46 SEPTEMBER 2013 • WORLD AQUACULTURE • WWW.WAS.ORG After a long period of spermatogenesis, spermatozoa of most fish species are delivered by males spawning in sea- or freshwater simultaneously with ova from females. In most cases, within a very brief period, these minute unicells need to reach a single entrance “hole” (micropyle) on the ova surface to allow sperm penetration for delivery of the male haploid genome to the ova. To accomplish this goal, the flagellum must become fully activated by the surrounding medium immediately on contact with seawater or freshwater to propel the sperm cell at a huge initial velocity. A fish sperm cell initiates motility through osmotic/ionic control. The duration of the short sperm motility period is regulated mainly by the decrease of energetic stores and intracellular ionic changes as a consequence of osmotic shock. Hyperactivity, which occurs immediately after motility activation, causes a very rapid consumption of intracellular ATP, outstripping the energy supply. Spermatozoa quickly become energetically exhausted because mitochondria cannot compensate for this high rate of energy consumption by flagella. Therefore, most spermatozoa become immotile before reaching the micropyle. Following activation, successive events occur during the brief period from full motility until full arrest of flagella activity. Present knowledge allows a good description of the activation mechanism and that of the parameters that characterize the motility period. This understanding is also derived from results obtained from in vitro experiments after removal of the flagellar membrane. In combination with consideration of sperm energetic (ATP) Activation Control of Fish Sperm Motility Jacky J. Cosson and Viktorya Dzyuba content, a general model offers a guideline for understanding the events governing the activity of sperm in fish species with external fertilization. Control of sperm motility during the swimming period is accomplished through successive steps, linearly arranged and occurring at different levels. External control is by surrounding factors, such as osmolarity, ions, gases, temperature and “housekeeping” control that occurs in the sperm flagellum of any species. Control at the sperm cell membrane level occurs by osmotic potential, ionic potential, aquaporins and gas diffusion. Transduction must occur after a signal gets across the membrane. Thus, specific control factors occur internally to the cell, including ionic concentration, ATP and complementarily small molecules, such as cAMP as a secondary signal and/ or phosphorylation of specific proteins. The last step in motility control occurs in the axoneme (motor part of the flagellum), the intracellular compartment where the signal is ultimately received. At the axoneme, dynein (ATP/energyconsuming enzymes) activation occurs, generating sliding and bending that leads to wave propagation and efficient sperm cell movement. Control of these steps occurs in the central structure of the axoneme, mostly via calcium ion signaling. These successive steps allow postulation of a schematic cascade of events leading from fish sperm motility activation to arrest after a short period. While many steps in this cascade have been characterized, detailed understanding has not yet been deciphered. The main goal of this paper is to present a survey of present knowledge on this topic in a simple and comprehensive way. FIGURE 1. Structure of fish spermatozoon and its axoneme. n = nucleus, m = mitochondrion, a = axoneme, m = membrane, c = cytoplasm. The green colored gradient indicates that ATP produced by the mitochondrion diffuses tipward in the flagellum and is rendered accessible to dynein motors distributed along the flagellum. FIGURE 2. Cross-section ultrastructure of a sperm flagellum. Electron microscopy section (left) and ultrastructure of the axoneme as drawn from such images (right). Microtubules are arranged according to the ubiquitous 9+2 structure, with peripheral doublets (red and green) plus two central singlet microtubules (red), which constitute the scaffold on which additional elements are bound. From periphery to center one can observe: 1) the inner and outer dynein arms (pink) which are the micromotors involved in transforming chemical (ATP) into mechanical energy, 2) the radial spokes (blue) involved in the cross-talk of information between peripheral motors and the central elements, 3) the central structure (pink) arranged around two central microtubules. In addition, some links (black) called nexin ensure the elastic junction between peripheral doublets.
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