Cell type‐specific structural plasticity of the ciliary transition zone in C. elegans
Background information The current consensus on cilia development posits that the ciliary transition zone (TZ) is formed via extension of nine centrosomal microtubules. In this model, TZ structure remains unchanged in microtubule number throughout the cilium life cycle. This model does not however e...
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Published in | Biology of the cell Vol. 111; no. 4; pp. 95 - 107 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
01.04.2019
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Subjects | |
Online Access | Get full text |
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Summary: | Background information
The current consensus on cilia development posits that the ciliary transition zone (TZ) is formed via extension of nine centrosomal microtubules. In this model, TZ structure remains unchanged in microtubule number throughout the cilium life cycle. This model does not however explain structural variations of TZ structure seen in nature and could also lend itself to the misinterpretation that deviations from nine‐doublet microtubule ultrastructure represent an abnormal phenotype. Thus, a better understanding of events that occur at the TZ in vivo during metazoan development is required.
Results
To address this issue, we characterized ultrastructure of two types of sensory cilia in developing Caenorhabditis elegans. We discovered that, in cephalic male (CEM) and inner labial quadrant (IL2Q) sensory neurons, ciliary TZs are structurally plastic and remodel from one structure to another during animal development. The number of microtubule doublets forming the TZ can be increased or decreased over time, depending on cilia type. Both cases result in structural TZ intermediates different from TZ in cilia of adult animals. In CEM cilia, axonemal extension and maturation occurs concurrently with TZ structural maturation.
Conclusions and Significance
Our work extends the current model to include the structural plasticity of metazoan transition zone, which can be structurally delayed, maintained or remodelled in cell type‐specific manner.
Research article: Summary model of age‐ and cell‐specific TZ structural changes. Ninefold symmetry of the centriole templates ninefold TZ symmetry of sensory cilia in C. elegans larvae. A centriolar structure is depicted as described in Pelletier et al. (2006). ‘Amphid’ refers to amphid channel cilia whose early ciliogenesis steps are described by Nechipurenko et al. (2017) and Serwas et al. (2017). Inset shows models of axonemal microtubule structures seen in TZ of IL2 and CEM cilia during L2 larva to young adult temporal window. |
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Bibliography: | These authors contributed equally to this work. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Authors’ contributions: Conceptualization: J. S. A., M.S., and M. M. B.; Methodology, investigation, and analysis: J. S. A., M. S., N.S.M., K. Q. N., W. J. R, D. H. H., and M. M. B.; Manuscript draft writing: J. S. A., M. S.; Writing and editing of the submitted manuscript: N. S. M., M. M. B. These authors contributed equally to this work |
ISSN: | 0248-4900 1768-322X |
DOI: | 10.1111/boc.201800042 |