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Bovine olfactory and nasal respiratory epithelium surfaces

High-voltage and scanning electron microscopy, and cryo-ultramicrotomy

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Summary

High-voltage transmission electron microscopy and cryo-ultramicrotomy together with scanning electron microscopy and some conventional transmission electron microscopy of ultrathin sections have been applied to the mucous surfaces of bovine olfactory and respiratory epithelia. Distal segments of olfactory cilia tend to run in parallel and could be followed over distances up to about 30 μm using high-voltage electron microscopy. This technique and scanning electron microscopy showed that on average 12–13 of such cilia could be observed per nerve ending. After correction for obscured cilia this number becomes about 17. High-voltage micrographs and micrographs made from sections prepared with a cryo-ultramicrotome showed the presence of electron-lucent pockets inside the olfactory mucus. The latter technique also showed that the mucus itself is not fibrous, but rather a continuum varying in electron density. The mucus layer contains various granular structures. Ciliary and microvillar membranes appear thicker with cryo-ultramicrotomy than when the sections are prepared with conventional techniques. The cores of the axonemal microtubules in olfactory as well as in respiratory cilia are darkly stained with this technique. Vesicles present inside the nerve endings are also darkly stained. Dimensions and some other numerical values of interest in olfaction are presented.

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References

  • Allen, R.D.: A reinvestigation of cross-sections of cilia. J. Cell Biol. 37, 825–831 (1968)

    Google Scholar 

  • Altner, H., Kolnberger, I.: The application of transmission electron microscopy on the study of the olfactory epithelium of vertebrates. In: Methods in olfactory research (D.G. Moulton, A. Turk and J.W. Johnston, Jr., eds.), pp. 163–190. London: Acad. Press 1975

    Google Scholar 

  • Andres, K.H.: Neue morphologische Grundlagen zur Physiologie des Riechens und Schmeckens. Arch. Oto-Rhino-Laryng. 210, 1–41 (1975)

    Google Scholar 

  • Andrews, P.M.: A scanning electron microscopic study of the extra pulmonary respiratory tract. Amer. J. Anat. 139, 399–423 (1974)

    Google Scholar 

  • Barber, V.C.: Cilia in sense organs. In: Cilia and flagella (M.A. Sleigh, ed.), pp. 403–433. London: Acad. Press 1974

    Google Scholar 

  • Beeston, B.E.P.: High voltage electron microscopy of biological specimens: some practical considerations. J. Microsc. (Oxf.) 98, 402–416 (1972)

    Google Scholar 

  • Bernhard, W., Viron, A.: Improved techniques for the preparation of ultrathin frozen sections. J. Cell Biol. 49, 731–746 (1971)

    Google Scholar 

  • Blank, D.L., Gesteland, R.C., Jansyn, E.M., Wagner, A.L.: Stimulus-related activity of olfactory receptor cilia. Fed. Proc. 37, 398, Abstr. 976 (1978)

    Google Scholar 

  • Boisvieux-Ulrich, E., Sandoz, D., Chailly, B.: A freeze-fracture and thin section study of the ciliary necklace in quail oviduct. Biol. Cell. 30, 245–252 (1977)

    Google Scholar 

  • Breipohl, W., Bijvank, G.J., Pfefferkorn, G.: Scanning electron microscopy of various sensory receptor cells in different vertebrates. In: Scanning electron microscopy, Vol 7 (O. Johari and I. Corvin, eds.), pp. 557–564. Chicago: IIT Res. Inst. 1974

    Google Scholar 

  • Breipohl, W., Bijvank, G.J., Zippel, H.P.: Rastermikroskopische Untersuchungen der olfaktorischen Rezeptoren im Riechepithel des Goldfisches (Carassius auratus). Z. Zellforsch. 138, 439–454 (1973)

    Google Scholar 

  • Breipohl, W., Fernández, M.: Scanning electron microscopic investigations of olfactory epithelium in the chick embryo. Cell Tiss. Res. 183, 105–114 (1977)

    Google Scholar 

  • Bronshtein, A.A.: Odour receptors of vertebrates. Monograph. Leningrad: Acadamy of Sciences USSR; Institute of comparative physiology and biochemistry 1977

    Google Scholar 

  • Bronshtein, A.A., Minor, A.V.: The regeneration of olfactory flagella and restoration of electroolfactogram after treatment of the olfactory mucosa with Triton X-100. Tsitologya (SSSR) 19, 33–39 (1977)

    Google Scholar 

  • Busuttil, A., More, I.A.R., McSeveney, D.: A reappraisal of the ultrastructure of the human respiratory nasal mucosa. J. Anat. (Lond.) 124, 445–458 (1977)

    Google Scholar 

  • Caprio, J., Raderman-Little, R.: Scanning electron microscopy of the channel catfish olfactory lamellae. Tissue & Cell 10, 1–9 (1978)

    Google Scholar 

  • Cavalier-Smith, T.: Basal body and flagellar development during the vegetative cell cycle and the sexual cycle of Chlamydomonas reinhardii. J. Cell Sci. 16, 529–556 (1974)

    Google Scholar 

  • Chapman, D., Wallach, D.F.H.: Recent physical studies of phospholipids and natural membranes. In: Biological membranes. Physical fact and function (D. Chapman, ed.), pp. 125–202. London: Acad. Press 1968

    Google Scholar 

  • DeLorenzo, A.J.D.: The olfactory neuron and the blood-brain barrier. In: Taste and smell in vertebrates (G.E.W. Wolstenholme and J. Knight, eds.), pp. 151–176. London: J. & A. Churchill1970

    Google Scholar 

  • Dirksen, R.E.: Centriole morphogenesis in developing ciliated epithelium of the mouse oviduct. J. Cell Biol. 51, 286–302 (1971)

    Google Scholar 

  • Dodd, G.H.: The adenosine triphosphate activities of the olfactory mucosae of some common animals. Comp. Biochem. Physiol. 36, 633–637 (1970)

    Google Scholar 

  • Dodson, H.C.: Ultrastructural and autoradiographic studies of the mammalian olfactory system. Ph.D. Thesis Guy's Hospital Medical School 1975

  • Echlin, P.: Sputter coating techniques for scanning electron microscopy. In: Scanning electron microscopy, Vol. 8 (O. Johari and I. Corvin, eds.), pp. 217–224. Chicago: IIT Res. Inst. 1975

    Google Scholar 

  • Farvard, P., Carasso, N.: The preparation and observation of thick biological sections in the high voltage electron microscope. J. Microsc. (Oxf.) 97, 59–81 (1973)

    Google Scholar 

  • Franks, F., Asquith, M.H., Hammond, C.C., Skaer, H. le B., Echlin, P.: Polymeric cryoprotectants in the preservation of biological ultrastructure. I. Low temperature states of aqueous solutions of hydrophilic polymers. J. Microsc. (Oxf.) 110, 223–238 (1977)

    Google Scholar 

  • Gasser, H.S.: Olfactory nerve fibers. J. gen. Physiol. 39, 473–496 (1956)

    Google Scholar 

  • Gilula, N.B., Satir, P.: The ciliary necklace. A ciliary membrane specilization. J. Cell Biol. 53, 494–509 (1972)

    Google Scholar 

  • Glauert, A.M.: The high voltage electron microscope in biology. J. Cell Biol. 63, 717–748 (1974)

    Google Scholar 

  • Glauert, A.M., Glauert, R.H.: Araldite as an embedding medium for electron microscopy. J. biophys. biochem. Cytol. 4, 191–194 (1958)

    Google Scholar 

  • Glees, P., Spoerri, P.E.: Surface processes of olfactory receptors. Cell Tiss. Res. 188, 149–152 (1978)

    Google Scholar 

  • Graziadei, P.P.C.: The olfactory mucosa of vertebrates. In: Handbook of sensory physiology, Vol. IV: Chemical senses, part 1: Olfaction (L.M. Beidler, ed.), pp. 27–58. Berlin-Heidelberg-New York: Springer 1971

    Google Scholar 

  • Graziadei, P.P.C.: The ultrastructure of vertebrates olfactory mucosa. In: The ultrastructure of sensory organs (I. Friedman, ed.), pp. 267–305. Amsterdam: North-Holland Publ. Co. 1973

    Google Scholar 

  • Graziadei, P.P.C.: The olfactory organ of vertebrates: A survey. In: Essays on the nervous system (R. Bellairs and E.G. Gray, eds.), pp. 191–222. Oxford: Clarendon Press 1974

    Google Scholar 

  • Graziadei, P.P.C.: Application of scanning electron microscopy and autoradiography in the study of olfactory mucosa. In: Methods in olfactory research (D.G. Moulton, A. Turk and J.W. Johnston, Jr., eds.), pp. 191–240. London: Acad. Press1975

    Google Scholar 

  • Graziadei, P., Bannister, L.H.: Some observations on the fine structure of the olfactory epithelium in the domestic duck. Z. Zellforsch. 80, 220–228 (1967)

    Google Scholar 

  • Heist, H.E., Mulvaney, B.D., Landis, D.J.: Odor sensing cell ultrastructure by electron microscopy. Final report Air Force Scientific Research Contract No. AF49(638)-1618. Hopkins, Minnesota: Honeywell Inc. Corporate Research Center 1967

    Google Scholar 

  • Holley, A., MacLeod, P.: Transduction et codage des informations olfactives chez les vertébrés. J. Physiol. (Paris) 73, 725–828 (1977)

    Google Scholar 

  • Ichikawa, M., Ueda, K.: Fine structure of the olfactory epithelium in the goldfish, Carassius auratus. Cell Tiss. Res. 183, 445–455 (1977)

    Google Scholar 

  • Karnovsky, M.J.: A formaldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137A-138A (1965)

    Google Scholar 

  • Kerjaschki, D.: Some freeze-etching data on the olfactory epithelium. In: Olfaction and taste, Vol. VI (J. LeMagnen and P. MacLeod, eds.), pp. 75–85. London and Washington: Information Retrieval Ltd. 1978

    Google Scholar 

  • Kerjaschki, D., Hörandner, H.: The development of mouse olfactory vesicles and their cell contacts: A freeze-etching study. J. Ultrastruct. Res. 54, 420–444 (1976)

    Google Scholar 

  • Kind, J., Krieg, J.: Unfixierte Cytomembranen in Gefrierultradünnschnitten. Cytobiology 7, 145–151 (1973)

    Google Scholar 

  • Koyama, N., Sawada, K., Kurihara, K.: Isolation and some properties of plasma membranes from bovine olfactory epithelium. Biochim. biophys. Acta (Amst.) 241, 42–48 (1971)

    Google Scholar 

  • Kratzing, J.E.: The olfactory mucosa of the sheep. Aust. J. biol. Sci. 23, 447–458 (1970)

    Google Scholar 

  • Kuhn III, C., Engleman, W.: The structure of the tips of mammalian respiratory cilia. Cell Tiss. Res. 186, 491–498 (1978)

    Google Scholar 

  • Lenz, H.: The human olfactory surface in the scanning electron microscope. Acta oto-laryng. (Stockh.) 84, 145–154 (1977)

    Google Scholar 

  • Lewis, E.R., Nemanic, M.K.: Critical point drying techniques. In: Scanning electron microscopy, Vol. 6 (O. Johari and I. Corvin, eds.), pp. 768–774. Chicago: IIT Res. Inst. 1973

    Google Scholar 

  • Locke, M., Krishnan, N.: Hot alcoholic phosphotungstic acid and uranyl acetate as routine stains for thick and thin sections. J. Cell Biol. 50, 550–557 (1971)

    Google Scholar 

  • Locke, M., Krishnan, N., McMahon, J.T.: A routine method for obtaining high contrast without staining sections. J. Cell Biol. 50, 540–544 (1971)

    Google Scholar 

  • Luftig, R.B., Wehrli, E., McMillan, P.N.: The unit membrane: A re-evaluation. Life Sci. 21, 285–300 (1977)

    Google Scholar 

  • Markham, R., Frey, S., Hills, G.J.: Methods for the enhancement of image detail and accentuation of structure in electron microscopy. Virology 20, 88–102 (1963)

    Google Scholar 

  • Masson, C., Kouprach, S., Giachetti, I., MacLeod, P.: Relation between intramembranous particle density of frog olfactory cilia and E.O.G. response. In: Olfaction and taste, Vol VI (J. LeMagnen and P. MacLeod, eds.), p. 195. London and Washington: Information Retrieval Ltd. 1978

    Google Scholar 

  • Menco, B.P.M.: A qualitative and quantitative investigation of olfactory and nasal respiratory mucosal surfaces of cow and sheep based on various ultrastructural and biochemical methods. Communications Agricultural University, Wageningen 77–13, 1–157 (1977)

    Google Scholar 

  • Menco, B.P.M.: Freeze-etch morphology of olfactory and respiratory nasal hairlets in rat, cow and frog. In: Olfaction and taste, Vol. VI (J. LeMagnen and P. MacLeod, eds.), p. 199. London and Washington: Information Retrieval Ltd. 1978

    Google Scholar 

  • Menco, B.P.M., Dodd, G.H., Davey, M., Bannister, L.H.: Presence of membrane particles in freezeetched bovine olfactory cilia. Nature (Lond.) 263, 597–599 (1976)

    Google Scholar 

  • Moran, D.T., Carter Rowley III, J., Zill, S.N., Varela, F.G.: The mechanism of sensory transduction in a mechanoreceptor. J. Cell Biol. 71, 832–847 (1976)

    Google Scholar 

  • Moran, D.T., Varela, F.H., Carter Rowley III, J.: Evidence for active role of cilia in sensory transduction. Proc. nat. Acad. Sci. (Wash.) 74, 793–797 (1977)

    Google Scholar 

  • Negus, V.: The comparative anatomy and physiology of the nose and paranasal sinuses. Edinburgh: E. & S. Livingstone 1958

    Google Scholar 

  • Nermut, M.V.: Negative staining. In: Methodensammlung der Elektronenmikroskopie (G. Schimmel and W. Vogell, eds.), 3.1.2.3. Stuttgart: Wissenschaftliche Verlagsgesellschaft 1973

    Google Scholar 

  • Nørrevang, A., Wingstrand, K.G.: On the occurrence and structure of choanocyte-like cells in some Echinoderms. Acta zool. (Stockh.) 51, 249–270 (1970)

    Google Scholar 

  • Ottoson, D., Shepherd, G.M.: Experiments and concepts in olfactory physiology. In: Progress in brain research Vol. 23, Sensory mechanisms (Y. Zotterman, ed.), pp. 83–138. Amsterdam: Elsevier Publ. Co. 1967

    Google Scholar 

  • Pitelka, D.R.: Basal bodies and root structures. In: Cilia and flagella (M.A. Sleigh, ed.), pp. 437–469. London: Acad. Press 1974

    Google Scholar 

  • Poulsen, J., Tos, M.: Goblet cells in the developing human nose. Acta oto-laryng. (Stockh.) 80, 434–442 (1975)

    Google Scholar 

  • Poynder, T.M.: Transduction mechanisms in chemoreception. London: Information Retrieval Ltd. 1974

    Google Scholar 

  • Saetersdal, T.S., Myklebust, R., Engedal, H., Ødegaarden, S.: Substructure of inner mitochondrial membranes of myocardial cells as shown by cryo-ultramicrotomy. Cell Tiss. Res. 186, 13–24 (1978)

    Google Scholar 

  • Seifert, K.: Die Ultrastruktur des Riechepithels beim Makrosmatiker. Eine elektronenmikroskopische Untersuchung. Normale und Pathologische Anatomie, Heft 21 (W. Bargmann and W. Doerr, eds.). Stuttgart: Georg Thieme Verlag 1970

    Google Scholar 

  • Spoendlin, H.: Auditory, vestibular, olfactory and gustatory organs. In: Ultrastructure of the peripheral nervous system and sense organs. Atlas of normal and pathologic anatomy (J. Bischoff, ed.), pp. 173–326, 447. Stuttgart: Georg Thieme Verlag 1970

    Google Scholar 

  • Summers, K.: The role of flagellar structures in motility. Biochim. biophys. Acta (Amst.) 416, 153–168 (1975)

    Google Scholar 

  • Tokuyasu, K.T.: Membranes as observed in frozen sections. J. Ultrastruct. Res. 55, 281–287 (1976)

    Google Scholar 

  • Usukura, J., Yamada, E.: Observations on the membrane fine structure of the newt olfactory cell by freeze replica method. Zool. Mag. (Tokyo) 84, 339 (1975)

    Google Scholar 

  • Usukura, J., Yamada, E.: Observations on the cytolemma of the olfactory receptor cell in the newt. 1. Freeze replica analysis. Cell Tiss. Res. 188, 83–98 (1978)

    Google Scholar 

  • Venable, J.H., Coggeshall, R.: A simplified lead citrate stain for use in electron microscopy. J. Cell Biol. 25, 407–408 (1965)

    Google Scholar 

  • Vinnikov, Ya.A.: Sensory reception. Cytology, molecular mechanisms and evolution. In: Molecular biology, biochemistry and biophysics, Vol. 17 (A. Kleinzeller, G.F. Springer and H.G. Wittman, eds.). Berlin-Heidelberg-New York: Springer 1974

    Google Scholar 

  • Vogel, F.: Cryo-ultramicrotomie — eine alternative Präparationsmethode zur konventionellen Objektpräparation in der Elektronenmikroskopie. Acta histochem. (Jena) Suppl. 17, 297–306 (1976

    Google Scholar 

  • Vogel, F.: Ultrastructure of unfixed plasma membranes in ultrathin frozen sections. J. Microsc. (Oxf.) 110, 277–280 (1977)

    Google Scholar 

  • Yamamoto, M.: An electron microscopic study of the olfactory mucosa in the bat and rabbit. Arch. histol. jap. 38, 359–412 (1976)

    Google Scholar 

  • Yamamoto, M., Ueda, K.: Comparative morphology of fish olfactory epithelium-I. Salmoniformes. Bull. Jap. Soc. Sci. Fish. 43, 1163–1174 (1977)

    Google Scholar 

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Menco, B.P.M., Leunissen, J.L.M., Bannister, L.H. et al. Bovine olfactory and nasal respiratory epithelium surfaces. Cell Tissue Res. 193, 503–524 (1978). https://doi.org/10.1007/BF00225347

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