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3D Architecture of the Trypanosoma brucei Flagella Connector, a Mobile Transmembrane Junction

Journal article
Authors Johanna L Höög
Sylvain Lacomble
Cedric Bouchet-Marquis
Laura Briggs
Kristin Park
Andreas Hoenger
Keith Gull
Published in PLoS Neglected Tropical Diseases
Volume 10
Issue 1
ISSN 1935-2727
Publication year 2016
Published at Department of Chemistry and Molecular Biology
Language en
Links dx.doi.org/10.1371/journal.pntd.000...
https://gup.ub.gu.se/file/205410
Keywords parasitology, african sleeping sickness, cilia, electron tomography, electron microscopy, cryo-electron microscopy
Subject categories Microbiology in the medical area, Morphology, Cell biology, Microbiology, Cell Biology, Structural Biology

Abstract

Background Cellular junctions are crucial for the formation of multicellular organisms, where they anchor cells to each other and/or supportive tissue and enable cell-to-cell communication. Some unicellular organisms, such as the parasitic protist Trypanosoma brucei, also have complex cellular junctions. The flagella connector (FC) is a three-layered transmembrane junction that moves with the growing tip of a new flagellum and attaches it to the side of the old flagellum. The FC moves via an unknown molecular mechanism, independent of new flagellum growth. Here we describe the detailed 3D architecture of the FC suggesting explanations for how it functions and its mechanism of motility. Methodology/Principal Findings We have used a combination of electron tomography and cryo-electron tomography to reveal the 3D architecture of the FC. Cryo-electron tomography revealed layers of repetitive filamentous electron densities between the two flagella in the interstitial zone. Though the FC does not change in length and width during the growth of the new flagellum, the interstitial zone thickness decreases as the FC matures. This investigation also shows interactions between the FC layers and the axonemes of the new and old flagellum, sufficiently strong to displace the axoneme in the old flagellum. We describe a novel filament, the flagella connector fibre, found between the FC and the axoneme in the old flagellum. Conclusions/Significance The FC is similar to other cellular junctions in that filamentous proteins bridge the extracellular space and are anchored to underlying cytoskeletal structures; however, it is built between different portions of the same cell and is unique because of its intrinsic motility. The detailed description of its structure will be an important tool to use in attributing structure / function relationships as its molecular components are discovered in the future. The FC is involved in the inheritance of cell shape, which is important for the life cycle of this human parasite.

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