Abstract
Sperm flagella of the sea urchin Tripneustes gratilla beat with asymmetrical bending waves after demembranation with Triton X-100 in the presence of EGTA and reactivation at pH 8.1 with 1 mM ATP in the presence of 2 mM MgSO4. Addition of 0.1--0.2 mM free Ca2+ to these reactivated sperm induces 70--95% of them to become quiescent. This quiescence can be reversed by reduction of the free Ca2% concentration with EGTA, or by dilution to reduce the MgATP2- concentration below 0.3 mM. The quiescent waveform is characterized by a sharp principal bend of approximately 5.6 rad in the proximal region of the flagellum, a slight reverse bend in the midregion that averages approximately 0.3 rad, and a principal bend of approximately 1.1 rad in the tip. The quiescent sperm are highly fragile mechanically, and disruption, including microtubule sliding, occurs spontaneously at a slow rate upon standing or immediately upon gentle agitation. Mild digestion by trypsin causes a gradual appearance of normal, symmetrical flagellar beating. Addition of increasing concentrations of vanadate to quiescent sperm causes a graded decrease in the proximal bend angle, with 50 micrometers vanadate reducing it to approximately 2.6 rad. In the presence of 0.1 mM free Ca2% and 10 micrometers vanadate, a characteristic, crescented stationary bend is induced in the demembranated sperm, without intermediate oscillatory beating, by the addition of either 0.1 or 1 mM ATP. In the absence of vanadate, these two concentrations of ATP produce asymmetric beating and quiescence, respectively. The results support the hypothesis that quiescence in live sperm is induced by an elevated concentration of intracellular Ca2%. In addition, they demonstrate that bending can occur in flagella in which oscillatory beating is inhibited and emphasize the close relationship between asymmetric beating and quiescence.
MeSH Terms
Adenosine Triphosphate/pharmacology
Animals
Calcium/pharmacology
Magnesium Sulfate/pharmacology
Male
Sea Urchins/physiology
Sperm Motility/drug effects
Sperm Tail/drug effects,physiology
Spermatozoa/cytology,drug effects
Trypsin/pharmacology
Vanadium/pharmacology
Chemicals
Vanadium
Magnesium Sulfate
Adenosine Triphosphate
Trypsin
Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gibbons B H
Gibbons I R
References (28)
28 references, click to expand
-
The molecular basis of flagellar motility in sea urchin spermatozoa.
Soc Gen Physiol Ser. 1975;30:207-32
PMID: 127384
-
Control of the orientation of cilia by adenosinetriphosphate, calcium, and zinc in glycerol-extracted Paramecium caudatum.
J Gen Physiol. 1969 May;53(5):517-29
PMID: 4976855
-
Effects of calcium on flagellar movement in the trypanosome Crithidia oncopelti.
J Exp Biol. 1976 Aug;65(1):229-42
PMID: 825606
-
Chromosome movement in lysed mitotic cells is inhibited by vanadate.
J Cell Biol. 1978 Nov;79(2 Pt 1):573-80
PMID: 152767
-
Isolated flagellar apparatus of Chlamydomonas: characterization of forward swimming and alteration of waveform and reversal of motion by calcium ions in vitro.
J Cell Sci. 1978 Oct;33:235-53
PMID: 31367
-
Calcium does not inhibit active sliding of microtubules from mussel gill cilia.
Nature. 1979 Mar 1;278(5699):69-70
PMID: 154066
-
Starting transients in sea urchin sperm flagella.
J Cell Biol. 1979 Jan;80(1):61-8
PMID: 33997
-
Reversible mechanochemical cycle in the contraction of Vorticella.
Nature. 1971 Jan 8;229(5280):127-8
PMID: 4992376
-
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):3092-6
PMID: 5289252
-
Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100.
J Cell Biol. 1972 Jul;54(1):75-97
PMID: 4261039
-
Observations of the structural components of flagellar axonemes and central pair microtubules from rat sperm.
J Ultrastruct Res. 1977 Oct;61(1):21-43
PMID: 915974
-
Physicochemical properties of rat testis Ca2+-dependent regulator protein of cyclic nucleotide phosphodiesterase. Relationship of Ca2+-binding, conformational changes, and phosphodiesterase activity.
J Biol Chem. 1977 Dec 10;252(23):8415-22
PMID: 200611
-
Motility of triton-demembranated sea urchin sperm flagella during digestion by trypsin.
J Cell Biol. 1977 Dec;75(3):650-65
PMID: 562884
-
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):1313-8
PMID: 149544
-
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):2220-4
PMID: 149986
-
Calcium control of ciliary arrest in mussel gill cells.
J Cell Biol. 1978 Oct;79(1):110-20
PMID: 359573
-
The effect of partial extraction of dynein arms on the movement of reactivated sea-urchin sperm.
J Cell Sci. 1973 Sep;13(2):337-57
PMID: 4760590
-
Control of ciliary activities by adenosinetriphosphate and divalent cations in triton-extracted models of Paramecium caudatum.
J Exp Biol. 1973 Jun;58(3):657-76
PMID: 4732944
-
Relationship between the latent adenosine triphosphatase state of dynein 1 and its ability to recombine functionally with KCl-extracted sea urchin sperm flagella.
J Biol Chem. 1979 Jan 10;254(1):197-201
PMID: 214441
-
Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa.
Biochem Biophys Res Commun. 1974 Jun 4;58(3):795-800
PMID: 4209286
-
Properties of flagellar "rigor waves" formed by abrupt removal of adenosine triphosphate from actively swimming sea urchin sperm.
J Cell Biol. 1974 Dec;63(3):970-85
PMID: 4215820
-
A sliding microtubule model incorporating axonemal twist and compatible with three-dimensional ciliary bending.
J Exp Biol. 1979 Feb;78:265-80
PMID: 438720
-
Effects of divalent cations on dynein cross bridging and ciliary microtubule sliding.
J Cell Biol. 1979 Mar;80(3):573-88
PMID: 156731
-
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):291-8
PMID: 158028
-
Calcium-induced asymmetrical beating of triton-demembranated sea urchin sperm flagella.
J Cell Biol. 1979 Aug;82(2):401-11
PMID: 479307
-
Intermittent swimming in live sea urchin sperm.
J Cell Biol. 1980 Jan;84(1):1-12
PMID: 6985611
-
STUDIES ON THE PROTEIN COMPONENTS OF CILIA FROM TETRAHYMENA PYRIFORMIS.
Proc Natl Acad Sci U S A. 1963 Nov;50:1002-10
PMID: 14082342
-
Ciliary inter-microtubule bridges.
J Cell Sci. 1976 Jan;20(1):101-14
PMID: 129478