Cilia functions in development - PubMed (original) (raw)
Review
Cilia functions in development
Iain A Drummond. Curr Opin Cell Biol. 2012 Feb.
Abstract
Recent advances in developmental genetics and human disease gene cloning have highlighted the essential roles played by cilia in developmental cell fate decisions, left-right asymmetry, and the pathology of human congenital disorders. Hedgehog signaling in sensory cilia illustrates the importance of trafficking receptors to the cilia membrane (Patched and Smoothened) and the concept of cilia 'gatekeepers' that restrict entry and egress of cilia proteins (Suppressor of fused: Gli complexes). Cilia-driven fluid flow in the embryonic node highlights the role of motile cilia in both generation and detection of mechanical signals in development. In this brief review I select examples of recent studies that have clarified and consolidated our understanding of the role of cilia in development.
Copyright © 2012 Elsevier Ltd. All rights reserved.
Figures
Figure 1
Recent advances in cilia-mediated Hedgehog signaling. For a complete overview of Hh signaling see Ref. [11]. (a) Resting cell state with Hh signaling inhibited. The Hedgehog receptor Patched acts as a sterol efflux transporter on the cilia membrane, restricting the amount of Smoothened seven transmembrane protein present on the cilium (2). Protein kinase A activity prevents access of Sufu:Gli complexes (3) to the cilium. Cytoplasmic processing of Gli to the Gli repressor form (4) and transit to the nucleus maintains Hh target genes in a repressed state (5). (b) Activation of Hh signaling in cilia by Hh ligand binding. (1) Hedgehog ligand binds Patched (1), promoting removal from the membrane and blocking its sterol efflux function (2). Sterol bound Smoothened accumulates in the cilia membrane (3), abrogates PKA inhibition of Sufu:Gli complex entry into the cilium, allowing transport of Sufu:Gli complexes to the cilia tip (4). Cilia tip accumulation of Sufu:Gli promotes dissociation of full-length activator Gli proteins by undefined mechanisms (5), allowing Gli activator egress from the cilia (6), transit to the nucleus (7) and activation of Hh target genes.
Figure 2
The ciliary gate. The ciliary necklace and transition zone lie just above the basal body and play important roles in limiting diffusion of cilia membrane proteins and regulating cilia protein traffic. Septin expression in the ciliary necklace demarcates the apical cell membrane (blue) from the cilia membrane (red). Other protein complexes contribute to Y-link structures (Cep290) and to regulated trafficking or retention of cilia proteins (Importin β/ran and complexes of NPHP/MKS proteins). Boxed proteins represent biochemically defined complexes identified in the noted references.
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References
- Fisch C, Dupuis-Williams P. Ultrastructure of cilia and flagella — back to the future! Biol Cell. 2011;103:249–270. - PubMed
- Pazour GJ, Rosenbaum JL. Intraflagellar transport and ciliadependent diseases. Trends Cell Biol. 2002;12:551–555. - PubMed
- Bloodgood RA. Sensory reception is an attribute of both primary cilia and motile cilia. J Cell Sci. 2010;123:505–509. - PubMed
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