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Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring

Flagellum motility is critical for normal human development and for transmission of pathogenic protozoa that cause tremendous human suffering worldwide. Biophysical principles underlying motility of eukaryotic flagella are conserved from protists to vertebrates. However, individual cells exhibit div...

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Autores principales: Hughes, Louise C., Ralston, Katherine S., Hill, Kent L., Zhou, Z. Hong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3250385/
https://www.ncbi.nlm.nih.gov/pubmed/22235240
http://dx.doi.org/10.1371/journal.pone.0025700
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author Hughes, Louise C.
Ralston, Katherine S.
Hill, Kent L.
Zhou, Z. Hong
author_facet Hughes, Louise C.
Ralston, Katherine S.
Hill, Kent L.
Zhou, Z. Hong
author_sort Hughes, Louise C.
collection PubMed
description Flagellum motility is critical for normal human development and for transmission of pathogenic protozoa that cause tremendous human suffering worldwide. Biophysical principles underlying motility of eukaryotic flagella are conserved from protists to vertebrates. However, individual cells exhibit diverse waveforms that depend on cell-specific elaborations on basic flagellum architecture. Trypanosoma brucei is a uniflagellated protozoan parasite that causes African sleeping sickness. The T. brucei flagellum is comprised of a 9+2 axoneme and an extra-axonemal paraflagellar rod (PFR), but the three-dimensional (3D) arrangement of the underlying structural units is poorly defined. Here, we use dual-axis electron tomography to determine the 3D architecture of the T. brucei flagellum. We define the T. brucei axonemal repeating unit. We observe direct connections between the PFR and axonemal dyneins, suggesting a mechanism by which mechanochemical signals may be transmitted from the PFR to axonemal dyneins. We find that the PFR itself is comprised of overlapping laths organized into distinct zones that are connected through twisting elements at the zonal interfaces. The overall structure has an underlying 57nm repeating unit. Biomechanical properties inferred from PFR structure lead us to propose that the PFR functions as a biomechanical spring that may store and transmit energy derived from axonemal beating. These findings provide insight into the structural foundations that underlie the distinctive flagellar waveform that is a hallmark of T. brucei cell motility.
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spelling pubmed-32503852012-01-10 Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring Hughes, Louise C. Ralston, Katherine S. Hill, Kent L. Zhou, Z. Hong PLoS One Research Article Flagellum motility is critical for normal human development and for transmission of pathogenic protozoa that cause tremendous human suffering worldwide. Biophysical principles underlying motility of eukaryotic flagella are conserved from protists to vertebrates. However, individual cells exhibit diverse waveforms that depend on cell-specific elaborations on basic flagellum architecture. Trypanosoma brucei is a uniflagellated protozoan parasite that causes African sleeping sickness. The T. brucei flagellum is comprised of a 9+2 axoneme and an extra-axonemal paraflagellar rod (PFR), but the three-dimensional (3D) arrangement of the underlying structural units is poorly defined. Here, we use dual-axis electron tomography to determine the 3D architecture of the T. brucei flagellum. We define the T. brucei axonemal repeating unit. We observe direct connections between the PFR and axonemal dyneins, suggesting a mechanism by which mechanochemical signals may be transmitted from the PFR to axonemal dyneins. We find that the PFR itself is comprised of overlapping laths organized into distinct zones that are connected through twisting elements at the zonal interfaces. The overall structure has an underlying 57nm repeating unit. Biomechanical properties inferred from PFR structure lead us to propose that the PFR functions as a biomechanical spring that may store and transmit energy derived from axonemal beating. These findings provide insight into the structural foundations that underlie the distinctive flagellar waveform that is a hallmark of T. brucei cell motility. Public Library of Science 2012-01-03 /pmc/articles/PMC3250385/ /pubmed/22235240 http://dx.doi.org/10.1371/journal.pone.0025700 Text en Hughes et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Hughes, Louise C.
Ralston, Katherine S.
Hill, Kent L.
Zhou, Z. Hong
Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring
title Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring
title_full Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring
title_fullStr Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring
title_full_unstemmed Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring
title_short Three-Dimensional Structure of the Trypanosome Flagellum Suggests that the Paraflagellar Rod Functions as a Biomechanical Spring
title_sort three-dimensional structure of the trypanosome flagellum suggests that the paraflagellar rod functions as a biomechanical spring
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3250385/
https://www.ncbi.nlm.nih.gov/pubmed/22235240
http://dx.doi.org/10.1371/journal.pone.0025700
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