Multi-scale alignment of respiratory cilia and its relation to mucociliary function

Schneiter, Martin; Halm, Sebastian; Odriozola, Adolfo; Mogel, Helga; Rička, J.; Stoffel, Michael Hubert; Zuber, Benoît; Frenz, Martin; Tschanz, Stefan A.

doi:10.1016/j.jsb.2020.107680

Cited by 19 publications

(19 citation statements)

References 55 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The position of the basal foot (cyan dotted line) stained with ψ-tubulin was used as a reference point to align the centrioles. A diagram of the average pattern in transverse view is shown, in which the direction of ciliary beat (Schneiter et al, 2021) is represented by a dotted arrow and the basal foot axis by a green line. Triplets are numbered counterclockwise from the LRRCC1 signal.…”

Section: Resultsmentioning

confidence: 99%

“…In mouse MCCs, Lrrcc1 is associated to triplets located not exactly opposite to the basal foot but with a clockwise shift of at least 20° from the basal foot axis. However, the beating direction was shown to be also shifted approximately 20° clockwise relative to the position of the basal foot in bovine tracheal MCCs (Schneiter et al, 2021) (Fig. 2d).…”

Section: Discussionmentioning

confidence: 95%

See 1 more Smart Citation

Evolutionary conservation of centriole rotational asymmetry in the human centrosome

Gaudin

Gil

Boumendjel

et al. 2021

Preprint

View full text Add to dashboard Cite

Centrioles are formed by microtubule triplets in a nine-fold symmetric arrangement. In flagellated protists and in multiciliated cells, accessory structures tethered to specific triplets render the centrioles rotationally asymmetric, a property that is key to cytoskeletal and cellular organization in these contexts. In contrast, centrioles within the centrosome of animal cells display no conspicuous rotational asymmetry. Here, we uncover rotationally asymmetric molecular features in human centrioles. Using ultrastructure expansion microscopy, we show that LRRCC1, the ortholog of a protein originally characterized in flagellate green algae, associates preferentially to two consecutive triplets in the distal lumen of human centrioles. LRRCC1 partially co-localizes and affects the recruitment of another distal component, C2CD3, which also has an asymmetric localization pattern in the centriole lumen. Together, LRRCC1 and C2CD3 delineate a structure reminiscent of a filamentous density observed by electron microscopy in flagellates, termed the acorn. Functionally, the depletion of LRRCC1 in human cells induced defects in centriole structure, ciliary assembly and ciliary signaling, supporting that LRRCC1 cooperates with C2CD3 to organizing the distal region of centrioles. Since a mutation in the LRRCC1 gene has been identified in Joubert syndrome patients, this finding is relevant in the context of human ciliopathies. Taken together, our results demonstrate that rotational asymmetry is a conserved ancient property of centrioles. Our work also reveals that asymmetrically localized proteins are key for primary ciliogenesis and ciliary signaling in human cells.

show abstract

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 95%

Evolutionary conservation of centriole rotational asymmetry in the human centrosome

Gaudin

Gil

Boumendjel

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…This would explain, why our attempt to establish a generally valid model for the interrelationship of the metachronal wave properties and the mucociliary transport was not successful. Besides the rheological conditions (Norton et al 2011;Sedaghat et al 2016), the geometrical conditions, such as the ciliary spacing (Elgeti and Gompper 2013;Lee et al 2011), the ciliary orientation (Schneiter et al 2021), the proportion and the distribution of ciliated cells (Plopper et al 1983;Ramirez-San Juan et al 2020), but also the depth of the mucus and the periciliary layer (Lee et al 2011), are known to also determine mucociliary transport, which, in turn, is contemporary seen to interact and to co-emerge with those rheological and geometrical conditions during the morphogenesis of the system under study.…”

Section: Discussionmentioning

confidence: 99%

“… 2011 ), the ciliary orientation (Schneiter et al. 2021 ), the proportion and the distribution of ciliated cells (Plopper et al. 1983 ; Ramirez-San Juan et al.…”

Section: Discussionmentioning

confidence: 99%

A quantitative interspecies comparison of the respiratory mucociliary clearance mechanism

et al. 2022

Self Cite

View full text Add to dashboard Cite

Collectively coordinated ciliary activity propels the airway mucus, which lines the luminal surface of the vertebrate respiratory system, in cranial direction. Our contemporary understanding on how the quantitative characteristics of the metachronal wave field determines the resulting mucociliary transport is still limited, partly due to the sparse availability of quantitative observational data. We employed high-speed video reflection microscopy to image and quantitatively characterize the metachronal wave field as well as the mucociliary transport in excised bovine, porcine, ovine, lapine, turkey and ostrich samples. Image processing techniques were used to determine the ciliary beating frequency (CBF), the velocity and wavelength of the metachronal wave and the mucociliary transport velocity. The transport direction was found to strongly correlate with the mean wave propagation direction in all six species. The CBF yielded similar values (10–15 Hz) for all six species. Birds were found to exhibit higher transport speeds (130–260 $$\upmu$$ μ m/s) than mammals (20–80 $$\upmu$$ μ m/s). While the average transport direction significantly deviates from the tracheal long axis in mammals, no significant deviation was found in birds. The metachronal waves were found to propagate at about 4–8 times the speed of mucociliary transport in mammals, whereas in birds they propagate at about the transport speed. The mucociliary transport in birds is fast and roughly follows the TLA, whereas the transport is slower and proceeds along a left-handed spiral in mammals. The longer wavelengths and the lower ratio between the metachronal wave speed and the mucociliary transport speed provide evidence that the mucociliary clearance mechanism operates differently in birds than in mammals.

show abstract

“…This would explain, why our attempt to establish a generally valid model for the interrelationship of the metachronal wave properties and the mucociliary transport was not successful. Besides the rheological conditions [11,70], the geometrical conditions, such as the ciliary spacing [12,71], the ciliary orientation [72], the proportion and the distribution of ciliated cells [73,74], but also the depth of the mucus and the periciliary layer [71], are known to also determine mucociliary transport, which, in turn, is contemporary seen to interact and to coemerge with those rheological and geometrical conditions during the morphogenesis of the system under study.…”

Section: Discussionmentioning

confidence: 99%

A Quantitative Interspecies Comparison of The Respiratory Mucociliary Clearance Mechanism

Burn

Schneiter

Ryser

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Background: Collectively coordinated ciliary activity constantly propels the airway surface liquid, which lines the luminal surface of the vertebrate respiratory system, in cranial direction – constituting mucociliary clearance, the primary defence mechanism of our airways. Our contemporary understanding on how the quantitative characteristics of the metachronal wave field determines the resulting mucociliary transport is still limited, which is partly due to the sparse availability of quantitative observational data. Methods: We employed high-speed video reflection contrast microscopy to simultaneously image and quantitatively characterize the metachronal wave field as well as the mucociliary transport in excised bovine, porcine, ovine, lapine, turkey and ostrich samples of the luminal tracheal wall. Advanced image processing techniques were used to determine the ciliary beating frequency (CBF), the velocity and the wavelength of the metachronal wave as well as the mucociliary transport velocity. Results: The mucociliary transport direction was found to strongly correlate with the mean wave propagation direction in all six species. The CBF yielded similar values (10−15 Hz) for all six species. Birds were found to exhibit considerably higher transport speeds (130−260 μm/s) than mammals (20−80 μm/s). While the average transport direction significantly deviates from the tracheal long axis (TLA) in mammals, no significant deviation from the TLA was found in birds. In comparison to mammals, longer metachronal wavelengths were found in birds. Finally, the metachronal waves were found to propagate at about 4−8 times the speed of mucociliary transport in mammals, whereas the metachronal waves propagate at about the speed of mucociliary transport in birds. Conclusions: The tracheal mucociliary clearance mechanism is based on a symplectic metachronsim in all examined species. The mucociliary transport in birds is fast and roughly follows the TLA, whereas the transport is slower and proceeds along a left-handed spiral in mammals. The longer wavelengths and the lower ratio between the metachronal wave speed and the mucociliary transport speed provide further evidence that the mucociliary clearance mechanism operates differently in birds than in mammals.

show abstract

Multi-scale alignment of respiratory cilia and its relation to mucociliary function

Cited by 19 publications

References 55 publications

Evolutionary conservation of centriole rotational asymmetry in the human centrosome

Evolutionary conservation of centriole rotational asymmetry in the human centrosome

A quantitative interspecies comparison of the respiratory mucociliary clearance mechanism

A Quantitative Interspecies Comparison of The Respiratory Mucociliary Clearance Mechanism

Contact Info

Product

Resources

About