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Substructure of solitary cilia in mouse kidney

Cell and Tissue Research volume 183, pages 281–290 (1977)Cite this article

Summary

Recent scanning electron microscopic studies confirm the presence of solitary cilia on most epithelial cells along the mammalian nephron and collecting ducts.

By transmission electron microscopy we have found that the axonemata of such cilia consist of a maximal number of 9 doublet and no singlet filaments. 10% of the cross-sectioned cilia contain 9 doublets arranged in a peripheral ring (9+0 pattern). 30 % of the cross-sections contain 8 or 7 doublets in peripheral ring and 1 or 2 doublets in the central region (8+1 and 7+2 patterns). Serial sections and goniometer tilt reveal the central doublets to originate as dislodged peripheral doublets. 60% of the sectioned cilia contain filament numbers between 8 and 4. In patterns of 5 and 4 filaments single microtubules predominate.

The functional significance of these atypical cilia is discussed.

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References

  • Afzelius, B.A.: Ultrastructure of cilia and flagella. In: Handbook of molecular cytology (Lima-de-Faria, ed.), pp. 1219–1242. Amsterdam: North-Holland 1969

    Google Scholar 

  • Afzelius, B.A., Eliasson, R., Johnson, Ø., Lindholmer, C.: Lack of dynein arms in immobile human spermatozoa. J. Cell Biol. 66, 225–232 (1975)

    PubMed  Article  CAS  Google Scholar 

  • Allen, F., Tisher, C.C.: Morphology of the ascending thick limb of Henle. Kidney International 9, 8–22 (1976)

    PubMed  Article  CAS  Google Scholar 

  • Andrews, P.M.: Scanning electron microscopy of human and Rhesus monkey kidneys. Lab. Invest. 32, 610–618 (1975)

    Google Scholar 

  • Andrews, P.M., Porter, K.R.: A scanning electron microscope study of the nephron. Amer. J. Anat. 140, 81–116 (1974)

    PubMed  Article  CAS  Google Scholar 

  • Archer, F.L., Wheatley, D.N.: Cilia in cell-cultured fibroblasts II. Incidence in mitotic and postmitotic BHK 21/C 13 fibroblasts. J. Anat. (Lond.) 109, 277–292 (1971)

    CAS  Google Scholar 

  • Barnes, B.G.: Ciliated secretory cells in the pars distalis of the mouse hypophysis. J. Ultrastruct. Res. 5, 453–467 (1961)

    PubMed  Article  CAS  Google Scholar 

  • Boquist, L.: Cilia in normal and regenerating islet tissue. An ultrastructural study in the Chinese hamster with particular reference to the β-cells and the ductular epithelium. Z. Zellforsch. 89, 519–532 (1968)

    Article  Google Scholar 

  • Bulger, R.E., Siegel, F.L., Pendergrass, R.: Scanning and transmission electron microscopy of the rat kidney. Amer. J. Anat. 139, 483–501 (1974)

    PubMed  Article  CAS  Google Scholar 

  • Bulger, R.E., Tisher, C.C., Myers, C.E., Trump, B.F.: Human renal ultrastructure II. The thin limb of Henle's loop and the interstitium in healthy individuals. Lab. Invest. 16, 124–141 (1967)

    PubMed  CAS  Google Scholar 

  • Currie, A.R., Whetley, D.N.: Cilia of a distinctive structure (9 + 0) in endocrine and other tissues. Postgrad. med. J. 42, 403–408 (1966)

    Article  Google Scholar 

  • Dahl, H.A.: Fine structure of cilia in rat cerebral cortex. Z. Zellforsch. 60, 369–386 (1963)

    PubMed  Article  CAS  Google Scholar 

  • Dahl, H.A.: On the cilium cell relationship in the adenohypophysis of the mouse. Z. Zellforsch. 83, 169–177 (1967)

    PubMed  Article  CAS  Google Scholar 

  • Duffy, L.J., Suzuki, Y.: Ciliated human renal proximal tubular cells. Observations in three cases of hypercalcaemia. Amer. J. Path. 53, 609–616 (1968)

    PubMed  CAS  Google Scholar 

  • Fawcett, D.W., Porter, K.R.: A study of the fine structure of ciliated epithelia. J. Morph. 94, 221–281 (1954)

    Article  Google Scholar 

  • Ferres-Torres, R.: Elektronenmikroskopische Untersuchungen über Zilien in menschlichen embryonalen Pankreas und ihre Bedeutung. Anat. Anz. 128, 311–315 (1971)

    Google Scholar 

  • Flood, P.R.: Dry-fracturing techniques for the study of soft internal biological tissues in the scanning electron microscope. In: Scanning electron microscopy (O. Johari and I. Corvin, eds.), pp. 287–294. Chicago: ITT Res. Inst. 1975

    Google Scholar 

  • Fonte, V.G., Searls, R.I., Hilfer, S.R.: The relationship of cilia with cell division and differentiation. J. Cell Biol. 49, 226–229 (1971)

    PubMed  Article  CAS  Google Scholar 

  • Hando, T., Okada, D.M., Zamboni, L.: Atypical cilia in human endometrium. J. Cell Biol. 39, 475–481 (1968)

    PubMed  Article  CAS  Google Scholar 

  • Hierholzer, K., Müller-Suur, R., Gutsche, H.-U., Butz, H., Lichtenstein, I.: Filtration in surface glomeruli as regulated by flow rate through the loop of Henle. Pflügers Arch. 352, 315–337 (1974)

    PubMed  Article  CAS  Google Scholar 

  • Kober, HJ., Herbst, R.: Die lumenseitige Oberfläche des Rattenoesophagus während der Ontogenese. Z. mikr.-anat. Forsch. 89, 399–409 (1975)

    CAS  Google Scholar 

  • Konrádová, V.: Atypical kinocilia in the tracheal epithelium. Folia morph. 21, 71–78 (1973)

    Google Scholar 

  • Kubota, K., Malloy, J.J., Low, F.N.: An unusual type of cilium. Amer. J. Anat. 144, 119–123 (1975)

    PubMed  Article  CAS  Google Scholar 

  • Latta, H., Maunsbach, A.B., Madden, S.C.: Cilia in different segments of the rat nephron. J. biophys. biochem. Cytol. 11, 248–252 (1961)

    PubMed  Article  CAS  Google Scholar 

  • Latta, H., Maunsbach, A.B., Osvaldo, L.: The fine structure of renal tubules in cortex and medulla. In: Ultrastructure of the kidney (A.J. Dalton and F. Haguenau, eds.), pp. 1–56. New York: Acad Press 1967

    Google Scholar 

  • Levieh, V.G.: Physicochemical hydrodynamics. London: Pentice Hall 1962

    Google Scholar 

  • Lucas, A.M., White, H.L.: Factors responsible for the abnormal distension of glomerular capsules in Necturus kidney. Anat. Rec. 53, 371–385 (1932)

    Article  Google Scholar 

  • Mannweiler, K., Bernard, W.: Recherches ultrastructurales sur une tumeur rénale expérimentale du Hamster. J. Ultrastruct. Res. 1, 158–169 (1957)

    PubMed  Article  CAS  Google Scholar 

  • Mollo, F., Canese, M.G., Bartoli, E.: Sulla presenza de ciglia in cellule epiteliali, endoteliali e mesangiali del corpusculo renale umano. Boll. Soc. Ital. biol. sper. 45, 185–187 (1969)

    PubMed  CAS  Google Scholar 

  • Myers, CE., Bulger, R.E., Tisher, C.C., Trump, B.F.: Human renal ultrastructure. IV. Collecting duct of healthy individuals. Lab. Invest 15, 1921–1950 (1966)

    PubMed  CAS  Google Scholar 

  • Nikai, H., Rose, G.G., Cattoni, M.: Electron microscopy of solitary cilia in human gingiva and rat oral mucosa. J. dent. Res. 49, 1141–1153 (1970)

    PubMed  Article  CAS  Google Scholar 

  • Patzelt, C., Singh, A., LeMarchand, Y., Jeanrenaud, B.: Characterization of hepatic microtubules: possible functional models. In: Microtubules and microtubule inhibitors (M. Borgers and M. de Brabander, eds.), pp. 165–176. Amsterdam: North-Holland 1975

    Google Scholar 

  • Pehlemann, F.-W.: Die amitotische Zellteilung. Eine elektronenmikroskopische Untersuchung an Interrenalzellen von Rana temporaria. Z. Zellforsch. 84, 516–548 (1968)

    PubMed  Article  CAS  Google Scholar 

  • Pfaller, W., Klima, J.: A critical reevaluation of the structure of the rat uriniferous tubule as revealed by scanning electron microscopy. Cell Tiss. Res. 166, 91–100 (1976)

    Article  CAS  Google Scholar 

  • Philips, D.M.: Structural variants in invertebrate sperm flagella and their relationship to motility. In: Cilia and flagella (MA. Sleigh, ed.), pp. 379–402. London: Academic Press 1974

    Google Scholar 

  • Rossman, P., Galle, P.: Mise en évidence de cellules renales ciliées chez l'homme. Nephron 5, 426–436 (1968)

    Article  Google Scholar 

  • Satir, P.: Studies on cilia. III. Further studies on the cilium tip and the “sliding filament” model of ciliary motility. J. Cell Biol. 39, 77–94 (1968)

    PubMed  Article  CAS  Google Scholar 

  • Satir, P.: How cilia move. Sci. Amer. 231, No. 4, 44–52 (1974)

    PubMed  CAS  Google Scholar 

  • Sorokin, S.: Centrioles and the formation of rudimentary cilia by fibroblasts and smooth muscle cells. J. Cell Biol. 15, 363–377 (1962)

    PubMed  Article  CAS  Google Scholar 

  • Sorokin, S.P.: Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 3, 207–230 (1968)

    PubMed  CAS  Google Scholar 

  • Sottiurai, V., Malvin, R.L.: The demonstration of cilia in canine macula densa cells. Amer. J. Anat. 135, 281–286 (1972)

    PubMed  Article  CAS  Google Scholar 

  • Stubblefield, E., Brinkley, B.R.: Cilia formation in Chinese hamster fibroblasts in vitro as a response to colcemid treatment. J. Cell Biol. 30, 645–652 (1966)

    PubMed  Article  CAS  Google Scholar 

  • Summers, K.E., Gibbons, I.R.: Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea urchin sperm. Proc. nat. Acad. Sci. (Wash.) 68, 3092–3096 (1971)

    Article  CAS  Google Scholar 

  • Thurau, K.: The influence of sodium concentration at macula densa cells on tubular sodium load. Ann. N.Y. Acad. Sci. 139, 388–399 (1966)

    PubMed  Article  CAS  Google Scholar 

  • Tisher, C.C., Bulger, R.E., Trump, B.E.: Human renal ultrastructure. I. Proximal tubule of healthy individuals. Lab. Invest. 15, 1357–1394 (1966)

    PubMed  CAS  Google Scholar 

  • Tonna, E.A., Lampen, N.M.: Electron microscopy of aging skeletal cells. I. Centrioles and solitary cilia. J. Gerontol. 27, 316–324 (1972)

    PubMed  CAS  Google Scholar 

  • Tyson, G.E., Bulger, R.E.: Effect of vinblastine sulfate on the fine structure of cells of the rat renal corpuscle. Amer. J. Anat. 135, 319–344 (1972)

    PubMed  Article  CAS  Google Scholar 

  • Valré, U., Coiley, A., Parsons, D.E.: The use of goniometer stages for the examination of nonmetallic and biological specimens. In: Electron microscopy 1964 (M. Tiltbach, ed.), Czech. Acad. Sci. Prague B, 21–22. (1964)

  • Warner, F.D., Satir, P.: The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. J. Cell Biol. 63, 35–63 (1974)

    PubMed  Article  CAS  Google Scholar 

  • Warr, J.R., McWittie, A., Randall, J., Hopkins, J.M.: Genetic control of flagellar structure in Chlamydomonas reinhardtii. Genet. Res. 7. 335–351 (1966)

    Article  Google Scholar 

  • Webber, W.A., Lee, J.: The ciliary pattern of the parietal layer of Bowman's capsule. Anat. Rec. 180, 449–456 (1974)

    PubMed  Article  CAS  Google Scholar 

  • Webber, W.A., Lee, J.: Fine structure of mammalian renal cilia. Anat. Rec. 182, 339–344 (1975)

    PubMed  Article  CAS  Google Scholar 

  • Wesson, L.G., Duckett, S.: Renal ciliated epithelium in acute necrotizing glomerulitis. Arch. Path. 96, 137–140 (1973)

    PubMed  CAS  Google Scholar 

  • Wheatley, D.N.: Cilia in cell-cultured fibroblasts. I. On their occurrence and relative frequencies in primary cultures and established cell lines. J. Anat. (Lond.) 105, 351–362 (1969)

    CAS  Google Scholar 

  • Zimmermann, K.W.: Beiträge zur Kenntniss einiger Drüsen und Epithelien. Arch. mikr. Anat. 52, 552–706 (1898)

    Article  Google Scholar 

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Affiliations

  1. Institute of Anatomy, University of Bergen, Bergen, Norway

    Per R. Flood & Geir K. Totland

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  1. Per R. Flood
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  2. Geir K. Totland
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Additional information

We are indebted to Prof. B. Afzelius and Prof. Th. Brun for valuable information and discussions during this work. The technical assistance of Miss K. Weltzin, Mr. E. Erichsen, Mr. R. Jensen and Mr. J. Røli is greatly appreciated

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Flood, P.R., Totland, G.K. Substructure of solitary cilia in mouse kidney. Cell Tissue Res. 183, 281–290 (1977). https://doi.org/10.1007/BF00226625

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Key words

  • Cilia
  • Nephron
  • Mouse