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Dynamics of cilia length in left – right development

View Article: PubMed Central - PubMed

ABSTRACT

Reduction in the length of motile cilia in the zebrafish left–right organizer (LRO), also known as Kupffer's vesicle, has a large impact on left–right development. Here we demonstrate through genetic overexpression in zebrafish embryos and mathematical modelling that the impact of increased motile cilia length in embryonic LRO fluid flow is milder than that of short cilia. Through Arl13b overexpression, which increases cilia length without impacting cilia beat frequency, we show that the increase in cilium length is associated with a decrease in beat amplitude, resulting in similar flow strengths for Arl13b overexpression and wild-type (WT) embryos, which were not predicted by current theory. Longer cilia exhibit pronounced helical beat patterns and, consequently, lower beat amplitudes relative to WT, a result of an elastohydrodynamic shape transition. For long helical cilia, fluid dynamics modelling predicts a mild (approx. 12%) reduction in the torque exerted on the fluid relative to the WT, resulting in a proportional reduction in flow generation. This mild reduction is corroborated by experiments, providing a mechanism for the mild impact on organ situs.

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Elastic shape transitions in KV cilia as length increases. (a) Cilium beat diameter as a function of the length of the beat envelope as viewed from the side. The plot shows three distinct regions (I) cilia act as straight rods whirling in a conical beat, (II) beat helicity onsets, trailing the cilium tip through the fluid and (III) cilia in fully developed helical beat patterns. (b) Short cilia (I), exert a pure torque upon the fluid. As helicity onsets (II), a small force perpendicular to the beat plane is exerted. For fully developed helical beating (III), this force is larger. (c) Representative beat patterns used for the fluid mechanics study of WT (left) versus injected (right) embryos (n = 30 cilia used for arl13b-injected measurements and for WT). Source data in http://dx.doi.org/10.5061/dryad.m541q [30].
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RSOS161102F3: Elastic shape transitions in KV cilia as length increases. (a) Cilium beat diameter as a function of the length of the beat envelope as viewed from the side. The plot shows three distinct regions (I) cilia act as straight rods whirling in a conical beat, (II) beat helicity onsets, trailing the cilium tip through the fluid and (III) cilia in fully developed helical beat patterns. (b) Short cilia (I), exert a pure torque upon the fluid. As helicity onsets (II), a small force perpendicular to the beat plane is exerted. For fully developed helical beating (III), this force is larger. (c) Representative beat patterns used for the fluid mechanics study of WT (left) versus injected (right) embryos (n = 30 cilia used for arl13b-injected measurements and for WT). Source data in http://dx.doi.org/10.5061/dryad.m541q [30].

Mentions: Thus, we see that it is possible to have the same flow strength with longer cilia provided the beat amplitude is decreased. As such, we measured the beat envelope diameter (twice the amplitude) of cilia in WT and arl13b-injected embryos, as well as for the short cilia mutant deltaD−/−, and plotted them as a function of cilium length (figure 3a). This plot revealed three distinct regions: (I) beat amplitude initially increases linearly as a function of length, (II) beat amplitude then decreases as a function of envelope length until (III) beat amplitude remains approximately constant as a function of envelope length. Note that in regions (II) and (III), the true length of the cilium is greater than the envelope length, indicating that these cilia are likely curled up in a helical pattern.Figure 3.


Dynamics of cilia length in left – right development
Elastic shape transitions in KV cilia as length increases. (a) Cilium beat diameter as a function of the length of the beat envelope as viewed from the side. The plot shows three distinct regions (I) cilia act as straight rods whirling in a conical beat, (II) beat helicity onsets, trailing the cilium tip through the fluid and (III) cilia in fully developed helical beat patterns. (b) Short cilia (I), exert a pure torque upon the fluid. As helicity onsets (II), a small force perpendicular to the beat plane is exerted. For fully developed helical beating (III), this force is larger. (c) Representative beat patterns used for the fluid mechanics study of WT (left) versus injected (right) embryos (n = 30 cilia used for arl13b-injected measurements and for WT). Source data in http://dx.doi.org/10.5061/dryad.m541q [30].
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5383854&req=5

RSOS161102F3: Elastic shape transitions in KV cilia as length increases. (a) Cilium beat diameter as a function of the length of the beat envelope as viewed from the side. The plot shows three distinct regions (I) cilia act as straight rods whirling in a conical beat, (II) beat helicity onsets, trailing the cilium tip through the fluid and (III) cilia in fully developed helical beat patterns. (b) Short cilia (I), exert a pure torque upon the fluid. As helicity onsets (II), a small force perpendicular to the beat plane is exerted. For fully developed helical beating (III), this force is larger. (c) Representative beat patterns used for the fluid mechanics study of WT (left) versus injected (right) embryos (n = 30 cilia used for arl13b-injected measurements and for WT). Source data in http://dx.doi.org/10.5061/dryad.m541q [30].
Mentions: Thus, we see that it is possible to have the same flow strength with longer cilia provided the beat amplitude is decreased. As such, we measured the beat envelope diameter (twice the amplitude) of cilia in WT and arl13b-injected embryos, as well as for the short cilia mutant deltaD−/−, and plotted them as a function of cilium length (figure 3a). This plot revealed three distinct regions: (I) beat amplitude initially increases linearly as a function of length, (II) beat amplitude then decreases as a function of envelope length until (III) beat amplitude remains approximately constant as a function of envelope length. Note that in regions (II) and (III), the true length of the cilium is greater than the envelope length, indicating that these cilia are likely curled up in a helical pattern.Figure 3.

View Article: PubMed Central - PubMed

ABSTRACT

Reduction in the length of motile cilia in the zebrafish left–right organizer (LRO), also known as Kupffer's vesicle, has a large impact on left–right development. Here we demonstrate through genetic overexpression in zebrafish embryos and mathematical modelling that the impact of increased motile cilia length in embryonic LRO fluid flow is milder than that of short cilia. Through Arl13b overexpression, which increases cilia length without impacting cilia beat frequency, we show that the increase in cilium length is associated with a decrease in beat amplitude, resulting in similar flow strengths for Arl13b overexpression and wild-type (WT) embryos, which were not predicted by current theory. Longer cilia exhibit pronounced helical beat patterns and, consequently, lower beat amplitudes relative to WT, a result of an elastohydrodynamic shape transition. For long helical cilia, fluid dynamics modelling predicts a mild (approx. 12%) reduction in the torque exerted on the fluid relative to the WT, resulting in a proportional reduction in flow generation. This mild reduction is corroborated by experiments, providing a mechanism for the mild impact on organ situs.

No MeSH data available.


Related in: MedlinePlus