Abstract
The aim of the present investigation is to determine whether or not hydrocephalus occurring in hydrocephalic Wistar-Imamichi strain rats (WIC-Hyd) is caused by functional and structural disorders of ependymal cilia. Ultrastructures and movement of cilia in the ependyma of the lateral, III and IV ventricles and aqueduct of Sylvius and in the trachea walls of the animals were examined by means of scanning electron microscopy (SEM), transmission electron microscopy (TEM), and light microscopy using a phase-contrast microscope equipped with a high-speed video recording system. SEM revealed that a marked decrease in the length and number of cilia in the ependymal and tracheal walls occurred in affected male WIC-Hyd. This finding was noted even before the development of ventricular dilatation and was not related to the degree of ventricular enlargement after development of hydrocephalus. A moderate decrease in length and number of cilia was also seen among the normal ciliary tufts in affected female rats which developed a mild degree of hydrocephalus. TEM cilia findings included abnormal axonemal structures such as a lack of dynein arms and displacement of microtubules. The incidence of these ultrastructural abnormalities was found to be greater in affected male rats than in affected female rats. All cilia in affected male rats before and after development of hydrocephalus were immotile. A variety of movement disorders such as immobile, rotatory, and vibratory cilia were observed beside normally beating cilia (motile cilia) in affected female rats which never developed hydrocephalus as severe as that seen in affected male rats. These results seem to indicate that there is a correlation between cilia movement disorder and the degree of ultrastructural abnormalities. Consequently, hydrocephalus developing in affected male and female WIC-Hyd appears to be caused by a motility disorder of ependymal cilia which is part of the primary ciliary dyskinesia (PCD) affecting these animals. The present study appears to indicate that the movement of ependymal cilia may play a role in cerebrospinal fluid circulation, and that dysfunction of ependymal ciliary movement may contribute to development of hydrocephalus in WIC-Hyd rats.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Adam H (1953) Kugelförmige Pigmentzellen als Anzeiger der Liquorstörung in den Gehirnventrikeln von Krallenfroschlarven. Z Naturforsch 8:250–258
Afzelius BA (1959) Electron microscopy of the sperm tail; results obtained with a new fixative. J Biophys Cytol 5:269–278
Afzelius BA (1976) A human syndrome caused by immotile cilia. Science 193:317–319
Afzelius BA (1979) The immotile-cilia syndrome and other ciliary disease. Int Rev Exp Pathol 19:1–43
Afzelius BA, Eliasson R (1979) Flagellar mutants in man: on the heterogeneity of the immotile-cilia syndrome. J Ultrastruct Res 69:43–52
Bannister CM, Chapman SA (1980) Ventricular ependyma of normal and hydrocephalic subjects: a scanning electron microscopic study. Dev Med Child Neurol 22:725–735
Bannister CM, Mundy JE (1979) Some scanning electron microscopic observations of the ependymal surface of the ventricles of hydrocephalic Hy3 mice and a human infant. Acta Neurochir (Wien) 46:159–168
Bering EA (1962) Circulation of the cerebrospinal fluid. Demonstration of the choroid plexuses as the generator of the force for flow of fluid and ventricular enlargement. J Neurosurg 19:405–413
Borit A, Sidman RL (1972) New mutant mouse with communicating hydrocephalus and secondary aqueductal stenosis. Acta Neuropathol (Berl) 21:316–331
Bryan JHD (1983) The immotile cilia syndrome. Mice versus man. Virchows Arch [A] 399:265–275
Cathcart RS III, Worthington WC (1964) Ciliary movement in the rat cerebral ventricles: clearing action and directions of currents. J Neuropathol Exp Neurol 22:725–735
Chu HY (1942) Ciliary movement and circulation of cerebrospinal fluid within brain ventricles in larval and adult anurans. Am J Physiol 136:223–228
De Santi MM, Magni A, Valletta EA, Gardi C, Lungarella G (1990) Hydrocephalus, bronchiectasis, and ciliary aplasia. Arch Dis Child 65:543–544
Eliasson R, Mossberg B, Camner P, Afzelius B (1977) The immotile cilia snydrome. A congenital ciliary abnormality as an etiologic factor in chronic airway infection and male sterility. N Engl J Med 297:1–6
Fawcett DW (1977) What makes cilia and sperm tails beat? N Engl J Med 297:46–48
Gibbons IR (1963) Studies on the protein components of cilia from Tetrahymena pyriformis. Proc Natl Acad Sci USA 50:1002–1010
Go KG, Stokroos I, Blaauw EH, Fuider-Veen F, Molenaar I (1976) Changes of ventricular ependyma and choroid plexus in experimental hydrocephalus, as observed by scanning electron microscopy. Acta Neuropathol (Berl) 34:55–64
Greenstone MA, Jones RW, Dewar A, Neville BG (1984) Hydrocephalus and primary ciliary dyskinesia. Arch Dis Child 59:481–482
Hoffmann-Berlin H (1955) Geisselmodelle und Adenosintriphosphat (ATP). Biochim Biophys Acta 16:146–154
Jabourian Z, Lublin FD, Adler A, Gonzales C, Northrup B, Zwillenberg D (1986) Hydrocephalus in Kartagener's snydrome. Ear Nose Throat J 65:468–472
Kartagener M (1933) Zur Pathologenese der Bronchiektasien; Bronchiektasien bei Situs viscerum inversus. Beitr Klin Tuberk 83:489–501
Kartagener M (1935) Das Problem der Kongenitalität und Heredität der Bronchiektasien. Ergeb Inn Med Kinderheilkd 49:378–442
Kohn DF, Chinookoswong N, Chou SM (1981) A new model of congenital hydrocephalus in the rat. Acta Neuropathol (Berl) 54:211–228
Konno I, Shiotani Y (1956) Some aspects of the ciliary movement of ependymal cells of the ventricles. Folia Psychiatr Neurol Jpn 10:1–4
Koto M, Adachi J, shimizu A (1987) A new mutation of primary ciliary dyskinesia with visceral inversion and hydrocephalus. Rat News Lett 18:14–15
Koto M, Miwa M, Shimizu A, Tsuji K, Okamoto M, Adachi J (1987) Inherited hydrocephalus in Csk; Wistar-Imamichi rats; Hyd strain: a new disease model for hydrocephalus. Jikken Dobutsu 36:157–162
Lindberg LA, Vasenius L, Talanti S (1977) The surface structure of the ependymal lining of the lateral ventricle in rats with hereditary hydrocephalus. Cell Tissue Res 179:121–129
Milhorat TH (1975) The third circulation revisited. J Neurosurg 42:628–645
Mohri H (1958) Adenosinetriphosphatases of sea-urchin spermatozoa. J Fac Sci Univ Tokyo (Sect 4) 8:307–315
Nelson DJ, Wright EM (1974) The distribution, activity, and function of the cilia in the frog brain. J Physiol (Lond) 243:63–78
Nielsen SL, Gauger GE (1974) Experimental hydrocephalus: surface alterations of the lateral ventricle. Scanning electron microscopic studies. Lab Invest 30:618–625
Olsen AM (1943) Bronchiectasis and dextrocardia: observations on aetiology of bronchiectasis Am Rev Tuberc 47:435–439
Page RB (1975) Scanning electron microscopy of the ventricular system in normal and hydrocephalic rabbits. J Neurosurg 42:646–664
Park AW, Nowosielski-Slepowron BJA (1979) Hydrocephalus in the laboratory rat. Acta Morphol Neerl Scand 17:191–207
Pedersen M, Mygind N (1980) Ciliary motility in the ‘immotile cilia syndrome’. First results of microphoto-oscillographic studies. Br J Dis Chest 74:239–244
Pedersen H, Rebbe H (1975) Absence of arms in the axonema of immobile human spermatozoa. Biol Reprod 12:541–544
Purkinje JE (1836) Ueber Flimmerbewegungen im Gehirn. Arch Anat Physiol 3:289–290
Rossman CM, Forrest JB, Lee RM, Leene W, Freenstra L (1980) The dyskinetic cilia syndrome. Ciliary motiliy in immotile cilia syndrome. Chest 78:580–582
Roth Y, Kimhi Y, Edery H, Aharonson E, Priel Z (1985) Ciliary motility in brain ventricular system and trachea of hamsters. Brain Res 330:291–297
Rutland J, Cole PJ (1980) Non-invasive sampling of nasal cilia for measurement of beat frequency and study of ultra-structure. Lancet 2:564–565
Sakai H (1983) Biological function of microtubules and related structures (in Japanese). Baifukan, Tokyo, pp 84–109
Satir P (1974) How cilia move. Sci Am 231:44–52
Satir P (1985) Switching mechanism in the control of ciliary motility. Mod Cell Biol 4:1–46
Siewert AK (1903) Ueber einen Fall von Bronchiectasie bei einem Patienten mit situs inversus viscerum. Berl Klin Wochenschr 41:139–141
Shimizu T (1988) Biochemistry of dynein, the ATPase from cilia or flagella (in Japanese). J Biochem 60:1148–1159
Shingyoji C, Takahashi K (1988) Microtubule sliding in ciliary and flagellar motility (in Japanese). Seitai No Kagaku 39:92–97
Sleigh MA, et al (1981) Primary ciliary dyskinesia. Lancet 2:476
Stoklasa L (1930) Ueber die Flimmerbewegung in den nervösen Zentralorganen der Wirbeltiere. Anat Anz 69:525–532
Sturgess JM, Chao J, Wong J, Aspin N, Turner JA (1979) Cilia with defective radial spokes. A cause of human respiratory disease. N Engl J Med 300:53–56
Sturgess JM, Chao J, Turner JA (1980) Transposition of ciliary microtubules: another cause of impaired ciliary motility. N Engl J Med 303:318–322
Summers KE, Gibbons IR (1971) Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci USA 68:3092–3096
Veerman AJ, Van der Baan AS, Weltevreden EF, Leene W, Feenstra L (1980) Cilia: immotile, dyskinetic, dysfunctional (Letter). Lancet 2:266
Vonwiller P, Wigodskaya RR (1933) Mikroskopische Beobachtung der Bewegung des Liquors im lebenden Gehirn. Z Anat Entwicklungsgesch 102:290–297
Wakefield S, Waite D (1980) Abnormal cilia in Polynesians with bronchiectasis. Am Rev Respir Dis 121:1003–1010
Weller RO, Wisniewski H, Shulman K, Terry RD (1971) Experimental hydrocephalus in young dogs: histological and ultrastructural study of the brain tissue damage. J Neuropathol Exp Neurol 30:613–620
Worthington WC, Cathcart RS III (1963) Ependymal cilia: distribution and activity in the adult human brain. Science 139:221–222
Worthington WC, Cathcart RS III (1966) Ciliary currents on ependymal surfaces Ann NY Acad Sci 130:944–950
Yamadori T (1983) The ependymal cell (in Japanese). Adv Neurol Sci 27:99–110
Yamadori T, Nara K (1979) The directions of ciliary beat on the wall of the lateral ventricle and the currents of the cerebrospinal fluid in the brain ventricles. Scanning Electron Microsc 3:335–340
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Shimizu, A., Koto, M. Ultrastructure and movement of the ependymal and tracheal cilia in congenitally hydrocephalic WIC-Hyd rats. Child's Nerv Syst 8, 25–32 (1992). https://doi.org/10.1007/BF00316558
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00316558