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Speract induces calcium oscillations in the sperm tail.

Wood CD, Darszon A, Whitaker M - J. Cell Biol. (2003)

Bottom Line: These data point to a model in which a messenger generated periodically in the tail diffuses to the head.Sperm are highly polarized cells.Our results indicate that a clear understanding of the link between [Ca2+]i and sperm motility will only be gained by analysis of [Ca2+]i signals at the level of the single sperm.

View Article: PubMed Central - PubMed

Affiliation: School of Cell and Molecular Biosciences, University of Newcastle upon Tyne, NE2 4HH, UK.

ABSTRACT
Sea urchin sperm motility is modulated by sperm-activating peptides. One such peptide, speract, induces changes in intracellular free calcium concentration ([Ca2+]i). High resolution imaging of single sperm reveals that speract-induced changes in [Ca2+]i have a complex spatiotemporal structure. [Ca2+]i increases arise in the tail as periodic oscillations; [Ca2+]i increases in the sperm head lag those in the tail and appear to result from the summation of the tail signal transduction events. The period depends on speract concentration. Infrequent spontaneous [Ca2+]i transients were also seen in the tail of unstimulated sperm, again with the head lagging the tail. Speract-induced fluctuations were sensitive to membrane potential and calcium channel blockers, and were potentiated by niflumic acid, an anion channel blocker. 3-isobutyl-1-methylxanthine, which potentiates the cGMP/cAMP-signaling pathways, abolished the [Ca2+]i fluctuations in the tail, leading to a very delayed and sustained [Ca2+]i increase in the head. These data point to a model in which a messenger generated periodically in the tail diffuses to the head. Sperm are highly polarized cells. Our results indicate that a clear understanding of the link between [Ca2+]i and sperm motility will only be gained by analysis of [Ca2+]i signals at the level of the single sperm.

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Ratio increases in [Ca2+]i from head and flagellum regions (measured in discrete regions of interest as indicated). Images acquired at 40 frames per second with 25-ms individual frame exposure time. (A) Typical spontaneous fluctuations in [Ca2+]i observed in resting sperm. Images above graphs are intensity images; images below graphs are ratio images against the frame immediately before the spontaneous increase occurred. (B) Typical response of an individual sperm to addition of speract to a final concentration of 125 nM. Images above graphs are intensity images; images below are ratio images against the frame immediately before speract addition. Note the markedly higher intensity of the head compared with the tail and that the fold increases in head and tail are comparable.
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fig2: Ratio increases in [Ca2+]i from head and flagellum regions (measured in discrete regions of interest as indicated). Images acquired at 40 frames per second with 25-ms individual frame exposure time. (A) Typical spontaneous fluctuations in [Ca2+]i observed in resting sperm. Images above graphs are intensity images; images below graphs are ratio images against the frame immediately before the spontaneous increase occurred. (B) Typical response of an individual sperm to addition of speract to a final concentration of 125 nM. Images above graphs are intensity images; images below are ratio images against the frame immediately before speract addition. Note the markedly higher intensity of the head compared with the tail and that the fold increases in head and tail are comparable.

Mentions: Around 3% of sperm in the observed field in each experiment undergo spontaneous fluctuations at any given moment, and in such sperm between 1 and 5 fluctuations were recorded over a 10-s period (median = 2, n = 33). As noted above, 95% of sperm with low levels of resting [Ca2+]i respond to speract; their response takes the form of fluctuations in the tail, with a sustained response in the head. Fig. 2 shows the kinetic characteristics of the spontaneous (A) and the speract-induced (B) [Ca2+]i fluctuations. Spontaneous fluctuations have a fast rise time (t1/2 = 100 ± 20 ms) and a relatively slow decay rate (t1/2 = 900 ± 125 ms), and the magnitude and kinetics of these fluctuations are different from those induced by speract (compare Fig. 2 A with Fig. 2 B). Table I is a comparison of the t1/2 of the increase and decay of individual speract-induced and spontaneous fluctuations, and a comparison of their magnitudes. All three criteria are significantly different (P < 0.001; unpaired two-tailed t test), suggesting that the mechanisms involved in the two types of [Ca2+]i fluctuation are distinct (though certain ionic transporters could be shared).


Speract induces calcium oscillations in the sperm tail.

Wood CD, Darszon A, Whitaker M - J. Cell Biol. (2003)

Ratio increases in [Ca2+]i from head and flagellum regions (measured in discrete regions of interest as indicated). Images acquired at 40 frames per second with 25-ms individual frame exposure time. (A) Typical spontaneous fluctuations in [Ca2+]i observed in resting sperm. Images above graphs are intensity images; images below graphs are ratio images against the frame immediately before the spontaneous increase occurred. (B) Typical response of an individual sperm to addition of speract to a final concentration of 125 nM. Images above graphs are intensity images; images below are ratio images against the frame immediately before speract addition. Note the markedly higher intensity of the head compared with the tail and that the fold increases in head and tail are comparable.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2172867&req=5

fig2: Ratio increases in [Ca2+]i from head and flagellum regions (measured in discrete regions of interest as indicated). Images acquired at 40 frames per second with 25-ms individual frame exposure time. (A) Typical spontaneous fluctuations in [Ca2+]i observed in resting sperm. Images above graphs are intensity images; images below graphs are ratio images against the frame immediately before the spontaneous increase occurred. (B) Typical response of an individual sperm to addition of speract to a final concentration of 125 nM. Images above graphs are intensity images; images below are ratio images against the frame immediately before speract addition. Note the markedly higher intensity of the head compared with the tail and that the fold increases in head and tail are comparable.
Mentions: Around 3% of sperm in the observed field in each experiment undergo spontaneous fluctuations at any given moment, and in such sperm between 1 and 5 fluctuations were recorded over a 10-s period (median = 2, n = 33). As noted above, 95% of sperm with low levels of resting [Ca2+]i respond to speract; their response takes the form of fluctuations in the tail, with a sustained response in the head. Fig. 2 shows the kinetic characteristics of the spontaneous (A) and the speract-induced (B) [Ca2+]i fluctuations. Spontaneous fluctuations have a fast rise time (t1/2 = 100 ± 20 ms) and a relatively slow decay rate (t1/2 = 900 ± 125 ms), and the magnitude and kinetics of these fluctuations are different from those induced by speract (compare Fig. 2 A with Fig. 2 B). Table I is a comparison of the t1/2 of the increase and decay of individual speract-induced and spontaneous fluctuations, and a comparison of their magnitudes. All three criteria are significantly different (P < 0.001; unpaired two-tailed t test), suggesting that the mechanisms involved in the two types of [Ca2+]i fluctuation are distinct (though certain ionic transporters could be shared).

Bottom Line: These data point to a model in which a messenger generated periodically in the tail diffuses to the head.Sperm are highly polarized cells.Our results indicate that a clear understanding of the link between [Ca2+]i and sperm motility will only be gained by analysis of [Ca2+]i signals at the level of the single sperm.

View Article: PubMed Central - PubMed

Affiliation: School of Cell and Molecular Biosciences, University of Newcastle upon Tyne, NE2 4HH, UK.

ABSTRACT
Sea urchin sperm motility is modulated by sperm-activating peptides. One such peptide, speract, induces changes in intracellular free calcium concentration ([Ca2+]i). High resolution imaging of single sperm reveals that speract-induced changes in [Ca2+]i have a complex spatiotemporal structure. [Ca2+]i increases arise in the tail as periodic oscillations; [Ca2+]i increases in the sperm head lag those in the tail and appear to result from the summation of the tail signal transduction events. The period depends on speract concentration. Infrequent spontaneous [Ca2+]i transients were also seen in the tail of unstimulated sperm, again with the head lagging the tail. Speract-induced fluctuations were sensitive to membrane potential and calcium channel blockers, and were potentiated by niflumic acid, an anion channel blocker. 3-isobutyl-1-methylxanthine, which potentiates the cGMP/cAMP-signaling pathways, abolished the [Ca2+]i fluctuations in the tail, leading to a very delayed and sustained [Ca2+]i increase in the head. These data point to a model in which a messenger generated periodically in the tail diffuses to the head. Sperm are highly polarized cells. Our results indicate that a clear understanding of the link between [Ca2+]i and sperm motility will only be gained by analysis of [Ca2+]i signals at the level of the single sperm.

Show MeSH
Related in: MedlinePlus