Summary
The “hairs” (stereocilia = stereovilli) of sensory cells from the inner ear of vertebrates are interconnected by several types of connectors, whose role is unknown. They appear to stabilize the hair bundle mechanically, and may be directly involved in mechano-electric transduction. Our transmission electron-microscopical investigation of sensory epithelia from two species of fish (Rutilus rutilus, Scardinius erythrophthalmus, both Leuciscidae) has shown that not only the connectors but also the surface charges of the membrane are important factors for determining the shape of the hair bundle and the spatial interrelation of the stereovilli. A reduction of the ionic strength in the medium leads to an increase in distance between the stereovilli. This may be the result of an extension of the spread of the surface potential of the membrane at low ionic strength. The connectors are not broken by the increase in distance between the stereovilli. They are EDTA (ethylene-diamine-tetra-acetic-acid) resistant as are some cell adhesion molecules such as N-CAM (nerve-cell adhesion molecule) and protein A from Dictyostelium discoideum. The connectors do not prevent polycation-induced fusion of adjacent stereovillar membranes.
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Bagger-Sjöbäck D, Wersäll J (1976) Toxic effects of gentamycin on the basilar papilla in the lizard Calotes versicolor. Acta Otolaryngol 81:57–65
Barber J (1982) Influence of surface charges on thylakoid structure and function. Ann Rev Plant Physiol 33:261–295
Bretscher A (1981) Characterization and ultrastructural role of the major components of the intestinal microvillus cytoskeleton. Cold Spring Harb Symp Quant Biol 46:871–879
Comis SD, Pickles JO, Osborne MP (1985) Osmium tetroxide postfixation in relation to the crosslinkage and spatial organization of stereocilia in the guinea-pig cochlea. J Neurocytol 14:113–130
Crawford AC, Fettiplace R (1985) The mechanical properties of ciliary bundles of turtle cochlear hair cells. J Physiol 364:359–379
Edelman GM (1985) Cell adhesion molecule expression and the regulation of morphogenesis. Cold Spring Harbor Symp Quant Biol 50:877–899
Edelman GM, Hoffman S, Chuong C-M, Tiery J-P, Brackenbury R, Gallin WJ, Grumet M, Greenberg ME, Hemperly JJ, Cohen C, Cunningham BA (1983) Structure and modulation of neural cell adhesion molecules in early and late embryogenesis. Cold Spring Harbor Symp Quant Biol 48:515–526
Engström B (1983) Stereocilia of sensory cells in normal and hearing impaired ears. A morphological, physiological and behavioural study. Scand Audiol [Suppl] 19
Flock A, Flock B, Murray E (1977) Studies on the sensory hairs of receptor cells in the inner ear. Acta Otolaryngol 83:85–91
Flock A, Bretscher A, Weber K (1982) Immunohistochemical localization of cytoskeletal proteins in inner ear sensory and supporting cells. Hear Res 6:75–89
Furness DN, Hackney CM (1985) Cross-links between the stereocilia in the guinea-pig cochlea. Hear Res 18:177–188
Gerisch G (1986) Inter-relation of cell adhesion and differentiation in Dictyostelium discoideum. J Cell Sci [Suppl] 4:201–219
Glenney jr. JR, Kaulfus P, Matsudaira P, Weber K. (1981) F-actin binding and bundling properties of fimbrin, a major cytoskeletal protein of microvillus core filaments. J Biol Chem 256:9283–9288
Hirokawa N, Tilney LG (1982) Interactions between actin filaments and between actin filaments and membranes in quick frozen and deeply etched hair cells of the chick inner ear. J Cell Biol 95:249–261
Hopwood D (1985) Cell and tissue fixation, 1972–1982. Histochem J 17:389–442
Hudspeth AJ (1983) Mechano electrical transduction by hair cells in the acousticolateralis sensory system. Ann Rev Neurosci 6:187–215
Hui SW, Isac T, Boni LT, Sen A (1985) Action of polyethylene glycol on the fusion of human erythrocyte membranes. J Membr Biol 84:137–146
Jahnke K (1975) The fine structure of freeze-fractured intercellular junctions in the guinea pig inner ear. Acta Otolaryngol [Suppl] 336:5–40
Kalina M, Pease DC (1977) The preservation of ultrastructure in saturated phosphatidyl cholines by tannic acid in model systems and type II pneumocytes. J Cell Biol 74:726–741
Küttner K (1974) Ultrahistochemische Darstellung der Glykokalyx an Zellen der Meerschweinchen-Cochlea durch RutheniumrotKontrastierung. Arch Oto-Rhino-Laryng 208:175–184
Little KF, Neugebauer D-Ch (1985) Interconnections between the stereovilli of the fish inner ear II. Systematic investigation of saccular hair bundles from Rutilus rutilus (Teleostei). Cell Tissue Res 242:427–432
Looseley-Millman ME, Rand RP, Parsegian VA (1982) Effects of monovalent ion binding and screening on measured electrostatic forces between charged phospholipid bilayers. Biophys J 40:221–232
Luft JH (1964) Electron microscopy of cell extraneous coats as revealed by ruthenium red staining. J Cell Biol 23:54A-55A
Maupin P, Pollard TD (1983) Improved preservation and staining of HeLa cell actin filaments, clathrin-coated membranes, and other cytoplasmic structures by tannic acid-glutaraldehyde-saponin fixation. J Cell Biol 96:51–62
McLaughlin S (1977) Electrostatic potentials at membrane-solution interfaces. Curr Top Membr Trans 9:71–144
Neugebauer D-C (1986a) The vestibular stereovillus membrane: An illustration of the “greater membrane” concept. J Oto Rhino-Laryngol 48:87–92
Neugebauer D-Ch (1986b) Interconnections between the stereovilli of the fish inner ear. III. Indications for developmental changes. Cell Tissue Res 246:441–453
Neugebauer D-Ch, Thurm U (1984) Chemical dissection of stereovilli from fish inner ear reveals differences from intestinal microvilli. J Neurocytol 13:797–808
Neugebauer D-Ch, Thurm U (1985) Interconnections between the stereovilli of the fish inner ear. Cell Tissue Res 240:449–453
Neugebauer D-Ch, Thurm U (1986) Surface charges influence the distances between vestibular stereovilli. Naturwissenschaften 73:508–509
Osborne MP, Comis SD, Pickles JO (1984) Morphology and cross-linkage of stereocilia in the guinea-pig labyrinth examined without the use of osmium as a fixative. Cell Tissue Res 237:43–48
Overbeek JThG (1952) The interaction between colloid particles. In: Kruyt HR (ed) Colloid Science Vol. 1. Elsevier Publ Comp, Amsterdam, Houston, New York, London pp 245–277
Panneels P, Lannoye R (1986) Variations de la fluorescence et de la densité de charge des membranes de thylakoides d'Orge en cours du verdissement. Photosynthetica 20:56–60
Parsegian VA (1973) Long-range physical forces in the biological milieu. Annu Rev Biophys Bioeng 2:221–255
Pickles JO (1985) Recent advances in cochlear physiology. Progr Neurobiol 24:1–42
Ross M (1974) The tectorial membrane of the rat. Am J Anat 139:449–482
Rusch A (1985) Sensorische und motorische Aktivität vestibulärer Haarsinneszellen im Jugendstadium des Aals Anguilla anguilla L. Diplomarbeit, Fachbereich Biologie, Universität Münster
Satir P (1977) Microvilli and cilia: surface specializations of mammalian cells. In: Jamieson GA, Robinson DN (eds) Mammalian cell membranes. Vol. II, Butterworths, London, Boston, pp 323–353
Schmidt B, Thurm U (1984) Structures transmitting stimulatory force to the sensory hairs (stereovilli) of the frog sacculus. Verh Dtsch Zool Ges 77:326
Scott J (1980) Collagen-proteoglucan interactions. Biochem J 187:887–891
Simionescu N, Simionescu M (1976) Galloylglucoses of low molecular weight as mordant in electron microscopy. I. Procedure, evidence for mordanting effect. J Cell Biol 70:608–621
Slepecky N, Chamberlain SC (1985) The cell coat of the inner ear sensory and supporting cells as demonstrated by ruthenium red. Hear Res 17:281–288
Sobin A, Anniko M (1983) Embryonic development of the specific vestibular hair cell pathology in a strain ot the waltzing guinea pig. Acta Otolaryng 96:397–405
Spurr AR (1969) A low viscosity resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43
Vassar PS, Hards JM, Brooks DE, Hagenberger B, Seaman GVF (1972) Physicochemical effects of aldehydes on the human erythrocyte. J Cell Biol 53:809–818
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Neugebauer, D.C., Thurm, U. Surface charges of the membrane and cell adhesion substances determine the structural integrity of hair bundles from the inner ear of fish. Cell Tissue Res. 249, 199–207 (1987). https://doi.org/10.1007/BF00215434
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DOI: https://doi.org/10.1007/BF00215434