scholarly journals Planar polarization of cilia in the zebrafish floor-plate involves Par3-mediated posterior localization of highly motile basal bodies

2019 ◽  
Author(s):  
Antoine Donati ◽  
Sylvie Schneider-Maunoury ◽  
Christine Vesque
Keyword(s):  
Cell Polarity ◽  
Basal Body ◽  
Planar Cell Polarity ◽  
Floor Plate ◽  
Basal Bodies ◽  
Ciliated Epithelium ◽  
Ciliary Beating ◽  
Directional Flow ◽  
Pulling Forces ◽  
Planar Orientation

ABSTRACTTo produce a directional flow, ciliated epithelia display a uniform orientation of ciliary beating. Oriented beating requires planar cell polarity (PCP), which leads to planar orientation and asymmetric positioning of the ciliary basal body (BB) along the polarity axis. We took advantage of the polarized mono-ciliated epithelium of the embryonic zebrafish floor plate to investigate by live-imaging the dynamics and mechanisms of BB polarization. We showed that BBs, although bearing a cilium, were highly motile along the antero-posterior axis. BBs contacted both the anterior and the posterior membranes, with a bias towards posterior contacts from early somitogenesis on. Contacts exclusively occurred at junctional Par3 local enrichments or “patches” and were often preceded by transient membrane digitations extending towards the BB, suggesting focused cortical pulling forces. Accordingly, BBs and Par3 patches were linked by dynamic microtubules. We showed that Par3 became posteriorly enriched prior to BB posterior positioning and that floor plate polarization was impaired upon Par3 patches disruption triggered by Par3 or aPKC overexpression. In the PCP mutant Vangl2, where floor plate cells fail to polarize, we observed that BB were still motile but presented behavioral defects, such as ectopic contacts with lateral membranes that correlated with Par3 patch fragmentation and spreading to lateral membranes. Our data lead us to propose an unexpected function for posterior local Par3 enrichment in controlling BB asymmetric positioning downstream of the PCP pathway via a microtubule capture/shrinkage mechanism.

scholarly journals Planar polarization of cilia in the zebrafish floor-plate involves Par3-mediated posterior localization of highly motile basal bodies

Development ◽  
2021 ◽  
Author(s):  
Antoine Donati ◽  
Isabelle Anselme ◽  
Sylvie Schneider-Maunoury ◽  
Christine Vesque
Keyword(s):  
Cell Polarity ◽  
Planar Cell Polarity ◽  
Apical Cell ◽  
Lateral Spreading ◽  
Floor Plate ◽  
Basal Bodies ◽  
Ciliated Epithelium ◽  
Pulling Forces ◽  
Membrane Contacts ◽  
Apical Junctions

Epithelial cilia, whether motile or primary, often display an off-centered planar localization within the apical cell surface. This form of planar cell polarity (PCP) involves the asymmetric positioning of the ciliary basal body (BB). Using the mono-ciliated epithelium of the embryonic zebrafish floor-plate, we investigated the dynamics and mechanisms of BB polarization by live-imaging. BBs were highly motile, making back-and-forth movements along the antero-posterior axis and contacting both the anterior and posterior membranes. Contacts exclusively occurred at junctional Par3 patches and were often preceded by membrane digitations extending towards the BB, suggesting focused cortical pulling forces. Accordingly, BBs and Par3 patches were linked by dynamic microtubules. Later, BBs became less motile and eventually settled at posterior apical junctions enriched in Par3. BB posterior positioning followed Par3 posterior enrichment and was impaired upon Par3 depletion or disorganization of Par3 patches. In the PCP mutant Vangl2, BBs were still motile but displayed poorly-oriented membrane contacts that correlated with Par3 patch fragmentation and lateral spreading. We propose an unexpected function for posterior Par3 enrichment in controlling BB positioning downstream of the PCP pathway.

scholarly journals Celsr1 and CAMSAP3 differently regulate intercellular and intracellular cilia orientation in oviduct multiciliated cells

2020 ◽  
Author(s):  
Fumiko Matsukawa Usami ◽  
Masaki Arata ◽  
Dongbo Shi ◽  
Sanae Oka ◽  
Yoko Higuchi ◽  
...  
Keyword(s):  
Cell Polarity ◽  
Planar Cell Polarity ◽  
Molecular Mechanisms ◽  
The Other ◽  
Basal Bodies ◽  
Generating Functional ◽  
Tissue Polarity ◽  
Other Hand ◽  
Multiciliated Cells ◽  
Polarity Regulation

SummaryThe molecular mechanisms by which cilia orientation is coordinated within and between multiciliated cells (MCCs) is not fully understood. By observing the orientation of basal bodies (BB) in MCCs of mouse oviducts, here, we show that Celsr1, a planar cell polarity (PCP) factor involved in tissue polarity regulation, is dispensable for determining BB orientation in individual cells, whereas CAMSAP3, a microtubule minus-end regulator, is critical for this process but not for PCP. MCCs exhibit a characteristic BB orientation and microtubule gradient along the tissue axis, and these intracellular polarities were maintained in the cells lacking Celsr1, although the intercellular coordination of the polarities was partly disrupted. On the other hand, CAMSAP3 regulated the assembly of microtubules interconnecting BBs by localizing at the BBs, and its mutation led to disruption of intracellular coordination of BB orientation, but not affecting PCP factor localization. Thus, both Celsr1 and CAMSAP3 are responsible for BB orientation but in distinct ways; and therefore, their cooperation should be critical for generating functional multiciliated tissues.

scholarly journals Asymmetrically localized proteins stabilize basal bodies against ciliary beating forces

2016 ◽  
Vol 215 (4) ◽  
pp. 457-466 ◽  
Author(s):  
Brian A. Bayless ◽  
Domenico F. Galati ◽  
Anthony D. Junker ◽  
Chelsea B. Backer ◽  
Jacek Gaertig ◽  
...  
Keyword(s):  
Basal Body ◽  
Mechanical Force ◽  
Basal Bodies ◽  
Mechanical Forces ◽  
Ciliary Beating ◽  
Motile Cilia ◽  
Molecular Components

Basal bodies are radially symmetric, microtubule-rich structures that nucleate and anchor motile cilia. Ciliary beating produces asymmetric mechanical forces that are resisted by basal bodies. To resist these forces, distinct regions within the basal body ultrastructure and the microtubules themselves must be stable. However, the molecular components that stabilize basal bodies remain poorly defined. Here, we determine that Fop1 functionally interacts with the established basal body stability components Bld10 and Poc1. We find that Fop1 and microtubule glutamylation incorporate into basal bodies at distinct stages of assembly, culminating in their asymmetric enrichment at specific triplet microtubule regions that are predicted to experience the greatest mechanical force from ciliary beating. Both Fop1 and microtubule glutamylation are required to stabilize basal bodies against ciliary beating forces. Our studies reveal that microtubule glutamylation and Bld10, Poc1, and Fop1 stabilize basal bodies against the forces produced by ciliary beating via distinct yet interdependent mechanisms.

scholarly journals Planar Cell Polarity Defects and Hearing Loss in Sperm-Associated Antigen 6 (Spag6)-Deficient Mice

2020 ◽  
Author(s):  
Xiaofei Li ◽  
Daogong Zhang ◽  
Lei Xu ◽  
Yuechen Han ◽  
Wenwen Liu ◽  
...  
Keyword(s):  
Hearing Loss ◽  
Inner Ear ◽  
Cell Polarity ◽  
Planar Cell Polarity ◽  
Structural Features ◽  
Sensory Cells ◽  
Basal Bodies ◽  
Cellular Polarity ◽  
Central Apparatus ◽  
Deficient Mice

Spag6 encodes an axoneme central apparatus protein that is required for normal flagellar and cilia motility. Recent findings suggest that Spag6 also plays a role in ciliogenesis, orientation of cilia basal feet, and planar polarity. Sensory cells of the inner ear display unique structural features that underlie their mechanosensitivity. They represent a distinctive form of cellular polarity, known as planar cell polarity (PCP). However, a role for Spag6 in the inner ear has not yet been explored. In the present study, the function of Spag6 in the inner ear was examined using Spag6-deficient mice. Our results demonstrate hearing loss in the Spag6 mutants, associated with abnormalities in cellular patterning, cell shape, stereocilia bundles and basal bodies, as well as abnormally distributed Frizzled class receptor 6 (FZD6), suggesting that Spag6 participates in PCP regulation. Moreover, we found that the sub-apical microtubule meshwork was disrupted. Our observations suggest new functions for Spag6 in hearing and PCP in the inner ear.

Basal bodies, kinocilia and planar cell polarity

2008 ◽  
Vol 40 (1) ◽  
pp. 10-11 ◽  
Author(s):  
Jeffrey D Axelrod
Keyword(s):  
Cell Polarity ◽  
Planar Cell Polarity ◽  
Basal Bodies

scholarly journals Bld10/Cep135 stabilizes basal bodies to resist cilia-generated forces

2012 ◽  
Vol 23 (24) ◽  
pp. 4820-4832 ◽  
Author(s):  
Brian A. Bayless ◽  
Thomas H. Giddings ◽  
Mark Winey ◽  
Chad G. Pearson
Keyword(s):  
Basal Body ◽  
Structural Integrity ◽  
Basal Bodies ◽  
Ciliary Beating ◽  
Full Complement ◽  
Domain Protein ◽  
Motile Cilia ◽  
The Stability

Basal bodies nucleate, anchor, and organize cilia. As the anchor for motile cilia, basal bodies must be resistant to the forces directed toward the cell as a consequence of ciliary beating. The molecules and generalized mechanisms that contribute to the maintenance of basal bodies remain to be discovered. Bld10/Cep135 is a basal body outer cartwheel domain protein that has established roles in the assembly of nascent basal bodies. We find that Bld10 protein first incorporates stably at basal bodies early during new assembly. Bld10 protein continues to accumulate at basal bodies after assembly, and we hypothesize that the full complement of Bld10 is required to stabilize basal bodies. We identify a novel mechanism for Bld10/Cep135 in basal body maintenance so that basal bodies can withstand the forces produced by motile cilia. Bld10 stabilizes basal bodies by promoting the stability of the A- and C-tubules of the basal body triplet microtubules and by properly positioning the triplet microtubule blades. The forces generated by ciliary beating promote basal body disassembly in bld10Δ cells. Thus Bld10/Cep135 acts to maintain the structural integrity of basal bodies against the forces of ciliary beating in addition to its separable role in basal body assembly.

scholarly journals Sonic Hedgehog switches on Wnt/planar cell polarity signaling in commissural axon growth cones by reducing levels of Shisa2

eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Keisuke Onishi ◽  
Yimin Zou
Keyword(s):  
Cell Polarity ◽  
Sonic Hedgehog ◽  
Planar Cell Polarity ◽  
Axon Growth ◽  
Growth Cones ◽  
Floor Plate ◽  
Commissural Axon ◽  
Commissural Axons ◽  
Midline Crossing ◽  
Regulatory Link

Commissural axons switch on responsiveness to Wnt attraction during midline crossing and turn anteriorly only after exiting the floor plate. We report here that Sonic Hedgehog (Shh)-Smoothened signaling downregulates Shisa2, which inhibits the glycosylation and cell surface presentation of Frizzled3 in rodent commissural axon growth cones. Constitutive Shisa2 expression causes randomized turning of post-crossing commissural axons along the anterior–posterior (A–P) axis. Loss of Shisa2 led to precocious anterior turning of commissural axons before or during midline crossing. Post-crossing commissural axon turning is completely randomized along the A–P axis when Wntless, which is essential for Wnt secretion, is conditionally knocked out in the floor plate. This regulatory link between Shh and planar cell polarity (PCP) signaling may also occur in other developmental processes.

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