Abstract
Direct measurements of microtubule sliding in the flagella of actively swimming, demembranated, spermatozoa have been made using submicron diameter gold beads as markers on the exposed outer doublet microtubules. With spermatozoa of the tunicate, Ciona, these measurements confirm values of sliding calculated indirectly by measuring angles relative to the axis of the sperm head. Both methods of measurement show a nonuniform amplitude of oscillatory sliding along the length of the flagellum, providing direct evidence that "oscillatory synchronous sliding" can be occurring in the flagellum, in addition to the metachronous sliding that is necessary to propagate a bending wave. Propagation of constant amplitude bends is not accomplished by propagation of a wave of oscillatory sliding of constant amplitude, and therefore appears to require a mechanism for monitoring and controlling the bend angle as bends propagate. With sea urchin spermatozoa, the direct measurements of sliding do not agree with the values calculated by measuring angles relative to the head axis. The oscillation in angular orientation of the sea urchin sperm head as it swims appears to be accommodated by flexure at the head- flagellum junction and does not correspond to oscillation in orientation of the basal end of the flagellum. Consequently, indirect calculations of sliding based on angles measured relative to the longitudinal axis of the sperm head can be seriously inaccurate in this species.
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Selected References
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- Brokaw C. J. A lithium-sensitive regulator of sperm flagellar oscillation is activated by cAMP-dependent phosphorylation. J Cell Biol. 1987 Oct;105(4):1789–1798. doi: 10.1083/jcb.105.4.1789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brokaw C. J. Bend propagation by a sliding filament model for flagella. J Exp Biol. 1971 Oct;55(2):289–304. doi: 10.1242/jeb.55.2.289. [DOI] [PubMed] [Google Scholar]
- Brokaw C. J., Benedict B. Mechanochemical coupling in flagella. II. Effects of viscosity and thiourea on metabolism and motility of Ciona spermatozoa. J Gen Physiol. 1968 Aug;52(2):283–299. doi: 10.1085/jgp.52.2.283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brokaw C. J. Calcium-induced asymmetrical beating of triton-demembranated sea urchin sperm flagella. J Cell Biol. 1979 Aug;82(2):401–411. doi: 10.1083/jcb.82.2.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brokaw C. J. Computerized analysis of flagellar motility by digitization and fitting of film images with straight segments of equal length. Cell Motil Cytoskeleton. 1990;17(4):309–316. doi: 10.1002/cm.970170406. [DOI] [PubMed] [Google Scholar]
- Brokaw C. J., Nagayama S. M. Modulation of the asymmetry of sea urchin sperm flagellar bending by calmodulin. J Cell Biol. 1985 Jun;100(6):1875–1883. doi: 10.1083/jcb.100.6.1875. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brokaw C. J. Sperm motility. Methods Cell Biol. 1986;27:41–56. [PubMed] [Google Scholar]
- Eshel D., Brokaw C. J. Determination of the average shape of flagellar bends: a gradient curvature model. Cell Motil Cytoskeleton. 1988;9(4):312–324. doi: 10.1002/cm.970090404. [DOI] [PubMed] [Google Scholar]
- Eshel D., Brokaw C. J. New evidence for a "biased baseline" mechanism for calcium-regulated asymmetry of flagellar bending. Cell Motil Cytoskeleton. 1987;7(2):160–168. doi: 10.1002/cm.970070208. [DOI] [PubMed] [Google Scholar]
- Gibbons I. R. Sliding and bending in sea urchin sperm flagella. Symp Soc Exp Biol. 1982;35:225–287. [PubMed] [Google Scholar]
- Gibbons I. R. Transient flagellar waveforms during intermittent swimming in sea urchin sperm. II. Analysis of tubule sliding. J Muscle Res Cell Motil. 1981 Mar;2(1):83–130. doi: 10.1007/BF00712063. [DOI] [PubMed] [Google Scholar]
- Gibbons I. R. Transient flagellar waveforms in reactivated sea urchin sperm. J Muscle Res Cell Motil. 1986 Jun;7(3):245–250. doi: 10.1007/BF01753557. [DOI] [PubMed] [Google Scholar]
- Goldstein S. F. Asymmetric waveforms in echinoderm sperm flagella. J Exp Biol. 1977 Dec;71:157–170. doi: 10.1242/jeb.71.1.157. [DOI] [PubMed] [Google Scholar]
- Goldstein S. F. Form of developing bends in reactivated sperm flagella. J Exp Biol. 1976 Feb;64(1):173–184. doi: 10.1242/jeb.64.1.173. [DOI] [PubMed] [Google Scholar]
- Goldstein S. F. Motility of basal fragments of sea urchin sperm flagella. J Cell Sci. 1981 Aug;50:65–77. doi: 10.1242/jcs.50.1.65. [DOI] [PubMed] [Google Scholar]
- Omoto C. K., Brokaw C. J. Structure and behaviour of the sperm terminal filament. J Cell Sci. 1982 Dec;58:385–409. doi: 10.1242/jcs.58.1.385. [DOI] [PubMed] [Google Scholar]
- Sale W. S. The axonemal axis and Ca2+-induced asymmetry of active microtubule sliding in sea urchin sperm tails. J Cell Biol. 1986 Jun;102(6):2042–2052. doi: 10.1083/jcb.102.6.2042. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Satir P. Studies on cilia. 3. Further studies on the cilium tip and a "sliding filament" model of ciliary motility. J Cell Biol. 1968 Oct;39(1):77–94. doi: 10.1083/jcb.39.1.77. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shingyoji C., Gibbons I. R., Murakami A., Takahashi K. Effect of imposed head vibration on the stability and waveform of flagellar beating in sea urchin spermatozoa. J Exp Biol. 1991 Mar;156:63–80. doi: 10.1242/jeb.156.1.63. [DOI] [PubMed] [Google Scholar]
- Silvester N. R., Holwill M. E. An analysis of hypothetical flagellar waveforms. J Theor Biol. 1972 Jun;35(3):505–523. doi: 10.1016/0022-5193(72)90148-8. [DOI] [PubMed] [Google Scholar]
- Warner F. D., Satir P. The structural basis of ciliary bend formation. Radial spoke positional changes accompanying microtubule sliding. J Cell Biol. 1974 Oct;63(1):35–63. doi: 10.1083/jcb.63.1.35. [DOI] [PMC free article] [PubMed] [Google Scholar]
