The signalling pathway and the behavioural strategy underlying chemotaxis of sperm are poorly understood. We have studied the cellular events and motor responses that mediate chemotaxis of sperm from the sea urchin Arbacia punctulata. Here we show that resact, a chemoattractant peptide, initiates a rapid and transient rise in the concentration of cyclic GMP, followed by a transient influx of Ca2+. The binding of a single resact molecule elicits a Ca2+ response, and 50-100 bound molecules saturate the response. The ability to register single molecules is reminiscent of the single-photon sensitivity of rod photoreceptors. Both resact and cyclic nucleotides cause a turn or brief tumbling in the swimming path of sperm. We conclude that a cGMP-mediated increase in the Ca2+ concentration induces the primary motor response of sperm to the chemoattractant.
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.
Sperm are attracted by chemical substances which are released by the egg. This process is called chemotaxis. Several molecules that are involved in chemotactic signaling of sperm from marine invertebrates are described and a model of the signaling pathway is presented. We discuss the motor response during chemotaxis and propose a model of the navigation strategy of sperm.
Chemotaxis of sperm is an important step toward fertilization. During chemotaxis, sperm change their swimming behavior in a gradient of the chemoattractant that is released by the eggs, and finally sperm accumulate near the eggs. A well established model to study chemotaxis is the sea urchin Arbacia punctulata. Resact, the chemoattractant of Arbacia, is a peptide that binds to a receptor guanylyl cyclase. The signaling pathway underlying chemotaxis is still poorly understood. Stimulation of sperm with resact induces a variety of cellular events, including a rise in intracellular pH (pHi) and an influx of Ca2+; the Ca2+ entry is essential for the chemotactic behavior. Previous studies proposed that the influx of Ca2+ is initiated by the rise in pHi. According to this proposal, a cGMP-induced hyperpolarization activates a voltage-dependent Na+/H+ exchanger that expels H+ from the cell. Because some aspects of the proposed signaling pathway are inconsistent with recent results (Kaupp, U.B., J. Solzin, J.E. Brown, A. Helbig, V. Hagen, M. Beyermann, E. Hildebrand, and I. Weyand. 2003. Nat. Cell Biol. 5:109–117), we reexamined the role of protons in chemotaxis of sperm using kinetic measurements of the changes in pHi and intracellular Ca2+ concentration. We show that for physiological concentrations of resact (<25 pM), the influx of Ca2+ precedes the rise in pHi. Moreover, buffering of pHi completely abolishes the resact-induced pHi signal, but leaves the Ca2+ signal and the chemotactic motor response unaffected. We conclude that an elevation of pHi is required neither to open Ca2+-permeable channels nor to control the chemotactic behavior. Intracellular release of cGMP from a caged compound does not cause an increase in pHi, indicating that the rise in pHi is induced by cellular events unrelated to cGMP itself, but probably triggered by the consumption and subsequent replenishment of GTP. These results show that the resact-induced rise in pHi is not an obligatory step in sperm chemotactic signaling. A rise in pHi is also not required for peptide-induced Ca2+ entry into sperm of the sea urchin Strongylocentrotus purpuratus. Speract, a peptide of S. purpuratus may act as a chemoattractant as well or may serve functions other than chemotaxis.
Both photosystems, PS 370 and PS 565, controlling behavioral responses in Halobacterium halobium [E. Hildebrand and N. Dencher, Nature 257, 46 - 48 (1975)] are reversibly inhibited when bacteria are grown in the presence of 1 mM nicotine which is known to block biosynthesis of retinal. Photobehavior can be restored within som e minutes to hours by adding retinal to nicotine-treated bacteria, PS 370 thereby reappearing earlier than PS 565. The reconstitution rate depends on the concentration and on the kind of retinal isomers applied. All-trans retinal is most effective. PS 370 becomes fully sensitive if reconstituted in the presence of nicotine. This rules out the possibility that the alkaloid may directly inhibit steps of signal transmission following photoreception. The action spectrum of PS 370 regenerated with retinal alone of H. h., strain R1L3 (a mutant deficient in carotenoids), fails to show all secondary peaks around 450 nm which in strain R1 occur besides the prominent maximum at 370 nm. Addition of carotenoids (mainly α-bacterioruberin) to reconstituted cells of R1L3 restores the sensitivity in that spectral region. Carotenoids or flavin solely added to nicotine-treated bacteria cannot restore photobehavior. We conclude that the active pigment o f PS 370, which mediates the photophobic response to increase of light intensity (step-up response), represents a retinal protein complex and that carotenoids participate in photoreceptor function as accessory pigments. The biochemical relation of the UV-absorbing retinal protein complex to bacteriorhodopsin is discussed.
Responses of Halobacterium halobium cells to chemical stimuli have been shown by a capillary technique. Cells were attacted by D-glucose and several amino acids and repelled by phenol. Certain chemicals, such as acetate, benzoate, indole, and NiSO4, that are known to act as repellents of Escherichia coli cells served as attractants for Halobacterium. In the presence of ethionine, sensitivity to attractants was reduced. Arsenate prevented the attraction by glucose without lowering the cellular adenosine 5'-triphosphate level. The ability for chemo-accumulation toward glucose and histidine was interfered with by the formation of photosensory systems. Light-induced motor responses and chemosensory behavior toward glucose and histidine became detectable in the late stationary growth phase only. The behavior toward acetate and indole was not connected to photobehavior in that way: both substances acted as attractants already in the late log phase. Inhibition of bacteriorhodopsin synthesis by L-nicotine allowed chemo-accumulation toward glucose and histidine already in the late logarithmic phase.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
10624 S. Eastern Ave., Ste. A-614
Henderson, NV 89052, USA
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.