Abstract
Several cell adhesion molecules are expressed in the developing inner ear. The present study focused on gicerin, a novel member of the immunoglobulin superfamily, in an attempt to improve our understanding of the development and regeneration of chick inner ear. Gicerin is known to homophilically interact with itself and to bind to neurite outgrowth factor (NOF). The data collected herein show that gicerin is highly expressed in auditory epithelium and acoustic ganglion during early embryogenesis. The immunoreactivity of gicerin in the auditory epithelium decreases more rapidly than that in the acoustic ganglion as the mature hair cells become distinguishable. At the post-hatch stage, the expression of gicerin is not observed. In contrast, NOF was expressed on the basement membranes around the auditory epithelium, and in the acoustic ganglion during development and after birth, but not in the auditory epithelium. Following noise damage, gicerin is transiently re-expressed on the damage receptor epithelium when active cell proliferation is observed in the epithelium. This positive reaction immediately disappears as immature short hair cells appear. These results suggest that gicerin may be associated with cell proliferation in the auditory epithelium, and play a role in neurite extension of the acoustic ganglion cells in conjunction with NOF.
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Cohen, G. M. & Fermin, C. D. (1978) The development of hair cells in the embryonic chick basilar papilla. Acta Oto-Laryngologica (Stockholm) 863, 342–58.
Corwin, J. T. & Cotanche, D. A. (1988) Regeneration of sensory hair cells after acoustic trauma. Science 240, 1772–4.
Cotanche, D. A. (1987) Regeneration of hair cell stereociliary bundles in the chick cochlea following acoustic trauma. Hearing Research 30, 181–94.
Cotanche, D. A., Lee, K. H., Stone, J. S. & Picard, D. A. (1994) Hair cell regeneration in the bird cochlea following noise damage or ototoxic drug damage. Anatomy and Embryology 189, 1–18.
Cotanche, D. A., Saunders, J. C. & Tilney, L. G. (1987) Hair cell damage produced by acoustic trauma in the chick cochlea. Hearing Research 25, 267–86.
Cruz, R. M., Lambert, P. R. & Rubel, E. W. (1987) Light microscopic evidence of hair cell regeneration after gentamycin toxicity in chick cochlea. Archives of Otolaryngology – Head & Neck Surgery 113, 1053–62.
D'amico-Martel, A. & Noden, D. M. (1983) Contributions of placodal and neural crest cells to avian cranial peripheral ganglia. American Journal of Anatomy 166, 445–68.
Duckert, L. G. & Rubel, E. W. (1990) Ultrastructural observation on regenerating hair cells in the chick basilar papilla. Hearing Research 48, 161–82.
Fermin, C. D. & Cohen, G. M. (1984a) Developmental gradients in the embryonic chick's basilar papilla. Acta Oto-Laryngologica (Stockholm) 97, 39–51.
Fermin, C. D. & Cohen, G. M. (1984b) Development of the embryonic chick's statoacoustic ganglion. Acta Oto-Laryngologica (Stockholm) 98, 42–52.
Ginzberg, R. D. & Gilula, N. B. (1979) Modulation of cell junctions during differentiation of the chicken otocyst sensory epithelium. Developmental Biology 68, 110–29.
Girod, D. A., Duckert, L. G. & Rubel, E. W. (1989) Possible precursors of regenerated hair cells in the avian cochlea following acoustic trauma. Hearing Research 42, 175–94.
Hamburger, V. & Hamilton, H. L. (1951) A series of normal stages in the development of the chick embryo. Journal of Morphology 88, 49–92.
Hayashi, Y. & Miki, N. (1985) Purification and characterization of a neurite outgrowth factor from chicken gizzard smooth muscle. Journal of Cell Biology 260, 14269–78.
Hayashi, T., Tauiura, H. & Miki, N. (1987) Interaction of monoclonal antibodies with a neurite outgrowth factor from chicken gizzard extract. Developmental Brain Research 35, 11–19.
Kaiser, A. (1992) The ontogeny of homeothermic regulation in post-hatching chicks: its influence on the development of hearing. Comparative Biochemistry and Physiology 103A, 105–111.
Kaj ikawa, H., Umemoto, M., Mishiro, Y., Sakagami, M., Kubo, T. & Yoneda, Y. (1997) Expression of highly polysialylated NCAM (NCAM-H) in developing and adult chicken auditory organ. Hearing Research 103, 123–30.
Kato, S., Negishi, K., Hayashi, Y. & Miki, N. (1983) Enhancement of neurite outgrowth and aspartate-glutamate uptake system in retinal explants cultured with chick gizzard extract. Journal of Neurochemistry 40, 929–38.
Kato, S., Taniura, H., Taira, E. & Miki, N. (1992) Involvement of a receptor for neurite outgrowth factor (NOFR) in cerebellar neurogenesis. Neuroscience Letters 140, 78–80.
Lippe, W. R., Westbrook, E. W. & Ryals, B. M. (1991) Hair cell regeneration in the chicken cochlea following aminoglycoside toxicity. Hearing Research 56, 203–10.
Lim, D. J. (1976) Ultrastructural cochlear changes following acoustic hyperstimulation and ototoxicity. Annals of Otology, Rhinology & Laryngology 85, 740–51.
Mbiene, J. P., Dechesne, C. J., Schachner, M. & Sans, A. (1989) Immunocytological characterization of the expression of cell adhesion molecule L1 during early innervation of mouse otocysts. Cell and Tissue Research 255, 81–8.
Meier, S. (1978a) Development of the embryonic chick otic placode. I. Light microscopic analysis. Anatomical Record 191, 447–58.
Meier, S. (1978b) Development of the embryonic chick otic placode. II. Electron microscopic analysis. Anatomical Record 191, 459–78.
Miki, N., Hayashi, Y. & Higashida, H. (1981) Characterization of chick gizzard extract that promotes neurite outgrowth in cultured ciliary neurons. Journal of Neurochemistry 37, 627–33.
Raphael, Y. (1992) Evidence for supporting cell mitosis in response to acoustic trauma in the avian inner ear. Journal of Neurocytology 21, 663–71.
Raphael, Y., Volk, T., Crossin, K. L., Edelman, G. M. & Geiger, B. (1988) The modulation of cell adhesion molecule expression and intercellular junction formation in the developing avian inner ear. Developmental Biology 128, 222–35.
Richardson, G. P., Crossin, K. L., Chuong, C. & Edelman, G. M. (1987) Expression of cell adhesion molecules during embryonic induction. III. Development of the otic placode. Developmental Biology 119, 217–30.
Robertson, D. & Johnstone, B. M. (1980) Acoustic trauma in the guinea pig cochlea: early changes in ultrastructure and threshold. Hearing Research 3, 167–79.
Ruben, R. J. (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Oto-Laryngologicca (Stockholm) 220, 4–44.
Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M. & Sunshine, J. (1988) The neural cell adhesion molecule (N-CAM) as a regulator of cell–cell interactions. Science 240, 53–7.
Ryals, B. M. & Rubel, E. W. (1982) Patterns of hair cell loss in chick basilar papilla after intense auditory stimulation. Acta Oto-Laryngologica (Stockholm) 93, 31–41.
Ryals, B. M. & Rubel, E. W. (1988) Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240, 1774–6.
Raphael, Y. (1992) Evidence of supporting cell mitosis in response to acoustic trauma in the avian inner ear. Journal of Neurocytology 21, 663–71.
Stone, J. S. & Cotanche, D. A. (1994) Identification of the timing of s phase and the patterns of cell proliferation during hair cell regeneration in the chick cochlea. Journal of Comparative Neurology 341, 50–67.
Taira, E., Takaha, N., Taniura, H., Kim, C.-H. & Miki, N. (1994) Molecular cloning and functional expression of gicerin, a novel cell adhesion molecule that binds to neurite outgrowth factor. Neuron 12, 861–72.
Takaha, N., Taira, E., Taniura, H., Nagino, T., Tsukamoto, Y., Matsumoto, T., Kotani, T., Sakuma, S. & Miki, N. (1995) Expression of gicerin in development, oncogenesis and regeneration of the chick kidney. Differentiation 58, 313–320.
Taniura, H., Kuo, C.-H. Hayashi, Y. & Miki, N. (1991) Purification and characterization of an 82-kD membrane protein as a neurite outgrowth factor binding protein: possible involvement of NOF binding protein in axonal outgrowth in developing retina. Journal of Cell Biology 112, 313–322.
Umemoto, M., Sakagami, M., Ashida, K., Fukazawa, K., Kubo, T., Senda, T. & Yoneda, Y. (1995) Hair cell regeneration in the chick inner ear following acoustic trauma: ultrastructural and immunohistochemical studies. Cell & Tissue Research 281, 435–43.
Umemoto, M., Sakagami, M., Ashida, K., Fukazawa, K., Matsunaga, T. & Senda, T. (1993) Regeneration of adult budgerigar's hair cells following acoustic trauma. ORL Journal of Oto-Rhino-Laryngology and its Related Specialities 55, 325–31.
Whitehead, M. C. & Morest, D. K. (1985) The development of innervation patterns in the avian cochlea. Neuroscience 14, 255–76.
Whitehead, M. C. & Morest, D. K.(1985b) The growth of the cochlear fibers and the formation of their synaptic endings in the avian inner ear: a study with the electron microscope. Neuroscience 14, 277–300.
Whitlon, D. S. (1993) E-cadherin in the mature and developing organ of Corti of the mouse. Journal of Neurocytology 22, 1030–38.
Whitlon, D. S. & Rutishauser, U. S. (1990) NCAM in the organ of Corti of the developing mouse. Journal of Neurocytology 19, 970–7.
Woolf, N. K., Koehrn, F. J. & Ryan, A. F. (1992) Immunohistochemical localization of fibronectin-like protein in the inner ear of the developing gerbil and rat. Developmental Brain Research 65, 21–33.
Yamashita, H., Bagger, S. D. & Wersall, J. (1991) The presence of laminin in the fetal human inner ear. European Archives of Oto-Rhino-Laryngology 248, 479–82.
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Kajikawa, H., Umemoto, M., Taira, E. et al. Expression of neurite outgrowth factor and gicerin during inner ear development and hair cell regeneration in the chick. J Neurocytol 26, 501–509 (1997). https://doi.org/10.1023/A:1018585508713
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DOI: https://doi.org/10.1023/A:1018585508713