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Journal of the Association for Research in Otolaryngology

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01-12-2011

Serial Analysis of Gene Expression in the Chicken Otocyst

Authors: Saku T. Sinkkonen, Veronika Starlinger, Deepa J. Galaiya, Roman D. Laske, Samuel Myllykangas, Kazuo Oshima, Stefan Heller

Published in: Journal of the Association for Research in Otolaryngology | Issue 6/2011

Abstract

The inner ear arises from multipotent placodal precursors that are gradually committed to the otic fate and further differentiate into all inner ear cell types, with the exception of a few immigrating neural crest-derived cells. The otocyst plays a pivotal role during inner ear development: otic progenitor cells sub-compartmentalize into non-sensory and prosensory domains, giving rise to individual vestibular and auditory organs and their associated ganglia. The genes and pathways underlying this progressive subdivision and differentiation process are not entirely known. The goal of this study was to identify a comprehensive set of genes expressed in the chicken otocyst using the serial analysis of gene expression (SAGE) method. Our analysis revealed several hundred transcriptional regulators, potential signaling proteins, and receptors. We identified a substantial collection of genes that were previously known in the context of inner ear development, but we also found many new candidate genes, such as SOX4, SOX5, SOX7, SOX8, SOX11, and SOX18, which previously were not known to be expressed in the developing inner ear. Despite its limitation of not being all-inclusive, the generated otocyst SAGE library is a practical bioinformatics tool to study otocyst gene expression and to identify candidate genes for developmental studies.

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Abraira VE, Del Rio T, Tucker AF, Slonimsky J, Keirnes HL, Goodrich LV (2008) Cross-repressive interactions between Lrig3 and netrin 1 shape the architecture of the inner ear. Development 135:4091–4099PubMedCrossRef

Adam J, Myat A, Le Roux I, Eddison M, Henrique D, Ish-Horowicz D, Lewis J (1998) Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 125:4645–4654PubMed

Alsina B, Abello G, Ulloa E, Henrique D, Pujades C, Giraldez F (2004) FGF signaling is required for determination of otic neuroblasts in the chick embryo. Dev Biol 267:119–134PubMedCrossRef

Barrionuevo F, Naumann A, Bagheri-Fam S, Speth V, Taketo MM, Scherer G, Neubuser A (2008) Sox9 is required for invagination of the otic placode in mice. Dev Biol 317:213–224PubMedCrossRef

Battisti AC, Fekete DM (2008) Slits and Robos in the developing chicken inner ear. Dev Dyn 237:476–484PubMedCrossRef

Bok J, Bronner-Fraser M, Wu DK (2005) Role of the hindbrain in dorsoventral but not anteroposterior axial specification of the inner ear. Development 132:2115–2124PubMedCrossRef

Brigande JV, Heller S (2009) Quo vadis hair cell regeneration? Nat Neurosci 12:679–685PubMedCrossRef

Diensthuber M, Oshima K, Heller S (2009) Stem/progenitor cells derived from the cochlear sensory epithelium give rise to spheres with distinct morphologies and features. J Assoc Res Otolaryngol 10:173–190PubMedCrossRef

Fekete DM (1996) Cell fate specification in the inner ear. Curr Opin Neurobiol 6:533–541PubMedCrossRef

Fekete DM, Campero AM (2007) Axon guidance in the inner ear. Int J Dev Biol 51:549–556PubMedCrossRef

Fekete DM, Wu DK (2002) Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12:35–42PubMedCrossRef

Frenz DA, Van de Water TR, Galinovic-Schwartz V (1991) Transforming growth factor beta: does it direct otic capsule formation? Ann Otol Rhinol Laryngol 100:301–307PubMed

Frenz DA, Galinovic-Schwartz V, Liu W, Flanders KC, Van de Water TR (1992) Transforming growth factor beta 1 is an epithelial-derived signal peptide that influences otic capsule formation. Dev Biol 153:324–336PubMedCrossRef

Frolova EI, Fokina VM, Beebe DC (2004) The expression pattern of opticin during chicken embryogenesis. Gene Expr Patterns 4:335–338PubMedCrossRef

Gong TW, Hegeman AD, Shin JJ, Lindberg KH, Barald KF, Lomax MI (1997) Novel genes expressed in the chick otocyst during development: identification using differential display of RNA. Int J Dev Neurosci 15:585–594PubMedCrossRef

Groves AK, Bronner-Fraser M (2000) Competence, specification and commitment in otic placode induction. Development 127:3489–3499PubMed

Guth SI, Wegner M (2008) Having it both ways: Sox protein function between conservation and innovation. Cell Mol Life Sci 65:3000–3018PubMedCrossRef

Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 195:231–272PubMedCrossRef

Hawkins RD, Bashiardes S, Powder KE, Sajan SA, Bhonagiri V, Alvarado DM, Speck J, Warchol ME, Lovett M (2007) Large scale gene expression profiles of regenerating inner ear sensory epithelia. PLoS ONE 2:e525PubMedCrossRef

Herbrand H, Guthrie S, Hadrys T, Hoffmann S, Arnold HH, Rinkwitz-Brandt S, Bober E (1998) Two regulatory genes, cNkx5-1 and cPax2, show different responses to local signals during otic placode and vesicle formation in the chick embryo. Development 125:645–654PubMed

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

Ito K, Nakamura H, Watanabe Y (2011) Protogenin mediates cell adhesion for ingression and re-epithelialization of paraxial mesodermal cells. Dev Biol 351:13–24PubMedCrossRef

Jia XQ, Nakashima T, Kadomatsu K, Muramatsu T (2001) Expression of midkine in the cochlea. Hear Res 160:10–14PubMedCrossRef

Katayama K, Zine A, Ota M, Matsumoto Y, Inoue T, Fritzsch B, Aruga J (2009) Disorganized innervation and neuronal loss in the inner ear of Slitrk6-deficient mice. PLoS ONE 4:e7786PubMedCrossRef

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 434:1031–1035PubMedCrossRef

Kimura I, Konishi M, Miyake A, Fujimoto M, Itoh N (2006) Neudesin, a secreted factor, promotes neural cell proliferation and neuronal differentiation in mouse neural precursor cells. J Neurosci Res 83:1415–1424PubMedCrossRef

Lewis AK, Frantz GD, Carpenter DA, de Sauvage FJ, Gao WQ (1998) Distinct expression patterns of notch family receptors and ligands during development of the mammalian inner ear. Mech Dev 78:159–163PubMedCrossRef

Li H, Liu H, Heller S (2003a) Pluripotent stem cells from the adult mouse inner ear. Nat Med 9:1293–1299PubMedCrossRef

Li H, Roblin G, Liu H, Heller S (2003b) Generation of hair cells by stepwise differentiation of embryonic stem cells. Proc Natl Acad Sci U S A 100:13495–13500PubMedCrossRef

Li H, Liu H, Corrales CE, Mutai H, Heller S (2004) Correlation of Pax-2 expression with cell proliferation in the developing chicken inner ear. J Neurobiol 60:61–70PubMedCrossRef

Li H, Ruan J, Durbin R (2008) Mapping short DNA sequencing reads and calling variants using mapping quality scores. Genome Res 18:1851–1858PubMedCrossRef

Lillevali K, Haugas M, Pituello F, Salminen M (2007) Comparative analysis of Gata3 and Gata2 expression during chicken inner ear development. Dev Dyn 236:306–313PubMedCrossRef

Liu M, Pereira FA, Price SD, Chu MJ, Shope C, Himes D, Eatock RA, Brownell WE, Lysakowski A, Tsai MJ (2000) Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev 14:2839–2854PubMedCrossRef

Liu W, Li G, Chien JS, Raft S, Zhang H, Chiang C, Frenz DA (2002) Sonic hedgehog regulates otic capsule chondrogenesis and inner ear development in the mouse embryo. Dev Biol 248:240–250PubMedCrossRef

Liu D, Chu H, Maves L, Yan YL, Morcos PA, Postlethwait JH, Westerfield M (2003) Fgf3 and Fgf8 dependent and independent transcription factors are required for otic placode specification. Development 130:2213–2224PubMedCrossRef

Liu W, Li L, Li G, Garritano F, Shanske A, Frenz DA (2008) Coordinated molecular control of otic capsule differentiation: functional role of Wnt5a signaling and opposition by sfrp3 activity. Growth Factors 26:343–354PubMedCrossRef

Lu X, Borchers AG, Jolicoeur C, Rayburn H, Baker JC, Tessier-Lavigne M (2004) PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430:93–98PubMedCrossRef

Ma Q, Anderson DJ, Fritzsch B (2000) Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J Assoc Res Otolaryngol 1:129–143PubMedCrossRef

Matilainen T, Haugas M, Kreidberg JA, Salminen M (2007) Analysis of Netrin 1 receptors during inner ear development. Int J Dev Biol 51:409–413PubMedCrossRef

Neves J, Kamaid A, Alsina B, Giraldez F (2007) Differential expression of Sox2 and Sox3 in neuronal and sensory progenitors of the developing inner ear of the chick. J Comp Neurol 503:487–500PubMedCrossRef

Oh SH, Johnson R, Wu DK (1996) Differential expression of bone morphogenetic proteins in the developing vestibular and auditory sensory organs. J Neurosci 16:6463–6475PubMed

Ohyama T, Groves AK (2004) Expression of mouse Foxi class genes in early craniofacial development. Dev Dyn 231:640–646PubMedCrossRef

Okano J, Takigawa T, Seki K, Suzuki S, Shiota K, Ishibashi M (2005) Transforming growth factor beta 2 promotes the formation of the mouse cochleovestibular ganglion in organ culture. Int J Dev Biol 49:23–31PubMedCrossRef

Oshima K, Grimm CM, Corrales CE, Senn P, Martinez Monedero R, Geleoc GS, Edge A, Holt JR, Heller S (2007) Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J Assoc Res Otolaryngol 8:18–31PubMedCrossRef

Oshima K, Shin K, Diensthuber M, Peng AW, Ricci AJ, Heller S (2010) Mechanosensitive hair cell-like cells from embryonic and induced pluripotent stem cells. Cell 141:704–716PubMedCrossRef

Pauley S, Lai E, Fritzsch B (2006) Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Dev Dyn 235:2470–2482PubMedCrossRef

Perrot V, Vazquez-Prado J, Gutkind JS (2002) Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J Biol Chem 277:43115–43120PubMedCrossRef

Pirvola U, Ylikoski J, Trokovic R, Hebert JM, McConnell SK, Partanen J (2002) FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35:671–680PubMedCrossRef

Powles N, Babbs C, Ficker M, Schimmang T, Maconochie M (2004) Identification and analysis of genes from the mouse otic vesicle and their association with developmental subprocesses through in situ hybridization. Dev Biol 268:24–38PubMedCrossRef

Puppo F, Thome V, Lhoumeau AC et al (2011) Protein tyrosine kinase 7 has a conserved role in Wnt/beta-catenin canonical signalling. EMBO Rep 12:43–49PubMedCrossRef

Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ (2002) Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16:2365–2378PubMedCrossRef

Saha S, Sparks AB, Rago C, Akmaev V, Wang CJ, Vogelstein B, Kinzler KW, Velculescu VE (2002) Using the transcriptome to annotate the genome. Nat Biotechnol 20:508–512PubMedCrossRef

Sanchez-Calderon H, Francisco-Morcillo J, Martin-Partido G, Hidalgo-Sanchez M (2007) Fgf19 expression patterns in the developing chick inner ear. Gene Expr Patterns 7:30–38PubMedCrossRef

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

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 261:149–164PubMedCrossRef

Stone JS, Rubel EW (1999) Delta1 expression during avian hair cell regeneration. Development 126:961–973PubMed

Streit A (2007) The preplacodal region: an ectodermal domain with multipotential progenitors that contribute to sense organs and cranial sensory ganglia. Int J Dev Biol 51:447–461PubMedCrossRef

Sudhof TC (2001) alpha-Latrotoxin and its receptors: neurexins and CIRL/latrophilins. Annu Rev Neurosci 24:933–962PubMedCrossRef

Swanson GJ, Howard M, Lewis J (1990) Epithelial autonomy in the development of the inner ear of a bird embryo. Dev Biol 137:243–257PubMedCrossRef

Tomarev SI, Nakaya N (2009) Olfactomedin domain-containing proteins: possible mechanisms of action and functions in normal development and pathology. Mol Neurobiol 40:122–138PubMedCrossRef

Uchikawa M, Kamachi Y, Kondoh H (1999) Two distinct subgroups of Group B Sox genes for transcriptional activators and repressors: their expression during embryonic organogenesis of the chicken. Mech Dev 84:103–120PubMedCrossRef

Urness LD, Paxton CN, Wang X, Schoenwolf GC, Mansour SL (2010) FGF signaling regulates otic placode induction and refinement by controlling both ectodermal target genes and hindbrain Wnt8a. Dev Biol 340:595–604PubMedCrossRef

Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487PubMedCrossRef

von Bartheld CS, Patterson SL, Heuer JG, Wheeler EF, Bothwell M, Rubel EW (1991) Expression of nerve growth factor (NGF) receptors in the developing inner ear of chick and rat. Development 113:455–470

Watanabe K, Takeda K, Katori Y, Ikeda K, Oshima T, Yasumoto K, Saito H, Takasaka T, Shibahara S (2000) Expression of the Sox10 gene during mouse inner ear development. Brain Res Mol Brain Res 84:141–145PubMedCrossRef

Webber A, Raz Y (2006) Axon guidance cues in auditory development. Anat Rec A Discov Mol Cell Evol Biol 288:390–396PubMed

Wong YH, Lu AC, Wang YC, Cheng HC, Chang C, Chen PH, Yu JY, Fann MJ (2010) Protogenin defines a transition stage during embryonic neurogenesis and prevents precocious neuronal differentiation. J Neurosci 30:4428–4439PubMedCrossRef

Wood HB, Episkopou V (1999) Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages. Mech Dev 86:197–201PubMedCrossRef

Wright TJ, Mansour SL (2003) Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130:3379–3390PubMedCrossRef

Yamashita H, Oesterle EC (1995) Induction of cell proliferation in mammalian inner-ear sensory epithelia by transforming growth factor alpha and epidermal growth factor. Proc Natl Acad Sci U S A 92:3152–3155PubMedCrossRef

Yen WW, Williams M, Periasamy A, Conaway M, Burdsal C, Keller R, Lu X, Sutherland A (2009) PTK7 is essential for polarized cell motility and convergent extension during mouse gastrulation. Development 136:2039–2048PubMedCrossRef

Zou P, Muramatsu H, Sone M, Hayashi H, Nakashima T, Muramatsu T (2006) Mice doubly deficient in the midkine and pleiotrophin genes exhibit deficits in the expression of beta-tectorin gene and in auditory response. Lab Invest 86:645–653PubMedCrossRef

Title: Serial Analysis of Gene Expression in the Chicken Otocyst
Authors: Saku T. Sinkkonen
Veronika Starlinger
Deepa J. Galaiya
Roman D. Laske
Samuel Myllykangas
Kazuo Oshima
Stefan Heller
Publication date: 01-12-2011
Publisher: Springer-Verlag
Published in: Journal of the Association for Research in Otolaryngology / Issue 6/2011
Print ISSN: 1525-3961
Electronic ISSN: 1438-7573
DOI: https://doi.org/10.1007/s10162-011-0286-z

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Serial Analysis of Gene Expression in the Chicken Otocyst

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