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

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 sodium–calcium (Na+/Ca2+) exchange. Membrane depolarization was slightly inhibited by a calcium channel blocker and markedly inhibited by a Na+/Ca2+ exchange inhibitor. Sodium efflux caused by SMIF-initiated motility was observed when using both extracellular and intracellular sodium probes. A Na+/Ca2+ 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+/Ca2+ exchanger. This antibody recognized a 120-kDa protein that comigrated with the canine myocyte Na+/Ca2+ exchanger. Sperm of Pacific herring are now shown to use reverse Na+/Ca2+ 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.

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