Axial patterning in the developing vertebrate inner ear

International Journal of Developmental Biology

Volumn 51, Issue 6-7, 2007, Pages 507-520

  Whitfield, Tanya T ^a   Hammond, Katherine L ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

Axial patterning; Axis; Inner ear; Otic vesicle; Otocyst

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; SONIC HEDGEHOG PROTEIN; WNT PROTEIN;

COCHLEA DUCT; ECTODERM; EMBRYO DEVELOPMENT; GENE EXPRESSION; HAIR CELL; HUMAN; INNER EAR; NEUROMERE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RHOMBENCEPHALON; SENSORY NERVE CELL; TISSUE REGENERATION; VERTEBRATE; VESTIBULE AQUEDUCT; ZEBRA FISH;

ANIMALS; BODY PATTERNING; EAR, INNER; EMBRYO, MAMMALIAN; EMBRYO, NONMAMMALIAN; EMBRYONIC INDUCTION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MODELS, BIOLOGICAL; MORPHOGENESIS; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; VERTEBRATES; WNT PROTEINS;

DANIO RERIO; VERTEBRATA;

EID: 36049013648     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: 10.1387/ijdb.072380tw     Document Type: Review

References (86)

1. ABELLÓ, G., KHATRI, S., GIRÁLDEZ, F. and ALSINA, B. (2007). Early regionalization of the otic placode and its regulation by the Notch signaling pathway. Mech. Dev. 124: 631-645.
2. ALSINA, B., ABELLÓ, G., ULLOA, E., HENRIQUE, D., PUJADES, C. and GIRALDEZ, F. (2004). FGF signaling is required for determination of otic neuroblasts in the chick embryo. Dev. Biol. 267: 119-134.
3. ADAMSKA, M., LÉGER, S., BRAND, M., HADRYS, T., BRAUN, T. and BOBER, E. (2000). Inner ear and lateral line expression of a zebrafish Nkx5-1 gene and its downregulation in the ears of FGF8 mutant, ace. Mech. Dev. 97: 161-165.
4. ALVAREZ, Y., ALONSO, M. T., VENDRELL, V., ZELARAYAN, L. C., CHAMERO, P., THEIL, T., BOSL, M. R., KATO, S., MACONOCHIE, M., RIETHMACHER, D. and SCHIMMANG, T. (2003). Requirements for FGF3 and FGF10 during inner ear formation. Development 130: 6329-6338.
5. ARNOLD, J. S., BRAUNSTEIN, E. M., OHYAMA, T., GROVES, A. K., ADAMS, J. C., BROWN, M. C. and MORROW, B. E. (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.
6. BOK, J., BRONNER-FRASER, M. and WU, D. K. (2005). Role of the hindbrain in dorsoventral but not anteroposterior axial specification of the inner ear. Development 132: 2115-2124.
7. BOK, J., DOLSON, D. K., HILL, P., RÜTHER, U., EPSTEIN, D. J. and WU, D. K. (2007). Opposing gradients of Gli repressor and activators mediate Shh signalling along the dorsoventral axis of the inner ear. Development 134: 1713-1722.
8. BRIGANDE, J. V., ITEN, L. E. and FEKETE, D. M. (2000a). A fate map of chick otic cup closure reveals lineage boundaries in the dorsal otocyst. Dev. Biol. 227: 256-270.
9. BRIGANDE, J. V., KIERNAN, A. E., GAO, X., ITEN, L. E. and FEKETE, D. M. (2000b). Molecular genetics of pattern formation in the inner ear: Do compartment boundaries play a role? Proc. Natl. Acad. Sci. 97: 11700-11706.
10. BROWN, A. S., RICCOMAGNO, M. and EPSTEIN, D. J. (2007). Ventral inner ear progenitors are direct targets of hedgehog signaling. Society for Developmental Biology Abstracts, p. 253.
11. BURGESS, S., REIM, G., CHEN, W., HOPKINS, N. and BRAND, M. (2002). The zebrafish spiel-ohne-grenzen (spg) gene encodes the POU domain protein Pou2 related to mammalian Oct4 and is essential for formation of the midbrain and hindbrain, and for pre-gastrula morphogenesis. Development 129: 905-916.
12. CHOO, D., WARD, J., REECE, A., DOU, H., LIN, Z. and GREINWALD, J. (2006). Molecular mechanisms underlying inner ear patterning defects in kreisler mutants. Dev. Biol. 289: 308-317.
13. DEOL, M. S. (1964). The abnormalities of the inner ear in kreisler mice. J. Embryol. exp. Morphol. 12: 475-490.
14. EKKER, S. C., MCGREW, L. L., LAI, C. J., LEE, J. J., VON KESSLER, D. P., MOON, R. T. and BEACHY, P. A. (1995). Distinct expression and shared activities of members of the hedgehog gene family of Xenopus laevis. Development 121: 2337-2347.
15. ELLIES, D. L., STOCK, D. W., HATCH, G., GIROUX, G., WEISS, K. M. and EKKER, M. (1997). Relationship between the genomic organisation and the overlapping embryonic expression patterns of the zebrafish dlx genes. Genomics 45: 580-590.
16. ERNEST, S., RAUCH, G.-J., HAFFTER, P., GEISLER, R., PETIT, C. and NICOLSON, T. (2000). Mariner is defective in myosin VIIA : a zebrafish model for human hereditary deafness. Hum. Mol. Genet. 9: 2189-2196.
17. FRITZSCH, B., BEISEL, K. W., JONES, K., FARIÑAS, I., MAKLAD, A., LEE, J. S. and REICHARDT, L. F. (2002). Development and evolution of inner ear sensory epithelia and their innervation. J. Neurobiol. 53: 143-156.
18. FRITZSCH, B., SIGNORE, M. and SIMEONE, A. (2001). Otx1 null mutant mice show partial segregation of sensory epithelia comparable to lamprey ears. Dev. Genes Evol. 211: 388-396.
19. HADDON, C., JIANG, Y.-J., SMITHERS, L. and LEWIS, J. (1998). Delta-Notch signalling and the patterning of sensory cell differentiation in the zebrafish ear: evidence from the mind bomb mutant. Development 125: 4637-4644.
20. HADDON, C. M. (1997). The development of the zebrafish ear and a quest for genes involved in sensory patterning. PhD Thesis, The Open University.
21. HADRYS, T., BRAUN, T., RINKWITZ-BRANDT, S., ARNOLD, H.-H. and BOBER, E. (1998). Nkx5-1 controls semicircular canal formation in the mouse inner ear. Development 125: 33-39.
22. HAGELIN, L. O. (1974). Development of the membranous labyrinth in lampreys. Acta Zool. Suppl: 1-218.
23. HALL, E. K. (1939). On the duration of the polarization process in the ear primordium of embryos of Amblystoma punctatum (Linn.). J. Exp. Zool. 82: 173-192.
24. HAMMOND, K. L., LOYNES, H. E., FOLARIN, A. A., SMITH, J. and WHITFIELD, T. T. (2003). Hedgehog signalling is required for correct anteroposterior patterning of the zebrafish otic vesicle. Development 130: 1403-1417.
25. HAMMOND, K. L. and WHITFIELD, T. T. (2006). The developing lamprey ear closely resembles the zebrafish otic vesicle: otx1 expression can account for all major patterning differences. Development 133: 1347-1357.
26. HARRISON, R. G. (1936). Relations of symmetry in the developing ear of Amblystoma punctatum. Proc. Natl. Acad. Sci. 22: 238-247.
27. HARRISON, R. G. (1945). Relations of symmetry in the developing embryo. Trans. Conn. Acad. Arts Sci. USA 22: 238-247.
28. HAUPTMANN, G., BELTING, H. G., WOLKE, U., LUNDE, K., SOLL, I., ABDELILAH-SEYFRIED, S., PRINCE, V. and DRIEVER, W. (2002). spiel ohne grenzen/pou2 is required for zebrafish hindbrain segmentation. Development 129: 1645-1655.
29. HERBRAND, H., GUTHRIE, S., HADRYS, T., HOFFMANN, S., ARNOLD, H. H., RINKWITZ-BRANDT, S. and 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: 645-654.
30. HERNANDEZ, R. E., RIKHOF, H. A., BACHMANN, R. and MOENS, C. B. (2004). vhnf1 integrates global RA patterning and local FGF signals to direct posterior hindbrain development in zebrafish. Development 131: 4511-4520.
31. HIDALGO-SÁNCHEZ, M., ALVARADO-MALLART, R. and ALVAREZ, I. S. (2000). Pax2, Otx2, Gbx2 and Fgf8 expression in early otic vesicle development. Mech. Dev. 95: 225-229.
32. KIERNAN, A. E., NUNES, F., WU, D. K. and FEKETE, D. M. (1997). The expression domain of two related homeobox genes defines a compartment in the chicken inner ear that may be involved in semicircular canal formation. Dev. Biol. 191: 215-229.
33. KIL, S.-H. and COLLAZO, A. (2001). Origins of inner ear sensory organs revealed by fate map and time-lapse analyses. Dev. Biol. 233: 365-379.
34. KIM, F. A., SING, L. A., KANEKO, T., BIEMAN, M., STALLWOOD, N., SADL, V. S. and CORDES, S. P. (2005). The vHNF1 homeodomain protein establishes early rhombomere identity by direct regulation of Kreisler expression. Mech. Dev. 122: 1300-1309.
35. KIMMEL, C. B., BALLARD, W. W., KIMMEL, S. R., ULLMANN, B. and SCHILLING, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203: 253-310.
36. KWAK, S.-J., PHILLIPS, B. T., HECK, R. and RILEY, B. B. (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.
37. KWAK, S. J., VEMARAJU, S., MOORMAN, S. J., ZEDDIES, D., POPPER, A. N. and RILEY, B. B. (2006). Zebrafish pax5 regulates development of the utricular macula and vestibular function. Dev. Dyn. 235: 3026-3038.
38. LECAUDEY, V., ANSELME, I., ROSA, F. and SCHNEIDER-MAUNOURY, S. (2004). The zebrafish Iroquois gene iro7 positions the r4/r5 boundary and controls neurogenesis in the rostral hindbrain. Development 131: 3121-3131.
39. LECAUDEY, V., ULLOA, E., ANSELME, I., STEDMAN, A., SCHNEIDER-MAUNOURY, S. and PUJADES, C. (2007). Role of the hindbrain in patterning the otic vesicle: A study of the zebrafish vhnf1 mutant. Dev. Biol. 303: 134-143.
40. LÉGER, S. and BRAND, M. (2002). Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech. Dev. 119: 91-108.
41. LILLEVÄLI, K., HAUGAS, M., MATILAINEN, T., PUSSINEN, C., KARIS, A. and SALMINEN, M. (2006). Gata3 is required for early morphogenesis and Fgf10 expression during otic development. Mech. Dev. 123: 415-429.
42. LIN, Z., CANTOS, R., PATENTE, M. and WU, D. K. (2005). Gbx2 is required for the morphogenesis of the mouse inner ear: a downstream candidate of hindbrain signaling. Development 132: 2309-2318.
43. LIU, W., LI, G., CHIEN, J. S., RAFT, S., ZHANG, H., CHIANG, C. and FRENZ, D. A. (2002). Sonic hedgehog regulates otic capsule chondrogenesis and inner ear development in the mouse embryo. Dev. Biol. 248: 240-250.
44. LUFKIN, T., DIERICH, A., LEMEUR, M., MARK, M. and 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.
45. MANSOUR, S. L., GODDARD, J. M. and CAPECCHI, M. R. (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.
46. MARK, M., LUFKIN, T., VONESCH, J.-L, RUBERTE, E., OLIVO, J.-C., DOLLÉ, P., GORRY, P., LUMSDEN, A. and CHAMBON, P. (1993). Two rhombomeres are altered in Hoxa-1 mutant mice. Development 119: 319-338.
47. MAVES, L. and KIMMEL, C. B. (2005). Dynamic and sequential patterning of the zebrafish posterior hindbrain by retinoic acid. Dev. Biol. 285: 593-605.
48. MCKAY, I. J., LEWIS, J. and 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.
49. MERLO, G. R., PALEARI, L., MANTERO, S., ZEREGA, B., ADAMSKA, M., RINKWITZ, S., BOBER, E. and LEVI, G. (2002). The Dlx5 homeobox gene is essential for vestibular morphogenesis in the mouse embryo through a BMP4-mediated pathway. Dev. Biol. 248: 157-169.
50. 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.
51. MIYAZAKI, H., KOBAYASHI, T., NAKAMURA, H. and FUNAHASHI, J. (2006). Role of Gbx2 and Otx2 in the formation of cochlear ganglion and endolymphatic duct. Dev. Growth Diff. 48: 429-438.
52. MOENS, C. B. and PRINCE, V. E. (2002). Constructing the hindbrain: insights from the zebrafish. Dev. Dyn. 224: 1-17.
53. MORSLI, H., TUORTO, F., CHOO, D., POSTIGLIONE, M. P., SIMEONE, A. and WU, D. K. (1999). Otx1 and Otx2 activities are required for the normal development of the mouse inner ear. Development 126: 2335-2343.
54. MOWBRAY, C., HAMMERSCHMIDT, M. and WHITFIELD, T. T. (2001). Expression of BMP signalling pathway members in the developing zebrafish inner ear and lateral line. Mech. Dev. 108: 179-184.
55. MURAKAMI, Y., PASQUALETTI, M., TAKIO, Y., HIRANO, S., RIJLI, F. M. and KURATANI, S. (2004). Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain. Development 131: 983-995.
56. NIEDERREITHER, K., VERMOT, J., SCHUHBAUR, B., CHAMBON, P. and DOLLÉ, P. (2000). Retinoic acid synthesis and hindbrain patterning in the mouse embryo. Development 127: 75-85.
57. OH, S.-H., JOHNSON, R. and WU, D. K. (1996). Differential expression of bone morphogenetic proteins in the developing vestibular and auditory sensory organs. J. Neurosci. 16: 6463-6475.
58. OTA, K. G., KURAKU, S. and KURATANI, S. (2007). Hagfish embryology with reference to the evolution of the neural crest. Nature 446: 672-675.
59. OTA, K. G. and KURATANI, S. (2006). The history of scientific endeavors towards understanding hagfish embryology. Zool. Science 23: 403-418.
60. OZAKI, H., NAKAMURA, K., FUNAHASHI, J., IKEDA, K., YAMADA, G., TOKANO, H., OKAMURA, H., KITAMURA, K., MUTO, S., KOTAKI, H., SUDO, K., HORAI, R., IWAKURA, Y. and KAWAKAMI, K. (2004). Six1 controls patterning of the mouse otic vesicle. Development 131: 551-562.
61. PERA, E. and KESSEL, M. (1999). Expression of DLX3 in chick embryos. Mech. Dev. 89: 189-193.
62. PFEFFER, P. L., GERSTER, T., LUN, K., BRAND, M. and BUSSLINGER, M. (1998). Characterization of three novel members of the zebrafish Pax2/5/8 family: dependency of Pax5 and Pax8 expression on the Pax2.1 (noi) function. Development 125: 3063-3074.
63. PIOTROWSKI, T., AHN, D.-G., SCHILLING, T. F., NAIR, S., RUVINSKY, I., GEISLER, R., RAUCH, G.-J., HAFFTER, P., ZON, L. I., ZHOU, Y., FOOTT, H., DAWID, I. B. and HO, R. K. (2003). The zebrafish van gogh mutation disrupts tbx1, which is involved in the DiGeorge deletion syndrome in humans. Development 130: 5043-5052.
64. PIRVOLA, U., SPENCER-DENE, B., XING-QUN, L., KETTUNEN, P., THESLEFF, I., FRITZSCH, B., DICKSON, C. and YLIKOSKI, J. (2000). FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. J. Neurosci. 20: 6125-6134.
65. QIU, X., XU, H., HADDON, C., LEWIS, J. and JIANG, Y. J. (2004). Sequence and embryonic expression of three zebrafish fringe genes: lunatic fringe, radical fringe, and manic fringe. Dev. Dyn. 231: 621-630.
66. RAFT, S., NOWOTSCHIN, S., LIAO, J. and MORROW, B. E. (2004). Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 131: 1801-1812.
67. 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: 2365-2378.
68. 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: 1612-1623.
69. RILEY, B. B., CHIANG, M., FARMER, L. and HECK, R. (1999). The deltaA gene of zebrafish mediates lateral inhibition of hair cells in the inner ear and is regulated by pax2.1. Development 126: 5669-5678.
70. RILEY, B. B., CHIANG, M. Y., STORCH, E. M., HECK, R., BUCKLES, G. R. and LEKVEN, A. C. (2004). Rhombomere boundaries are Wnt signaling centers that regulate metameric patterning in the zebrafish hindbrain. Dev. Dyn. 231: 278-291.
71. RILEY, B. B., ZHU, C., JANETOPOULOS, C. and AUFDERHEIDE, K. J. (1997). A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish. Dev. Biol. 191: 191-201.
72. ROBLEDO, R. F. and LUFKIN, T. (2006). Dlx5 and Dlx6 homeobox genes are required for specification of the mammalian vestibular apparatus. Genesis 44: 425-437.
73. SÁNCHEZ-CALDERÓN, H., MARTÍN-PARTIDO, G. and HIDALGO-SÁNCHEZ, M. (2002). Differential expression of Otx2, Gbx2, Pax2, and Fgf8 in the developing vestibular and auditory sensory organs. Brain Res. Bull. 57: 321-323.
74. SAUKA-SPENGLER, T., LE MENTEC, C., LEPAGE, M. and MAZAN, S. (2002). Embryonic expression of Tbx1, a DiGeorge syndrome candidate gene, in the lamprey Lampetra fluviatilis. Gene Exp. Patt. 2: 99-103.
75. SU, Y. and MENG, A. (2002). The expression of gbx-2 during zebrafish embryogenesis. Mech. Dev. 113: 107-110.
76. WALDMAN, E. H., CASTILLO, A. and COLLAZO, A. (2007). Ablation studies on the developing inner ear reveal a propensity for mirror duplications. Dev. Dyn. 236: 1237-1248.
77. WALSHE, J. and MASON, I. (2003). Fgf signalling is required for formation of cartilage in the head. Dev. Biol. 264: 522-536.
78. WANG, W., CHAN, E. K., BARON, S., VAN DE WATER, T. and LUFKIN, T. (2001). Hmx2 homeobox gene control of murine vestibular morphogenesis. Development 128: 5017-5029.
79. WANG, W., GRIMMER, J. F., VAN DE WATER, T. R. and LUFKIN, T. (2004). Hmx2 and Hmx3 homeobox genes direct development of the murine inner ear and hypothalamus and can be functionally replaced by Drosophila Hmx. Dev. Cell 7: 439-453.
80. WANG, W., VAN DE WATER, T. and LUFKIN, T. (1998). Inner ear and maternal reproductive defects in mice lacking the Hmx3 homeobox gene. Development 125: 621-634.
81. WRIGHT, T. J. and MANSOUR, S. L. (2003). Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130: 3379-3390.
82. WU, D. K., NUNES, F. D. and CHOO, D. (1998). Axial specificiation for sensory organs versus non-sensory structures of the chicken inner ear. Development 125: 11-20.
83. WU, D. K. and OH, S.-H. (1996). Sensory organ generation in the chick inner ear. J. Neurosci. 16: 6454-6462.
84. XU, H., VIOLA, A., ZHANG, Z., GERKEN, C. P., LINDSAY-ILLINGWORTH, E. A. and BALDINI, A. (2007). Tbx1 regulates population, proliferation and cell fate determination of otic epithelial cells. Dev. Biol. 302: 670-682.
85. YNTEMA, C. L. (1955). Ear and Nose. In Analysis of Development, (ed. B. H. Willier P. A. Weiss and V. Hamburger), pp. 415-428. Philadelphia and London: W. B. Saunders.
86. ZHENG, W., HUANG, L., WEI, Z.-B., SILVIUS, D., TANG, B. and XU, P.-X. (2003). The role of Six1 in mammalian auditory system development. Development 130: 3989-4000.