Reversible intracellular ATP changes in intact rat spermatozoa and effects on flagellar sperm movement

Abstract

The initiation of motility and modification of energy metabolism of rat caudal epididymal spermatozoa can be induced by dilution in a saline medium. We have investigated in these cells the relationships between the energy reserve (sperm ATP content measured by bioluminescence) and flagellar movement (high speed videomicrography, 200 frames/sec). A steady state was observed in sperm ATP content, progressive velocity (Vp) and flagellar beat frequency (F) with sperm dilution in a medium with glucose, lactate, pyruvate and acetate substrates after 30 minutes of incubation. Without these substrates, changes in metabolic pathways occurred immediately and initially disturbed the relationship between ATP levels and F, suggesting differences in motility initiation when energy is from an endogenous origin via mitochondrial oxidative phosphorylation. This "energy crisis" was reversed by the addition of substrates to the medium. The three-dimensional flagellar movement observed in the presence of substrates quickly became two-dimensional in their absence. The flagellar beat envelope became more splayed, the mean amplitude of lateral head displacement increased and F decreased. The resulting high flagellar beat efficiency can be compared to that observed during hyperactivation which is a physiological event related to a fall in intracellular ATP level. In both media, the displacement of the flagellum in relation to the wave axis varied sinusoidally. The sine period increased with time when the spermatozoa were incubated in the medium without substrates. These results suggest a gradual slowing-down of the velocity of wave formation in the proximal part of the flagellum.

Status Specific Tailoring of Sperm Behavior in an External Fertilizer

“…These results are similar to that previously well-documented in Arctic charr Vaz Serrano et al, 2006;Haugland et al, 2008) and also in Bluegill (Lepomis macrochirus; Burness et al, 2004). ATP stored in spermatozoa prior to ejaculation provides the necessary chemical energy to sustain sperm motility (Jeulin and Soufir, 1992), and in Bluegills, sperm from subordinates have about 1.5 times more ATP than sperm from dominants (Burness et al, 2004). Further, sperm ATP is positively associated with sperm velocity (Burness et al, 2004;Figenschou et al, 2013) and could be the proximate explanation for the differences in sperm velocity observed previously between males in the two mating roles when activated in water (see Haugland et al, 2008).…”

On the relative effect of spawning asynchrony, sperm quantity, and sperm quality on paternity under sperm competition in an external fertilizer

“…Yet, the velocity reduction is in accordance with Parker's (1990) theoretical model of ejaculate investments under sperm competition which suggest that "..if mating order is non-random, the favored male should expend less on sperm." One might speculate that the metabolic resources for sperm production and sperm velocity, are traded-off differently in dominant and subordinate males over the entire spawning season (Jeulin and Soufir, 1992;Burness et al, 2004, but see Burness et al, 2005) and that dominants in need of more energy for guarding activities, potentially resulting in positional advantages under synchronized spawning, might have to reduce energy investments in sperm. This explanation, which relies heavily on energy being a limited resource for reproductively active males, fits the observations that ATP-levels in sperm of charr is positively related to sperm velocity and negatively related to measures of high social status (i.e., dominance) (Figenschou et al, 2013).…”

Purinergic signalling in the reproductive system in health and disease

“…Spermatozoal ATP concentrations decrease during passage through the epididymis [129]. High flagellar beat efficiency that occurs during hyperactivation is related to a fall in intracellular ATP levels [182]. ATP-supplemented medium has been used for the conservation of human semen for use in artificial insemination [91].…”