Summary
Olfactory axons and apical structures of olfactory epithelia and of nasal respiratory epithelia of rat embryos were studied with the freeze-fracture technique; adult tissue samples of the same sources were used for comparison. At the onset of epithelial differentiation (14th gestational day) intramembranous particle densities are the same for all structures in both epithelial types. During further development, particle densities in membranes of primary cilia remain lower than those in membranes of other apical structures. Otherwise, I found the following from the 14th to the 19th day of gestation.a. Olfactory receptor cells of embryos of all age groups have axons wherein the membrane particle densities are about half those of adults. These densities are always lower than those of dendritic ending structures. Dendritic endings with primary cilia have lower densities than endings with secondary cilia; densities mainly increase when the endings sprout secondary cilia. Adult values are reached at the 18th day of gestation.b. Olfactory supporting cells with only globular particles in their apices gradually transform into, or are replaced by, supporting cells which also have dumbbell-shaped particles in their apices. Particle densities are always higher in apical structures of supporting cells than in apical structures of receptor cells. Adult values are reached at the 17th day of gestation.c. Putative ciliated and ciliated respiratory epithelial cells have considerably lower particle densities in membranes of their apical structures than do olfactory epithelial cells. Of special interest is that this is also true for secondary respiratory and olfactory cilia; as soon as genesis of secondary cilia in either epithelial type begins, their membrane features differ. Also, in contrast to apical structures of the olfactory epithelium, particle densities in apical structures of the respiratory epithelium do not systematically change during pre-natal development, and resemble the density values of adults. An exception are the microvilli of the respiratory cells with secondary cilia, membranes of which have considerably higher particle densities in adults than in embryos. In conclusion: Transformations of olfactory receptor cell dendritic endings with primary cilia into endings with secondary cilia, and of olfactory supporting cells with globular particles in their apices into cells with dumbbell-shaped particles in their apices are accompanied by increases in the densities of their intramembranous particles. These developmental changes parallel the electrophysiological onset of olfactory receptor cell specificity.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Allen WK, Akeson R (1986) Identification of an olfactory receptor neuron subelass: Cellular and molecular analysis during development. Dev Biol 109:392–401
Arima T, Yamamoto T (1983) A freeze-fracture study of perinatal changes of intramembranous particles in microvilli of absorbtive cells in mouse small intestine. Cell Tissue Res 233:549–561
Besharse JC, Forestner DM, Defoe DM (1985) Membrane assembly in retinal photoreceptors. III. Distinct membrane domains in the connecting cilium of developing rods. J Neurosci 5:1035–1048
Black JA, Foster RE, Waxman SC (1983) Freeze-fracture ultrastructure of developing and adult non-myelinated ganglion cell axolemma in the retinal nerve fibre layer. J Neurocytol 12:201–212
Branton D, Bullivant S, Gilula NB, Karnovsky MJ, Moor H, Mühlethaler K, Northcote DH, Packer L, Satir B, Satir P, Speth V, Staehelin LA, Steere RL, Weinstein S (1975) Freeze-etching nomenclature Science 190:54–56
Breipohl W, Mendoza AS, Miragall F (1982) Freeze-fracturing studies on the main and vomeronasal olfactory sensory epithelia in NMRI-mice. In: Breipohl W (ed) Olfaction and endocrine regulation. IRL Press Ltd, London, pp 309–322
Bridgman PC, Nakajima AS, Greenberg AS, Nakajima Y (1984) Freeze-fracture and electrophysiological studies of newly developed acetylcholine receptors inXenopus embryonic muscle cells. J Cell Biol 98:2160–2173
Brown D, Ilic V, Orci L (1982) Rod-shaped particles in the plasma membrane of the mitochondria-rich cell of the amphibian epidermis. Anat Rec 192:269–275
Carr VMcM, Farbman AI, Colletti LM, Lidow MS, Hempstead JL, Morgan JI (1988) Developmental expression of reactivity to monoclonal antibodies generated against olfactory epithelia. J Neurosci (in press)
Chailley B, Boisvieux-Ulrich E (1985) Detection of plasma membrane cholesterol by filipin during microvillogenesis and ciliogenesis in quail oviduct. J Histochem Cytochem 33:1–10
Chailley B, Boisvieux-Ulrich E, Sandoz D (1982) Ciliary membrane events during ciliogenesis of the quail oviduct. Biol Cell 46:51–64
Chailley B, Boisvieux-Ulrich E, Sandoz D (1983) Evolution of filipin-sterol complexes and intramembrane particle distribution during ciliogenesis. J Submicrosc Cytol 15:275–280
Cosson MP, Gulik A (1982) Description of the mitochondria-axoneme junction in sea urchin spermatozoa: Presence of a flagellar necklace. J Ultrastruct Res 79:47–57
Cuschieri A, Bannister LH (1975) The development of the olfactory mucosa in the mouse: electron microscopy. J Anat 119:471–498
Farbman AI (1986) Prenatal development of mammalian olfactory receptor cells. Chem Sens 11:3–18
Farbman AI, Carr VMcM, Morgan JI, Hempstead JL (1987) Immunofluorescent studies of the development of rat olfactory epithelium. Ann NY Acad Sci 510:271–272
Farbman AI, Menco BPhM (1986) Development of olfactory epithelium in the rat. In: Breipohl W (ed) Ontogeny of olfaction. Principles of olfactory maturation in vertebrates. Springer, Berlin Heidelberg New York, pp 45–56
Favre D, Bagger-Sjöback D, Mbiene J-P, Sans, A (1986) Freeze-fracture study of the vestibular hair cell surface during development. Anat Embryol 175:69–76
Garcia-Segura LM, Perrelet A (1981) Freeze-fracture of developing plasma membrane in postnatal cerebellum. Brain Res 208:19–33
Gesteland RC, Yancey RA, Farbman AI (1982) Development of olfactory receptor neuron selectivity in the rat fetus. Neuroscience 7:3127–3136
Getchell ML, Zielinski B, DeSimone JA, Getchell TV (1987) Odorant stimulation of secretory and neural processes in the salamander olfactory mucosa. J Comp Physiol A 160:155–168
Getchell TV (1986) Functional properties of vertebrate olfactory receptor neurons. Physiol Rev 66:772–818
Gilula NB, Satir P (1972) The ciliary necklace. A ciliary membrane specialization. J Cell Biol 53:494–509
Holley A, Mac Leod P (1977) Transduction et codage des informations olfactives chez les vertébrés. J Physiol (Paris) 73:725–848
Hörandner H, Kerjaschki D, Stockinger L (1974) Rodshaped particles in epithelial free surface membranes. In: Sanders JV, Goodchild DJ (eds) Proceedings eighth international congress on electron microscopy, vol II. Australian Academy of Sciences, Canberra, pp 210–211
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137–138
Kerjaschki D (1977) Some freeze-etching data on the olfactory epithelium. In: Le Magnen J, Mac Leod P (eds) Olfaction and taste VI. Information Retrieval, London, pp 75–85
Kerjaschki D, Hörandner H (1976) The development of mouse olfactory vesicles and their contacts: A freeze-etching study. J Ultrastruct Res 54:420–444
Köling A, Rask-Andersen H, Deuschl H (1986) A freeze-fracture study of receptor axons and Schwann cells in the human olfactory mucosa. Acta Otolaryngol (Stockh) 102:494–499
Lancet D (1986) Vertebrate olfactory reception. Ann Rev Neurosci 9:329–355
Lessner U, Rehn B (1987) Ultrastructural analysis of the mouse nasal septum. Respiratory cilia prior to and after birth. A quantitative freeze-fracture study. Acta Anat 130:232–236
Lidow MS, Menco BPhM (1984) Observations on axonemes and membranes of olfactory and respiratory cilia in frogs and rats using tannic acid-supplemented fixation and photographic rotation. J Ultrastruct Res 86:18–30
Lidow MS, Farbman AI, Morgan JI, Hempstead J (1987) In vivo and in vitro studies of the localization of antigens recognized by monoclonal antibodies Neu-4, Neu-5 and Neu-9 in rat olfactory epithelium. Chemsens 12:676
Mania-Farnell B, Farbman AI (1987) Immunohistochemical localization of GTP-binding protein in rat olfactory epithelium during prenatal development. Chemsens 12:678
Margolis, FL, Kawano T, Grillo M (1986) Ontogeny of carnosine, olfactory marker protein and neurotransmitter enzymes in olfactory bulb and olfactory mucosa of the rat. In: Breipohl W (ed) Ontogeny of olfaction. Principles of olfactory maturation in vertebrates. Springer, Berlin Heidelberg New York, pp 107–116
Menco BPhM (1977) A qualitative and quantitative investigation of olfactory and nasal respiratory mucosal surfaces of cow and sheep based on various ultrastructural and biochemical techniques. Commun Agricult Univ Wageningen 77–13:1–157
Menco BPhM (1980a) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory structures of frog, ox, rat, and dog. I. A general survey. Cell Tissue Res 207:183–209
Menco BPhM (1980b) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory epithelial surfaces of frog, ox, rat, and dog. II. Cell apices, cilia, and microvilli. Cell Tissue Res 211:5–30
Menco BPhM (1980c) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory epithelial surfaces of frog, ox, rat, and dog. III. Tight-junctions. Cell Tissue Res 211:361–373
Menco BPhM (1980d) Qualitative and quantitative freeze-fracture studies on olfactory and nasal respiratory epithelial surfaces of frog, ox, rat, and dog. IV. Ciliogenesis and ciliary necklaces (Including high-voltage observations). Cell Tissue Res 212:1–16
Menco BPhM (1983) The ultrastructure of olfactory and nasal respiratory epithelium surfaces. In: Reznik G, Stinson SF (eds) Nasal tumors in animals and man, vol. 1, anatomy, physiology and epidemiology. CRC Press Inc, Boca Raton, Florida, pp 45–102
Menco BPhM (1984) Ciliated and microvillous structures of rat olfactory and nasal respiratory epithelia. A study using ultrarapid cryo-fixation followed by freeze-substitution or freezeetching. Cell Tissue Res 235:225–241
Menco BPhM (1986) A survey of ultra-rapid cryofixation methods with particular emphasis on applications to freeze-fracturing, freeze-etching, and freeze-substitution. J Electron Microsc Techn 4:177–240
Menco BPhM (1987a) A freeze-fracture study on the prenatal development of ciliated surfaces in rat olfactory epithelia. Ann NY Acad Sci 510:491–493
Menco BPhM (1987b) The freeze-fracture morphology of developing rat olfactory epithelium surfaces. Neuroscience: S130 [Abstr] 387P
Menco BPhM (1988a) Tight-junctional strands first appear in regions where three cells meet in differentiating olfactory epithelium. A freeze-fracture study. J Cell Sci 89:495–503
Menco BPhM (1988b) Pre-natal development of rat nasal epithelia. V. Freeze-fracturing on necklaces of primary and secondary cilia of olfactory and respiratory epithelial cells. Anat Embryol (in press)
Menco BPhM, Dodd GH, Davey M, Bannister LH (1976) Presence of membrane particles in freeze-etched bovine olfactory cilia. Nature 263:597–599
Menco BPhM, Farbman AI (1985a) Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. I. Olfactory epithelium, qualitative studies. J Cell Sci 78:283–310
Menco BPhM, Farbman AI (1985b) Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. II. Olfactory epithelium, a morphometric analysis. J Cell Sci 78:311–336
Menco BPhM, Farbman AI (1985c) Membranes versus cytoskeleton; their respective roles in olfactory reception. Chem Sens 10:391 [Abstr] 11
Menco BPhM, Farbman AI (1987) Genesis of cilia and microvilli of rat nasal epithelia during pre-natal development. III. Respiratory epithelium surface, including a comparison with the surface of the olfactory epithelium. J Anat 152:145–160
Menco BPhM, Minner EW (1986) Freeze-fracture studies on primary and developing secondary cilia of olfactory and nasal respiratory epithelia in rat fetuses. J Electron Microsc 35 [Suppl]:2601–2602
Menco BPhM, Minner EW, Farbman AI (1988) Preliminary observations on rapidly-frozen, freeze-fractured and deep-etched rat olfactory cilia rotary-replicated with tantalum/tungsten. J Electron Microsc Techn 8:441–442
Miragall F, Breipohl W, Naguro T, Voss-Wermbler G (1984) Freeze-fracture study of the plasma membranes of the septal organ of Masera. J. Neurocytol 13:111–125
Morgan JI (1986) Immunocytochemical studies on the maturation of the rodent olfactory mucosa. In: Breipohl W (ed) Ontogeny of olfaction. Principles of olfactory maturation in vertebrates. Springer, Berlin Heidelberg New York, pp 95–103
Nakamura T, Gold GH (1987) A cyclic nucleotide-gated conductance in olfactory receptor cilia. Nature 325:442–444
Pace U, Hanski E, Solomon Y, Lancet D (1985) Odorant-sensitive adenylate cyclase may mediate olfactory reception. Nature 316:255–258
Rafols JA, Getchell TV (1983) Morphological relations between the receptor cell neurons, sustentacular cells and Schwann cells in the olfactory mucosa of the salamander. Anat Rec 206:87–101
Small RK, Pfenninger KH (1984) Components of the plasma membrane of growing axons. I. Size and distribution of intramembrane particles. J Cell Biol 98:1422–1433
Small RK, Blank M, Ghez R, Pfenninger KH (1984) Components of the plasma membrane of growing axons. II. Diffusion of membrane protein complexes. J Cell Biol 98:1434–1443
Smuts MS (1977) Concanavalin A binding to the epithelial surface of the developing mouse olfactory placode. Anat Rec 188:29–37
Taniguchi K, Taniguchi K, Mochizoki K (1982) Comparative developmental studies on the fine structure of the vomeronasal sensory and the olfactory epithelia in the golden hamster. Jpn J Vet Sci 44:881–890
Trotier D, Mac Leod P (1986) Intracellular recordings from salamander olfactory supporting cells. Brain Res 374:205–211
Usukura J, Yamada E (1978) Observations on the cytolemma of the olfactory receptor cell in the newt. 1. Freeze replica analysis. Cell Tissue Res 188:83–98
Whiteley HE, Young S (1985) Cilia in the fetal and neonatal canine retina. Tissue Cell 17:335–340
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Menco, B.P.M. Pre-natal development of rat nasal epithelia. Anat Embryol 178, 309–326 (1988). https://doi.org/10.1007/BF00698662
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00698662