Dynamic Expression of Lgr5, a Wnt Target Gene, in the Developing and Mature Mouse Cochlea

Renjie Chai1, Anping Xia1, Tian Wang1, Taha A. Jan1, Toshinori Hayashi2,3, Olivia Bermingham‐McDonogh2, Alan G. Cheng1
1Department of Otolaryngology—Head and Neck Surgery, Stanford University, Stanford, USA
2Department of Biological Structure, University of Washington, Seattle, USA
3Division of Bio-signaling, School of Life Science, Faculty of Medicine, Tottori University, Yonage City, Japan

Tóm tắt

Từ khóa


Tài liệu tham khảo

Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ et al (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449:1003–1007

Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH, Sato T, Stange DE, Begthel H, van den Born M et al (2010) Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 6:25–36

Barolo S (2006) Transgenic Wnt/TCF pathway reporters: all you need is Lef? Oncogene 25:7505–7511

Barolo S, Posakony JW (2002) Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling. Genes Dev 16:1167–1181

Bermingham-McDonogh O, Oesterle EC, Stone JS, Hume CR, Huynh HM, Hayashi T (2006) Expression of Prox1 during mouse cochlear development. J Comp Neurol 496:172–186

Chen ZY, Corey DP (2002) An inner ear gene expression database. J Assoc Res Otolaryngol 3:140–148

Chen P, Segil N (1999) p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581–1590

Chen P, Johnson JE, Zoghbi HY, Segil N (2002) The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129:2495–2505

Dabdoub A, Kelley MW (2005) Planar cell polarity and a potential role for a Wnt morphogen gradient in stereociliary bundle orientation in the mammalian inner ear. J Neurobiol 64:446–457

Dabdoub A, Donohue MJ, Brennan A, Wolf V, Montcouquiol M, Sassoon DA, Hseih JC, Rubin JS, Salinas PC, Kelley MW (2003) Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 130:2375–2384

Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KS, Pevny LH, Kelley MW (2008) Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc Natl Acad Sci USA 105:18396–18401

DasGupta R, Fuchs E (1999) Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126:4557–4568

Daudet N, Ripoll C, Moles JP, Rebillard G (2002) Expression of members of Wnt and Frizzled gene families in the postnatal rat cochlea. Brain Res Mol Brain Res 105:98–107

DeAlmeida VI, Miao L, Ernst JA, Koeppen H, Polakis P, Rubinfeld B (2007) The soluble wnt receptor Frizzled8CRD-hFc inhibits the growth of teratocarcinomas in vivo. Cancer Res 67:5371–5379

Dessimoz J, Bonnard C, Huelsken J, Grapin-Botton A (2005) Pancreas-specific deletion of beta-catenin reveals Wnt-dependent and Wnt-independent functions during development. Curr Biol 15:1677–1683

Geng X, Xiao L, Lin GF, Hu R, Wang JH, Rupp RA, Ding X (2003) Lef/Tcf-dependent Wnt/beta-catenin signaling during Xenopus axis specification. FEBS Lett 547:1–6

Hartman BH, Basak O, Nelson BR, Taylor V, Bermingham-McDonogh O, Reh TA (2009) Hes5 expression in the postnatal and adult mouse inner ear and the drug-damaged cochlea. J Assoc Res Otolaryngol 10:321–340

Hayashi T, Cunningham D, Bermingham-McDonogh O (2007) Loss of Fgfr3 leads to excess hair cell development in the mouse organ of Corti. Dev Dyn 236:525–533

Hayashi T, Ray CA, Bermingham-McDonogh O (2008) Fgf20 is required for sensory epithelial specification in the developing cochlea. J Neurosci 28:5991–5999

Hollyday M, McMahon JA, McMahon AP (1995) Wnt expression patterns in chick embryo nervous system. Mech Dev 52:9–25

Hsu SY, Liang SG, Hsueh AJ (1998) Characterization of two LGR genes homologous to gonadotropin and thyrotropin receptors with extracellular leucine-rich repeats and a G protein-coupled, seven-transmembrane region. Mol Endocrinol 12:1830–1845

Hume CR, Bratt DL, Oesterle EC (2007) Expression of LHX3 and SOX2 during mouse inner ear development. Gene Expr Patterns 7:798–807

Ikeya M, Lee SM, Johnson JE, McMahon AP, Takada S (1997) Wnt signalling required for expansion of neural crest and CNS progenitors. Nature 389:966–970

Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H, Toftgard R (2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40:1291–1299

Jasoni C, Hendrickson A, Roelink H (1999) Analysis of chicken Wnt-13 expression demonstrates coincidence with cell division in the developing eye and is consistent with a role in induction. Dev Dyn 215:215–224

Jho EH, Zhang T, Domon C, Joo CK, Freund JN, Costantini F (2002) Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol Cell Biol 22:1172–1183

Kalani MY, Cheshier SH, Cord BJ, Bababeygy SR, Vogel H, Weissman IL, Palmer TD, Nusse R (2008) Wnt-mediated self-renewal of neural stem/progenitor cells. Proc Natl Acad Sci USA 105:16970–16975

Kiernan AE, Pelling AL, Leung KK, Tang AS, Bell DM, Tease C, Lovell-Badge R, Steel KP, Cheah KS (2005) Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434:1031–1035

Lee YS, Liu F, Segil N (2006) A morphogenetic wave of p27Kip1 transcription directs cell cycle exit during organ of Corti development. Development 133:2817–2826

Li C, Xiao J, Hormi K, Borok Z, Minoo P (2002) Wnt5a participates in distal lung morphogenesis. Dev Biol 248:68–81

Lillevali K, Haugas M, Matilainen T, Pussinen C, Karis A, Salminen M (2006) Gata3 is required for early morphogenesis and Fgf10 expression during otic development. Mech Dev 123:415–429

Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20:781–810

Lustig B, Jerchow B, Sachs M, Weiler S, Pietsch T, Karsten U, van de Wetering M, Clevers H, Schlag PM, Birchmeier W et al (2002) Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol Cell Biol 22:1184–1193

Majumdar A, Vainio S, Kispert A, McMahon J, McMahon AP (2003) Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130:3175–3185

Maretto S, Cordenonsi M, Dupont S, Braghetta P, Broccoli V, Hassan AB, Volpin D, Bressan GM, Piccolo S (2003) Mapping Wnt/beta-catenin signaling during mouse development and in colorectal tumors. Proc Natl Acad Sci USA 100:3299–3304

Morita H, Mazerbourg S, Bouley DM, Luo CW, Kawamura K, Kuwabara Y, Baribault H, Tian H, Hsueh AJ (2004) Neonatal lethality of LGR5 null mice is associated with ankyloglossia and gastrointestinal distension. Mol Cell Biol 24:9736–9743

Morrison A, Hodgetts C, Gossler A, Hrabe de Angelis M, Lewis J (1999) Expression of Delta1 and Serrate1 (Jagged1) in the mouse inner ear. Mech Dev 84:169–172

Morsli H, Choo D, Ryan A, Johnson R, Wu DK (1998) Development of the mouse inner ear and origin of its sensory organs. J Neurosci 18:3327–3335

Oesterle EC, Campbell S, Taylor RR, Forge A, Hume CR (2008) Sox2 and JAGGED1 expression in normal and drug-damaged adult mouse inner ear. J Assoc Res Otolaryngol 9:65–89

Ohyama T, Mohamed OA, Taketo MM, Dufort D, Groves AK (2006) Wnt signals mediate a fate decision between otic placode and epidermis. Development 133:865–875

Ootani A, Li X, Sangiorgi E, Ho QT, Ueno H, Toda S, Sugihara H, Fujimoto K, Weissman IL, Capecchi MR et al (2009) Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche. Nat Med 15:701–706

Qian D, Jones C, Rzadzinska A, Mark S, Zhang X, Steel KP, Dai X, Chen P (2007) Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306:121–133

Radde-Gallwitz K, Pan L, Gan L, Lin X, Segil N, Chen P (2004) Expression of Islet1 marks the sensory and neuronal lineages in the mammalian inner ear. J Comp Neurol 477:412–421

Reya T, Clevers H (2005) Wnt signalling in stem cells and cancer. Nature 434:843–850

Riccomagno MM, Takada S, Epstein DJ (2005) Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev 19:1612–1623

Riese J, Yu X, Munnerlyn A, Eresh S, Hsu SC, Grosschedl R, Bienz M (1997) LEF-1, a nuclear factor coordinating signaling inputs from wingless and decapentaplegic. Cell 88:777–787

Rubel EW (1978) Ontogeny of structure and function in the vertebrate auditory system. In: Jacobson M (ed) Handbook of sensory physiology, IX. Springer, New York, pp 135–237

Ruben RJ (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol Suppl 220:221–244

Sahly I, El-Amraoui A, Abitbol M, Petit C, Dufier JL (1997) Expression of myosin VIIA during mouse embryogenesis. Anat Embryol (Berl) 196:159–170

Sajan SA, Warchol ME, Lovett M (2007) Toward a systems biology of mouse inner ear organogenesis: gene expression pathways, patterns and network analysis. Genetics 177:631–653

Sasaki Y, Kosaka H, Usami K, Toki H, Kawai H, Shiraishi N, Ota T, Nakamura K, Furuya A, Satoh M et al (2010) Establishment of a novel monoclonal antibody against LGR5. Biochem Biophys Res Commun 394:498–502

Shi F, Cheng YF, Wang XL, Edge AS (2010) Beta-catenin up-regulates Atoh1 expression in neural progenitor cells by interaction with an Atoh1 3′ enhancer. J Biol Chem 285:392–400

Sienknecht UJ, Fekete DM (2008) Comprehensive Wnt-related gene expression during cochlear duct development in chicken. J Comp Neurol 510:378–395

Sienknecht UJ, Fekete DM (2009) Mapping of Wnt, frizzled, and Wnt inhibitor gene expression domains in the avian otic primordium. J Comp Neurol 517:751–764

Soshnikova N, Zechner D, Huelsken J, Mishina Y, Behringer RR, Taketo MM, Crenshaw EB 3rd, Birchmeier W (2003) Genetic interaction between Wnt/beta-catenin and BMP receptor signaling during formation of the AER and the dorsal–ventral axis in the limb. Genes Dev 17:1963–1968

Stevens CB, Davies AL, Battista S, Lewis JH, Fekete DM (2003) Forced activation of Wnt signaling alters morphogenesis and sensory organ identity in the chicken inner ear. Dev Biol 261:149–164

Willert K, Brown JD, Danenberg E, Duncan AW, Weissman IL, Reya T, Yates JR 3rd, Nusse R (2003) Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423:448–452

Yamaguchi TP, Bradley A, McMahon AP, Jones S (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211–1223

Zeng YA, Nusse R (2010) Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 6:568–577

Zheng QY, Johnson KR, Erway LC (1999) Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses. Hear Res 130:94–107