Abstract
We present the normal patterns of programmed cell death in the developing inner ears of a primitive anuran, Xenopus laevis, and an ostariophysan fish, Danio rerio. A prominent ventromedial focus of cell death was described previously in the developing chicken and mouse otocysts. We hypothesize that this focus of cell death might be associated with a signaling center that directs morphogenesis of the surrounding tissue. Amphibian and fish ear anatomies differ considerably from those of birds and mammals, particularly in the structures derived from the ventral part (pars inferior) of the otic vesicle. We reasoned that these anatomical differences between species might result from a difference in the size, location, or presence of a putative morphogenetic signaling center. Using in situ terminal deoxynucleotidyl transferase (TdT)-mediated dUTP nick-end labeling (TUNEL) to detect apoptotic cells, we show that developing Xenopus and zebrafish ears have apoptotic cells in the eighth cranial ganglia, the developing sensory patches, and in various positions in the otocyst wall. However, both species lack the persistent ventromedial hot spot of cell death that is prominently situated between the pars superior and pars inferior in the chicken and mouse otocysts.
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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 Drosophilasense-organ development. Development 125, 4645–4654.
Ard, M. D.& Morest, D. K.(1984) Cell death during development of the cochlear and vestibular ganglia of the chick. International Journal of Developmental Neuroscience 2, 535–547.
Bartolami, S., Goodyear, R.& Richardson, G.(1991) Appearance and distribution of the 275kD haircell antigen during development of the avian inner ear. The Journal of Comparative Neurology 314, 777–788.
Bissonnette, J. P.& Fekete, D. M.(1996) Standard atlas of the gross anatomy of the developing inner ear of the chicken. The Journal of Comparative Neurology 368, 620–630.
Carney, P. R.& Silver, J.(1983) Studies on cell migration and axon guidance in the developing distal auditory system of the mouse. The Journal of Comparative Neurology 215, 359–369.
Cole, L. K.& Ross, L. S.(1996) Apoptosis in the developing sensory organs of the zebrafish embryo. Developmental Biology 175, 392.
Cotanche, D. A.& Sulik, K. K.(1984) The development of stereociliary bundles in the cochlear duct of chick embryos. Developmental Brain Research 16, 181–193.
Fekete, D. M., Homburger, S. A., Waring, M. T., Riedl, A. E.& Garcia, L. F.(1997) Involvement of programmed cell death in morphogenesis of the vertebrate inner ear. Development 124, 2451–2461.
Fox, G. Q.& Richardson, G. P.(1982) The developmental morphology of Torpedo marmorata: Electric lobeelectromotoneuron proliferation and cell death. Journal of Comparative Neurology 207, 183–190.
Fritzsch, B.(1998) Evolution of the vestibulo-ocular system. Otolaryngology—Head and Neck Surgery 119, 182–192.
GlÜcksmann, A.(1951) Cell deaths in normal vertebrate ontogeny. Biological Reviews 26, 59–86.
Haddon, C.& Lewis, J.(1996) Early ear development in the embryo of the zebrafish, Danio rerio. The Journal of Comparative Neurology 365, 113–128.
Haddon, C. M.& Lewis, J. H.(1991) Hyaluronan as a propellant for epithelial movement: The development of semicircular canals in the inner ear of Xenopus. Development 112, 541–550.
Hemond, S. G.& Morest, D. K.(1991) Ganglion formation from the otic placode and the otic crest in the chick embryo: Mitosis, migration, and the basal lamina. Anatomy and Embryology 184, 1–13.
Hemond, S. G.& Morest, D. K.(1992) Tropic effects of otic epithelium on cochleo-vestibular ganglion fiber growth in vitro. The Anatomical Record 232, 273–284.
Hertwig, I.(1987) Morphogenesis of the inner ear of Rana temporaria(Amphibia, Anura). Zoomorphology 107, 103–114.
Ishizuya-Oka, A.& Shimozawa, A.(1992) Programmed cell death and heterolysis of larval epithelial cells by macrophage-like cells in the anuran small intestine in vivoand in vitro. Journal of Morphology 213, 185–195.
Jeffery, W. R.& Martasian, D. P.(1998) Evolution of eye regression in the cavefish Astyanax: Apoptosis and the Pax-6gene. American Zoologist 38, 685–696.
Jernvall, J., Aberg, T., Kettunen, P., Keranen, S.& Thesleff, I.(1998) The life history of an embryonic signaling center: BMP-4 induces p21and is associated with apoptosis in the mouse tooth enamel knot. Development 125, 161–169.
Kimmel, C. B., Ballard, W. W., Kimmel, S. R. Ullmann, B.& Schilling, T. F.(1995) Stages of embryonic development of the zebrafish. Developmental Dynamics 203, 253–310.
Knowlton, V. Y.(1967) Correlation of the development of membranous and bony labyrinths, acoustic ganglia, nerves, and brain centers in the chick embryo. Journal of Morphology 121, 179–208.
Lang, H., Bever, M. M.& Fekete, D. M.(2000) Cell proliferation and cell death in the developing chick inner ear: Spatial and temporal patterns. The Journal of Comparative Neurology 417, 205–220.
Lewis, E. R.(1992) Convergence of design in vertebrate acoustic sensors. In The Evolutionary Biology of Hearing(edited by Webster, D. B., Fay, R. R.& Popper, A. N.) pp. 163–184. New York: Springer-Verlag.
Lowenstein, O.(1971) The labyrinth. In Fish Physiology V: Sensory Organs and Electric Organs(edited by Hoar, W. S.& Randall, D. J.) pp. 207–240. New York: Academic Press.
Marovitz, W. F., Khan, K. M.& Schulte, T.(1977) Ultrastructural development of the early rat otocyst. Annals of Otology, Rhinology, and Laryngology 86, 9–28.
Marovitz, W. F., Shugar, J. M. A.& Khan, K. M.(1976) The role of cellular degeneration in the normal development of (rat) otocyst. Laryngoscopy 86, 1413–1425.
Nieuwkoop, P. D.& Faber, J.1994. Normal Table of Xenopus laevis(Daudin): A systematical and chronological survey of the development from the fertilized egg till the end of metamorphosis, 2nd ed. New York: Garland Publishing, Inc.
Nishikawa, A.& Hayashi, H.(1995) Spatial, temporal and hormonal regulation of programmed muscle cell death during metamorphosis of the frog Xenopus laevis. Differentiation 59, 207–214.
Nishikawa, A.& Hayashi, H.(1999) T3-hydrocortisone synergism on adult-type erythroblast proliferation and T3-mediated apoptosis of larval-type erythroblasts during erythropoietic conversion in Xenopus laevis. Histochemistry and Cell Biology 111, 325–334.
Nishikori, T., Atta, T., Awauchi, H.& Tani, H.(1999) Apoptosis during inner ear development in human and mouse embryos: An analysis by computerassisted three-dimensional reconstruction. Anatomy and Embryology 200, 19–26.
Nishizaki, K., Anniko, M., Orita, Y., Karita, K., Masuda, Y.& Yoshino, T.(1998) Programmed cell death in the developing epithelium of the mouse inner ear. Acta Otolaryngology (Stockh) 118, 96–100.
Nishizaki, K., Anniko, M., Orita, Y., Masuda, Y.& Yoshino, T.(1997) Programmed cell death in the mouse cochleovestibular ganglion during development. ORL Journal of Otorhinolaryngology and Its Related Specialties 60, 267–271.
Nishizaki, K., Yoshino, T., Orita, Y., Nomiya, S.& Masuda, Y.(1999) TUNEL staining of inner ear structures may reflect autolysis, not apoptosis. Hearing Research 130, 131–136.
Nohno, T., Kawakami, Y., Ohuchi, H., Fujiwara, A., Yoshioka, H.& Noji, S.(1995) Involvement of the sonic hedgehoggene in chick feather formation. Biochemical and Biophysical Research Communications 206, 33–39.
Norris, H. W.(1892) Studies on the development of the ear of Amblystoma. I. Develoment of the auditory vesicle. Journal of Morphology 7, 23–34.
Paterson, N. F.(1948) The development of the inner ear of Xenopus laevis. Proceedings of the Zoological Society of London 119, 269–291.
Popper, A. N., Platt, C.& Edds, P. L.(1992) Evolution of the vertebrate inner ear: An overview of ideas. In The Evolutionary Biology of Hearing(edited by Webster, D. B., Fay, R. R.& Popper, A. N.) pp. 49–57. New York: Springer-Verlag.
Represa, J. J., Moro, J. A., Pastor, F., Gato, A.& Barbosa, E.(1990) Patterns of epithelial cell death during early development of the human inner ear. Annals of Otology, Rhinology, and Laryngology 99, 482–488.
Riley, B. B., Zhu, C., Janetopoulos, C.& Aufderheide, K. J.(1997) A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish. Developmental Biology 191, 191–201.
Rojo, M. C.& Gonzalez, M. E.(1998) In situ detection of apoptotic cells by TUNEL in the gill epithelium of the developing brown trout (Salmo trutta). Journal of Anatomy 193, 391–398.
Sanders, E. J.& Wride, M. A.(1995) Programmed cell death in development. International Review of Cytology 163, 105–73.
Schellart, N. A. M.& Popper, A. N.(1992) Functional aspects of the evolution of the auditory system of actinopterygian fish. In The Evolutionary Biology of Hearing(edited by Webster, D. B., Fay, R. R.& Popper, A. N.) pp. 295–322. New York: Springer-Verlag.
Sokolowski, B. H. A.& Popper, A. N.(1987) Gross and ultrastructural development of the saccule of the toadfish Opsanus tau. Journal of Morphology 194, 323–348.
Soutschek, J.& Zupanc, G. K. H.(1996) Apoptosis in the cerebellum of adult teleost fish, Apteronotus leptorhynchus. Developmental Brain Research 97, 279–286.
Tabin, C.(1995) The initiation of the limb bud: Growth factors, Hoxgenes, and retinoids. Cell 80, 671–674.
Tornusciolo, D. R. Z., Schmidt, R. E.& Roth, K. A.(1995) Simultaneous detection of TdT-mediated dUTP-biotin nick end-labeling (TUNEL)-positive cells and multiple immunohistochemical markers in single tissue sections. Biotechniques 19, 800–805.
Von Bartheld, C. S., Patterson, S. L., Heuer, J. G., Wheeler, E. F., Bothwell, M.& Rubel, E. W.(1991) Expression of nerve growth factor (NGF) receptors in the developing inner ear of chick and rat. Development 113, 455–470.
Waterman, R. E.& Bell, D. H.(1984) Epithelial fusion during early semicircular canal formation in the embryonic zebrafish, Brachydanio rerio. The Anatomical Record 210, 101–114.
Westerfield, M.1994. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish(Brachydanio rerio), 2.1 ed. Eugene, OR: University of Oregon Press.
Wever, E. G.1985. The Amphibian Ear. Princeton, NJ: Princeton University Press.
Wyllie, A. H., Kerr, J. F. R.& Currie, A. R.(1980) Cell death: The significance of apoptosis. International Review of Cytology 68, 251–306.
Zheng, J. L.& Gao, W.-Q.(1997) Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker. Journal of Neuroscience 17, 8270–8282.
Zupanc, G. K., Kompass, K. S., Horschke, I., Ott, R.& Schwarz, H.(1998) Apoptosis after injuries in the cerebellum of adult teleost fish. Experimental Neurology 152, 221–30.
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Bever, M.M., Fekete, D.M. Ventromedial focus of cell death is absent during development of Xenopus and zebrafish inner ears. J Neurocytol 28, 781–793 (1999). https://doi.org/10.1023/A:1007005702187
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DOI: https://doi.org/10.1023/A:1007005702187