Literature DB >> 30890052

Flagellar ultrastructure suppresses buckling instabilities and enables mammalian sperm navigation in high-viscosity media.

Hermes Gadêlha1,2, Eamonn A Gaffney2.   

Abstract

Eukaryotic flagellar swimming is driven by a slender motile unit, the axoneme, which possesses an internal structure that is essentially conserved in a tremendous diversity of sperm. Mammalian sperm, however, which are internal fertilizers, also exhibit distinctive accessory structures that further dress the axoneme and alter its mechanical response. This raises the following two fundamental questions. What is the functional significance of these structures? How do they affect the flagellar waveform and ultimately cell swimming? Hence we build on previous work to develop a mathematical mechanical model of a virtual human sperm to examine the impact of mammalian sperm accessory structures on flagellar dynamics and motility. Our findings demonstrate that the accessory structures reinforce the flagellum, preventing waveform compression and symmetry-breaking buckling instabilities when the viscosity of the surrounding medium is increased. This is in agreement with previous observations of internal and external fertilizers, such as human and sea urchin spermatozoa. In turn, possession of accessory structures entails that the progressive motion during a flagellar beat cycle can be enhanced as viscosity is increased within physiological bounds. Hence the flagella of internal fertilizers, complete with accessory structures, are predicted to be advantageous in viscous physiological media compared with watery media for the fundamental role of delivering a genetic payload to the egg.

Entities:  

Keywords:  bending wave modulation; buckling instability; elastohydrodynamics; flagella; high viscosity; spermatozoa

Mesh:

Year:  2019        PMID: 30890052      PMCID: PMC6451407          DOI: 10.1098/rsif.2018.0668

Source DB:  PubMed          Journal:  J R Soc Interface        ISSN: 1742-5662            Impact factor:   4.118


  54 in total

1.  Nonlinear instability in flagellar dynamics: a novel modulation mechanism in sperm migration?

Authors:  H Gadêlha; E A Gaffney; D J Smith; J C Kirkman-Brown
Journal:  J R Soc Interface       Date:  2010-05-12       Impact factor: 4.118

2.  Beating patterns of filaments in viscoelastic fluids.

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Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2008-10-21

Review 3.  Sperm motility: is viscosity fundamental to progress?

Authors:  Jackson C Kirkman-Brown; David J Smith
Journal:  Mol Hum Reprod       Date:  2011-06-08       Impact factor: 4.025

4.  Functional significance of the outer dense fibers of mammalian sperm examined by computer simulations with the geometric clutch model.

Authors:  C B Lindemann
Journal:  Cell Motil Cytoskeleton       Date:  1996

5.  The counterbend dynamics of cross-linked filament bundles and flagella.

Authors:  Rachel Coy; Hermes Gadêlha
Journal:  J R Soc Interface       Date:  2017-05       Impact factor: 4.118

6.  Spontaneous oscillations of elastic filaments induced by molecular motors.

Authors:  Gabriele De Canio; Eric Lauga; Raymond E Goldstein
Journal:  J R Soc Interface       Date:  2017-11       Impact factor: 4.118

7.  Elastohydrodynamic Synchronization of Adjacent Beating Flagella.

Authors:  Raymond E Goldstein; Eric Lauga; Adriana I Pesci; Michael R E Proctor
Journal:  Phys Rev Fluids       Date:  2016-11-01       Impact factor: 2.537

8.  Human sperm swimming in a high viscosity mucus analogue.

Authors:  Kenta Ishimoto; Hermes Gadêlha; Eamonn A Gaffney; David J Smith; Jackson Kirkman-Brown
Journal:  J Theor Biol       Date:  2018-02-17       Impact factor: 2.691

9.  Coarse-Graining the Fluid Flow around a Human Sperm.

Authors:  Kenta Ishimoto; Hermes Gadêlha; Eamonn A Gaffney; David J Smith; Jackson Kirkman-Brown
Journal:  Phys Rev Lett       Date:  2017-03-23       Impact factor: 9.161

10.  From flagellar undulations to collective motion: predicting the dynamics of sperm suspensions.

Authors:  Simon F Schoeller; Eric E Keaveny
Journal:  J R Soc Interface       Date:  2018-03       Impact factor: 4.118

View more
  6 in total

Review 1.  Collective dynamics of sperm cells.

Authors:  Simon F Schoeller; William V Holt; Eric E Keaveny
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2020-07-27       Impact factor: 6.237

2.  Flagellar kinematics reveals the role of environment in shaping sperm motility.

Authors:  Jeffrey S Guasto; Jonathan B Estrada; Filippo Menolascina; Lisa J Burton; Mohak Patel; Christian Franck; A E Hosoi; Richard K Zimmer; Roman Stocker
Journal:  J R Soc Interface       Date:  2020-09-09       Impact factor: 4.118

3.  Curvature in the reproductive tract alters sperm-surface interactions.

Authors:  Mohammad Reza Raveshi; Melati S Abdul Halim; Sagar N Agnihotri; Moira K O'Bryan; Adrian Neild; Reza Nosrati
Journal:  Nat Commun       Date:  2021-06-08       Impact factor: 14.919

4.  Human sperm uses asymmetric and anisotropic flagellar controls to regulate swimming symmetry and cell steering.

Authors:  Hermes Gadêlha; Paul Hernández-Herrera; Fernando Montoya; Alberto Darszon; Gabriel Corkidi
Journal:  Sci Adv       Date:  2020-07-31       Impact factor: 14.136

5.  The steering gaits of sperm.

Authors:  A Gong; S Rode; U B Kaupp; G Gompper; J Elgeti; B M Friedrich; L Alvarez
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2019-12-30       Impact factor: 6.237

6.  The multi-scale architecture of mammalian sperm flagella and implications for ciliary motility.

Authors:  Miguel Ricardo Leung; Marc C Roelofs; Ravi Teja Ravi; Paula Maitan; Heiko Henning; Min Zhang; Elizabeth G Bromfield; Stuart C Howes; Bart M Gadella; Hermes Bloomfield-Gadêlha; Tzviya Zeev-Ben-Mordehai
Journal:  EMBO J       Date:  2021-03-10       Impact factor: 11.598

  6 in total

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