Role of Ion Channels in the Maintenance of Sperm Motility and Swimming Behavior in a Marine Teleost

Abstract

In oviparous marine fishes, the hyperosmotic induction of sperm motility in seawater (SW) is well established, however, the potential function of ion channels in the maintenance of post activated spermatozoon swimming performance remains largely unknown. Here, we investigated the influence of ion channels on the spermatozoon swimming parameters using the gilthead seabream (Sparus aurata) as a model for modern marine teleosts. Our data show that the SW-induced activation of seabream sperm motility requires three concomitant processes, the hyperosmotic shock, an ion-flux independent increase of the intracellular concentration of Ca2+ ([Ca2+]i), but not of [K+]i or [Na+]i, and the alkalization of the cytosol. The combination of all three processes is obligatory to trigger flagellar beating. However, the time-course monitoring of sperm motion kinetics and changes in the [Ca2+]i, [K+]i and [Na+]i in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca2+ and K+. A meta-analysis of a seabream sperm transcriptome uncovered the expression of multiple ion channels, some of which were immunolocalized in the head and/or tail of the spermatozoon. Selective pharmacological inhibition of these ion channel families impaired the long-term motility, progressivity, and velocity of SW-activated spermatozoa. The data further revealed that some antagonists of K+-selective or Ca2+-selective channels, as well as of stretch-activated and mechanosensitive channels, altered the trajectory of spermatozoa, suggesting that these ion channels are likely involved in the control of the swimming pattern of the post activated spermatozoon. These combined findings provide new insight into the signaling pathways regulating spermatozoon activation and swimming performance in marine fishes.

The Mature COC Promotes the Ampullary NPPC Required for Sperm Release from Porcine Oviduct Cells

“…The cGMP-sensitive CNG channels inhibitor l-cis -Diltiazem, but not the CatSper channel inhibitor NNC 055-0396, blocked NPPC-induced increase of sperm motility ( Table S2 ). The activation of CNG channels can increase Ca 2+ levels in spermatozoa [ 30 ], and Ca 2+ signaling is required for sperm motility [ 31 ]. Thus, we examined the effect of NPPC on Ca 2+ levels in porcine spermatozoa by measuring Ca 2+ fluorescence intensity.…”

Making immotile sperm motile using high-frequency ultrasound

“…Several potential mechanisms can contribute to the reduction in MMP upon exposure to ultrasound. Ultrasound could enhance mitochondrial Ca 2+ uptake through the activation of mechanosensitive ion channels (57) to adapt OXPHOS substrate supply for ATP needs (27,58) and contribute to maintaining motility (59)(60)(61)(62). Depolarization of the MMP could also be explained by the reverse operation of the mitochondrial shuttle systems as a result of the increased rate of glycolysis in the principal piece upon exposure, which subsequently leads to the depolarization of the reduced form of nicotinamide adenine dinucleotide (NAD + ):NAD + redox potential (63, 64) Another plausible explanation for the drop in MMP is the increase in the rate of ATP hydrolysis in the flagellum in response to ultrasound, which leads to a less negative ATP hydrolysis free energy and dissipation of the proton motive force (65,66).…”

Research progress on ion channels and their molecular regulatory mechanisms in the human sperm flagellum

“…1,2 Many studies have indicated that most of these physiological reactions are closely related to the movement of the sperm tail. 3,4 The tail of sperm is also called the flagellum and is composed of the midpiece, principal, and terminal parts, [5][6][7] which are implicated in sperm metabolism and movement. [8][9][10] The maintenance of ionic balance, determined by ion channels in flagella, is the premise for the metabolism and motility of flagella.…”