The molecular biology of ear development - "Twenty years are nothing"

International Journal of Developmental Biology

Volumn 51, Issue 6-7, 2007, Pages 429-438

  Giraldez, Fernando ^a   Fritzsch, Bernd ^b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell fate; Evolution; Hair cell; Morphogenesis; Otic neuron; Patterning; Regeneration

Indexed keywords

CELL POLARITY; COCHLEA; EAR; ECTODERM; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE INTERACTION; GENEALOGY; HAIR CELL; HUMAN; MECHANOTRANSDUCTION; MESODERM; MOLECULAR BIOLOGY; MORPHOGENESIS; NONHUMAN; ORGANOGENESIS; PRIORITY JOURNAL; REVIEW; SENSE ORGAN;

ANIMALS; BODY PATTERNING; EAR; EMBRYO, MAMMALIAN; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; MODELS, BIOLOGICAL; MOLECULAR BIOLOGY; MORPHOGENESIS;

VERTEBRATA;

EID: 36049010017     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.072390fg     Document Type: Review

References (105)

1. ABELLO, G and ALSINA, B. (2007) Establishment of a proneural field in the inner ear. Int J Dev Biol 51: 483-493. DOI: 10.1387/ijdb.072343ga
2. ADAM, J., MYAT, A., LE ROUX, I., EDDISON, M., HENRIQUE, D., ISH-HOROWICZ, D. and 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: 4645-54.
3. ALSINA, B., GIRALDEZ, F. and VARELA-NIETO, I. (2003). Growth factors and early development of otic neurons: interactions between intrinsic and extrinsic signals. Curr Top Dev Biol 57: 177-206.
4. 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. 267:119-34.
5. ARENDT, D., TESSMAR-RAIBLE, K., SNYMAN, H., DORRESTEIJN, A.W. and WITTBRODT, J. (2004). Ciliary photoreceptors with a vertebrate-type opsin in an invertebrate brain. Science 306: 869-71.
6. ARD M.D., MOREST, D.K. and HAUGER, S.H. (1985) Trophic interactions between the cochleovestibular ganglion of the chick embryo and its synaptic targets in culture Neuroscience. 16:151-70.
7. BERMINGHAM, N.A., HASSAN, B.A., PRICE, S.D., VOLLRATH, M.A., BEN-ARIE, N., EATOCK, R.A., BELLEN, H.J., LYSAKOWSKI, A. and ZOGHBI, H.Y. (1999). Math1: an essential gene for the generation of inner ear hair cells. Science 284: 1837-41.
8. BERTRAND, N., CASTRO, D.S. and GUILLEMOT, F. (2002). Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3: 517-30.
9. BIBEL, M., HOPPE, E. and BARDE, Y.A. (1999). Biochemical and functional interactions between the neurotrophin receptors trk and p75NTR. EMBO J 18: 616-22.
10. BOK, J., CHANG, W. and WU, D.K. (2007) Patterning and morphogenesis of the vertebrate inner ear. Int J Dev Biol 51: 521-533. DOI: 10.1387/ijdb.072381jb
11. BOYER, L.A., LEE, T.I., COLE, M.F., JOHNSTONE, S.E., LEVINE, S.S., ZUCKER, J.P., GUENTHER, M.G., KUMAR, R.M., MURRAY, H.L., JENNER, R.G. et al. (2005). Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122: 947-56.
12. CAMARERO, G., AVENDAÑO, C., FERNANDEZ-MORENO, C., VILLAR, A., CONTRERAS, J., DE PABLO, F., PICHEL, J.G. and VARELA-NIETO, I. (2001). Delayed inner ear maturation and neuronal loss in postnatal Igf-1-deficient mice. J Neurosci 21: 7630-41.
13. CAMARERO, G., LEON, Y., GOROSPE, I., DE PABLO, F., ALSINA, B., GIRALDEZ, F. and VARELA-NIETO, I. (2003). Insulin-like growth factor 1 is required for survival of transit-amplifying neuroblasts and differentiation of otic neurons. Dev Biol 262: 242-53.
14. CHEN, P., JOHNSON, J.E., ZOGHBI, H.Y. and 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.
15. CHISAKA, O. and CAPECCHI, M.R. (1991) Regionally restricted developmental defects resulting from targeted disruption of the mouse homeobox gene hox-1.5. Nature 350: 473-9.
16. COLE, L.K., LE ROUX, I., NUNES, F., LAUFER, E., LEWIS, J. and WU, D.K. (2000). Sensory organ generation in the chicken inner ear: contributions of bone morphogenetic protein 4, serrate1 and lunatic fringe. J Comp Neurol 424: 509-20.
17. CREMERS, C.W.R.J., GRAHAM, J., PARVING, A. and RUBEN, R.J. (1988) Biology of sensorineural hearing loss in children. Report of symposium held in Holte, Denmark, 14-17 June, 1987. Int. J. Pediatric Otorhynolayrngology 15: 1-15
18. D'AMICO-MARTEL, A. (1982) Temporal patterns of neurogenesis in avian cranial sensory and autonomic ganglia. Am J Anat. 163:351-372.
19. D'AMICO-MARTEL, A. and NODEN, D.M. (1983) Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. Am J Anat. 166:445-68.
20. DAUDET, N. and LEWIS, J. (2005). Two contrasting roles for Notch activity in chick inner ear development: specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132: 541-51.
21. DU, X., JENSEN, P., GOLDOWITZ, D. and HAMRE, K.M. (2007). Wild-type cells rescue genotypically Math1-null hair cells in the inner ears of chimeric mice. Dev Biol 305: 430-8.
22. EBERL, D.F. and BOEKHOFF-FALK, G. (2007) Development of Johnston's organ in Drosophila. Int J Dev Biol 51: 679-687. DOI: 10.1387/ijdb.072364de
23. FEKETE, D.M. (1996). Cell fate specification in the inner ear. Curr Opin Neurobiol 6: 533-41.
24. FEKETE, D.M. and WU, D.K. (2002) Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol. 12:35-42.
25. FEKETE, D.M. and CAMPERO, A.M. (2007) Axon guidance in the inner ear. Int J Dev Biol 51: 549-556. DOI: 10.1387/ijdb.072341df
26. FRIEDMAN, L.M., DROR, A.A. and AVRAHAM, K.B. (2007) Mouse models to study inner ear development and hereditary hearing loss. Int J Dev Biol 51: 609-631. DOI: 10.1387/ijdb.072365lf
27. FRITZSCH, B., BARALD, K. and LOMAX, M. (1998). Early embryology of the vertebrate ear. In Springer Handbook of Auditory Research. Vol XII. Development of the Auditory System.. (ed. RUBEL, E. W.POPPER, A. N. and FAY, R. R.). Springer Verlag, New York, pp.80-145.
28. FRITZSCH, B., BEISEL, K.W. and BERMINGHAM, N.A. (2000). Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. Neuroreport 11: R35-44.
29. FRITZSCH, B., BEISEL, K.W., JONES, K., FARINAS, I., MAKLAD, A., LEE, J. and REICHARDT, L.F. (2002). Development and evolution of inner ear sensory epithelia and their innervation. J Neurobiol 53: 143-56.
30. FRITZSCH, B., MATEI, V.A., NICHOLS, D.H., BERMINGHAM, N., JONES, K., BEISEL, K.W. and WANG, V.Y. (2005). Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. Dev Dyn 233: 570-83.
31. FRITZSCH, B., BEISEL, K.W. and HANSEN, L.A. (2006). The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration? Bioessays 28: 1181-93.
32. FRITZSCH, B., BEISEL, K., PAULEY, S. and SOUKUP, G. (2007) Molecular evolution of the vertebrate mechanosensory cell and ear. Int J Dev Biol 51: 663-678. DOI: 10.1387/ijdb.072367bf
33. GALLAGHER, B.C, HENRY, JJ and GRAINGER, R.M. (1996). Inductive processes leading to inner ear formation during Xenopus development. Dev Biol. 10:95-107
34. GARCIA-BELLIDO, A. Genetic analysis of the achaete-scute system of Drosophila melanogaster. Genetics 91, 491-520 (1979).
35. GHYSEN, A. and DAMBLY-CHAUDIERE, C. (2000). A genetic programme for neuronal connectivity. Trends Genet 16: 221-6.
36. GÓMEZ-SKARMETA, J.L., CAMPUZANO, S. and MODOLELL, J. (2003) Half a century of neural prepatterning: the story of a few bristles and many genes. Nat Rev Neurosci. 2003 Jul;4(7):587-98.
37. GOROSPE, I., SANCHEZ-GALIANO, S., CANON, S., CAMARERO, G., CONTRERAS, J., CEDIEL, R. et al. (2004). Trophic effects of insulin-like growth factor-I (IGF-I) in the inner ear. Hear Res 196: 19-25.
38. GRAHAM V, KHUDYAKOV J, ELLIS P, PEVNY L (2003) SOX2 functions to maintain neural progenitor identity. Neuron 39:749-65.
39. GROVES, A.K. and Bronner-Fraser, M. (2000) Competence, specification and commitment in otic placode induction. Development 127:3489-99.
40. GURDON, J.B. (1987) Embryonic induction - molecular prospects. Development 99:285-306.
41. HAGSTROM, S.A., PAUER, G.J., REID, J., SIMPSON, E., CROWE, S., MAUMENEE, I.H.,AND TRABOULSI, E.I. (2005) SOX2 mutation causes anophthalmia, hearing loss and brain anomalies. Am J Med Genet A. 138:95-8.
42. HARRISON (1945) Relations of symmetry in the developing embryo. Trans. Conn. Acad. Arts Sci. USA 22: 238-247
43. HEMOND, S.G. and MOREST, D.K. (1992) Tropic effects of otic epithelium on cochleo-vestibular ganglion fiber growth in vitro. Anat Rec. 232:273-84.
44. HENRIQUE, D,. Adam,J., Myat, A., Chitnis, A., Lewis, J. and, Ish-Horowicz D (1995) Expression of a Delta homologue in prospective neurons in the chick. Nature 29;375:787-90.
45. JACOB, F. (1947) Quoted by Gilbert (1997) Developmental Biology. Ch2, page 47, Sinauer Associates Inc. Publishers, Sunderland, Massachusetts.
46. JACOB, F. (1976) The Logic of Life by François Jacob, English edition by Princeton University Press 1993
47. JACOBSON, A.G. (1966) Inductive processes in embryonic development. Science 152: 25-34
48. JAENISCH, R., HOCHEDLINGER, K., BLELLOCH, R., YAMADA, Y., BALDWIN, K. and EGGAN, K. (2004) Nuclear cloning, epigenetic reprogramming and cellular differentiation. Cold Spring Harb Symp Quant Biol. 69:19-27.
49. KAGEYAMA, R., OHTSUKA, T., HATAKEYAMA, J. and OHSAWA, R. (2005). Roles of bHLH genes in neural stem cell differentiation. Exp Cell Res 306: 343-8.
50. KAGEYAMA, R., OHTSUKA, T. and KOBAYASHI, T. (2007). The Hes gene family: repressors and oscillators that orchestrate embryogenesis. Development 134: 1243-51.
51. KARIS, A., PATA, I., VAN DOORNINCK, J.H., GROSVELD, F., DE ZEEUW, C.I., DE CAPRONA, D. and FRITZSCH, B. (2001). Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429: 615-30.
52. KELLER, R. (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science. 298:1950-4.
53. KELLEY, M.W. (2007). Cellular commitment and differentiation in the organ of Corti. Int J Dev Biol 51: 571-583. DOI: 10.1387/ijdb.072388mk
54. KELLY, M. and CHEN, P. (2007) Shaping the mammalian auditory sensory organ by the planar cell polarity pathway. Int J Dev Biol 51: 535-547. DOI: 10.1387/ ijdb.072344mk
55. 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.
56. KIM, W.Y., FRITZSCH, B., SERLS, A., BAKEL, L.A., HUANG, E.J., REICHARDT, L.F., BARTH, D.S. and LEE, J.E. (2001). NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128: 417-26.
57. KOUNDAKJIAN, E., APPLER, J. and GOODRICH, L. (2007) Transgenic Mouse: a Tool to Fate Map Cells in the Mouse Inner Ear. ARO 2007, Abstract 962
58. LEWIS, J. (1991) Rules for the production of sensory cells. In: Regeneration of vertebrate sensory receptor cells. Ciba Found Symp. 160:25-39; discussion 40-53. Wiley, Chicester,
59. LIU J.J., SHIN, J.H., HYRC, K.L., LIU, S., LEI, D., HOLLEY, M.C. and BAO, J. (2006) Stem cell therapy for hearing loss: Math1 overexpression in VOT-E36 cells. Otol Neurotol. 27:414-421.
60. MA, Q., CHEN, Z., DEL BARCO BARRANTES, I., DE LA POMPA, J.L. and ANDERSON, D.J. (1998). Neurogenic is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20: 469-82.
61. MA, Q., ANDERSON, D.J. and 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: 129-43.
62. MANTELA, J., JIANG, Z., YLIKOSKI, J., FRITZSCH, B., ZACKSENHAUS, E. and PIRVOLA, U. (2005). The retinoblastoma gene pathway regulates the postmitotic state of hair cells of the mouse inner ear. Development 132: 2377-88.
63. MARTINEZ-MONEDERO, R. and EDGE, A.S.B. (2007) Stem cells for the replacement of inner ear neurons and hair cells. Int J Dev Biol 51: 655-661. DOI: 10.1387/ijdb.072372rm
64. MCGINNIS W, HART CP, GEHRING WJ and RUDDLE FH. (1984) Molecular cloning and chromosome mapping of a mouse DNA sequence homologous to homeotic genes of Drosophila. Cell 38(3):675-80
65. MILLIMAKI, B.B., SWEET, E.M., DHASON, M.S. and RILEY, B.B. (2007) Zebrafish Atoh1 genes: classic proneural activity in the inner ear and regulation by Fgf and Notch. Development 134: 295-305.)
66. MYAT A, HENRIQUE D, ISH-HOROWICZ D. and LEWIS J. (1996) A chick homologue of Serrate and its relationship with Notch and Delta homologues during central neurogenesis. Dev Biol. 174:233-47.
67. NAYAK, G.D., RATNAYAKA, H.S.K., GOODYEAR, R.J. and RICHARDSON, G.P. (2007) Development of the hairbundle and mechanotransduction. Int J Dev Biol 51: 597-608. DOI: 10.1387/ijdb.072392gn
68. NEVES, J. KAMAID, A., ALSINA, B. and 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. 503:487-500.
69. OHYAMA, T., GROVES, A.K. and MARTIN, K. (2007) The first steps towards hearing: mechanisms of otic placode induction. Int J Dev Biol 51:463-472. DOI: 10.1387/ijdb.072320to
70. PAULEY, S., LAI, E. and FRITZSCH, B. (2006). Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Dev Dyn 235: 2470-82.
71. PAULEY, S., WRIGHT, T.J., PIRVOLA, U., ORNITZ, D., BEISEL, K. and FRITZSCH, B. (2003). Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 227: 203-15.
72. PIRVOLA, U., ZHANG, X., MANTELA, J., ORNITZ, D.M. and YLIKOSKI, J. (2004). Fgf9 signaling regulates inner ear morphogenesis through epithelial-mesenchymal interactions. Dev Biol 273: 350-60.
73. RAMÓN Y CAJAL, S (1904) trad: Texture of the Nervous System of Man and the Vertebrates Cajal, S. R.; Pasik, Pedro; Pasik, Tauba ISBN: 3211832025 Editorial: Springer Verlag Wien, 2002
74. a Ed., 1940
75. RAPHAEL, Y., KIM, Y.H., OSUMI, Y. and IZUMIKAWA, M. (2007) Non-sensory cells in the deafened organ of Corti: approaches for repair. Int J Dev Biol 51: 649-654. DOI: 10.1387/ijdb.072370yr
76. RETZIUS (1884). Das Gehörorgan der Wirbeltiere: II. Das Gehörorgan der Amnioten. Stockholm: Samson und Wallin.
77. REX, M., ORME, A., UWANOGHO, D., TOINTON, K., WIGMORE, P.M., SHARPE. P.T. and SCOTTING P.J. (1997) Dynamic expression of chicken Sox2 and Sox3 genes in ectoderm induced to form neural tissue. Dev Dyn. 209:323-32
78. RICCOMAGNO, M.M., MARTINU, L., MULHEISEN, M., WU, D.K. and EPSTEIN, D.J. (2002). Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16: 2365-78.
79. RICCOMAGNO, M.M., TAKADA, S. and EPSTEIN, D.J. (2005). Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev 19: 1612-23.
80. ROCHA-SANCHEZ, S.M.S. and BEISEL, K.W. (2007) Pocket proteins and cell cycle regulation in inner ear development. Int J Dev Biol 51: 585-595. DOI: 10.1387/ijdb.072387sr
81. ROMAND, R. (1992) Development of Auditory and Vestibular systems 2. Romand, R. ed. Elsevier, Oxford, 1992
82. RUBEL, EW (1984) Ontogeny of auditory system function. Annu Rev Physiol. 46: 213-29.
83. RUBEL, E.W. and FRITZSCH, B. (2002). Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51-101.
84. SAIKI, R.K., Scharf, S., Faloona, F., Mullis, K.B., Horn, G.T., Erlich, H.A. and Arnheim, N. (1985) Enzymatic amplification of beta-globin genomic sequences and restriction site analysis for diagnosis of sickle cell anemia. Science 230:1350-1354.
85. SÁNCHEZ-CALDERÓN, H., MILO, M., LEÓN, Y. and VARELA-NIETO, I. (2007) A network of growth and transcription factors controls neuronal differentation and survival in the developing ear. Int J Dev Biol 51: 557-570. DOI: 10.1387/ ijdb.072373hs
86. SATO, T., DOI, K., TANIGUCHI, M., YAMASHITA, T., KUBO, T. and TOHYAMA, M. (2006). Progressive hearing loss in mice carrying a mutation in the p75 gene. Brain Res 1091: 224-34.
87. SATOH, T. and FEKETE, D.M. (2005). Clonal analysis of the relationships between mechanosensory cells and the neurons that innervate them in the chicken ear. Development 132: 1687-97.
88. SCHIMMANG, T. (2007) Expression and functions of FGF ligands during early otic development. Int J Dev Biol 51: 473-481. DOI: 10.1387/ijdb.072334ts
89. SCHNEIDER-MAUNOURY, S. and PUJADES, C. (2007) Hindbrain signals in otic regionalization: walk on the wild side. Int J Dev Biol 51: 495-506. DOI: 10.1387/ ijdb.072345ss
90. nd. ed Cambridge University Press. Cambridge, U.K.
91. STONE, J.S. and COTANCHE, D.A. Hair cell regeneration in the avian auditory epithelium (2007) Int J Dev Biol 51: 633-647. DOI: 10.1387/ijdb.072408js
92. 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: 447-461. DOI: 10.1387/ijdb.072327as
93. TAN, J. and SHEPHERD, R.K. (2006). Aminoglycoside-induced degeneration of adult spiral ganglion neurons involves differential modulation of tyrosine kinase B and p75 neurotrophin receptor signaling. Am J Pathol 169: 528-43
94. TESSAROLLO, L., COPPOLA, V. and FRITZSCH, B. (2004). NT-3 replacement with brain-derived neurotrophic factor redirects vestibular nerve fibers to the cochlea. J Neurosci 24: 2575-84.
95. TODI, S.V., FRANKE, J.D., KIEHART, D.P. and EBERL, D.F. (2005). Myosin VIIA defects, which underlie the Usher 1B syndrome in humans, lead to deafness in Drosophila. Curr Biol 15: 862-8.
96. TORRES, M and GIRALDEZ, F.(1998).The development of the vertebrate inner ear. Mech Dev 71: 5-21
97. VON KUPFFER, C. (1895). Studien zur vergleichenden Entwicklungsgeschichte des Kopfes der Kraniolen, Vol 3. Die Entwicklung der Kopfnerven van Ammocoetes planen. Lehmann. Munich, pp. 80
98. WHITE, P.M., DOETZLHOFER, A., LEE, Y.S., GROVES, A.K. and SEGIL, N. (2006). Mammalian cochlear supporting cells can divide and trans-differentiate into hair cells. Nature 441: 984-7.
99. WHITEFIELD, T., HADDON, C. and LEWIS, J. (1997) Intercellular signals and cell-fate choices in the developing inner ear: origins of global and of fine-grained pattern. Semin Cell Dev Biol. 1997 Jun;8(3):239-247
100. WHITFIELD, T.T. and HAMMOND, K.L. (2007) Axial patterning in the vertebrate inner ear. Int J Dev Biol 51: 507-520. DOI: 10.1387/ijdb.072380tw
101. WOLPERT, L. (2002) Principles of Deveopment, Oxford Univesity Press, Oxford, U.K.
102. WOODS, C., MONTCOUQUIOL, M. and KELLEY, M.W. (2004). Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 7: 1310-8.
103. WU, D.K. and OH, S.H.(1996) Sensory organ generation in the chick inner ear. J Neurosci. 1996 Oct 15;16(20):6454-62
104. YNTEMA (1933) Experiments on the determination of the ear ectoderm in the embryo of Amblyostoma Punctatum. J. Exp. Zool. 65: 317-357
105. YNTEMA (1955) An analysis of induction of the ear from foreign ectoderm in the salamander embryo. J. Exp. Zool. 113: 211-244.