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Actin and Microtubules Drive Differential Aspects of Planar Cell Polarity in Multiciliated Cells

Overview
Journal J Cell Biol
Specialty Cell Biology
Date 2011 Sep 28
PMID 21949415
Citations 109
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Abstract

Planar cell polarization represents the ability of cells to orient within the plane of a tissue orthogonal to the apical basal axis. The proper polarized function of multiciliated cells requires the coordination of cilia spacing and cilia polarity as well as the timing of cilia beating during metachronal synchrony. The planar cell polarity pathway and hydrodynamic forces have been shown to instruct cilia polarity. In this paper, we show how intracellular effectors interpret polarity to organize cellular morphology in accordance with asymmetric cellular function. We observe that both cellular actin and microtubule networks undergo drastic reorganization, providing differential roles during the polarized organization of cilia. Using computational angular correlation analysis of cilia orientation, we report a graded cellular organization downstream of cell polarity cues. 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.

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References
1.
Chailley B, Nicolas G, Laine M . Organization of actin microfilaments in the apical border of oviduct ciliated cells. Biol Cell. 1989; 67(1):81-90. DOI: 10.1111/j.1768-322x.1989.tb03012.x. View

2.
Ravanelli A, Klingensmith J . The actin nucleator Cordon-bleu is required for development of motile cilia in zebrafish. Dev Biol. 2010; 350(1):101-11. PMC: 3022090. DOI: 10.1016/j.ydbio.2010.11.023. View

3.
Sandoz D, Chailley B, Boisvieux-Ulrich E, Lemullois M, Laine M, Bautista-Harris G . Organization and functions of cytoskeleton in metazoan ciliated cells. Biol Cell. 1988; 63(2):183-93. DOI: 10.1016/0248-4900(88)90057-3. View

4.
Gottlieb T, Ivanov I, Adesnik M, Sabatini D . Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol. 1993; 120(3):695-710. PMC: 2119548. DOI: 10.1083/jcb.120.3.695. View

5.
Guirao B, Joanny J . Spontaneous creation of macroscopic flow and metachronal waves in an array of cilia. Biophys J. 2006; 92(6):1900-17. PMC: 1861806. DOI: 10.1529/biophysj.106.084897. View