSUmezawaAOkuyamaRNishimoriKImpaired hair placode formation with reduced expression of hair follicle-related genes in mice lacking LGR4Dev Dyn200823782235224218651655
  • YamashitaRTakegawaYSakumotoMDefective development of the gall bladder and cystic duct in LGR4- hypomorphic miceDev Dyn20092384993100019301403
  • LuoJZhouWZhouXRegulation of bone formation and remodeling by G-protein-coupled receptor 48Development2009136162747275619605502
  • StyrkarsdottirUThorleifssonGSulemPNonsense mutation in the LGR4 gene is associated with several human diseases and other traitsNature2013497745051752023644456
  • MoritaHMazerbourgSBouleyDMNeonatal lethality of LGR5 null mice is associated with ankyloglossia and gastrointestinal distensionMol Cell Biol200424229736974315509778
  • BuczackiSJZecchiniHINicholsonAMIntestinal label-retaining cells are secretory precursors expressing LGR5Nature20134957439656923446353
  • SangiorgiECapecchiMRBmi1 is expressed in vivo in intestinal stem cellsNat Genet200840791592018536716
  • TianHBiehsBWarmingSA reserve stem cell population in small intestine renders LGR5-positive cells dispensableNature2011478736825525921927002
  • YamamotoYSakamotoMFujiiGOverexpression of orphan G-protein-coupled receptor, Gpr49, in human hepatocellular carcinomas with beta-catenin mutationsHepatology200337352853312601349
  • HuchMDorrellCBojSFIn vitro expansion of single LGR5+ liver stem cells induced by Wnt-driven regenerationNature2013494743624725023354049
  • ZhuLGibsonPCurrleDSProminin 1 marks intestinal stem cells that are susceptible to neoplastic transformationNature2009457722960360719092805
  • SnippertHJvan EsJHvan den BornMProminin-1/CD133 marks stem cells and early progenitors in mouse small intestineGastroenterology2009136721872194. e119324043
  • ShmelkovSVButlerJMHooperATCD133 expression is not restricted to stem cells, and both CD133+ and CD133− metastatic colon cancer cells initiate tumorsJ Clin Invest200811862111212018497886
  • MizrakDBrittanMAlisonMCD133: molecule of the momentJ Pathol200821413918067118
  • BarkerNRidgwayRAvan EsJHCrypt stem cells as the cells-of-origin of intestinal cancerNature2009457722960861119092804
  • WalkerFZhangHHOdorizziABurgessAWLGR5 is a negative regulator of tumourigenicity, antagonizes Wnt signalling and regulates cell adhesion in colorectal cancer cell linesPLoS One201167e2273321829496
  • AguileraCNakagawaKSanchoRChakrabortyAHendrichBBehrensAc-Jun N-terminal phosphorylation antagonises recruitment of the Mbd3/NuRD repressor complexNature2011469732923123521196933
  • Al-KharusiMRSmarttHJGreenhoughALGR5 promotes survival in human colorectal adenoma cells and is upregulated by PGE2: implications for targeting adenoma stem cells with NSAIDsCarcinogenesis20133451150115723349017
  • de SousaEMFColakSBuikhuisenJMethylation of cancer-stem-cell-associated Wnt target genes predicts poor prognosis in colorectal cancer patientsCell Stem Cell20119547648522056143
  • SanchoRNateriASde VinuesaAGJNK signalling modulates intestinal homeostasis and tumourigenesis in miceEmbo J200928131843185419521338
  • van der FlierLGvan GijnMEHatzisPTranscription factor achaete scute-like 2 controls intestinal stem cell fateCell2009136590391219269367
  • TaneseKFukumaMYamadaTG-protein-coupled receptor GPR49 is up-regulated in basal cell carcinoma and promotes cell proliferation and tumor formationAm J Pathol2008173383584318688030
  • MardaryevANMeierNPoterlowiczKLhx2 differentially regulates Sox9, Tcf4 and LGR5 in hair follicle stem cells to promote epidermal regeneration after injuryDevelopment2011138224843485222028024
  • KasperMJaksVAreAWounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytesProc Natl Acad Sci U S A2011108104099410421321199
  • da Silva-DizVSole-SanchezSValdes-GutierrezAProgeny of LGR5-expressing hair follicle stem cell contributes to papillomavirus-induced tumor development in epidermisOncogene201332323732374322945646
  • QuigleyDAToMDPerez-LosadaJGenetic architecture of mouse skin inflammation and tumour susceptibilityNature2009458723750550819136944
  • Van KeymeulenARochaASOussetMDistinct stem cells contribute to mammary gland development and maintenanceNature2011479737218919321983963
  • de VisserKECiampricottiMMichalakEMDevelopmental stage-specific contribution of LGR5(+) cells to basal and luminal epithelial lineages in the postnatal mammary glandJ Pathol2012228330030922926799
  • StinglJEirewPRicketsonIPurification and unique properties of mammary epithelial stem cellsNature2006439707999399716395311
  • ShackletonMVaillantFSimpsonKJGeneration of a functional mammary gland from a single stem cellNature20064397072848816397499
  • OskarssonTAcharyyaSZhangXHBreast cancer cells produce tenascin C as a metastatic niche component to colonize the lungsNat Med201117786787421706029
  • NakataSCamposBBageritzJLGR5 is a marker of poor prognosis in glioblastoma and is required for survival of brain cancer stem-like cellsBrain Pathol2013231607222805276
  • WangYDongJLiDLGR4 regulates mammary gland development and stem cell activity through the pluripotency transcription factor Sox2Stem Cells20133191921193123712846
  • HermeyGMethnerASchallerHCHermans-BorgmeyerIIdentification of a novel seven-transmembrane receptor with homology to glycoprotein receptors and its expression in the adult and developing mouseBiochem Biophys Res Commun199925412732799920770
  • ShiFKempfleJSEdgeASWnt-responsive LGR5-expressing stem cells are hair cell progenitors in the cochleaJ Neurosci201232289639964822787049
  • ChaiRKuoBWangTWnt signaling induces proliferation of sensory precursors in the postnatal mouse cochleaProc Natl Acad Sci U S A2012109218167817222562792
  • O’BrienCAPollettAGallingerSDickJEA human colon cancer cell capable of initiating tumour growth in immunodeficient miceNature2007445712310611017122772
  • MaoXGSongSJXueXYLGR5 is a proneural factor and is regulated by OLIG2 in glioma stem-like cellsCell Mol Neurobiol201333685186523793848
  • GoidtsVBageritzJPuccioLRNAi screening in glioma stem-like cells identifies PFKFB4 as a key molecule important for cancer cell survivalOncogene201231273235324322056879
  • FischerUKellerALeidingerPA different view on DNA amplifications indicates frequent, highly complex, and stable amplicons on 12q13-21 in gliomaMol Cancer Res20086457658418403636
  • BarretinaJTaylorBSBanerjiSSubtype-specific genomic alterations define new targets for soft-tissue sarcoma therapyNat Genet201042871572120601955
  • RotSTaubertHBacheMA novel splice variant of the stem cell marker LGR5/GPR49 is correlated with the risk of tumor-related death in soft-tissue sarcoma patientsBMC Cancer20111142921978106
  • ScannellCAPedersenEAMosherJTLGR5 is Expressed by Ewing sarcoma and potentiates Wnt/beta-catenin signalingFront Oncol201338123596566
  • BauerLLangerRBeckerKExpression profiling of stem cell-related genes in neoadjuvant-treated gastric cancer: a NOTCH2, GSK3B and beta-catenin gene signature predicts survivalPLoS One201279e4456622970250
  • WuCXieYGaoFLGR5 expression as stem cell marker in human gastric gland and its relatedness with other putative cancer stem cell markersGene20135251182523664892
  • VoonDCWangHKooJKEMT-induced stemness and tumorigenicity are fueled by the EGFR/Ras pathwayPLoS One201388e7042723950932
  • RyugeSSatoYJiangSXThe clinicopathological significance of LGR5 expression in lung adenocarcinomaLung Cancer201382114314823915911
  • Merlos-SuarezABarrigaFMJungPThe intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapseCell Stem Cell20118551152421419747
  • VermeulenLTodaroMde Sousa MelloFSingle-cell cloning of colon cancer stem cells reveals a multi-lineage differentiation capacityProc Natl Acad Sci U S A200810536134271343218765800
  • KanwarSSYuYNautiyalJPatelBBMajumdarAPThe Wnt/betacatenin pathway regulates growth and maintenance of colonospheresMol Cancer2010921220691072
  • KemperKPrasetyantiPRDe LauWRodermondHCleversHMedemaJPMonoclonal antibodies against LGR5 identify human colorectal cancer stem cellsStem Cells201230112378238622969042
  • AnastasJNMoonRTWNT signalling pathways as therapeutic targets in cancerNat Rev Cancer2013131112623258168
  • TakebeNHarrisPJWarrenRQIvySPTargeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathwaysNat Rev Clin Oncol2011829710621151206
  • HollandJDKlausAGarrattANBirchmeierWWnt signaling in stem and cancer stem cellsCurr Opin Cell Biol201325225426423347562
  • GeorgeSRO’DowdBFLeeSPG-protein-coupled receptor oligomerization and its potential for drug discoveryNat Rev Drug Discov200211080882012360258
  • SalonJALodowskiDTPalczewskiKThe significance of G protein-coupled receptor crystallography for drug discoveryPharmacol Rev201163490193721969326
  • JacobsonKACostanziSNew insights for drug design from the X-ray crystallographic structures of G-protein-coupled receptorsMol Pharmacol201282336137122695719
  • SasakiYKosakaHUsamiKEstablishment of a novel monoclonal antibody against LGR5Biochem Biophys Res Commun2010394349850220197059
  • SchuijersJCleversHAdult mammalian stem cells: the role of Wnt, Lgr5 and R-spondinsEMBO J201231122685269622617424