Trout sperm swimming patterns and role of intracellular Ca⁺⁺

Abstract

We investigated the swimming patterns of trout sperm using computer-assisted analyses of video microscopy. Under full activation conditions, in which 80-100% of sperm activate their motility, sperm swim in circular paths for 2-5 sec, followed by 30-60 sec of a more linear swimming, and, finally, cessation of movement, with a straightening of the flagella. Threshold activation, in which 50% of the sperm activate, is characterized by circular patterns of swimming for less than 20 sec, with straightened flagella upon cessation. Full activation and threshold activation are observed in low-K' solution or in an Mg+ +-supplemented K + solution. Similarities in swimming patterns in low-K+ solution and in a Mg + +-supplemented K' solution suggest a common underlying mechanism of activation. Initiation of movement in solutions with high C a t ' to K + ratio is similar to activation in K'-free solution. However, sperm in C a t + -supplemented media resume circular swimming within 20-25 sec after activation, and, upon cessation of movement, the flagella are frequently cane shaped or bent. Differences in swimming patterns upon activation by high Cat

Membrane hyperpolarization removes inactivation of Ca 2+ channels, leading to Ca 2+ influx and subsequent initiation of sperm motility in the common carp

“…It was also shown by Okuno and Morisawa (32) that demembranated trout sperm showed vigorous motility in the reactivating solution containing Ca 2ϩ in a concentration below 10 Ϫ8 M, suggesting that the initiation of fish sperm motility requires a transient influx of Ca 2ϩ , although its origin, from intracellular storage or of extracellular origin, is controversial (29). The present results suggest that the presence of extracellular Ca 2ϩ is necessary for the initiation of sperm motility in carp.…”

“…An increase in intracellular calcium is a prerequisite for the initiation of sperm motility in rainbow trout (28)(29)(30)(31). It was also shown by Okuno and Morisawa (32) that demembranated trout sperm showed vigorous motility in the reactivating solution containing Ca 2ϩ in a concentration below 10 Ϫ8 M, suggesting that the initiation of fish sperm motility requires a transient influx of Ca 2ϩ , although its origin, from intracellular storage or of extracellular origin, is controversial (29).…”

“…Membrane hyperpolarization (29) through the direct effect of transmembrane K ϩ efflux (30,31) is the first trigger for the initiation of sperm motility in salmonid fishes. Membrane hyperpolarization also triggers the activation of ascidian sperm motility through hyperpolarization-induced direct activation of adenylyl cyclase to synthesize cAMP in Ciona (35).…”

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

“…Krasznai et al (8) demonstrated that the activation of voltagegated calcium channels is required in carp sperm for motility initiation; this activation depends upon membrane hyperpolarization through opening of K ϩ channels and a K ϩ efflux. In other teleosts, there has been debate over the source of the Ca 2ϩ and thus the need for Ca 2ϩ channels during the [Ca 2ϩ ] i increase at motility initiation (36). Although some studies have suggested that Ca 2ϩ from intracellular stores may be sufficient for motility initiation (36) or may participate in the initiation of motility as has been described in puffer fish (9), most studies have suggested that it is the influx of external Ca 2ϩ after membrane hyperpolarization that is required for motility (5,8).…”

“…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)(3)(4)(5)(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).…”