Actin and microtubules drive differential aspects of planar cell polarity in multiciliated cells

Werner, Michael; Hwang, Peter K.; Huisman, F. M.; Taborek, P.; Yu, Clare C.; Mitchell, Brian J.

doi:10.1083/jcb.201106110

Cited by 176 publications

(297 citation statements)

References 36 publications

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“…Finally, we note that, although the cilium's internal structure of microtubules and dynein motors has been highly conserved throughout evolution and across cilia from various cell types, other structural and physiological constraints at the cell surface could influence the beating kinematics, especially in light of recent reports suggesting that spatiotemporal coordination of ciliary beating strongly dependent on cytoskeletal connections between neighboring cilia 49,50 .…”

Section: Discussionmentioning

confidence: 99%

Cilia beating patterns are not hydrodynamically optimal

Guo¹,

Nawroth²,

Ding³

et al. 2014

Physics of Fluids

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We examine the hydrodynamic performance of two cilia beating patterns reconstructed from experimental data. In their respective natural systems, the two beating patterns correspond to: (A) pumping-specialized cilia, and (B) swimming-specialized cilia. We compare the performance of these two cilia beating patterns as a function of the metachronal coordination in the context of two model systems: the swimming of a ciliated cylinder and the fluid pumping by a ciliated carpet. Three performance measures are used for this comparison: (i) average swimming speed/pumping flow rate; (ii) maximum internal moments generated by the cilia; and (iii) swimming/pumping efficiencies. We found that, in both models, pattern (B) outperforms pattern (A) in almost all three measures, including hydrodynamic efficiency. These results challenge the notion that hydrodynamic efficiency dictates the cilia beating kinematics, and suggest that other biological functions and constraints play a role in explaining the wide variety of cilia beating patterns observed in biological systems.Comment: 15 pages, 8 figure

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Section: Discussionmentioning

confidence: 99%

Cilia beating patterns are not hydrodynamically optimal

Guo¹,

Nawroth²,

Ding³

et al. 2014

Physics of Fluids

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“…Because a well-organized actin cytoskeleton is required for the migration and docking of the basal bodies to the apical plasma membrane, and for cilia elongation (Boisvieux-Ulrich et al, 1990;Pan et al, 2007;Ravanelli and Klingensmith, 2011;Tamm and Tamm, 1988), a sept7b-dependent disruption of actin organization could contribute to the defects in ciliogenesis. Alternatively, the reduced number of basal bodies upon sept7b knockdown could also lead to reduced cortical actin, as a dense apical actin cap has been shown to form around basal bodies after their apical docking (Pan et al, 2007;Werner et al, 2011). In addition, a sub-apical actin network connects neighboring cilia to coordinate the synchronized beating of cilia (Werner et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Sept7bis essential for pronephric function and development of left-right asymmetry in zebrafish embryogenesis

Dash

Lehtonen

Wasik

et al. 2014

Journal of Cell Science

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The conserved septin family of filamentous small GTPases plays important roles in mitosis, cell migration and cell morphogenesis by forming scaffolds and diffusion barriers. Recent studies in cultured cells in vitro indicate that a septin complex of septin 2, 7 and 9 is required for ciliogenesis and cilia function, but septin function in ciliogenesis in vertebrate organs in vivo is not understood. We show that sept7b is expressed in ciliated cells in different tissues during early zebrafish development. Knockdown of sept7b by using morpholino antisense oligonucleotides caused misorientation of basal bodies and cilia, reduction of apical actin and the shortening of motile cilia in Kupffer's vesicle and pronephric tubules. This resulted in pericardial and yolk sac edema, body axis curvature and hydrocephaly. Notably, in sept7b morphants we detected strong leftright asymmetry defects in the heart and lateral plate mesoderm (situs inversus), reduced fluid flow in the kidney, the formation of kidney cysts and loss of glomerular filtration barrier function. Thus, sept7b is essential during zebrafish development for pronephric function and ciliogenesis, and loss of expression of sept7b results in defects that resemble human ciliopathies.

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“…Subdistal appendages are structurally similar to the basal foot that decorates centrioles in sponge choanocytes and in multiciliated cells from a variety of animal species, and indeed their assembly relies on at least one common component [101,105,106]. Like subdistal appendages, the basal foot anchors microtubules required for controlling the position of the centrioles within the plane of the membrane, which in turn determines ciliary beating orientation [105,107,108]. Unlike subdistal appendages, basal feet are observed in all basal metazoan lineages, suggesting that it is an ancestral trait associated with planar ciliary beating [109][110][111][112].…”

Section: (Iv) Evolution Of Centrosome Structure In Animalsmentioning

confidence: 99%

Exploring the evolutionary history of centrosomes

Azimzadeh

2014

Phil. Trans. R. Soc. B

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The centrosome is the main organizer of the microtubule cytoskeleton in animals, higher fungi and several other eukaryotic lineages. Centrosomes are usually located at the centre of cell in tight association with the nuclear envelope and duplicate at each cell cycle. Despite a great structural diversity between the different types of centrosomes, they are functionally equivalent and share at least some of their molecular components. In this paper, we explore the evolutionary origin of the different centrosomes, in an attempt to understand whether they are derived from an ancestral centrosome or evolved independently from the motile apparatus of distinct flagellated ancestors. We then discuss the evolution of centrosome structure and function within the animal lineage.

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Actin and microtubules drive differential aspects of planar cell polarity in multiciliated cells

Abstract: Actin dynamics are required for proper cilia spacing, global coordination of cilia polarity, and coordination of metachronic cilia beating, whereas cytoplasmic microtubule dynamics are required for local coordination of polarity between neighboring cilia.

Cited by 176 publications

References 36 publications

Cilia beating patterns are not hydrodynamically optimal

Cilia beating patterns are not hydrodynamically optimal

Sept7bis essential for pronephric function and development of left-right asymmetry in zebrafish embryogenesis

Exploring the evolutionary history of centrosomes

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