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      Two-dimensional slither swimming of sperm within a micrometre of a surface

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          Abstract

          Sperm motion near surfaces plays a crucial role in fertilization, but the nature of this motion has not been resolved. Using total internal reflection fluorescence microscopy, we selectively imaged motile human and bull sperm located within one micron of a surface, revealing a distinct two-dimensional (2D) ‘slither' swimming mode whereby the full cell length (50–80 μm) is confined within 1 μm of a surface. This behaviour is distinct from bulk and near-wall swimming modes where the flagellar wave is helical and the head continuously rotates. The slither mode is intermittent (∼1 s, ∼70 μm), and in human sperm, is observed only for viscosities over 20 mPa·s. Bull sperm are slower in this surface-confined swimming mode, owing to a decrease in their flagellar wave amplitude. In contrast, human sperm are ∼50% faster—suggesting a strategy that is well suited to the highly viscous and confined lumen within the human fallopian tube.

          Abstract

          Sperm motion near surfaces plays a key role in fertilization, but a description of how this motion differs from bulk swimming is lacking. Here, Nosrati et al. visualize sperm swimming within 1 μm of a glass surface and describe a ‘slither' swimming mode which differs from bulk helical swimming, and increases the velocity of human sperm.

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          Most cited references54

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          Swimming in circles: motion of bacteria near solid boundaries.

          Near a solid boundary, Escherichia coli swims in clockwise circular motion. We provide a hydrodynamic model for this behavior. We show that circular trajectories are natural consequences of force-free and torque-free swimming and the hydrodynamic interactions with the boundary, which also leads to a hydrodynamic trapping of the cells close to the surface. We compare the results of the model with experimental data and obtain reasonable agreement. In particular, the radius of curvature of the trajectory is observed to increase with the length of the bacterium body.
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            A self-organized vortex array of hydrodynamically entrained sperm cells.

            Many patterns in biological systems depend on the exchange of chemical signals between cells. We report a spatiotemporal pattern mediated by hydrodynamic interactions. At planar surfaces, spermatozoa self-organized into dynamic vortices resembling quantized rotating waves. These vortices formed an array with local hexagonal order. Introducing an order parameter that quantifies cooperativity, we found that the array appeared only above a critical sperm density. Using a model, we estimated the hydrodynamic interaction force between spermatozoa to be approximately 0.03 piconewtons. Thus, large-scale coordination of cells can be regulated hydrodynamically, and chemical signals are not required.
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              Total internal reflection fluorescence microscopy in cell biology.

              Key events in cellular trafficking occur at the cell surface, and it is desirable to visualize these events without interference from other regions deeper within. This review describes a microscopy technique based on total internal reflection fluorescence which is well suited for optical sectioning at cell-substrate regions with an unusually thin region of fluorescence excitation. The technique has many other applications as well, most notably for studying biochemical kinetics and single biomolecule dynamics at surfaces. A brief summary of these applications is provided, followed by presentations of the physical basis for the technique and the various ways to implement total internal reflection fluorescence in a standard fluorescence microscope.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Pub. Group
                2041-1723
                10 November 2015
                2015
                : 6
                : 8703
                Affiliations
                [1 ]Department of Mechanical and Industrial Engineering, University of Toronto , Toronto, Ontario, Canada M5S 3G8
                [2 ]Department of Biochemistry, University of Toronto , Toronto, Ontario, Canada M5S 1A8
                [3 ]Institute of Biomaterials and Biomedical Engineering, Terrence Donnelly Centre for Cellular and Biomolecular Research, University of Toronto , Toronto, Ontario, Canada M5S 3E1
                [4 ]Department of Chemical Engineering and Applied Chemistry, University of Toronto , Toronto, Ontario, Canada M5S 3E5
                Author notes
                Article
                ncomms9703
                10.1038/ncomms9703
                4667638
                26555792
                f235d577-7ae0-400e-be8e-3aa5d3a383d1
                Copyright © 2015, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 07 February 2015
                : 22 September 2015
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