Abstract
Mechanical activation of the microtubule sliding mechanism in cilia and flagella1–3 by local passive bending has been postulated to be essential for the initiation and propagation of bending waves along the axoneme4,5. In addition, responsiveness of cilia to hydrodynamic forces imposed externally by their neighbours is thought to be responsible for metachronal coordination of ciliary activity6–10, as well as for synchronal beating of component cilia within compound ciliary organalles11,12. Direct tests of the mechanosensitivity of motile cilia are limited, but generally support these views7,10,11,13–18. It remains problematical, however, whether mechanical interaction between cilia operates continuously during both the effective and recovery phases of the asymmetrical beat cycle. Moreover, the directional sensitivity and temporal responsiveness of motile cilia to mechanical stimuli have been explored in only a few cases7,10.14. Finally, the continuous nature of the ciliary beat cycle has hindered investigation of the ‘switch point hypothesis’ in which doublet sliding is assumed to be activated sequentially on the two halves of the axoneme to produce bends in opposite directions19. Here we report that macrocilia20 on the ctenophore Beroë beat discontinuously with separate effective and recovery strokes, resulting in ‘split-cycle’ waves of metachronal coordination. This new pattern of ciliary beating is used to investigate the motile responses of cilia to controlled mechanical stimuli during each phase of the beat cycle.
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References
Satir, P. J. Cell Biol. 26, 805–834 (1965).
Satir, P. J. Cell Biol. 39, 77–94 (1968).
Summers, K. E. & Gibbons, I. R. Proc. natn. Acad. Sci. U.S.A. 68, 3092–3096 (1971).
Machin, K. E. J. exp. Biol. 35, 796–806 (1958).
Brokaw, C. J. Nature 209, 161–163 (1966).
Machemer, H. in Cilia and Flagella (ed. Sleigh, M. A.) 199–286 (Academic, London, 1974).
Murakami, A. J. Fac. Sci. Univ. Tokyo IV 10, 23–35 (1963).
Tamm, S. L. J. exp. Biol. 59, 231–245 (1973).
Sleigh, M. A. in Cilia and Flagella (ed. Sleigh, M. A.) 287–304 (Academic, London, 1974).
Tamm, S. L. in Electrical Conduction and Behaviour in ‘Simple’ Invertebrates (ed. Shelton, G. A. B.) 266–358 (Oxford University Press, 1982).
Tsuchiya, T. Annotnes zool. jap. 42, 113–125 (1969).
Tamm, S. L. Biol. Bull. 159, 446 (1980).
Kinosita, H. & Kamada, T. Jap. J. Zool. 8, 291–310 (1939).
Thurm, U. Symp. zool. Soc. Lond. 23, 199–216 (1968).
Murakami, A. & Machemer, H. J. comp. Physiol. 145, 351–362 (1982).
Okuno, M. & Hiramoto, Y. J. exp. Biol. 65, 401–413 (1976).
Sleigh, M. A. & Jarman, M. J. mechanochem. Cell Motility 2, 61–68 (1973).
Baba, S. Nature 282, 717–720 (1979).
Wais-Steider, J. & Satir, P. J. supramolec. Struct. 11, 339–347 (1979).
Horridge, G. A. Proc. R. Soc. B162, 351–364 (1965).
Corey, D. P. & Hudspeth, A. J. J. Neurosci. Meth. 3, 183–202 (1980).
Sugino, K. & Naitoh, Y. Nature 295, 609–611 (1982).
Gray, J. Proc. R. Soc. B107, 313–332 (1930).
Sanderson, M. J. & Sleigh, M. A. J. Cell Sci. 47, 331–347 (1981).
Swanberg, N. Mar. Biol. 24, 69–76 (1974).
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Tamm, S. Motility and mechanosensitivity of macrocilia in the ctenophore Beroë. Nature 305, 430–433 (1983). https://doi.org/10.1038/305430a0
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DOI: https://doi.org/10.1038/305430a0
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