Cell fate specification in the inner ear

Current Opinion in Neurobiology

Volumn 6, Issue 4, 1996, Pages 533-541

  Fekete, Donna M ^a  

^a BOSTON COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTROPHIN;

CELL TYPE; GENE EXPRESSION; HAIR CELL; INNER EAR; MOLECULAR GENETICS; MOUSE; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSE ORGAN; ZEBRA FISH;

EID: 0030218736     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(96)80061-4     Document Type: Article

References (59)

1. Fritzsch B, Barald KF, Lomax MI. Early embryology of the vertebrate ear. of outstanding interest Auditory Physiol. 1996; This is an excellent comprehensive review of ear development. Topics covered include comparative anatomy, classical embryology, genes involved in ear development and deafness, diversification of the otic epithelium and the development of ear innervation.
2. Corwin JT, Warchol ME, Kelley MW. Hair cell development. Curr Biol. 3:1993;32-37.
3. Gallagher BC, Henry JJ, Grainger RM. Inductive processes leading to inner ear formation during Xenopus development. Dev Biol. 175:1996;95-107.
4. Gurdon JB. Community effects and related phenomena in development. Cell. 75:1993;831-834.
5. Jessell TM, Melton DA. Diffusible factors in vertebrate embryonic induction. Cell. 68:1992;257-270.
6. Gurdon JB. The generation of diversity and pattern in animal development. Cell. 68:1992;185-199.
7. of special interest Haddon CH, Lewis J. Early ear development in the embryo of the zebrafish, Danio rerio. of outstanding interest J Comp Neurol. 365:1996;113-128 An important baseline study of normal inner ear development in the zebrafish required for interpretation of the mutant phenotypes found in the large-scale screens performed in Boston [37] and in Tübingen [36].
8. Lewis J. Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol. 6:1996;3-10.
9. Ekker M, Akimenko MA, Bremiller R, Westerfield M. Regional expression of three homeobox transcripts in the inner ear of zebrafish embryos. Neuron. 9:1992;27-35.
10. Akimenko MA, Ekker M, Wegner J, Lin W, Westerfield M. Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci. 14:1994;3475-3486.
11. Stadler HS, Solursh M. Characterization of the homeobox-containing gene GH6 identifies novel regions of homeobox gene expression in the developing chick embryo. Dev Biol. 161:1994;251-262.
12. Deitcher DL, Fekete DM, Cepko CL. Asymmetric expression of a novel homeobox gene in vertebrate sensory organs. J Neurosci. 14:1994;486-498.
13. Li Y, Allende ML, Finkelstein R, Weinberg ES. Expression of two zebrafish orthodenticle-related genes in the embryonic brain. Mech Dev. 48:1994;229-244.
14. Simeone A, Acampora D, Mallamaci A, Storaiuolo A, D'Apice MR, Nigro V, Boncinelli E. A vertebrate gene related to orthodenticle contains a homeodomain of the bicoid class and demarcates anterior neuroectoderm in the gastrulating mouse embryo. EMBO J. 12:1993;2735-2747.
15. Rinkwitz-Brandt S, Justus M, Oldenettel I, Arnold H-H, Bober E. Distinct temporal expression of mouse Nkx-5.1 and Nkx-5.2 homeobox genes during brain and ear development. of special interest Mech Dev. 52:1995;371-381 Nkx-5.1 expression is compared side-by-side in 20 somite stage whole-mount mouse embryos to the expression patterns of two other genes, Pax-2 and sek. The expression domains of the three genes are clearly different in the otic vesicle, and demonstrate unequivocally that the ear is heterogeneous with respect to gene transcription at this stage.
16. Gaunt SJ, Blum M, DeRobertis EM. Expression of the mouse goosecoid gene during mid-embryogenesis may mark mesenchymal cell lineages in the developing head, limbs and body wall. Development. 117:1993;769-778.
17. Krauss S, Johansen T, Korzh V, Fjose A. Expression of the zebrafish paired box gene pax[zf-b] during early neurogenesis. Development. 113:1991;1193-1206.
18. Barald KF, Lindberg KH, Hardiman K, Kavka AI, Lewis JE, Victor JC, Gardner CA, Poniatowski A. Immortalized cell lines from embryonic avian and murine otocysts: tools for molecular studies of the developing inner ear. Int J Dev Neurosci. 1996;. in press.
19. McKay IJ, Lewis J, Lumsden A. The role of FGF-3 in early inner ear development: an analysis in normal and kreisler mutant mice. of outstanding interest Dev Biol. 174:1996;370-378 The expression of FGF-3 is described in normal and kreisler mutant mice. A new domain of expression is reported: the entire otic field was shown to express FGF-3 mRNA prior to thickening of the otic placode. At slightly later stages, FGF-3 was expressed in the anteroventrolateral part of the otic vesicle. Interestingly, the expression domain of FGF-3 at the otic vesicle stage showed a pronounced shift in position in kreisler compared to normals, occupying instead an anteroventromedial position.
20. Hollyday M, McMahon JA, McMahon AP. Wnt expression patterns in chick embryo nervous system. Mech Dev. 52:1995;9-25.
21. McGrew LL, Otte A, Moon R. Analysis of Xwnt-4 in embryos of Xenopus laevis: a Wnt family member expressed in the brain and floor plates. Development. 115:1992;463-473.
22. Wu DK, Oh S-H. Sensory organ generation in the chick inner ear. of outstanding interest J Neurosci. 1996; This important study is a systematic analysis of sensory organ formation in the chick inner ear using molecular markers, including BMP-4, Msx-1 and p75NGF-R. Used in combination, these markers can distinguish the different sensory organs even when they are still contiguous patches within the otic epithelium, well in advance of overt sensory organ differentiation. As a result, sensory organs were identifiable much earlier than in previous studies using histological criteria [28]. The study comes to a new conclusion about the timing and spatial origin of the eight different sensory organs in the chick ear.
23. of special interest Oh SH, Johnson R, Wu DK. Differential expression of bone morphogenic proteins in the developing vestibular and auditory sensory organs. of outstanding interest J Neurosci. 1996; This paper is a companion [22], extending the study of BMP expression in the developing inner ear to and beyond histological differentiation of the sensory organs. Spatial and temporal differences in expression of BMP-4, BMP-5 and BMP-7 define different, partially overlapping domains of the developing otic vesicle at early stages. At later stages, one of the interesting conclusions is that the auditory and vestibular organs differ in their expression and segregation of the different BMPs to different tissues (sensory organ versus non-sensory) and/or cell types (hair cells versus supporting cells).
24. Robertson K, Mason I. Expression in ret in the chicken embryo suggests roles in regionalisation of the vagal neural tube and somites and in development of multiple neural crest and placodal lineages. Mech Dev. 53:1995;329-344.
25. Artavanis-Tsakonas S, Matsuno K, Fortini ME. Notch signalling. Science. 267:1995;225-232.
26. Ingham PW, Martinez Arias A. Boundaries and fields in early embryos. Cell. 68:1992;221-235.
27. Lawrence PA, Struhl G. Morphogens, compartments and pattern: lessons from Drosophila? of outstanding interest Cell. 85:1996;951-961 An excellent review of the concepts and principles underlying the hypothesis that compartments and boundaries can direct pattern formation within embryonic fields by determining the source of secreted morphogens. The focus is on the developing wing of Drosophila as a model system to exemplify the principles.
28. Knowlton VY. Correlation of the development of membranous and bony labyrinths, acoustic ganglia, nerves, and brain centers in the chick embryo. J Morphol. 121:1967;179-208.
29. Von Bartheld CS, Patterson SL, Heuer JG, Wheeler EF, Bothwell M, Rubel EW. Expression of nerve growth factor (NGF) receptors in the developing inner ear of chick and rat. Development. 113:1991;455-470.
30. Hallbook F, Ibanez CF, Ebendal T, Personn H. Cellular localization of brain-derived neurotrophic factor and neurotrophin-3 mRNA expression in the early chicken embryo. Eur J Neurosci. 5:1993;1-14.
31. Myat A, Henrique D, Ish-Horowicz D, Lewis J. A chick homologue of Serrate, and its relationship with Notch and Delta homologues during central neurogenesis. Dev Biol. 174:1996;233-247.
32. Swanson GJ, Howard M, Lewis J. Epithelial autonomy in the development of the inner ear of a bird embryo. Dev Biol. 137:1990;243-257.
33. Mark M, Lufkin T, Vonesch JL, Ruberte E, Olivo JC, Dolle P, Gorry P, Lumsden A, Chambon P. Two rhombomeres are altered in Hoxa-1 mutant mice. Development. 119:1993;319-338.
34. Chisaka O, Musci TS, Capecchi MR. Developmental defects of the ear, cranial nerves and hindbrain resulting from targeted disruption of the mouse homeobox gene Hox-1.6. Nature. 355:1992;516-520.
35. Mansour SL, Goddard JM, Capecchi MR. Mice homozygous for a targeted disruption of the proto-oncogene int-2 have developmental defects in the tail and inner ear. Development. 117:1993;13-28.
36. Whitfield TT, Granato M, Van Eeden FJM, Schach U, Brand M, Furutani-Seiki M, Haffter P, Hammerschmidt M, Heisenberg C-P, Jiang Y-J, et al. Mutations affecting development of the zebrafish inner ear and lateral line. of outstanding interest Development. 1996; Inner ear mutants that were found in the course of the Tübingen large-scale screen for developmental mutants in the zebrafish embryo are described. Although the screens were performed without being able to visualize the sensory organs directly, subsequent analysis using rhodamine-phalloidin or in situ hybridization with mshC or otx-1 provides key information. Mutants in ear shape, size and morphogenesis, numbers of otoliths, and numbers and types of sensory organs are described.
37. Malicki J, Schier A, Krezel LS, Stemple DL, Neuhauss SCF, Stainier DYR, Abdelilah S, Rangini Z, Zwartkruis F, Driever W. Mutations affecting development of the zebrafish ear. of outstanding interest Development. 1996; Inner ear mutants that were found in the course of the Boston large-scale screen for developmental mutants in the zebrafish embryo are described. Screens were performed without being able to visualize the sensory organs directly. A few mutants were subsequently analyzed with the sensory organ marker msxC, although most have yet to be studied in detail with respect to the number or type of sensory organs formed. Mutants are described that affect specification of the otic field, ear morphogenesis and growth, and the number of otoliths.
38. Meinhardt H. A boundary model for pattern formation in vertebrate limbs. J Embryol Exp Morphol. 76:1983;115-137.
39. Meinhardt H. Cell determination boundaries as organizing regions for secondary embryonic fields. Dev Biol. 96:1983;375-385.
40. Martin G. Why thumbs are up. Nature. 374:1995;410-411.
41. Vincent J-P, Lawrence PA. It takes three to distalize. Nature. 372:1994;132-133.
42. Keynes R, Krumlauf R. Hox genes and regionalization of the nervous system. Annu Rev Neurosci. 17:1994;109-132.
43. Cotanche DA. Regeneration of hair cell stereociliary bundles in the chick cochlea following severe acoustic trauma. Hear Res. 18:1987;29-39.
44. Corwin JT, Jones JE, Katayama A, Kelley MW, Warchol ME. Hair cell regeneration: the identities of progenitor cells, potential triggers and instructive cues. Bock GR, Whelan J. Regeneration of Vertebrate Sensory Receptor Cells. 1991;103-130 Wiley, Chichester, England.
45. Lewis J. Rules for the production of sensory cells. Bock GR, Whelan J. Regeneration of Vertebrate Sensory Receptor Cells. 1991;25-53 Wiley, Chichester, England.
46. Katayama A, Corwin JT. Cell production in the chicken cochlea. J Comp Neurol. 281:1989;129-135.
47. Goodyear R, Holley M, Richardson G. Hair and supporting-cell differentiation during the development of the avian inner ear. of outstanding interest J Comp Neurol. 351:1995;81-93 A spatial and temporal comparison between the onset of differentiation of hair cells and supporting cells in three sensory organs of the chick ear. Hair cells were identified with antibodies against the 275 kDa hair cell antigen. Supporting cells were labelled with an antibody directed against an extracellular component of the tectorial membrane (in cochlea) or the otolith (in saccule and utricle, only). Because hair cells were not always seen to develop first, alternative variants of a lateral inhibitory model of cell fate specification were proposed. Computerized versions of these models are available from the authors upon request.
48. Chitnis A, Henrique D, Lewis J, Ish-Horowicz I, Kintner C. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogenic gene Delta. Nature. 375:1995;761-766.
49. Henrique D, Adam J, Myat A, Chitnis A, Lewis J, Ish-Horowicz D. Expression of a Delta homologue in prospective neurons in the chick. Nature. 375:1995;787-790.
50. Conlon RA, Reaume AG, Rossant J. Notch1 is required for the coordinate segmentation of somites. Development. 121:1995;1533-1545.
51. Ard MD, Morest DK. Cell death during development of the cochlear and vestibular ganglia of the chick. Int J Dev Neurosci. 2:1984;535-547.
52. Ernfors P, Van de Water T, Loring J, Jaenisch R. Complementary roles of BDNF and NT-3 in vestibular and auditory development. of outstanding interest Neuron. 14:1995;1153-1164 Mutant mice lacking the neurotrophin genes BDNF or NT-3, alone or in combination, showed loss of neurons in the inner ear. BDNF(-/-) mice lost 79% of vestibular ganglion neurons, 7% of spiral ganglion neurons (presumed type II ganglion cells), and afferent innervation to the outer hair cells. NT-3(-/-) mice lost 34% of vestibular neurons, 87% of the spiral ganglion neurons (presumed type I ganglion cells) and afferent innervation to the inner hair cells. The results of BDNF(-/-) NT-3(-/-) double mutant mice were additive, with nearly 100% loss of all vestibular and auditory cranial ganglion neurons.
53. Minichiello L, Piehl F, Vazquez E, Schimmang T, Hökfelt T, Represa J, Klein R. Differential effects of combined trk receptor mutations on dorsal root ganglion and inner ear sensory neurons. of outstanding interest Development. 121:1995;4067-4075 Mice were generated that lacked one or two neurotrophin receptors. trkB(-/-) trkC(-/-) double mutant mice showed no further loss of vestibular ganglion neurons than trkB(-/-) single mutant mice, at 56-58% loss. This is despite the fact that trkC(-/-) single mutant mice also show a 16% loss in vestibular ganglion neurons. Thus, some of the vestibular neurons must require both receptors for survival. In contrast, for the cochlear ganglion neurons, the effects of the double knockouts were mostly additive compared to the single knockouts. This supports previous results that suggested that type I spiral ganglion neurons are selectively lost with a trkC knockout, whereas type II spiral ganglion neurons are selectively lost with a trkB knockout (see [55]).
54. Ernfors P, Lee KF, Jaenisch R. Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature. 368:1994;147-150.
55. Schimmang T, Minichiello L, Vazquez E, San Jose I, Giraldez F, Klein R, Represa J. Developing inner ear sensory neurons require TrkB and TrkC receptors for innervation of their peripheral targets. of outstanding interest Development. 121:1995;3381-3391 Loss of VIIIg neurons were found in the inner ears of mice lacking trkB, which encodes the receptor for BDNF, or trkC, which encodes the receptor for NT-3. Ganglion cells were present at embryonic day 14.5, but subsequently died by the first postnatal day. Absence of trkB decreased the number of vestibular neurons by 56%. In addition, trkB(-/-) mice had significant loss of small-bodied spiral ganglion neurons, presumed to be the type II ganglion cells. In support of this, outer hair cell innervation was shown to be absent by birth. Absence of trkC decreased the number of neurons in the vestibular ganglion by 15%, and in the spiral ganglion by 51%. In addition, the cochlear sensory epithelium was disrupted in the trkC(-/-) mice.
56. Jones KR, Farinas I, Backus C, Reichardt LF. Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell. 76:1994;989-999.
57. Farinas I, Jones KR, Backus C, Wang XY, Reichardt LF. Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature. 369:1994;658-661.
58. Fritzsch B. The afferent innervation of the ear: only two neurotrophins (BDNF, NT-3) and two neurotrophin tyrosine kinase receptors (Trk B, Trk C) support afferent innervation of the inner ear. Neural Notes. 1:1996;11-13.
59. Erkman L, McEvilly RJ, Lou L, Ryan AK, Hooshmand F, O'Connell SM, Keithley EM, Rapaport DH, Ryan AF, Rosenfeld MG. Role of transcription factors Brn-3.1 and Brn-3.2 in auditory and visual system development. Nature. 381:1996;603-606.