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Multi-scale spatial heterogeneity enhances particle clearance in airway ciliary arrays

View ORCID ProfileGuillermina R. Ramirez-San Juan, View ORCID ProfileArnold J. T. M. Mathijssen, Mu He, View ORCID ProfileLily Jan, Wallace Marshall, View ORCID ProfileManu Prakash
doi: https://doi.org/10.1101/665125
Guillermina R. Ramirez-San Juan
1Department of Biophysics and Biochemistry, University of California, San Francisco, CA 94158
2Department of Bioengineering, Stanford University, Stanford, CA 94305
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  • ORCID record for Guillermina R. Ramirez-San Juan
Arnold J. T. M. Mathijssen
2Department of Bioengineering, Stanford University, Stanford, CA 94305
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  • ORCID record for Arnold J. T. M. Mathijssen
Mu He
3Department of Physiology, University of California, San Francisco, CA 94158
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Lily Jan
1Department of Biophysics and Biochemistry, University of California, San Francisco, CA 94158
3Department of Physiology, University of California, San Francisco, CA 94158
4Howard Hughes Medical Institute, University of California, San Francisco, CA 94158
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Wallace Marshall
1Department of Biophysics and Biochemistry, University of California, San Francisco, CA 94158
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Manu Prakash
2Department of Bioengineering, Stanford University, Stanford, CA 94305
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  • For correspondence: manup@stanford.edu
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Abstract

Mucus clearance constitutes the primary defence of the respiratory system against viruses, bacteria and environmental insults [1]. This transport across the entire airway emerges from the integrated activity of thousands of multiciliated cells, each containing hundreds of cilia, which together must coordinate their spatial arrangement, alignment and motility [2, 3]. The mechanisms of fluid transport have been studied extensively at the level of an individual cilium [4, 5], collectively moving metachronal waves [6–10], and more generally the hydrodynamics of active matter [11, 12]. However, the connection between local cilia architecture and the topology of the flows they generate remains largely unexplored. Here, we image the mouse airway from the sub-cellular (nm) to the organ scales (mm), characterising quantitatively its ciliary arrangement and the generated flows. Locally we measure heterogeneity in both cilia organisation and flow structure, but across the trachea fluid transport is coherent. To examine this result, a hydrodynamic model was developed for a systematic exploration of different tissue architectures. Surprisingly, we find that disorder enhances particle clearance, whether it originates from fluctuations, heterogeneity in multiciliated cell arrangement or ciliary misalignment. This resembles elements of ‘stochastic resonance’ [13–15] in a self-assembled biological system. Taken together, our results shed light on how the microstructure of an active carpet [16, 17] determines its emergent dynamics. Furthermore, this work is also directly applicable to human airway pathologies [1], which are the third leading cause of deaths worldwide [18].

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Posted June 09, 2019.
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Multi-scale spatial heterogeneity enhances particle clearance in airway ciliary arrays
Guillermina R. Ramirez-San Juan, Arnold J. T. M. Mathijssen, Mu He, Lily Jan, Wallace Marshall, Manu Prakash
bioRxiv 665125; doi: https://doi.org/10.1101/665125
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Multi-scale spatial heterogeneity enhances particle clearance in airway ciliary arrays
Guillermina R. Ramirez-San Juan, Arnold J. T. M. Mathijssen, Mu He, Lily Jan, Wallace Marshall, Manu Prakash
bioRxiv 665125; doi: https://doi.org/10.1101/665125

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