Modelling a tethered mammalian sperm cell undergoing hyperactivation

Handle URI:
http://hdl.handle.net/10754/598864
Title:
Modelling a tethered mammalian sperm cell undergoing hyperactivation
Authors:
Curtis, M.P.; Kirkman-Brown, J.C.; Connolly, T.J.; Gaffney, E.A.
Abstract:
The beat patterns of mammalian sperm flagella can be categorised into two different types. The first involves symmetric waves propagating down the flagellum with a net linear propulsion of the sperm cell. The second, hyperactive, waveform is classified by vigorous asymmetric waves of higher amplitude, lower wavenumber and frequency propagating down the flagellum resulting in highly curved trajectories. The latter beat pattern is part of the capacitation process whereby sperm prepare for the prospective penetration of the zona pellucida and fusion with the egg. Hyperactivation is often observed to initiate as sperm escape from epithelial and ciliary bindings formed within the isthmic regions of the female oviducts, leading to a conjecture in the literature that this waveform is mechanically important for sperm escape. Hence, we explore the mechanical effects of hyperactivation on a tethered sperm, focussing on a Newtonian fluid. Using a resistive force theory model we demonstrate that hyperactivation can indeed generate forces that pull the sperm away from a tethering point and consequently a hyperactivated sperm cell bound to an epithelial surface need not always be pushed by its flagellum. More generally, directions of the forces generated by tethered flagella are insensitive to reductions in beat frequency and the detailed flagellar responses depend on the nature of the binding at the tethering point. Furthermore, waveform asymmetry and amplitude increases enhance the tendency for a tethered flagellum to start tugging on its binding. The same is generally predicted to be true for reductions in the wavenumber of the flagellum beat, but not universally so, emphasising the dynamical complexity of flagellar force generation. Finally, qualitative observations drawn from experimental data of human sperm bound to excised female reproductive tract are also presented and are found to be consistent with the theoretical predictions. © 2012 Elsevier Ltd.
Citation:
Curtis MP, Kirkman-Brown JC, Connolly TJ, Gaffney EA (2012) Modelling a tethered mammalian sperm cell undergoing hyperactivation. Journal of Theoretical Biology 309: 1–10. Available: http://dx.doi.org/10.1016/j.jtbi.2012.05.035.
Publisher:
Elsevier BV
Journal:
Journal of Theoretical Biology
KAUST Grant Number:
KUK-C1-013-04
Issue Date:
Sep-2012
DOI:
10.1016/j.jtbi.2012.05.035
PubMed ID:
22727894
Type:
Article
ISSN:
0022-5193
Sponsors:
This publication is based on work supported by Award No. KUK-C1-013-04, made by King Abdullah University of Science and Technology (KAUST). We are also grateful to Dr. David Smith, University of Birmingham, for informative discussions.
Appears in Collections:
Publications Acknowledging KAUST Support

Full metadata record

DC FieldValue Language
dc.contributor.authorCurtis, M.P.en
dc.contributor.authorKirkman-Brown, J.C.en
dc.contributor.authorConnolly, T.J.en
dc.contributor.authorGaffney, E.A.en
dc.date.accessioned2016-02-25T13:42:40Zen
dc.date.available2016-02-25T13:42:40Zen
dc.date.issued2012-09en
dc.identifier.citationCurtis MP, Kirkman-Brown JC, Connolly TJ, Gaffney EA (2012) Modelling a tethered mammalian sperm cell undergoing hyperactivation. Journal of Theoretical Biology 309: 1–10. Available: http://dx.doi.org/10.1016/j.jtbi.2012.05.035.en
dc.identifier.issn0022-5193en
dc.identifier.pmid22727894en
dc.identifier.doi10.1016/j.jtbi.2012.05.035en
dc.identifier.urihttp://hdl.handle.net/10754/598864en
dc.description.abstractThe beat patterns of mammalian sperm flagella can be categorised into two different types. The first involves symmetric waves propagating down the flagellum with a net linear propulsion of the sperm cell. The second, hyperactive, waveform is classified by vigorous asymmetric waves of higher amplitude, lower wavenumber and frequency propagating down the flagellum resulting in highly curved trajectories. The latter beat pattern is part of the capacitation process whereby sperm prepare for the prospective penetration of the zona pellucida and fusion with the egg. Hyperactivation is often observed to initiate as sperm escape from epithelial and ciliary bindings formed within the isthmic regions of the female oviducts, leading to a conjecture in the literature that this waveform is mechanically important for sperm escape. Hence, we explore the mechanical effects of hyperactivation on a tethered sperm, focussing on a Newtonian fluid. Using a resistive force theory model we demonstrate that hyperactivation can indeed generate forces that pull the sperm away from a tethering point and consequently a hyperactivated sperm cell bound to an epithelial surface need not always be pushed by its flagellum. More generally, directions of the forces generated by tethered flagella are insensitive to reductions in beat frequency and the detailed flagellar responses depend on the nature of the binding at the tethering point. Furthermore, waveform asymmetry and amplitude increases enhance the tendency for a tethered flagellum to start tugging on its binding. The same is generally predicted to be true for reductions in the wavenumber of the flagellum beat, but not universally so, emphasising the dynamical complexity of flagellar force generation. Finally, qualitative observations drawn from experimental data of human sperm bound to excised female reproductive tract are also presented and are found to be consistent with the theoretical predictions. © 2012 Elsevier Ltd.en
dc.description.sponsorshipThis publication is based on work supported by Award No. KUK-C1-013-04, made by King Abdullah University of Science and Technology (KAUST). We are also grateful to Dr. David Smith, University of Birmingham, for informative discussions.en
dc.publisherElsevier BVen
dc.subjectBeat patternsen
dc.subjectCapacitationen
dc.subjectFlagellumen
dc.subjectResistive force theoryen
dc.subjectSperm bindingen
dc.titleModelling a tethered mammalian sperm cell undergoing hyperactivationen
dc.typeArticleen
dc.identifier.journalJournal of Theoretical Biologyen
dc.contributor.institutionUniversity of Oxford, Oxford, United Kingdomen
dc.contributor.institutionNHS Foundation Trust, Leeds, United Kingdomen
dc.contributor.institutionUniversity of Birmingham, Birmingham, United Kingdomen
kaust.grant.numberKUK-C1-013-04en

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