Summary
Auditory hair cells that survive mechanical injury in culture begin their recovery by reforming the kinocilium. This study is based on cultures of the organ of Corti of newborn mice and two control animals. The axonemal patterns were examined in 165 kinocilia in cross-section. In the immature and regenerating kinocilium, one of the normally peripheral doublets is frequently located inward, forming the modified 8 + 1 (double) form; the distribution of the remainingmicrotubules is irregular. As the cell matures, the 9 + 0 form predominates. Overall, 34–61% of auditory kinocilia consist of 9 + 0 microtubules. The 9+2 (single) form, previously thought to characterize the organelle, occurs only in about 3–14%, whereas the remaining population comprises the modified 8 + 1 (double) form. Normally, the kinocilium lasts only about 10 postnatal days; however, post-traumatic hair cells reform their kinocilia regardless of age. Concomitant with the regrowth of the kinocilium, the basal body and its cilium take a central location in the cuticular plate, stereocilia regrow, and the cytoplasmic area adjacent to the basal body displays pericentriolar fibrous densities, growth vesicles, and microtubules, all surrounded by actin filaments. Pericentriolar bodies nucleate microtubules. Involvement of microtubules is seen in the alignment of actin filaments and in the formation of the filamentous matrix of the cuticular plate. We propose that reformation of the kinocilium in recovering post-traumatic hair cells indicates the possible role of its basal body in the morphogenesis and differentiation of cuticular plates and stereocilia.
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Afzelius, B. A. (1963) Cilia and flagella that do not conform to the 9 + 2 pattern. I. Aberrant members within normal populations.Journal of Ultrastructure Research 9, 381–92.
Allen, R. A. (1965) Isolated cilia in inner retinal neurons and in retinal pigment epithelium.Journal of Ultrastructure Research 12, 730–47.
Anderson, R. G. W. (1972) The three-dimensional structure of the basal body from the rhesus monkey oviduct.Journal of Cell Biology 54, 246–65.
Anniko, M. (1983a) Cytodifferentiation of cochlear hair cells.American Journal of Otolaryngology 4, 375–88.
Anniko, M. (1983b) Embryonic development of vestibular sense organs and their innervation. InDevelopment of Auditory and Vestibular Systems (edited byRomand, R.) pp. 375–423. New York: Academic Press.
Barnes, B. G. (1961) Ciliated secretory cells in the pars distalis of the mouse hypophysis.Journal of Ultrastructure Research 5, 453–67.
Bergmann, J. E., Tokuyasu, K. T. &Singer, S. J. (1981) Passage of an integral membrane protein, the vesicular stomatitis virus glycoprotein, through the Golgi apparatus en route to the plasma membrane.Proceedings of National Academy of Sciences (USA) 78, 1746–50.
Bonneville, M. A. &Weinstock, M. (1970) Brush border development in the intestinal absorptive cells ofXenopus during metamorphosis.Journal of Cell Biology 44, 151–71.
Bunge, M. B. (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture.Journal of Cell Biology 56, 713–35.
Burda, H. &Branis, M. (1988) Postnatal development of the organ of Corti in the wild house mouse, laboratory mouse, and their hybrid.Hearing Research 36, 97–106.
Burda, H., Ballast, L. &Bruns, V. (1988) Cochlea in old world mice and rats (Muridae).Journal of Morphology 198, 269–85.
Calarco-Gillam, P. D., Siebert, M. C., Hubble, R., Mitchison, T. &Kirschner, M. (1983) Centrosome development in early mouse embryos as defined by an autoantibody against pericentriolar material.Cell 35, 621–9.
Cotanche, D. A. &Sulik, K. K. (1984) The development of stereociliary bundles in the cochlear duct of chick embryos.Developmental Brain Research 16, 181–93.
Coupland, R. E. (1965) Electron microscopic observations on the structure of the rat adrenal medulla. I. The ultrastructure and organization of chromaffin cells in the normal adrenal medulla.Journal of Anatomy 99, 231–54.
Dahl, H. A. (1963) Fine structure of cilia in rat cerebral cortex.Zeitschrift für Zellforschung und mikroskopische Anatomie 60, 369–86.
De Robertis, E. (1956) Electron microscope observations on the submicroscopic organization of the retinal rods.Journal of Biophysical and Biochemical Cytology 2, 319–37.
De Robertis, E. &Lasansky, A. (1958) Submicroscopic organization of retinal cones of the rabbit.Journal of Biophysical and Biochemical Cytology 4, 743–53.
Derosier, D. J. &Tilney, L. G. (1989) The structure of the cuticular plate, anin vivo actin gel.Journal of Cell Biology 109, 2853–67.
Ehret, G. (1977) Postnatal development in the acoustic system of the house mouse in the light of developing masked thresholds.Journal of the Acoustical Society of America 62, 143–8.
Engström, H., Ades, H. W. &Hawkins, J. E. J. (1962) Structure and functions of the sensory hairs of the inner ear.Journal of the Acoustical Society of America 34, 1356–63.
Engström, B., Flock, A. &Borg, E. (1983) Ultrastructural studies of stereocilia in noise-exposed rabbits.Hearing Research 12, 251–64.
Farquhar, M. G. &Palade, G. E. (1981) The Golgi apparatus (complex) — (1954-1981) — from artifact to centre stage.Journal of Cell Biology 91, 77s-103s.
Fawcett, D. (1961) Cilia and flagella. InThe Cell (edited byBrachet, J. &Mirsky, A. E.) pp. 217–97. New York: Academic Press.
Flock, A. (1965) Electron microscopic and electrophysiological studies on the lateral line canal organ.Acta Otolaryngologica Supplementum 199, 1–90.
Flock, A., Cheung, H. C., Flock, B. &Utter, G. (1981) Three sets of actin filaments in sensory cells of the inner ear. Identification and functional orientation determined by gel electrophoresis, immunofluorescence and electron microscopy.Journal of Neurocytology 10, 133–47.
Friedmann, I., Cawthorne, T. &Bird, E. S. (1965) The laminated cytoplasmic inclusions in the sensory epithelium of the human macula: further electron microscopic observations in Ménièrés disease.Journal of Ultrastructure Research 12, 92–103.
Furness, D. N., Richardson, G. P. &Russell, I. J. (1989) Stereociliary bundle morphology in organotypic cultures of the mouse cochlea.Hearing Research 38, 95–110.
Furness, D. N., Hackney, C. M. &Steyger, P. S. (1990) Organization of microtubules in cochlear hair cells.Journal of Electron Microscopy Technique 15, 261–79.
Gawadi, N. (1974) Characterization and distribution of microfilaments in dividing locust testis cells.Cytobios 10, 17–35.
Griffin, J. W., Price, D. L., Drachman, D. B. &Morris, J. (1981) Incorporation of axonally transported glycoproteins into axolemma during nerve regeneration.Journal of Cell Biology 88, 205–14.
Griffith, L. M. &Pollard, T. D. (1978) Evidence for actin filament-microtubule interaction mediated by microtubule-associated proteins.Journal of Cell Biology 78, 958–65.
Griffith, L. M. &Pollard, T. D. (1982) The interaction of actin filaments with microtubules and microtubule-associated proteins.Journal of Biological Chemistry 257, 9143–51.
Guillery, R. W., Sobkowicz, H. M. &Scott, G. L. (1970) Relationships between glial and neuronal elements in the development of long term cultures of the spinal cord of the fetal mouse.Journal of Comparative Neurology 140, 1–34.
Kaltenbach, J. A., Falzarano, P. R. &Simpson, T. H. (1994) Postnatal development of the hamster cochlea. II. Growth and differentiation of stereocilia bundles.Journal of Comparative Neurology 350, 187–98.
Karr, T. L. &Alberts, B. M. (1986) Organization of the cytoskeleton in earlyDrosophila embryos.Journal of Cell Biology 102, 1494–509.
Kikuchi, K. &Hilding, D. A. (1965) The development of the organ of Corti in the mouse.Acta Otolaryngologica 60, 207–22.
Kimura, R. S. (1966) Hairs of the cochlear sensory cells and their attachment to the tectorial membrane.Acta Otolaryngologica 61, 55–72.
Konradova, V. (1973) Atypical kinocilia in the tracheal epithelium.Folia Morphologica 21, 71–8.
Konradova, V., Hlouskova, Z. &Tomanek, A. (1975) Atypical kinocilia in human epithelium from large bronchus.Folia Morphologica 23, 293–5.
Kupfer, A., Louvard, D. &Singer, S. J. (1982) Polarization of the Golgi apparatus and the microtubule-organizing centre in cultured fibroblasts at the edge of an experimental wound.Proceedings of the National Academy of Sciences (USA) 79, 2603–7.
Lodish, H. F., Zilberstein, A. &Porter, M. (1981) Synthesis and assembly of transmembrane viral and cellular glycoproteins.Methods in Cell Biology 23, 5–25.
Mcardle, C. B., Dowling, J. E. &Masland, R. H. (1977) Development of outer segments and synapses in the rabbit retina.Journal of Comparative Neurology 175, 253–74.
Mikaelian, D. &Ruben, R. J. (1965) Development of hearing in the normal CBA-J mouse.Acta Otolaryngologica 59, 451–61.
Munger, B. L. &Roth, S. I. (1963) The cytology of the normal parathyroid glands of man and Virginia deer.Journal of Cell Biology 16, 379–400.
Nilsson, S. E. G. (1964) Receptor cell outer segment development and ultrastructure of the disk membranes in the retina of the tadpole (Rana pipiens).Journal of Ultrastructure Research 11, 581–620.
Nishida, E., Kotani, S., Kuwaki, T. &Sakai, H. (1982) Phosphorylation of microtubule-associated proteins (MAPs) controls both microtubule assembly and MAPs-actin interaction. InBiological Functions of Microtubules and Related Structures (edited bySakai, H., Mohri, H. &Borisy, G. G.) pp. 285–95. New York: Academic Press.
Olney, J. W. (1968) An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina.Investigative Ophthalmology 7, 250–68.
Pfenninger, K. H. &Maylié-Pfenninger, M.-F. (1981) Lectin labeling of sprouting neurons. II. Relative movement and appearance of glycoconjugates during plasmalemmal expansion.Journal of Cell Biology 89, 547–59.
Pollard, T. D., Selden, S. C. &Maupin, P. (1984) Interaction of actin filaments with microtubules.Journal of Cell Biology 99, 33s-37s.
Poole, C. A., Flint, M-. H. &Beaumont, B. W. (1985) Analysis of the morphology and function of primary cilia in connective tissues: a cellular cybernetic probe?Cell Motility 5, 175–93.
Raff, J. W. &Glover, D. M. (1989) Centrosomes, and not nuclei, initiate pole cell formation inDrosophila embryos.Cell 57, 611–19.
Reed, W., Avolio, J. &Satir, P. (1984) The cytoskeleton of the apical border of the lateral cells of freshwater mussel gill: structural integration of microtubule and actin filament-based organelles.Journal of Cell Science 68, 1–33.
Roth, L. E. &Shigenaka, Y. (1964) The structure and formation of cilia and filaments in rumen protozoa.Journal of Cell Biology 20, 249–70.
Ruben, R. J. (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses.Acte Otolaryngologica Supplementum 220, 1–44.
Ruela, C., Tavares, M. A. &Paula-Barbosa, M. M. (1981) Cilia in stellate neurons of the rat cerebellum.Experientia 37, 197–8.
Sattilaro, R. F. &Dentler, W. L. (1982) The association of MAP-2 with microtubules, actin filaments, and coated vesicles. InBiological Functions of Microtubules and Related Structures (edited bySakai, H., Mohri, H. &Borisy, G. G.) pp. 297–309. New York: Academic Press.
Sattilaro, R. P., Dentler, W. L. &Lecluyse, E. L. (1981) Microtubule-associated proteins (MAPs) and the organization of actin filaments in vitro.Journal of Cell Biology 90, 467–73.
Saunders, J. C., Dear, S. P. &Schneider, M. E. (1985) The anatomical consequences of acoustic injury: a review and tutorial.Journal of the Acoustical Society of America 78, 833–60.
Selden, S. C. &Pollard, T. D. (1986) Interaction of actin filaments with microtubules is mediated by microtubule-associated proteins and regulated by phosphorylation.Annals of the New York Academy of Science 466, 803–12.
Shnerson, A. &Pujol, R. (1982) Age-related changes in the C57BL/6J mouse cochlea. I. Physiological findings.Developmental Brain Research 2, 65–75.
Slepecky, N., Hamernik, R. &Henderson, D. (1981) The consistent occurrence of a striated organelle (Friedmann Body) in the inner hair cells of the normal chinchilla.Acte Otolaryngologica 91, 189–98.
Sobkowicz, H. M. &Slapnick, S. M. (1992) Neuronal sprouting and synapse formation in response to injury in the mouse organ of Corti in culture.International Journal of Developmental Neuroscience 10, 545–66.
Sobkowicz, H. M., Bereman, B. &Rose, J. E. (1975) Organotypic development of the organ of Corti in culture.Journal of Neurocytology 4, 543–72.
Sobkowicz, H. M., Rose, J. E., Scott, G. L. &Holy, J. M. (1984) The ultrastructure of the developing organ of Corti of the mouse in culture. InUltrastructural Atlas of the Inner Ear (edited byFriedmann, I. &Ballantyne, J.) pp. 61–97. London: Butterworths.
Sobkowicz, H. M., August, B. K. &Slapnick, S. M. (1992) Epithelial repair following mechanical injury of the developing organ of Corti in culture: an electron microscopic and autoradiographic study.Experimental Neurology 115, 44–9.
Sobkowicz, H. M., Loftus, J. M. &Slapnick, S. M. (1993a) Tissue culture of the organ of Corti.Acte Otolaryngologica Supplementum 502, 3–36.
Sobkowicz, H. M., Slapnick, S. M. &August, B. K. (1993b) Axonemal forms and the Morphogenetic role of the kinocilium in auditory hair cells.Society for Neuroscience Abstracts 19, 1420.
Spira, A. W. (1975)In utero development and maturation of the retina of a non-primate mammal: a light and electron microscopic study of the guinea pig.Anatomy and Embryology 146, 279–300.
Spoendlin, H. H. (1964) Organization of the sensory hairs in the gravity receptors in utricule and saccule of the squirrel monkey.Zeitschrift für Zellforschung und Mikroskopische Anatomie 62, 701–16.
Staecker, H., Lefebvre, P., Malgrange, B., Moonen, G. &Van De Water, T. R. (1995) Technical Comments: regeneration and mammalian auditory hair cells (response toS. Chardin & R. Romand).Science 267, 707–11.
Steyger, P. S., Furness, D. N., Hackney, C. M. &Richardson, G. P. (1989) Tubulin and microtubules in cochlear hair cells: comparative immunocytochemistry and ultrastructure.Hearing Research 42, 1–16.
Takasaka, T. &Smith, C. A. (1971) The structure and innervation of the pigeon's basilar papilla.Journal of Ultrastructure Research 35, 20–65.
Tamm, S. &Tamm, S. L. (1988) Development of macrociliary cells inBeroe: L Actin bundles and centriole migration.Journal of Cell Science 89, 67–80.
Tilney, L. G. &Goddard, J. (1970) Nucleating sites for the assembly of cytoplasmic microtubules in the ectodermal cells of blastulae ofArbacia punctulata.Journal of Cell Biology 46, 564–75.
Tilney, L. G., Bonder, E. M. &Derosier, D. J. (1981) Actin filaments elongate from their membrane-associated ends.Journal of Cell Biology 90, 485–94.
Tilney, L. G., Tilney, M. S., Saunders, J. S. &Derosier, D. J. (1986) Actin filaments, stereocilia, and hair cells of the bird cochlea: III. The development and differentiation of hair cells and stereocilia.Developmental Biology 116, 100–18.
Tokuyasu, K. &Yamada, E. (1959) The fine structure of the retina studied with the electron microscope: IV. Morphogenesis of outer segments of retinal rods.Journal of Biophysical and Biochemical Cytology 6, 225–37.
Tucker, J. B., Paton, C. C., Richardson, G. P., Mogensen, M. M. &Russell, I. J. (1992) A cell surface-associated centrosomal layer of microtubule-organizing material in the inner pillar cell of the mouse cochlea.Journal of Cell Science 102, 215–26.
Wiederhold, M. L. (1976) Mechanosensory transduction in ‘sensory’ and ‘motile’ cilia.Annual Review of Biophysical Bioengineering 5, 39–62.
Zeigel, R. F. (1962) On the occurrence of cilia in several cell types of the chick pancreas.Journal of Ultrastructure Research 7, 286–92.
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Sobkowicz, H.M., Slapnick, S.M. & August, B.K. The kinocilium of auditory hair cells and evidence for its morphogenetic role during the regeneration of stereocilia and cuticular plates. J Neurocytol 24, 633–653 (1995). https://doi.org/10.1007/BF01179815
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DOI: https://doi.org/10.1007/BF01179815