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Compartmentalized Calcium Signaling in Cilia Regulates Intraflagellar Transport

Compartmentalized Calcium Signaling in Cilia Regulates Intraflagellar Transport
Compartmentalized Calcium Signaling in Cilia Regulates Intraflagellar Transport
Intraflagellar transport (IFT) underpins many of the important cellular roles of cilia and flagella in signaling and motility [1,2,3,4]. The microtubule motors kinesin-2 and cytoplasmic dynein 1b drive IFT particles (protein complexes carrying ciliary component proteins) along the axoneme to facilitate the assembly and maintenance of cilia. IFT is regulated primarily by cargo loading onto the IFT particles, although evidence suggests that IFT particles also exhibit differential rates of movement [5,6,7]. Here we demonstrate that intraflagellar Ca2+ elevations act to directly regulate the movement of IFT particles. IFT-driven movement of adherent flagella membrane glycoproteins in the model alga Chlamydomonas enables flagella-mediated gliding motility [8,9,10]. We find that surface contact promotes the localized accumulation of IFT particles in Chlamydomonas flagella. Highly compartmentalized intraflagellar Ca2+ elevations initiate retrograde transport of paused IFT particles to modulate their accumulation. Gliding motility induces mechanosensitive intraflagellar Ca2+ elevations in trailing (dragging) flagella only, acting to specifically clear the accumulated microtubule motors from individual flagella and prevent a futile tug-of-war. Our results demonstrate that compartmentalized intraciliary Ca2+ signaling can regulate the movement of IFT particles and is therefore likely to play a central role in directing the movement and distribution of many ciliary proteins.
0960-9822
2311-2318
Collingridge, Peter
b7b8b73b-815d-48af-a637-c0b10f2b55b4
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a
Collingridge, Peter
b7b8b73b-815d-48af-a637-c0b10f2b55b4
Brownlee, Colin
2af37c1c-b2bf-4832-8370-d9c35e7b3385
Wheeler, Glen L.
80ee477b-ceb3-4051-923c-399098bb746a

Collingridge, Peter, Brownlee, Colin and Wheeler, Glen L. (2013) Compartmentalized Calcium Signaling in Cilia Regulates Intraflagellar Transport. Current Biology, 23 (22), 2311-2318. (doi:10.1016/j.cub.2013.09.059).

Record type: Article

Abstract

Intraflagellar transport (IFT) underpins many of the important cellular roles of cilia and flagella in signaling and motility [1,2,3,4]. The microtubule motors kinesin-2 and cytoplasmic dynein 1b drive IFT particles (protein complexes carrying ciliary component proteins) along the axoneme to facilitate the assembly and maintenance of cilia. IFT is regulated primarily by cargo loading onto the IFT particles, although evidence suggests that IFT particles also exhibit differential rates of movement [5,6,7]. Here we demonstrate that intraflagellar Ca2+ elevations act to directly regulate the movement of IFT particles. IFT-driven movement of adherent flagella membrane glycoproteins in the model alga Chlamydomonas enables flagella-mediated gliding motility [8,9,10]. We find that surface contact promotes the localized accumulation of IFT particles in Chlamydomonas flagella. Highly compartmentalized intraflagellar Ca2+ elevations initiate retrograde transport of paused IFT particles to modulate their accumulation. Gliding motility induces mechanosensitive intraflagellar Ca2+ elevations in trailing (dragging) flagella only, acting to specifically clear the accumulated microtubule motors from individual flagella and prevent a futile tug-of-war. Our results demonstrate that compartmentalized intraciliary Ca2+ signaling can regulate the movement of IFT particles and is therefore likely to play a central role in directing the movement and distribution of many ciliary proteins.

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More information

Published date: 7 November 2013
Organisations: Ocean and Earth Science

Identifiers

Local EPrints ID: 361124
URI: http://eprints.soton.ac.uk/id/eprint/361124
ISSN: 0960-9822
PURE UUID: 1aacb4cc-fb24-4c2d-ab8d-38d11b01828d

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Date deposited: 13 Jan 2014 16:42
Last modified: 08 Jan 2022 09:13

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Contributors

Author: Peter Collingridge
Author: Colin Brownlee
Author: Glen L. Wheeler

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