A Sustained Increase in Intracellular Ca2+ Is Required for the Acrosome Reaction in Sea Urchin Sperm

González-Martı́nez, Marco T.; Galindo, Blanca E.; Torre, Lucía de De la; Zapata, Otilia; Rodríguez, Eric Murillo; Florman, Harvey M.; Darszon, Alberto

doi:10.1006/dbio.2001.0323

Cited by 60 publications

(50 citation statements)

References 43 publications

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“…Although it is possible that herring sperm motility initiation, maintenance, and the accompanying increase in [Ca 2ϩ ] i , could involve store-operated Ca 2ϩ channels, the presence of such channels in teleost fish sperm has not been investigated. Store-operated Ca 2ϩ channels have been shown to function in the sperm acrosome reaction in mammals and sea urchins (37,38), but teleost fish sperm lack acrosomes and it is unclear whether such channels would be involved in motility.…”

Section: Discussionmentioning

confidence: 99%

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Vines

Yoshida

Griffin

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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Sperm of the Pacific herring, Clupea pallasi, are unique in that they are immotile upon spawning in the environment. Herring sperm have evolved to remain motionless for up to several days after spawning, yet are still capable of fertilizing eggs. An egg chorion ligand termed ''sperm motility initiation factor'' (SMIF) induces motility in herring sperm and is required for fertilization. In this study, we show that SMIF induces calcium influx, sodium efflux, and a membrane depolarization in herring sperm. Sperm motility initiation by SMIF depended on decreased extracellular sodium (<350 mM) and could be induced in the absence of SMIF in very low sodium seawater. Motility initiation depended on > 1 mM extracellular calcium. Calcium influx caused by SMIF involved both the opening of voltage-gated calcium channels and reverse sodiumcalcium (Na ؉ ͞Ca 2؉ ) exchange. Membrane depolarization was slightly inhibited by a calcium channel blocker and markedly inhibited by a Na ؉ ͞Ca 2؉ exchange inhibitor. Sodium efflux caused by SMIF-initiated motility was observed when using both extracellular and intracellular sodium probes. A Na ؉ ͞Ca 2؉ exchange antigen was shown to be present on the surface of the sperm, primarily over the midpiece, by using an antibody to the canine Na ؉ ͞Ca 2؉ exchanger. This antibody recognized a 120-kDa protein that comigrated with the canine myocyte Na ؉ ͞Ca 2؉ exchanger. Sperm of Pacific herring are now shown to use reverse Na ؉ ͞Ca 2؉ exchange in motility initiation. This mechanism of regulation of motility initiation may have evolved for both maintenance of immotility after spawning as well as ligand-induced motility initiation.T eleost fish sperm are quiescent within the testes and seminal plasma before spawning, but most initiate motility after dilution into the external medium (freshwater or seawater for most species) in which spawning occurs (1). In salmonids, motility initiation occurs with dilution in freshwater, specifically from a reduction in extracellular potassium that drives a membrane hyperpolarization and an increase in intracellular calcium ([Ca 2ϩ ] i ) (2-6). Changes in the concentrations of specific ions (Ca 2ϩ , K ϩ , and possibly Na ϩ and Cl Ϫ ) also have been linked to motility initiation in Atlantic croaker sperm (7). A hyperpolarization of the sperm membrane also has been documented in carp sperm, reportedly linked to the opening of voltage-gated Ca 2ϩ channels and an increase in [Ca 2ϩ ] i (8). In other freshwater teleost sperm (goldfish, zebra fish), as well as in marine teleost sperm (puffer, flounder), motility is believed to occur as a result of nonspecific hypo-or hyperosmotic changes that drive changes in intracellular ion concentrations (5, 9, 10). Thus, in all systems studied to date, a membrane hyperpolarization leads to an increase in [Ca 2ϩ ] i and the initiation of motility.Although the stimulation of sperm motility in the vicinity of eggs has been reported in some teleost fish, only herring sperm have been shown to require an egg chorion-derived ligand for ...

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Section: Discussionmentioning

confidence: 99%

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Vines

Yoshida

Griffin

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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“…Capacitative Ca 2ϩ entry replenishes the internal Ca 2ϩ stores and is mediated by a signal transduction process (32). In regard to sperm function, a SOC is known to be involved in the acrosome reaction (23,(33)(34)(35). However, there is as yet no evidence suggesting that the channel is involved in sperm motility, although sperm activation and chemotaxis usually require extracellular Ca 2ϩ (36,37).…”

Section: Discussionmentioning

confidence: 99%

Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm

Yoshida

Ishikawa

Izumi

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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The sperm-activating and -attracting factor released from the eggs of the ascidians Ciona intestinalis and Ciona savignyi requires extracellular Ca 2؉ for activating sperm motility and eliciting chemotactic behavior of the activated sperm toward the egg. Here, we show that modulators of the store-operated Ca 2؉ channel, SK&F96365, Ni 2؉ , 2-aminoethoxydiphenylborane, and thapsigargin inhibit the chemotactic behavior of the ascidian sperm; on the other hand, blockers of voltage-dependent Ca 2؉ channels did not inhibit the chemotaxis, even though they inhibited the sperm activation operated by voltage-dependent Ca 2؉ channels. The blockers of store-operated Ca 2؉ channels also inhibited the asymmetrical flagellar beating and turning movements of the ascidian sperm, which are typical signs of sperm chemotaxis. Depletion of internal Ca 2؉ stores by thapsigargin induced capacitative Ca 2؉ entry into the sperm, which was blocked by SK&F96365. These results suggest that the intracellular Ca 2؉ concentration increase through the store-operated Ca 2؉ channels induces asymmetrical flagellar movements to establish the chemotactic behavior of the sperm. I t is now well known that many cells, e.g., leukocytes, starved amoebae of Dictyostelium discoideum, bacteria, and migrating axon cells during development, can detect an extracellular chemical gradient and migrate toward the source of the chemicals, that is, exhibit chemotactic behavior. There is a variety of factors inducing chemotaxis of cells, e.g., food, pathogens, partner cells, etc., and chemotactic behavior of cells is one of the important communication systems between separated cells. Chemotactic behavior of the sperm toward an egg during fertilization in animal species is a typical case, first reported in hydrozoans (1). This phenomenon is now widely known to occur, from sponges to humans (2-4), and much effort has been devoted to clarifying the mechanisms underlying sperm chemotaxis.Extracellular Ca 2ϩ is generally accepted as being an important factor in the induction of chemotactic behavior of sperm in many plant and animal species (5-8). In the case of the sea urchin, Arbacia punctulata, a peptide named resact in the jelly layer of the egg has been shown to have sperm-activating and -attracting activities (7). The peptide increases the intracellular Ca 2ϩ concentration ([Ca 2ϩ ] i ) via cAMP-gated Ca 2ϩ channels (9, 10), which, in turn, induces asymmetrical flagellum movements (5, 11, 12) that result in reorientation of the sperm swimming direction (13). The role of extracellular Ca 2ϩ -induced asymmetrical flagellar movement in inducing sperm chemotaxis has also been reported in hydrozoan species (14). Ascidian sperm chemotactic behavior is also characterized by abrupt turning movements of the sperm (15, 16). Furthermore, it has been shown that the sperm-attracting activity in the ascidians Ciona intestinalis and Ciona savignyi does not originate from the overall surface of the egg coats, such as follicle cells, but from the vegetal pole of the egg (17). We al...

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“…With 10.6 g/ml 5h-hFSP, the increased [Ca 2ϩ ] i /K d value was 0.08 both with and without nifedipine, whereas seawater control was 0.03 (Fig. 6B) (4). To test whether 5h-hFSP opens the second channel, Ni 2ϩ was used at 300 M, a concentration at which neither a sustained [Ca 2ϩ ] i increase nor the AR are induced (4).…”

Section: Resultsmentioning

confidence: 99%

“…Undiluted semen (4 ϫ 10 10 cells/ml) was suspended in 4 volumes of dye loading buffer (artificial seawater containing 10 mM HEPES, 1 mM CaCl 2 , and 0.1 mg/ml soybean trypsin inhibitor at pH 7.0; Ref. 4). The sperm suspension was placed in a 15-ml round bottom polystyrene tube with dimethyl sulfoxide (final concentration 0.6%) containing either fura-2/AM or BCECF/AM at a final concentration of 12 M, and the tube was incubated at least 8 h before washing.…”

Section: Methodsmentioning

confidence: 99%

“…There are two plasma membrane Ca 2ϩ channels involved in AR induction: the first is receptor-operated and opens 1 s after sperm contact EJ, the second opens 5 s after the first in response to increased intracellular pH (pH i ). The second channel can also transport Mn 2ϩ (2)(3)(4). The Ca 2ϩ channel blocker nisoldipine does not block Mn 2ϩ movement through the second channel but does block the first channel and hence also blocks the AR (3).…”

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confidence: 99%

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High Molecular Mass Egg Fucose Sulfate Polymer Is Required for Opening Both Ca2+ Channels Involved in Triggering the Sea Urchin Sperm Acrosome Reaction

Hirohashi

Vacquier

2002

Journal of Biological Chemistry

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A linear fucose sulfate polymer (FSP), >106 daltons, is a major component of sea urchin egg jelly. FSP induces the sperm acrosome reaction (AR), an exocytotic process required for animal fertilization. Two Ca 2؉ channels activate during AR induction, the first opens 1 s after FSP addition, and the second opens 5 s after the first. Mild acid hydrolysis of FSP results in a linear decrease in polymer size. The ability of FSP to induce the AR and activate sperm Ca 2؉ channels decreases with increasing time of hydrolysis. Hydrolyzed FSP of ϳ60 kDa blocks intact FSP from inducing the AR. At 44 g/ml hydrolyzed FSP, Ca 2؉ entry into sperm is almost equal to that occurring in 3.8 g/ml intact FSP; however the AR is not induced. The sperm acrosome reaction (AR) 1 is required for animal fertilization and is a potential target for the development of novel methods of non-hormonal contraception. Sea urchin spermatozoa are ideal for studying signal transduction underlying the animal sperm AR because they can be obtained as pure cells in vast quantities at low cost. The AR is triggered when sperm contact the jelly layer surrounding the egg (EJ). Morphologically, the AR involves the exocytosis of the acrosomal vesicle and the polymerization of actin to form the acrosomal process; both events are required for sperm to bind to and fuse with eggs. Physiologically, the AR requires the influx of Ca 2ϩ and Na ϩ and the efflux of H ϩ and K ϩ ions (1, 2). There are two plasma membrane Ca 2ϩ channels involved in AR induction: the first is receptor-operated and opens 1 s after sperm contact EJ, the second opens 5 s after the first in response to increased intracellular pH (pH i ). The second channel can also transport Mn 2ϩ (2-4). The Ca 2ϩ channel blocker nisoldipine does not block Mn 2ϩ movement through the second channel but does block the first channel and hence also blocks the AR (3). Eighty percent of the mass of sea urchin EJ is a fucose sulfate polymer (FSP) of Ͼ1 million daltons (5). Purified FSP, having no amino acid content, induces the AR (5, 6). However, oligosaccharides of EJ glycoproteins substantially potentiate the FSP-induced AR, suggesting there is more than one receptor system regulating ion channels that trigger the AR (7). 2FSP is a linear polymer of ␣-L-1,3-fucose with a species-specific pattern of sulfation of the fucosyl residues (8). The sulfation pattern is responsible for FSP's species-specific induction of the AR (9, 10). FSP is also a potent inhibitor of human blood coagulation through its high affinity binding to heparin cofactor II (11).Receptor for egg jelly-1 (REJ1) is a 1450-amino acid glycoprotein located in the plasma membrane over the sea urchin sperm acrosomal vesicle and also on the sperm flagellum. Available data support the hypothesis that REJ1 is at least one of the sperm receptors for FSP (6, 12). Purified REJ1 neutralizes the AR activity of EJ (12). An affinity column of REJ1 binds only FSP when crude EJ is applied (6). Monoclonal antibodies to REJ1 induce Ca 2ϩ influx into sperm (13) and induce...

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A Sustained Increase in Intracellular Ca2+ Is Required for the Acrosome Reaction in Sea Urchin Sperm

Cited by 60 publications

References 43 publications

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Motility initiation in herring sperm is regulated by reverse sodium-calcium exchange

Store-operated calcium channel regulates the chemotactic behavior of ascidian sperm

High Molecular Mass Egg Fucose Sulfate Polymer Is Required for Opening Both Ca2+ Channels Involved in Triggering the Sea Urchin Sperm Acrosome Reaction

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