Journal Article

Rheotaxis facilitates upstream navigation of mammalian sperm cells

Goldstein, Raymond E, Dunkel, Jörn, Kantsler, Vasily, Blayney, Martyn

2014

Overview

A major puzzle in biology is how mammalian sperm maintain the correct swimming direction during various phases of the sexual reproduction process. Whilst chemotaxis may dominate near the ovum, it is unclear which cues guide spermatozoa on their long journey towards the egg. Hypothesized mechanisms range from peristaltic pumping to temperature sensing and response to fluid flow variations (rheotaxis), but little is known quantitatively about them. We report the first quantitative study of mammalian sperm rheotaxis, using microfluidic devices to investigate systematically swimming of human and bull sperm over a range of physiologically relevant shear rates and viscosities. Our measurements show that the interplay of fluid shear, steric surface-interactions, and chirality of the flagellar beat leads to stable upstream spiralling motion of sperm cells, thus providing a generic and robust rectification mechanism to support mammalian fertilisation. A minimal mathematical model is presented that accounts quantitatively for the experimental observations. A sperm cell must complete a long and taxing journey to stand a chance of fertilising an egg cell. This quest covers a distance that is thousands of times longer than the length of a sperm cell. It also passes through the diverse environments of the cervix, the uterus and, finally, the oviduct, where there might be an egg to fertilise. How the sperm cells manage to stay on course over this distance is a mystery, although it has been suggested that many different factors, including chemical signals and fluid flow, are involved. The fluids that the sperm cells travel through are not static. Evidence suggests that contractions of the cervix and uterus help to pump sperm cells along the first part of their journey. However, mucus flows out of the oviduct in the opposite direction to way the sperm cells need to go. Sperm cells mostly move along the walls of the cervix, uterus, and oviduct. This means that sperm cells must contend with two properties of the fluids they travel through—the viscosity (or ‘thickness’) of the fluid, and the fact that different parts of the fluid will flow at different speeds, depending on how close it is to the wall (‘shear flow’). Kantsler et al. have now used a technique called microfluidics—which involves forcing tiny amounts of liquid to flow through very narrow channels—to study how the movement of human and bull sperm cells along a surface is affected by the viscosity and flow rate of the fluid they are swimming through. The sperm cells were found to swim upstream, moving along the walls of the channels in a spiral movement. This is likely to help the sperm cells to find the egg, because spiralling around the oviduct will increase the chances of meeting the egg. Kantsler et al. also built a mathematical model that describes how the sperm cells move. Although further work is needed to better understand the role played by chemical signals, understanding how fluid flow and viscosity influence sperm cells could lead to more effective artificial insemination techniques.

• Publisher: eLife Sciences Publications Ltd,eLife Sciences Publications, Ltd
• Subject: Animals / Biophysics and Structural Biology / Cattle / Chemotaxis / Chirality / Experiments / Fertilization / Fertilization - physiology / Flagella / Fluid flow / Human Biology and Medicine / Humans / Lab-On-A-Chip Devices / Male / Mammals / Mathematical models / Mechanical stimuli / Microfluidics / Models, Theoretical / Motility / Ovum - physiology / Rheotaxis / Sexual reproduction / Sperm / Sperm Motility - physiology / Spermatozoa - physiology / Swimming