Mammalian sperm interactions with the female reproductive tract

Abstract

The mammalian female reproductive tract interacts with sperm in various ways in order to facilitate sperm migration to the egg while impeding migrations of pathogens into the tract, to keep sperm alive during the time between mating and ovulation, and to select the fittest sperm for fertilization. The two main types of interactions are physical and molecular. Physical interactions include the swimming responses of sperm to the microarchitecture of walls, to fluid flows, and to fluid viscoelasticity. When sperm encounter walls, they have a strong tendency to remain swimming along them. Sperm will also orient their swimming into gentle fluid flows. The female tract seems to use these tendencies of sperm to guide them to the site of fertilization. When sperm hyperactivate, they are better able to penetrate highly viscoelastic media, such as the cumulus matrix surrounding eggs. Molecular interactions include communications of sperm surface molecules with receptors on the epithelial lining of the tract. There is evidence that specific sperm surface molecules are required to enable sperm to pass through the uterotubal junction into the oviduct. When sperm reach the oviduct, most bind to the oviductal epithelium. This interaction holds sperm in a storage reservoir until ovulation and serves to maintain the fertilization competence of stored sperm. When sperm are released from the reservoir, they detach from and re-attach to the epithelium repeatedly while ascending to the site of fertilization. We are only beginning to understand the communications that may pass between sperm and epithelium during these interactions.

Keywords: Cervix; Fallopian tubes; Microfluidics; Oviduct; Spermatozoa.

Fig 1

Human sperm in a microchannel designed to guide them to swim counterclockwise (curved arrow). The input site for sperm is indicated by the large, straight arrow. The insert shows a higher magnification of tracks of sperm swimming within the microchannel. Images were collected at 4 frames per second and the location of sperm heads (tiny dots) in 200 consecutive frames were summed to produce this figure (from Denissenko et al. 2012).

Fig 2

Scanning electron micrograph of the surface that lines the bovine uterotubal junction. The junction has been opened longitudinally and is oriented such that the uterus would lie to the left. Notice that mucosal folds form blunt arrows that point into the oviduct (from Yaniz et al. 2000).

Fig 3

A microfluidic device designed to model fluid flows and microgrooves within the cervix. a. Diagrams of bull sperm and Tritrichomonas foetus. b. Illustration of a bovine female reproductive tract (from Roberts et al. 1986). The pink arrow points in the direction of fluid flow through the cervix. c. Microgrooves are seen in PAS/hematoxylin-stained frozen sections of the bovine cervix (detailed methods in Suarez et al. 1997). d. Diagram of the microfluidic device that re-creates the microgrooves and fluid flows of the bovine cervix. The sperm seeding port is on the left side and the flow inlet on the right; they are connected by channels with and without microgrooves. e. Details of the channel design in the middle of the device. There are six channels for parallel experimentation: G denotes a channel with microgrooves in the upper surface and F denotes a control channel lacking microgrooves. f. A 3D drawing illustrates the details of a grooved channel. Here the main channel is 120 [μ]m in height and the microgrooves have a sectional area of 20 [μ]m × 20 [μ]m… Drawing not to scale.

Fig 4

Scanning electron micrograph of bull sperm bound to cilia on the epithelium of the oviductal isthmus. The sperm are located in grooves between secondary folds of oviductal mucosa (bar = 10 μm; from Lefebvre et al. 1995).

Fig 5

Tracings of video images and swimming tracks of activated (a) and hyperactivated (b) bull sperm. The tracings of sperm (below) represent three successive video images taken at 30 images/sec. The swimming tracks (above) are shown as lines connecting the positions of the head/tail junctions on successive video frames (30/sec) over a 1 sec period. (modified from Ho et al. 2002).