Bend propagation in the flagella of migrating human sperm, and its modulation by viscosity

Abstract

A pre-requisite for sexual reproduction is successful unification of the male and female gametes; in externally-fertilising echinoderms the male gamete is brought into close proximity to the female gamete through chemotaxis, the associated signalling and flagellar beat changes being elegantly characterised in several species. In the human, sperm traverse a relatively high-viscosity mucus coating the tract surfaces, there being a tantalising possible role for chemotaxis. To understand human sperm migration and guidance, studies must therefore employ similar viscous in vitro environments. High frame rate digital imaging is used for the first time to characterise the flagellar movement of migrating sperm in low and high viscosities. While qualitative features have been reported previously, we show in precise spatial and temporal detail waveform evolution along the flagellum. In low viscosity the flagellum continuously moves out of the focal plane, compromising the measurement of true curvature, nonetheless the presence of torsion can be inferred. In high viscosities curvature can be accurately determined and we show how waves propagate at approximately constant speed. Progressing waves increase in curvature approximately linearly except for a sharper increase over a distance approximately 20-27 microm from the head/midpiece junction. Curvature modulation, likely influenced by the outer dense fibres, creates the characteristic waveforms of high viscosity swimming, with remarkably effective cell progression against greatly increased resistance, even in high viscosity liquids. Assessment of motility in physiological viscosities will be essential in future basic research, studies of chemotaxis and novel diagnostics.

Effect of viscosity on motion characteristics of bovine sperm

“…Therefore, the observation of the present experiment showed similar results to those obtained by Rikmenspoel [28]. Furthermore, the difference with respect to the viscosity was similarly noted by Smith et al [23]. The thickness of the flagellum is nonuniform, with the flagellum becoming thinner from the midpiece to the end piece.…”

“…Smith et al [23] experimentally investigated the effect of viscosity on sperm motion characteristics using methylcellulose as the fluid surrounding the sperm. Consequently, they obtained experimental results indicating that as the viscosity increases, it has little influence on the straight-line velocity.…”

Considerations of viscosity in the preliminaries to mammalian fertilisation

“…The flagellar movements of human spermatozoa migrating in solutions of low or high viscosity have been characterised [55]. The rolling rate, planarity, torsion, waveform, trajectory and progression per flagellar beat are significantly altered by viscosity, but not the progressive velocity.…”

Coarse-Graining the Fluid Flow around a Human Sperm

“…Gd,87.19.ru The flagellum is a moving whip-like cellular appendage found on numerous protozoa and the spermatozoa of almost all species. In particular, the subject of male sub-fertility has led to extensive quantitative studies of human sperm motility [1][2][3][4], while even single cell studies can generate extensive information, in particular from digital imaging microscopy. However, the tools for examining human sperm digital imaging microscopy are founded from an era where only the cell body, and not the flagellum, could be readily resolved [1,2].…”

“…The experimental methodology is further detailed in Smith et al [3]. In summary, human sperm samples were collected from a normozoospermic research A time sequence of flagellar position data in the microscope focal plane was extracted from the imaging data, using custom MATLAB c ⃝ software [3].…”