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Fgf3 and Fgf16 expression patterns define spatial and temporal domains in the developing chick inner ear

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Abstract

The inner ear is a morphologically complex sensory structure with auditory and vestibular functions. The developing otic epithelium gives rise to neurosensory and non-sensory elements of the adult membranous labyrinth. Extrinsic and intrinsic signals manage the patterning and cell specification of the developing otic epithelium by establishing lineage-restricted compartments defined in turn by differential expression of regulatory genes. FGF3 and FGF16 are excellent candidates to govern these developmental events. Using the chick inner ear, we show that Fgf3 expression is present in the borders of all developing cristae. Strong Fgf16 expression was detected in a portion of the developing vertical and horizontal pouches, whereas the cristae show weaker or undetected Fgf16 expression at different developmental stages. Concerning the rest of the vestibular sensory elements, both the utricular and saccular maculae were Fgf3 positive. Interestingly, strong Fgf16 expression delimited these Fgf16-negative sensory patches. The Fgf3-negative macula neglecta and the Fgf3-positive macula lagena were included within weakly Fgf16-expressing areas. Therefore, different FGF-mediated mechanisms might regulate the specification of the anterior (utricular and saccular) and posterior (neglecta and lagena) maculae. In the developing cochlear duct, dynamic Fgf3 and Fgf16 expression suggests their cooperation in the early specification and later cell differentiation in the hearing system. The requirement of Fgf3 and Fgf16 genes in endolymphatic apparatus development and neurogenesis are discussed. Based on these observations, FGF3 and FGF16 seem to be key signaling pathways that control the inner ear plan by defining epithelial identities within the developing otic epithelium.

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Abbreviations

ac:

Anterior crista

AG:

Acoustic ganglion

asc:

Anterior semicircular canal

AVG:

Acoustic-vestibular ganglion

bp:

Basilar papilla

cc:

Common crus

cd:

Cochlear duct

ed:

Endolymphatic duct

es:

Endolymphatic sac

HB:

Hindbrain

hp:

Horizontal pouch

lc:

Lateral crista

lsc:

Lateral semicircular canal

ml:

Macula lagena

mn:

Macula neglecta

ms:

Macula sacculi

mu:

Macula utriculi

pc:

Posterior crista

psc:

Posterior semicircular canal

rh:

Rhombomere

s:

Saccule

tv:

Tegmentum vasculosum

u:

Utricle

vp:

Vertical pouch

References

  • Abelló G, Khatri S, Giráldez F, Alsina B (2007) Early regionalization of the otic placode and its regulation by the Notch signaling pathway. Mech Dev 124:631–645

    Article  PubMed  CAS  Google Scholar 

  • Abelló G, Khatri S, Radosevic M, Scotting PJ, Giráldez F, Alsina B (2010) Independent regulation of Sox3 and Lmx1b by FGF and BMP signaling influences the neurogenic and non-neurogenic domains in the chick otic placode. Dev Biol 339:166–178

    Article  PubMed  CAS  Google Scholar 

  • 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 125:4645–4654

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Alsmadi O, Meyer BF, Alkuraya F, Wakil S, Alkayal F, Al-Saud H, Ramzan K, Al-Sayed M (2009) Syndromic congenital sensorineural deafness, microtia and microdontia resulting from a novel homoallelic mutation in fibroblast growth factor 3 (FGF3). Eur J Hum Genet 17:14–21

    Article  CAS  PubMed  Google Scholar 

  • Álvarez Y, Alonso MT, Vendrell V, Zelarayan LC, Chamero P, Theil T, Bosl MR, Kato S, Maconochie M, Riethmacher D, Schimmang T (2003) Requirements for FGF3 and FGF10 during inner ear formation. Development 130:6329–6338

    Article  PubMed  CAS  Google Scholar 

  • Aragón F, Pujades C (2009) FGF signaling controls caudal hindbrain specification through Ras-ERK1/2 pathway. BMC Dev Biol 9:61

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Aragón F, Vazquez-Echeverría C, Ulloa E, Reber M, Cereghini S, Alsina B, Giráldez F, Pujades C (2005) vHnf1 regulates specification of caudal rhombomere identity in the chick hindbrain. Dev Dyn 234:567–576

    Article  PubMed  CAS  Google Scholar 

  • Arnold JS, Braunstein EM, Ohyama T, Groves AK, Adams JC, Brown MC, Morrow BE (2006) Tissue-specific roles of Tbx1 in the development of the outer, middle and inner ear, defective in 22q11DS patients. Hum Mol Genet 15:1629–1639

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Bok J, Chang W, Wu DK (2007) Patterning and morphogenesis of the vertebrate inner ear. Int J Dev Biol 51:521–533

    Article  CAS  PubMed  Google Scholar 

  • Brigande JV, Kiernan AE, Gao X, Iten LE, Fekete DM (2000) Molecular genetics of pattern formation in the inner ear: do compartment boundaries play a role? Proc Natl Acad Sci USA 97:11700–11706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cadot S, Frenz D, Maconochie M (2012) A novel method for retinoic acid administration reveals differential and dose-dependent downregulation of Fgf3 in the developing inner ear and anterior CNS. Dev Dyn 241:741–58

    Article  CAS  PubMed  Google Scholar 

  • Cantos R, Cole LK, Acampora D, Simeone A, Wu DK (2000) Patterning of the mammalian cochlea. Proc Natl Acad Sci 97:11707–11713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang W, Brigande JV, Fekete DM, Wu DK (2004) The development of semicircular canals in the inner ear: role of FGFs in sensory cristae. Development 131:4201–4211

    Article  CAS  PubMed  Google Scholar 

  • Chapman SC, Cai Q, Bleyl SB, Schoenwolf GC (2006) Restricted expression of Fgf16 within the developing chick inner ear. Dev Dyn 235:2276–2281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chatterjee S, Kraus P, Lufkin T (2010) A symphony of inner ear developmental control genes. BMC Genet 11:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen J, Streit A (2013) Induction of the inner ear: stepwise specification of otic fate from multipotent progenitors. Hear Res 297:3–12

    Article  PubMed  Google Scholar 

  • Choo D, Ward J, Reece A, Dou H, Lin Z, Greinwald J (2006) Molecular mechanisms underlying inner ear patterning defects in kreisler mutants. Dev Biol 289:308–317

    Article  CAS  PubMed  Google Scholar 

  • Deol MS (1964) The abnormalities of the inner ear in Kreisler mice. J Embryol Exp Morphol 12:475–490

    CAS  PubMed  Google Scholar 

  • Domínguez-Frutos E, Vendrell V, Álvarez Y, Zelarayan LC, Lopez-Hernández I, Ros M, Schimmang T (2009) Tissue-specific requirements for FGF8 during early inner ear development. Mech Dev 126:873–881

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Frenz DA, Liu W, Cvekl A, Xie Q, Wassef L, Quadro L, Niederreither K, Maconochie M, Shanske A (2010) Retinoid signaling in inner ear development: A “Goldilocks” phenomenon. Am J Med Genet 152A:2947–2961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freter S, Muta Y, Mak SS, Rinkwitz S, Ladher RK (2008) Progressive restriction of otic fate: the role of FGF and Wnt in resolving inner ear potential. Development 135:3415–3424

    Article  CAS  PubMed  Google Scholar 

  • Fritzsch B, Pauley S, Beisel KW (2006) Cells, molecules and morphogenesis: the making of the vertebrate ear. Brain Res 1091:151–171

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fritzsch B, Pan N, Jahan I, Duncan JS, Kopecky BJ, Elliott KL, Kersigo J, Yang T (2013) Evolution and development of the tetrapod auditory system: an organ of Corti-centric perspective. Evol Dev 15:63–79

    Article  PubMed  PubMed Central  Google Scholar 

  • Gregory-Evans CY, Moosajee M, Hodges MD, Mackay DS, Game L, Vargesson N, Bloch-Zupan A, Ruschendorf F, Santos-Pinto L, Wackens G, Gregory-Evans K (2007) SNP genome scanning localizes oto-dental syndrome to chromosome 11q13 and microdeletions at this locus implicate FGF3 in dental and inner-ear disease and FADD in ocular coloboma. Hum Mol Genet 16:2482–2493

    Article  CAS  PubMed  Google Scholar 

  • Groves AK, Fekete DM (2012) Shaping sound in space: the regulation of inner ear patterning. Development 139:245–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hamburger V, Hamilton HL (1951) A series of normal stages in the development of the chick embryo. J Morphol 88:49–92

    Article  CAS  PubMed  Google Scholar 

  • Hammond KL, Whitfield TT (2011) Fgf and Hh signalling act on a symmetrical pre-pattern to specify anterior and posterior identity in the zebrafish otic placode and vesicle. Development 138:3977–3987

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hans S, Westerfield M (2007) Changes in retinoic acid signaling alter otic patterning. Development 134:2449–2458

    Article  CAS  PubMed  Google Scholar 

  • Hatch EP, Noyes CA, Wang X, Wright TJ, Mansour SL (2007) Fgf3 is required for dorsal patterning and morphogenesis of the inner ear epithelium. Development 134:3615–3625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hatch EP, Urness LD, Mansour SL (2009) Fgf16(IRESCre) mice: a tool to inactivate genes expressed in inner ear cristae and spiral prominence epithelium. Dev Dyn 238:358–366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hidalgo-Sánchez M, Alvarado-Mallart R, Álvarez IS (2000) Pax2, Otx2, Gbx2 and Fgf8 expression in early otic vesicle development. Mech Dev 95:225–229

    Article  PubMed  Google Scholar 

  • Hill J, Clarke JD, Vargesson N, Jowett T, Holder N (1995) Exogenous retinoic acid causes specific alterations in the development of the midbrain and hindbrain of the zebrafish embryo including positional respecification of the Mauthner neuron. Mech Dev 50:3–16

    Article  CAS  PubMed  Google Scholar 

  • Imamura T (2014) Physiological functions and underlying mechanisms of fibroblast growth factor (FGF) family members: recent findings and implications for their pharmacological application. Biol Pharm Bull 37:1081–1089

    Article  CAS  PubMed  Google Scholar 

  • Itoh N, Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20:563–569

    Article  CAS  PubMed  Google Scholar 

  • Karabagli H, Karabagli P, Ladher RK, Schoenwolf GC (2002) Comparison of the expression patterns of several fibroblast growth factors during chick gastrulation and neurulation. Anat Embryol 205:365–370

    Article  CAS  PubMed  Google Scholar 

  • Kil SH, Streit A, Brown ST, Agrawal N, Collazo A, Zile MH, Groves AK (2005) Distinct roles for hindbrain and paraxial mesoderm in the induction and patterning of the inner ear revealed by a study of vitamin-A-deficient quail. Dev Biol 285:252–271

    Article  CAS  PubMed  Google Scholar 

  • Koo SK, Hill JK, Hwang CH, Lin ZS, Millen KJ, Wu DK (2009) Lmx1a maintains proper neurogenic, sensory, and non-sensory domains in the mammalian inner ear. Dev Biol 333:14–25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwak SJ, Phillips BT, Heck R, Riley BB (2002) An expanded domain of fgf3 expression in the hindbrain of zebrafish valentino mutants results in mis-patterning of the otic vesicle. Development 129:5279–5287

    CAS  PubMed  Google Scholar 

  • Ladher RK, Wright TJ, Moon AM, Mansour SL, Schoenwolf GC (2005) FGF8 initiates inner ear induction in chick and mouse. Genes Dev 19:603–613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ladher RK, O’Neill P, Begbie J (2010) From shared lineage to distinct functions: the development of the inner ear and epibranchial placodes. Development 137:1777–1785

    Article  CAS  PubMed  Google Scholar 

  • Leger S, Brand M (2002) Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech Dev 119:91–108

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Lin Z, Cantos R, Patente M, Wu DK (2005) Gbx2 is required for the morphogenesis of the mouse inner ear: a downstream candidate of hindbrain signaling. Development 132:2309–2318

    Article  CAS  PubMed  Google Scholar 

  • Liu W, Levi G, Shanske A, Frenz DA (2008) Retinoic acid-induced inner ear teratogenesis caused by defective Fgf3/Fgf10-dependent Dlx5 signaling. Birth Defects Res B Dev Reprod Toxicol 83:134–144

    Article  CAS  PubMed  Google Scholar 

  • Lombardo A, Isaacs HV, Slack JM (1998) Expression and functions of FGF-3 in Xenopus development. Int J Dev Biol 42:1101–1107

    CAS  PubMed  Google Scholar 

  • Lufkin T, Dierich A, LeMeur M, Mark M, Chambon P (1991) Disruption of the Hox-1.6 homeobox gene results in defects in a region corresponding to its rostral domain of expression. Cell 66:1105–1119

    Article  CAS  PubMed  Google Scholar 

  • Mahmood R, Kiefer P, Guthrie S, Dickson C, Mason I (1995) Multiple roles for FGF-3 during cranial neural development in the chicken. Development 121:1399–1410

    CAS  PubMed  Google Scholar 

  • Mahmood R, Mason IJ, Morriss-Kay GM (1996) Expression of Fgf-3 in relation to hindbrain segmentation, otic pit position and pharyngeal arch morphology in normal and retinoic acid-exposed mouse embryos. Anat Embryol 194:13–22

    Article  CAS  PubMed  Google Scholar 

  • Mansour SL (1994) Targeted disruption of int-2 (fgf-3) causes developmental defects in the tail and inner ear. Mol Reprod Dev 39:62–67

    Article  CAS  PubMed  Google Scholar 

  • Mansour SL, Goddard JM, Capecchi MR (1993) Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development 117:13–28

    CAS  PubMed  Google Scholar 

  • Maroon H, Walshe J, Mahmood R, Kiefer P, Dickson C, Mason I (2002) Fgf3 and Fgf8 are required together for formation of the otic placode and vesicle. Development 129:2099–2108

    CAS  PubMed  Google Scholar 

  • Maves L, Jackman W, Kimmel CB (2002) FGF3 and FGF8 mediate a rhombomere 4 signaling activity in the zebrafish hindbrain. Development 129:3825–3837

    CAS  PubMed  Google Scholar 

  • McCarroll MN, Lewis ZR, Culbertson MD, Martin B, Kimelman D, Nechiporuk AV (2012) Graded levels of Pax2a and Pax8 regulate cell differentiation during sensory placode formation. Development 139:2740–2750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McKay IJ, Lewis J, Lumsden A (1996) The role of FGF-3 in early inner ear development: an analysis in normal and kreisler mutant mice. Dev Biol 174:370–378

    Article  CAS  PubMed  Google Scholar 

  • Millimaki BB, Sweet EM, Dhason MS, Riley BB (2007) Zebrafish atoh1 genes: classic proneural activity in the inner ear and regulation by Fgf and Notch. Development 134:295–305

    Article  CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Murakami A, Ishida S, Thurlow J, Revest JM, Dickson C (2001) SOX6 binds CtBP2 to repress transcription from the Fgf-3 promoter. Nucleic Acids Res 29:3347–3355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murakami A, Shen H, Ishida S, Dickson C (2004) SOX7 and GATA-4 are competitive activators of Fgf-3 transcription. J Biol Chem 279:28564–28573

    Article  CAS  PubMed  Google Scholar 

  • Nechiporuk A, Raible DW (2008) FGF-dependent mechanosensory organ patterning in zebrafish. Science 320:1774–1777

    Article  CAS  PubMed  Google Scholar 

  • Nomura R, Kamei E, Hotta Y, Konishi M, Miyake A, Itoh N (2006) Fgf16 is essential for pectoral fin bud formation in zebrafish. Biochem Biophys Res Commun 347:340–346

    Article  CAS  PubMed  Google Scholar 

  • Noramly S, Grainger RM (2002) Determination of the embryonic inner ear. J Neurobiol 53:100–128

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ohuchi H, Yasue A, Ono K, Sasaoka S, Tomonari S, Takagi A, Itakura M, Noji S, Moriyama K, Nohno T (2005) Identification of cis-element regulating expression of the mouse Fgf10 gene during inner ear development. Dev Dyn 233:177–187

    Article  CAS  PubMed  Google Scholar 

  • Ohyama T, Groves AK, Martin K (2007) The first steps towards hearing: mechanisms of otic placode induction. Int J Dev Biol 51:463–472

    Article  CAS  PubMed  Google Scholar 

  • Ozaki H, Nakamura K, Funahashi J, Ikeda K, Yamada G, Tokano H, Okamura HO, Kitamura K, Muto S, Kotaki H, Sudo K, Horai R, Iwakura Y, Kawakami K (2004) Six1 controls patterning of the mouse otic vesicle. Development 131:551–562

    Article  CAS  PubMed  Google Scholar 

  • Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K, Fritzsch B (2003) Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 227:203–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paxton CN, Bleyl SB, ChapmanSC Schoenwolf GC (2010) Identification of differentially expressed genes in early inner ear development. Gene Expr Patterns 10:31–43

    Article  CAS  PubMed  Google Scholar 

  • Perez SE, Rebelo S, Anderson DJ (1999) Early specification of sensory neuron fate revealed by expression and function of neurogenins in the chick embryo. Development 126:1715–1728

    CAS  PubMed  Google Scholar 

  • Phillips BT, Bolding K, Riley BB (2001) Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction. Dev Biol 235:351–365

    Article  CAS  PubMed  Google Scholar 

  • Pickles JO (2001) The expression of ¢broblast growth factors and their receptors in the embryonic and neonatal mouse inner ear. Hear Res 155:54–62

    Article  CAS  PubMed  Google Scholar 

  • Pickles JO, Chir B (2002) Roles of fibroblast growth factors in the inner ear. Audiol Neurootol 7:36–39

    Article  CAS  PubMed  Google Scholar 

  • Pirvola U, Spencer-Dene B, Xing-Qun L, Kettunen P, Thesleff I, Fritzsch B, Dickson C, Ylikoski J (2000) FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. J Neurosci 20:6125–6134

    CAS  PubMed  Google Scholar 

  • Powles N, Marshall H, Economou A, Chiang C, Murakami A, Dickson C, Krumlauf R, Maconochie M (2004) Regulatory analysis of the mouse Fgf3 gene: control of embryonic expression patterns and dependence upon sonic hedgehog (Shh) signalling. Dev Dyn 230:44–56

    Article  CAS  PubMed  Google Scholar 

  • Raft S, Nowotschin S, Liao J, Morrow BE (2004) Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 131:1801–1812

    Article  CAS  PubMed  Google Scholar 

  • Riazuddin S, Ahmed ZM, Hegde RS, Khan SN, Nasir I, Shaukat U, Butman JA, Griffith AJ, Friedman TB, Choi BY (2011) Variable expressivity of FGF3 mutations associated with deafness and LAMM syndrome. BMC Med Genet 12:21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sánchez-Calderón H, Martín-Partido G, Hidalgo-Sánchez M (2002) Differential expression of Otx2, Gbx2, Pax2, and Fgf8 in the developing vestibular and auditory sensory organs. Brain Res Bull 57:321–332

    Article  PubMed  Google Scholar 

  • Sánchez-Calderón H, Martín-Partido G, Hidalgo-Sánchez M (2004) Otx2, Gbx2, and Fgf8 expression patterns in the chick developing inner ear and their possible roles in otic specification and early innervation. Gene Expr Patterns 4:659–669

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Calderón H, Martín-Partido G, Hidalgo-Sánchez M (2005) Pax2 expression patterns in the developing chick inner ear. Gene Expr Patterns 5:763–773

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Calderón H, Francisco-Morcillo J, Martín-Partido G, Hidalgo-Sánchez M (2007a) Fgf19 expression patterns in the developing chick inner ear. Gene Expr Patterns 7:30–38

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Calderón H, Milo M, León Y, Varela-Nieto I (2007b) A network of growth and transcription factors controls neuronal differentiation and survival in the developing ear. Int J Dev Biol 51:557–570

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Guardado LO, Ferran JL, Mijares J, Puelles L, Rodríguez-Gallardo L, Hidalgo-Sánchez M (2009) Raldh3 gene expression pattern in the developing chicken inner ear. J Comp Neurol 514:49–65

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Guardado LO, Ferran JL, Rodríguez-Gallardo L, Puelles L, Hidalgo-Sánchez M (2011) Meis gene expression patterns in the developing chicken inner ear. J Comp Neurol 519:125–147

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Guardado LO, Puelles L, Hidalgo-Sánchez M (2013) Fgf10 expression patterns in the developing chick inner ear. J Comp Neurol 521:1136–1164

    Article  PubMed  CAS  Google Scholar 

  • Sánchez-Guardado LO, Puelles L, Hidalgo-Sánchez M (2014) Fate map of the chicken otic placode. Development 141:2302–2312

    Article  PubMed  CAS  Google Scholar 

  • Schimmang T (2007) Expression and functions of FGF ligands during early otic development. Int J Dev Biol 51:473–481

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sinkkonen ST, Starlinger V, Galaiya DJ, Laske RD, Myllykangas S, Oshima K, Heller S (2011) Serial analysis of gene expression in the chicken otocyst. J Assoc Res Otolaryngol 12:697–710

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Storey KG, Crossley JM, De Robertis EM, Norris WE, Stern CD (1992) Neural induction and regionalisation in the chick embryo. Development 114:729–741

    CAS  PubMed  Google Scholar 

  • Sweet EM, Vemaraju S, Riley BB (2011) Sox2 and Fgf interact with Atoh1 to promote sensory competence throughout the zebrafish inner ear. Dev Biol 358:113–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tekin M, Hismi BO, Fitoz S, Ozdag H, Cengiz FB, Sirmaci A, Aslan I, Inceoglu B, Yuksel-Konuk EB, Yilmaz ST, Yasun O, Akar N (2007) Homozygous mutations in fibroblast growth factor 3 are associated with a new form of syndromic deafness characterized by inner ear agenesis, microtia, and microdontia. Am J Hum Genet 80:338–344

    Article  CAS  PubMed  Google Scholar 

  • Tekin M, Ozturkmen Akay H, Fitoz S, Birnbaum S, Cengiz FB, Sennaroglu L, Incesulu A, Yuksel Konuk EB, Hasanefendioglu Bayrak A, Senturk S, Cebeci I, Utine GE, Tunçbilek E, Nance WE, Duman D (2008) Homozygous FGF3 mutations result in congenital deafness with inner ear agenesis, microtia, and microdontia. Clin Genet 73:554–565

    Article  CAS  PubMed  Google Scholar 

  • Torres M, Giráldez F (1998) The development of the vertebrate inner ear. Mech Dev 71:5–21

    Article  CAS  PubMed  Google Scholar 

  • 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 340:595–604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vazquez-Echeverría C, Domínguez-Frutos E, Charnay P, Schimmang T, Pujades C (2008) Analysis of mouse kreisler mutants reveals new roles of hindbrain-derived signals in the establishment of the otic neurogenic domain. Dev Biol 322:167–178

    Article  PubMed  CAS  Google Scholar 

  • Vendrell V, Carnicero E, Giráldez F, Alonso MT, Schimmang T (2000) Induction of inner ear fate by FGF3. Development 127:2011–2029

    CAS  PubMed  Google Scholar 

  • Vendrell V, Vazquez-Echeverría C, López-Hernández I, Alonso BD, Martínez S, Pujades C, Schimmang T (2013) Roles of Wnt8a during formation and patterning of the mouse inner ear. Mech Dev 130:160–168

    Article  CAS  PubMed  Google Scholar 

  • Walshe J, Mason I (2003) Fgf signalling is required for formation of cartilage in the head. Dev Biol 264:522–536

    Article  CAS  PubMed  Google Scholar 

  • Walshe J, Maroon H, McGonnell IM, Dickson C, Mason I (2002) Establishment of hindbrain segmental identity requires signaling by FGF3 and FGF8. Curr Biol 12:1117–1123

    Article  CAS  PubMed  Google Scholar 

  • Whitfield TT, Hammond KL (2007) Axial patterning in the developing vertebrate inner ear. Int J Dev Biol 51:507–520

    Article  CAS  PubMed  Google Scholar 

  • Wilkinson DG, Bhatt S, McMahon AP (1989) Expression pattern of the FGF-related proto-oncogene int-2 suggests multiple roles in fetal development. Development 105:131–136

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wu DK, Oh SH (1996) Sensory organ generation in the chick inner ear. J Neurosci 16:6454–6462

    CAS  PubMed  Google Scholar 

  • Yamada T, Placzek M, Tanaka H, Dodd J, Jessell TM (1991) Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64:635–647

    Article  CAS  PubMed  Google Scholar 

  • Zelarayan LC, Vendrell V, Alvarez Y, Dominguez-Frutos E, Theil T, Alonso MT, Maconochie M, Schimmang T (2007) Differential requirements for FGF3, FGF8 and FGF10 during inner ear development. Dev Biol 308:379–391

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M, Ornitz DM (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281:15694–15700

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng W, Huang L, Wei ZB, Silvius D, Tang B, Xu PX (2003) The role of Six1 in mammalian auditory system development. Development 130:3989–4000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank the members of our scientific group for helpful discussions. This work was supported by grants BFU2010-19461 and GR10152 (Gobierno de Extremadura) to Matías Hidalgo-Sánchez, BFU2005-09378-C02-01 and BFU2008-04156 to Luis Puelles, and NIH DC011819 to Gary C. Schoenwolf. L-O.S-G received a Junta-de-Extremadura predoctoral fellowship (PRE/08031).

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Correspondence to Matías Hidalgo-Sánchez.

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Olaya-Sánchez, D., Sánchez-Guardado, L.Ó., Ohta, S. et al. Fgf3 and Fgf16 expression patterns define spatial and temporal domains in the developing chick inner ear. Brain Struct Funct 222, 131–149 (2017). https://doi.org/10.1007/s00429-016-1205-1

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  • DOI: https://doi.org/10.1007/s00429-016-1205-1

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