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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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Quantitative modeling of calcium changes in the head of individual sperm undergoing speract-induced and spontaneous increases in [Ca2+]i. For details of the model, see Materials and methods. (A) Typical increase in [Ca2+]i of sperm treated with 100 nM speract (indicated by arrow) with increases in both head and tail. The increase in the head can be modeled by diffusion from the tail through a bottleneck with an apparent rate constant of 2 s−1. (B) Typical increase in [Ca2+]i of sperm undergoing spontaneous fluctuation, with the increase in the head modeled using the same rate constant. Modeling suggests that extrusion or destruction of the diffusing signal is not significant on these timescales. (C) Schematic diagram showing proposed model of speract-induced Ca2+ entry into the heads of sea urchin sperm. Activation of the speract receptor localized to the flagellum results in up-regulation of the activity of adenylate cyclase, also predominantly localized to the flagellum, via increases in pH, [Ca2+]i and/or changes in Em. cAMP then diffuses into the head, opening the cAMP-dependent Ca2+ channels localized there. Calcium efflux pathways are also shown.
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fig10: Quantitative modeling of calcium changes in the head of individual sperm undergoing speract-induced and spontaneous increases in [Ca2+]i. For details of the model, see Materials and methods. (A) Typical increase in [Ca2+]i of sperm treated with 100 nM speract (indicated by arrow) with increases in both head and tail. The increase in the head can be modeled by diffusion from the tail through a bottleneck with an apparent rate constant of 2 s−1. (B) Typical increase in [Ca2+]i of sperm undergoing spontaneous fluctuation, with the increase in the head modeled using the same rate constant. Modeling suggests that extrusion or destruction of the diffusing signal is not significant on these timescales. (C) Schematic diagram showing proposed model of speract-induced Ca2+ entry into the heads of sea urchin sperm. Activation of the speract receptor localized to the flagellum results in up-regulation of the activity of adenylate cyclase, also predominantly localized to the flagellum, via increases in pH, [Ca2+]i and/or changes in Em. cAMP then diffuses into the head, opening the cAMP-dependent Ca2+ channels localized there. Calcium efflux pathways are also shown.

Mentions: It occurred to us that a simple explanation that might account for these results was that a signal originated periodically in the tail in response to speract and diffused to the head, where it was summed or integrated. This simple hypothesis is supported by quantitative modeling (Fig. 10) , though by itself this by no means constitutes proof.


Speract induces calcium oscillations in the sperm tail.

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

Quantitative modeling of calcium changes in the head of individual sperm undergoing speract-induced and spontaneous increases in [Ca2+]i. For details of the model, see Materials and methods. (A) Typical increase in [Ca2+]i of sperm treated with 100 nM speract (indicated by arrow) with increases in both head and tail. The increase in the head can be modeled by diffusion from the tail through a bottleneck with an apparent rate constant of 2 s−1. (B) Typical increase in [Ca2+]i of sperm undergoing spontaneous fluctuation, with the increase in the head modeled using the same rate constant. Modeling suggests that extrusion or destruction of the diffusing signal is not significant on these timescales. (C) Schematic diagram showing proposed model of speract-induced Ca2+ entry into the heads of sea urchin sperm. Activation of the speract receptor localized to the flagellum results in up-regulation of the activity of adenylate cyclase, also predominantly localized to the flagellum, via increases in pH, [Ca2+]i and/or changes in Em. cAMP then diffuses into the head, opening the cAMP-dependent Ca2+ channels localized there. Calcium efflux pathways are also shown.
© Copyright Policy
Related In: Results  -  Collection

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

fig10: Quantitative modeling of calcium changes in the head of individual sperm undergoing speract-induced and spontaneous increases in [Ca2+]i. For details of the model, see Materials and methods. (A) Typical increase in [Ca2+]i of sperm treated with 100 nM speract (indicated by arrow) with increases in both head and tail. The increase in the head can be modeled by diffusion from the tail through a bottleneck with an apparent rate constant of 2 s−1. (B) Typical increase in [Ca2+]i of sperm undergoing spontaneous fluctuation, with the increase in the head modeled using the same rate constant. Modeling suggests that extrusion or destruction of the diffusing signal is not significant on these timescales. (C) Schematic diagram showing proposed model of speract-induced Ca2+ entry into the heads of sea urchin sperm. Activation of the speract receptor localized to the flagellum results in up-regulation of the activity of adenylate cyclase, also predominantly localized to the flagellum, via increases in pH, [Ca2+]i and/or changes in Em. cAMP then diffuses into the head, opening the cAMP-dependent Ca2+ channels localized there. Calcium efflux pathways are also shown.
Mentions: It occurred to us that a simple explanation that might account for these results was that a signal originated periodically in the tail in response to speract and diffused to the head, where it was summed or integrated. This simple hypothesis is supported by quantitative modeling (Fig. 10) , though by itself this by no means constitutes proof.

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