Abstract
We have used the unique properties of macrocilia from the lips of the ctenophore Beroe to test whether the ciliary beat cycle is caused by sequential activation of doublet sliding on opposite sides of the axoneme (Satir, P., 1982, Soc. Exp. Biol. Symp., 35: 179-201; Sugino, K., and Y. Naitoh, 1982, Nature (Lond.), 295: 609-611; Wais-Steider, J., and P. Satir, 1979, J. Supramol. Struct., 11:339-347). Macrocilia contain several hundred axonemes linked into rows by lamellae between doublets 3 and 8. These connections provide morphological markers for numbering the doublet microtubules in thin sections. Demembranated, detached macrocilia undergo ATP-induced sliding disintegration by extrusion of thick fragments and finer fibers from the proximal end. Disintegration can easily be followed with low-magnification brightfield or phase-contrast optics. Sliding occurs with or without added elastase, and is reversibly inhibited by vanadate. Thin sections through 16 ATP-disintegrated macrocilia showed two mutually exclusive patterns of doublet extrusion with equal frequency. Doublets 9, 1, and 2 or doublets 5, 6, and 7 were usually extruded, but not both groups. We conclude that both subsets of doublets slide by their own active arms, and that the two extrusion patterns represent alternate activation and inactivation of doublet sliding on opposite halves of the axoneme. These findings provide the first direct experimental support for a switching mechanism regulating microtubule sliding in cilia.
Full Text
The Full Text of this article is available as a PDF (1.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- AFZELIUS B. A. The fine structure of the cilia from ctenophore swimming-plates. J Biophys Biochem Cytol. 1961 Feb;9:383–394. doi: 10.1083/jcb.9.2.383. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brokaw C. J. Elastase digestion of demembranated sperm flagella. Science. 1980 Mar 21;207(4437):1365–1367. doi: 10.1126/science.6898364. [DOI] [PubMed] [Google Scholar]
- Doughty M. J. Control of ciliary activity in paramecium--IV. Ca2+ modification of Mg2+ dependent dynein ATPase activity. Comp Biochem Physiol B. 1979;64(3):255–266. doi: 10.1016/0305-0491(79)90140-8. [DOI] [PubMed] [Google Scholar]
- Fawcett D. W. The mammalian spermatozoon. Dev Biol. 1975 Jun;44(2):394–436. doi: 10.1016/0012-1606(75)90411-x. [DOI] [PubMed] [Google Scholar]
- Gibbons I. R., Cosson M. P., Evans J. A., Gibbons B. H., Houck B., Martinson K. H., Sale W. S., Tang W. J. Potent inhibition of dynein adenosinetriphosphatase and of the motility of cilia and sperm flagella by vanadate. Proc Natl Acad Sci U S A. 1978 May;75(5):2220–2224. doi: 10.1073/pnas.75.5.2220. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kobayashi T., Martensen T., Nath J., Flavin M. Inhibition of dynein ATPase by vanadate, and its possible use as a probe for the role of dynein in cytoplasmic motility. Biochem Biophys Res Commun. 1978 Apr 28;81(4):1313–1318. doi: 10.1016/0006-291x(78)91279-2. [DOI] [PubMed] [Google Scholar]
- Mohri H., Yano Y. Reactivation and microtubule sliding in rodent spermatozoa. Prog Clin Biol Res. 1982;80:143–147. doi: 10.1002/cm.970020727. [DOI] [PubMed] [Google Scholar]
- Olson G. E., Linck R. W. Observations of the structural components of flagellar axonemes and central pair microtubules from rat sperm. J Ultrastruct Res. 1977 Oct;61(1):21–43. doi: 10.1016/s0022-5320(77)90004-1. [DOI] [PubMed] [Google Scholar]
- Sale W. S., Gibbons I. R. Study of the mechanism of vanadate inhibition of the dynein cross-bridge cycle in sea urchin sperm flagella. J Cell Biol. 1979 Jul;82(1):291–298. doi: 10.1083/jcb.82.1.291. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sale W. S., Satir P. Direction of active sliding of microtubules in Tetrahymena cilia. Proc Natl Acad Sci U S A. 1977 May;74(5):2045–2049. doi: 10.1073/pnas.74.5.2045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Satir P. Mechanisms and controls of microtubule sliding in cilia. Symp Soc Exp Biol. 1982;35:179–201. [PubMed] [Google Scholar]
- Summers K. E., Gibbons I. R. Adenosine triphosphate-induced sliding of tubules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci U S A. 1971 Dec;68(12):3092–3096. doi: 10.1073/pnas.68.12.3092. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tamm S. L. Motility and mechanosensitivity of macrocilia in the ctenophore Beroë. 1983 Sep 29-Oct 5Nature. 305(5933):430–433. doi: 10.1038/305430a0. [DOI] [PubMed] [Google Scholar]
- Wais-Steider J., Satir P. Effect of vanadate on gill cilia: switching mechanism in ciliary beat. J Supramol Struct. 1979;11(3):339–347. doi: 10.1002/jss.400110309. [DOI] [PubMed] [Google Scholar]
- Wolniak S. M., Cande W. Z. Physiological requirements for ciliary reactivation of bracken fern spermatozoids. J Cell Sci. 1980 Jun;43:195–207. doi: 10.1242/jcs.43.1.195. [DOI] [PubMed] [Google Scholar]
