Abstract
The role of the primary cilium in key signaling pathways depends on dynamic regulation of ciliary membrane protein composition, yet we know little about the motors or membrane events that regulate ciliary membrane protein trafficking in existing organelles. Recently, we showed that cilium-generated signaling in Chlamydomonas induced rapid, anterograde IFT-independent, cytoplasmic microtubule-dependent redistribution of the membrane polypeptide, SAG1-C65, from the plasma membrane to the periciliary region and the ciliary membrane. Here, we report that the retrograde IFT motor, cytoplasmic dynein 1b, is required in the cytoplasm for this rapid redistribution. Furthermore, signaling-induced trafficking of SAG1-C65 into cilia is unidirectional and the entire complement of cellular SAG1-C65 is shed during signaling and can be recovered in the form of ciliary ectosomes that retain signal-inducing activity. Thus, during signaling, cells regulate ciliary membrane protein composition through cytoplasmic action of the retrograde IFT motor and shedding of ciliary ectosomes.
Highlights
The primary cilium provides a unique cellular compartment for interaction with the extracellular milieu
The signaling functions of the ciliary membrane are crucial for development and homeostasis, we are just beginning to learn the cellular and molecular mechanisms that underlie the dynamic regulation of ciliary membrane protein composition in existing cilia during cilium-generated signaling (Pazour and Bloodgood, 2008; Nachury et al, 2010; Hu and Nelson, 2011; Malicki and Avidor-Reiss, 2014)
The retrograde intraflagellar transport (IFT) motor is required for apical polarization and ciliary enrichment of SAG1-C65 during cilium-generated signaling
Summary
The primary cilium provides a unique cellular compartment for interaction with the extracellular milieu. Initiated by discoveries in chemosensation in Caenorhabditis elegans, of ciliary defects in polycystic kidney disease, and of the central role of cilia in the vertebrate hedgehog (Hh) signaling pathway, we know that the organelle is a signaling node for multiple pathways in development, disease, and homeostasis (reviewed in Gerdes et al, 2009; Lancaster and Gleeson, 2009; Goetz and Anderson, 2010). The signaling functions of the ciliary membrane are crucial for development and homeostasis, we are just beginning to learn the cellular and molecular mechanisms that underlie the dynamic regulation of ciliary membrane protein composition in existing cilia during cilium-generated signaling (Pazour and Bloodgood, 2008; Nachury et al, 2010; Hu and Nelson, 2011; Malicki and Avidor-Reiss, 2014). Soluble proteins are delivered into the organelle by intraflagellar transport (IFT) (Pedersen and Rosenbaum, 2008).
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