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Behavioral mechanisms of mammalian sperm guidance.

Perez-Cerezales S, Boryshpolets S, Eisenbach M - Asian J. Androl. (2015 Jul-Aug)

Bottom Line: In mammals, sperm guidance in the oviduct appears essential for successful sperm arrival at the oocyte.Hitherto, three different potential sperm guidance mechanisms have been recognized: thermotaxis, rheotaxis, and chemotaxis, each of them using specific stimuli - a temperature gradient, fluid flow, and a chemoattractant gradient, respectively.Here, we review sperm behavioral in these mechanisms and indicate commonalities and differences between them.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Chemistry, The Weizmann Institute of Science, 7610001 Rehovot, Israel.

ABSTRACT
In mammals, sperm guidance in the oviduct appears essential for successful sperm arrival at the oocyte. Hitherto, three different potential sperm guidance mechanisms have been recognized: thermotaxis, rheotaxis, and chemotaxis, each of them using specific stimuli - a temperature gradient, fluid flow, and a chemoattractant gradient, respectively. Here, we review sperm behavioral in these mechanisms and indicate commonalities and differences between them.

No MeSH data available.


Related in: MedlinePlus

Mammalian sperm rheotaxis. (a and b) Trajectories of mouse spermatozoa in fluid flow (for 3 and 4 s, respectively), analyzed by CASA. Scale bars represent 200 μm. (c and d) Trajectories of human spermatozoa in fluid flow (5 s), analyzed by CASA. Scale bars represent 100 μm. (e) Schematic representation (not drawn to scale) describing the conical envelope of the flagellar beat that holds the spermatozoa close to the surface. The vertical flow gradient exerts a torque that turns the spermatozoa against the flow, but is counteracted by a torque from the chirality of the flagellar wave, resulting in a mean diagonal upstream motion. (f) Rotation rate of individual turning spermatozoa over time. Red line indicates a turning spermatozoon; other lines indicate sperm swimming in a straight line against fluid flow. (g) Fluid flow (red arrows) reorients a spermatozoon (yellow arrows) into the flow to reduce shear as the spermatozoon rotates (orange arrow) and propels itself upstream. Rotation maps out a three-dimensional cone shape in space, which orients spermatozoa consistently into the flow (positive rheotaxis). Tangential forces on the anterior part of the flagellum produce a clockwise force (as seen from above) whereas those on the posterior part provoke a counterclockwise force (Panels a–d, f and g are taken with permission from Miki and Clapham.1 Panel e is taken with permission from Kantsler et al.29).
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Figure 3: Mammalian sperm rheotaxis. (a and b) Trajectories of mouse spermatozoa in fluid flow (for 3 and 4 s, respectively), analyzed by CASA. Scale bars represent 200 μm. (c and d) Trajectories of human spermatozoa in fluid flow (5 s), analyzed by CASA. Scale bars represent 100 μm. (e) Schematic representation (not drawn to scale) describing the conical envelope of the flagellar beat that holds the spermatozoa close to the surface. The vertical flow gradient exerts a torque that turns the spermatozoa against the flow, but is counteracted by a torque from the chirality of the flagellar wave, resulting in a mean diagonal upstream motion. (f) Rotation rate of individual turning spermatozoa over time. Red line indicates a turning spermatozoon; other lines indicate sperm swimming in a straight line against fluid flow. (g) Fluid flow (red arrows) reorients a spermatozoon (yellow arrows) into the flow to reduce shear as the spermatozoon rotates (orange arrow) and propels itself upstream. Rotation maps out a three-dimensional cone shape in space, which orients spermatozoa consistently into the flow (positive rheotaxis). Tangential forces on the anterior part of the flagellum produce a clockwise force (as seen from above) whereas those on the posterior part provoke a counterclockwise force (Panels a–d, f and g are taken with permission from Miki and Clapham.1 Panel e is taken with permission from Kantsler et al.29).

Mentions: When mammalian spermatozoa (thus far demonstrated with human and mouse spermatozoa) sense a flow of fluid, about one half or more of them (both capacitated and noncapacitated spermatozoa) change their path direction and swim against the flow (Figure 3a–3d).1 When the viscosity of the medium is raised to a level that mimics the environment of the oviductal lumen, differences between capacitated and noncapacitated spermatozoa are observed. Noncapacitated spermatozoa move in a more planar path, increasing their chance to stick to the oviductal epithelium. Capacitated spermatozoa rotate around their longitude axis faster than noncapacitated spermatozoa. It was proposed that this faster rotation might enhance the detachment of capacitated spermatozoa from the oviductal surface and might enable them to swim into the main fluid current.1 When they are in the current, the spermatozoa encounter tangential forces that become stronger as they swim perpendicularly to the flow; these forces presumably reorient the spermatozoa against the flow.1 It was proposed that his reorientation is an active process due to the spiral rotation of the sperm tail.1 At least in the case of human spermatozoa, the upstream swimming involves spiral swimming against the shear flow (Figure 3e).29 Since the Ca2+ channel CatSper is apparently essential for rheotaxis, and since this channel is required for hyperactivation, it is reasonable to assume that the release of capacitated spermatozoa from the surface into the main fluid flow and their reorientation in this flow are dependent on hyperactivation.1 Because the hyperactivated flagellar waveform is both asymmetric and of larger amplitude, the flagellum receives larger tangential forces, especially in high-viscosity solution, which points the sperm into flowing solution.1 Once spermatozoa are swimming against the flow, their original rotation rate around their longitude axis is resumed and they swim more linearly (Figure 3f and 3g).


Behavioral mechanisms of mammalian sperm guidance.

Perez-Cerezales S, Boryshpolets S, Eisenbach M - Asian J. Androl. (2015 Jul-Aug)

Mammalian sperm rheotaxis. (a and b) Trajectories of mouse spermatozoa in fluid flow (for 3 and 4 s, respectively), analyzed by CASA. Scale bars represent 200 μm. (c and d) Trajectories of human spermatozoa in fluid flow (5 s), analyzed by CASA. Scale bars represent 100 μm. (e) Schematic representation (not drawn to scale) describing the conical envelope of the flagellar beat that holds the spermatozoa close to the surface. The vertical flow gradient exerts a torque that turns the spermatozoa against the flow, but is counteracted by a torque from the chirality of the flagellar wave, resulting in a mean diagonal upstream motion. (f) Rotation rate of individual turning spermatozoa over time. Red line indicates a turning spermatozoon; other lines indicate sperm swimming in a straight line against fluid flow. (g) Fluid flow (red arrows) reorients a spermatozoon (yellow arrows) into the flow to reduce shear as the spermatozoon rotates (orange arrow) and propels itself upstream. Rotation maps out a three-dimensional cone shape in space, which orients spermatozoa consistently into the flow (positive rheotaxis). Tangential forces on the anterior part of the flagellum produce a clockwise force (as seen from above) whereas those on the posterior part provoke a counterclockwise force (Panels a–d, f and g are taken with permission from Miki and Clapham.1 Panel e is taken with permission from Kantsler et al.29).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 3: Mammalian sperm rheotaxis. (a and b) Trajectories of mouse spermatozoa in fluid flow (for 3 and 4 s, respectively), analyzed by CASA. Scale bars represent 200 μm. (c and d) Trajectories of human spermatozoa in fluid flow (5 s), analyzed by CASA. Scale bars represent 100 μm. (e) Schematic representation (not drawn to scale) describing the conical envelope of the flagellar beat that holds the spermatozoa close to the surface. The vertical flow gradient exerts a torque that turns the spermatozoa against the flow, but is counteracted by a torque from the chirality of the flagellar wave, resulting in a mean diagonal upstream motion. (f) Rotation rate of individual turning spermatozoa over time. Red line indicates a turning spermatozoon; other lines indicate sperm swimming in a straight line against fluid flow. (g) Fluid flow (red arrows) reorients a spermatozoon (yellow arrows) into the flow to reduce shear as the spermatozoon rotates (orange arrow) and propels itself upstream. Rotation maps out a three-dimensional cone shape in space, which orients spermatozoa consistently into the flow (positive rheotaxis). Tangential forces on the anterior part of the flagellum produce a clockwise force (as seen from above) whereas those on the posterior part provoke a counterclockwise force (Panels a–d, f and g are taken with permission from Miki and Clapham.1 Panel e is taken with permission from Kantsler et al.29).
Mentions: When mammalian spermatozoa (thus far demonstrated with human and mouse spermatozoa) sense a flow of fluid, about one half or more of them (both capacitated and noncapacitated spermatozoa) change their path direction and swim against the flow (Figure 3a–3d).1 When the viscosity of the medium is raised to a level that mimics the environment of the oviductal lumen, differences between capacitated and noncapacitated spermatozoa are observed. Noncapacitated spermatozoa move in a more planar path, increasing their chance to stick to the oviductal epithelium. Capacitated spermatozoa rotate around their longitude axis faster than noncapacitated spermatozoa. It was proposed that this faster rotation might enhance the detachment of capacitated spermatozoa from the oviductal surface and might enable them to swim into the main fluid current.1 When they are in the current, the spermatozoa encounter tangential forces that become stronger as they swim perpendicularly to the flow; these forces presumably reorient the spermatozoa against the flow.1 It was proposed that his reorientation is an active process due to the spiral rotation of the sperm tail.1 At least in the case of human spermatozoa, the upstream swimming involves spiral swimming against the shear flow (Figure 3e).29 Since the Ca2+ channel CatSper is apparently essential for rheotaxis, and since this channel is required for hyperactivation, it is reasonable to assume that the release of capacitated spermatozoa from the surface into the main fluid flow and their reorientation in this flow are dependent on hyperactivation.1 Because the hyperactivated flagellar waveform is both asymmetric and of larger amplitude, the flagellum receives larger tangential forces, especially in high-viscosity solution, which points the sperm into flowing solution.1 Once spermatozoa are swimming against the flow, their original rotation rate around their longitude axis is resumed and they swim more linearly (Figure 3f and 3g).

Bottom Line: In mammals, sperm guidance in the oviduct appears essential for successful sperm arrival at the oocyte.Hitherto, three different potential sperm guidance mechanisms have been recognized: thermotaxis, rheotaxis, and chemotaxis, each of them using specific stimuli - a temperature gradient, fluid flow, and a chemoattractant gradient, respectively.Here, we review sperm behavioral in these mechanisms and indicate commonalities and differences between them.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Chemistry, The Weizmann Institute of Science, 7610001 Rehovot, Israel.

ABSTRACT
In mammals, sperm guidance in the oviduct appears essential for successful sperm arrival at the oocyte. Hitherto, three different potential sperm guidance mechanisms have been recognized: thermotaxis, rheotaxis, and chemotaxis, each of them using specific stimuli - a temperature gradient, fluid flow, and a chemoattractant gradient, respectively. Here, we review sperm behavioral in these mechanisms and indicate commonalities and differences between them.

No MeSH data available.


Related in: MedlinePlus