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Intracellular connections between basal bodies promote the coordinated behavior of motile cilia

Adam W. J. Soh, Louis G. Woodhams, Anthony D. Junker, Cassidy M. Enloe, Benjamin E. Noren, Adam Harned, Christopher J. Westlake, Kedar Narayan, John S. Oakey, Philip V. Bayly, View ORCID ProfileChad G. Pearson
doi: https://doi.org/10.1101/2022.05.06.490816
Adam W. J. Soh
1Anschutz Medical Campus, Department of Cell and Developmental Biology, University of Colorado, Aurora, CO 80045
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Louis G. Woodhams
2Department of Mechanical Engineering and Material Science, Washington University in St. Louis, St. Louis, MO 63130
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Anthony D. Junker
1Anschutz Medical Campus, Department of Cell and Developmental Biology, University of Colorado, Aurora, CO 80045
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Cassidy M. Enloe
3College of Engineering and Applied Science, Department of Chemical Engineering, University of Wyoming, Laramie, WY 82071
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Benjamin E. Noren
3College of Engineering and Applied Science, Department of Chemical Engineering, University of Wyoming, Laramie, WY 82071
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Adam Harned
5Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda 20892, Maryland, USA
6Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick 21702, Maryland, USA
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Christopher J. Westlake
4Laboratory of Cell and Developmental Signaling, Center for Cancer Research, National Cancer institute, National Institutes of Health, Frederick, MD 21702
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Kedar Narayan
5Center for Molecular Microscopy, Center for Cancer Research, National Cancer Institute, National Institutes of Health, Bethesda 20892, Maryland, USA
6Cancer Research Technology Program, Frederick National Laboratory for Cancer Research, Frederick 21702, Maryland, USA
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John S. Oakey
3College of Engineering and Applied Science, Department of Chemical Engineering, University of Wyoming, Laramie, WY 82071
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Philip V. Bayly
2Department of Mechanical Engineering and Material Science, Washington University in St. Louis, St. Louis, MO 63130
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Chad G. Pearson
1Anschutz Medical Campus, Department of Cell and Developmental Biology, University of Colorado, Aurora, CO 80045
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  • ORCID record for Chad G. Pearson
  • For correspondence: Chad.Pearson@cuanschutz.edu
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Summary

Hydrodynamic flow produced by multi-ciliated cells is critical for fluid circulation and cell motility. Hundreds of cilia beat with metachronal synchrony for fluid flow. Cilia-driven fluid flow produces extracellular hydrodynamic forces that cause neighboring cilia to beat in a synchronized manner. However, hydrodynamic coupling between neighboring cilia is not the sole mechanism that drives cilia synchrony. Cilia are nucleated by basal bodies (BBs) that link to each other and to the cell’s cortex via BB-associated appendages. The intracellular BB and cortical network is hypothesized to synchronize ciliary beating by transmitting cilia coordination cues. The extent of intracellular ciliary connections and the nature of these stimuli remain unclear. Moreover, how BB connections influence the dynamics of individual cilia has not been established. We show by FIB-SEM imaging that cilia are coupled both longitudinally and laterally in the ciliate Tetrahymena thermophila by the underlying BB and cortical cytoskeletal network. To visualize the behavior of individual cilia in live, immobilized Tetrahymena cells, we developed Delivered Iron Particle Ubiety Live Light-(DIPULL) microscopy. Quantitative and computer analyses of ciliary dynamics reveal that BB connections control ciliary waveform and coordinate ciliary beating. Loss of BB connections reduces cilia-dependent fluid flow forces.

Summary Soh et al investigate whether intracellular connections between basal bodies control ciliary behavior in multi-ciliated cells. Using a Tetrahymena live cell immobilization technique to quantify ciliary dynamics, they show that inter-BB connections are required for effective ciliary waveform and coordinated ciliary beating that promotes fluid flow.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Abbreviations: polydimethylsiloxane, PDMS. basal body, BB. striated fiber, SF. focused ion beam scanning electron microscopy, FIB-SEM. multi-ciliary array, MCA. resistive force theory, RFT

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted May 06, 2022.
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Intracellular connections between basal bodies promote the coordinated behavior of motile cilia
Adam W. J. Soh, Louis G. Woodhams, Anthony D. Junker, Cassidy M. Enloe, Benjamin E. Noren, Adam Harned, Christopher J. Westlake, Kedar Narayan, John S. Oakey, Philip V. Bayly, Chad G. Pearson
bioRxiv 2022.05.06.490816; doi: https://doi.org/10.1101/2022.05.06.490816
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Intracellular connections between basal bodies promote the coordinated behavior of motile cilia
Adam W. J. Soh, Louis G. Woodhams, Anthony D. Junker, Cassidy M. Enloe, Benjamin E. Noren, Adam Harned, Christopher J. Westlake, Kedar Narayan, John S. Oakey, Philip V. Bayly, Chad G. Pearson
bioRxiv 2022.05.06.490816; doi: https://doi.org/10.1101/2022.05.06.490816

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