Ca2+ spikes in the flagellum control chemotactic behavior of sperm

Abstract

The events that occur during chemotaxis of sperm are only partly known. As an essential step toward determining the underlying mechanism, we have recorded Ca 2 þ dynamics in swimming sperm of marine invertebrates. Stimulation of the sea urchin Arbacia punctulata by the chemoattractant or by intracellular cGMP evokes Ca 2 þ spikes in the flagellum. A Ca 2 þ spike elicits a turn in the trajectory followed by a period of straight swimming ('turn-andrun'). The train of Ca 2 þ spikes gives rise to repetitive loop-like movements. When sperm swim in a concentration gradient of the attractant, the Ca 2 þ spikes and the stimulus function are synchronized, suggesting that precise timing of Ca 2 þ spikes controls navigation. We identified the peptide asterosap as a chemotactic factor of the starfish Asterias amurensis. The Ca 2 þ spikes and swimming behavior of sperm from starfish and sea urchin are similar, implying that the signaling pathway of chemotaxis has been conserved for almost 500 million years.

Niflumic acid disrupts marine spermatozoan chemotaxis without impairing the spatiotemporal detection of chemoattractant gradients

“…Sperm chemotaxis of marine invertebrates requires the strict coupling of the Ca 2+ oscillations with the direction or polarity of the chemoattractant gradient (Böhmer et al, 2005;Shiba et al, 2008;Guerrero et al, 2010a;Kashikar et al, 2012). We found that L. pictus spermatozoa are able to suppress the onset of Ca 2+ fluctuations while swimming toward the center of a speract gradient.…”

“…The relationship between the timing of the [Ca 2+ ] i fluctuations and the shape of the chemical gradient determines the positioning of the turn-and-run motility response (Böhmer et al, 2005;Shiba et al, 2008;Guerrero et al, 2010a;Guerrero et al, 2010b;Kashikar et al, 2012). Supplementary material Fig.…”

“…The redirection is driven by Ca 2+ -dependent increases in flagellar bending asymmetry during the turns, and decreases in asymmetry during the straighter swimming episodes (Miller and Brokaw, 1970;Kaupp et al, 2003;Wood et al, 2005;Shiba et al, 2008). Notably, the path curvature does not strictly follow the [Ca 2+ ]i, as spermatozoa remain swimming on straighter paths at elevated [Ca 2+ ] i (Wood et al, 2005;Shiba et al, 2008;Böhmer et al, 2005;Guerrero et al, 2010a). Recent findings indicate that the sperm swimming pathway is controlled by the [Ca 2+ ]i time derivative , however the responsible molecular mechanisms involved are not fully understood.…”

Sperm Chemotaxis: The First Authentication Events Between Conspecific Gametes Before Fertilization

“…Ca 2+ plays a key role in the regulation of fl agellar beating, and in the case of sea urchin spermatozoa, the sperm attractant triggers [Ca 2+ ] i fl uctuations (Böhmer et al 2005 ;Wood et al 2005 ) that appear to correlate with the asymmetrical beating of sperm fl agella (Brokaw et al 1974 ;Brokaw 1979 ). In the hydrozoan siphonophore s, the diameters of the sperm trajectories decrease on approach of the sperm to the cupule (a spermattracting accessory organ of the egg), but the sperm trajectories are unchanged in the absence of Ca 2+ (Cosson et al 1984 ).…”

“…Chemoattractants such as "resact " in sea urchins (Ward et al 1985 ;Guerrero et al 2010 ), "sepsap " in cuttlefi sh (Zatylny et al 2002 ), and "asterosap " in starfi sh (Böhmer et al 2005 ) are peptides. A 21-kDa protein named "allurin " in the amphibian Xenopus laevis (Olson et al 2001 ) and tryptophan in abalone (Riffell et al 2002 ) act as sperm chemoattractants.…”