Institute of Agrifood Research and Technology (IRTA)-Institute of Biotechnology and Biomedicine (IBB), Universitat Autònoma de Barcelona, 08193 Barcelona, Spain.
Institute of Marine Sciences, Spanish National Research Council (CSIC), 08003 Barcelona, Spain.
Int J Mol Sci. 2022 Oct 11;23(20):12113. doi: 10.3390/ijms232012113.
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 () 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 Ca ([Ca]), but not of [K] or [Na], 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 [Ca], [K] and [Na] in SW or in non-ionic activation media, showed that the post activated maintenance of spermatozoa motility is dependent on extracellular Ca 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 Ca-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.
在卵生海洋鱼类中,海水(SW)中精子活力的高渗诱导已经得到很好的证实,然而,离子通道在维持激活后精子游动性能方面的潜在功能在很大程度上仍然未知。在这里,我们以真鲷()为现代海洋硬骨鱼的模型,研究了离子通道对精子游动参数的影响。我们的数据表明,SW 诱导的真鲷精子活力的激活需要三个同时发生的过程,即高渗冲击、细胞内 Ca([Ca])浓度的离子通量独立增加,但 [K]或[Na]没有增加,以及细胞质的碱化。这三个过程的组合是触发鞭毛摆动的必要条件。然而,对精子运动动力学的时间过程监测以及在 SW 或非离子激活介质中 [Ca]、[K]和[Na]的变化表明,激活后精子运动的维持依赖于细胞外 Ca 和 K。对真鲷精子转录组的荟萃分析揭示了多种离子通道的表达,其中一些在精子的头部和/或尾部被免疫定位。这些离子通道家族的选择性药理学抑制会损害 SW 激活的精子的长期活力、渐进性和速度。数据进一步表明,一些 K 选择性或 Ca 选择性通道、伸展激活和机械敏感通道的拮抗剂改变了精子的轨迹,这表明这些离子通道可能参与了对激活后精子游动模式的控制。这些综合发现为调节海洋鱼类精子激活和游动性能的信号通路提供了新的见解。