Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging

Summary: Cilia are built and maintained by intraflagellar transport (IFT), driving IFT trains back and forth along the ciliary axoneme. How IFT brings about the intricate ciliary structure and how this structure affects IFT are not well understood. We identify, using single-molecule super-resolution...

Full description

Bibliographic Details
Main Authors: Felix Oswald, Bram Prevo, Seyda Acar, Erwin J.G. Peterman
Format: Article
Language:English
Published: Elsevier 2018-10-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124718314499
id doaj-cb502b0474614ea4862f6872a5d88d3e
record_format Article
spelling doaj-cb502b0474614ea4862f6872a5d88d3e2020-11-24T21:43:40ZengElsevierCell Reports2211-12472018-10-01251224235Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution ImagingFelix Oswald0Bram Prevo1Seyda Acar2Erwin J.G. Peterman3Department of Physics and LaserLaB Amsterdam, Vrije Universiteit Amsterdam, Amsterdam, 1081HV, the NetherlandsDepartment of Physics and LaserLaB Amsterdam, Vrije Universiteit Amsterdam, Amsterdam, 1081HV, the NetherlandsDepartment of Physics and LaserLaB Amsterdam, Vrije Universiteit Amsterdam, Amsterdam, 1081HV, the NetherlandsDepartment of Physics and LaserLaB Amsterdam, Vrije Universiteit Amsterdam, Amsterdam, 1081HV, the Netherlands; Corresponding authorSummary: Cilia are built and maintained by intraflagellar transport (IFT), driving IFT trains back and forth along the ciliary axoneme. How IFT brings about the intricate ciliary structure and how this structure affects IFT are not well understood. We identify, using single-molecule super-resolution imaging of IFT components in living C. elegans, ciliary subdomains, enabling correlation of IFT-train dynamics to ciliary ultra-structure. In the transition zone, IFT dynamics are impaired, resulting in frequent pauses. At the ciliary base and tip, IFT trains show intriguing turnaround dynamics. Surprisingly, deletion of IFT motor kinesin-II not only affects IFT-train dynamics but also alters ciliary structure. Super-resolution imaging in these mutant animals suggests that the arrangement of IFT trains with respect to the axonemal microtubules is different than in wild-type animals. Our results reveal a complex, mutual interplay between ciliary ultrastructure and IFT-train dynamics, highlighting the importance of physical cues in the control of IFT dynamics. : Oswald et al. use trajectories of single intraflagellar transport proteins in the chemosensory cilia of C. elegans to generate super-resolution fluorescence maps. Local motility properties can be correlated to ciliary ultrastructure. They find that in the absence of kinesin-II, the ciliary ultrastructure is substantially altered. Keywords: single-molecule fluorescence microscopy, super-resolution microscopy, intraflagellar transport, intracellular transport, cilia, motor cooperation, molecular motor proteinshttp://www.sciencedirect.com/science/article/pii/S2211124718314499
collection DOAJ
language English
format Article
sources DOAJ
author Felix Oswald
Bram Prevo
Seyda Acar
Erwin J.G. Peterman
spellingShingle Felix Oswald
Bram Prevo
Seyda Acar
Erwin J.G. Peterman
Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging
Cell Reports
author_facet Felix Oswald
Bram Prevo
Seyda Acar
Erwin J.G. Peterman
author_sort Felix Oswald
title Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging
title_short Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging
title_full Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging
title_fullStr Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging
title_full_unstemmed Interplay between Ciliary Ultrastructure and IFT-Train Dynamics Revealed by Single-Molecule Super-resolution Imaging
title_sort interplay between ciliary ultrastructure and ift-train dynamics revealed by single-molecule super-resolution imaging
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2018-10-01
description Summary: Cilia are built and maintained by intraflagellar transport (IFT), driving IFT trains back and forth along the ciliary axoneme. How IFT brings about the intricate ciliary structure and how this structure affects IFT are not well understood. We identify, using single-molecule super-resolution imaging of IFT components in living C. elegans, ciliary subdomains, enabling correlation of IFT-train dynamics to ciliary ultra-structure. In the transition zone, IFT dynamics are impaired, resulting in frequent pauses. At the ciliary base and tip, IFT trains show intriguing turnaround dynamics. Surprisingly, deletion of IFT motor kinesin-II not only affects IFT-train dynamics but also alters ciliary structure. Super-resolution imaging in these mutant animals suggests that the arrangement of IFT trains with respect to the axonemal microtubules is different than in wild-type animals. Our results reveal a complex, mutual interplay between ciliary ultrastructure and IFT-train dynamics, highlighting the importance of physical cues in the control of IFT dynamics. : Oswald et al. use trajectories of single intraflagellar transport proteins in the chemosensory cilia of C. elegans to generate super-resolution fluorescence maps. Local motility properties can be correlated to ciliary ultrastructure. They find that in the absence of kinesin-II, the ciliary ultrastructure is substantially altered. Keywords: single-molecule fluorescence microscopy, super-resolution microscopy, intraflagellar transport, intracellular transport, cilia, motor cooperation, molecular motor proteins
url http://www.sciencedirect.com/science/article/pii/S2211124718314499
work_keys_str_mv AT felixoswald interplaybetweenciliaryultrastructureandifttraindynamicsrevealedbysinglemoleculesuperresolutionimaging
AT bramprevo interplaybetweenciliaryultrastructureandifttraindynamicsrevealedbysinglemoleculesuperresolutionimaging
AT seydaacar interplaybetweenciliaryultrastructureandifttraindynamicsrevealedbysinglemoleculesuperresolutionimaging
AT erwinjgpeterman interplaybetweenciliaryultrastructureandifttraindynamicsrevealedbysinglemoleculesuperresolutionimaging
_version_ 1725912620308889600