Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells
Abstract Eukaryotic flagella (synonymous with cilia) rely on a microtubule-based axoneme, together with accessory filaments to carryout motility and signaling functions. While axoneme structures are well characterized, 3D ultrastructure of accessory filaments and their axoneme interface are mostly u...
Main Authors: | , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Publishing Group
2021-07-01
|
Series: | Cell Discovery |
Online Access: | https://doi.org/10.1038/s41421-021-00281-2 |
id |
doaj-38ab5ac8917f4d0eae531c22cc5973cf |
---|---|
record_format |
Article |
spelling |
doaj-38ab5ac8917f4d0eae531c22cc5973cf2021-07-18T11:47:27ZengNature Publishing GroupCell Discovery2056-59682021-07-017111710.1038/s41421-021-00281-2Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cellsJiayan Zhang0Hui Wang1Simon Imhof2Xueting Zhou3Shiqing Liao4Ivo Atanasov5Wong H. Hui6Kent L. Hill7Z. Hong Zhou8Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)California NanoSystems Institute, UCLACalifornia NanoSystems Institute, UCLADepartment of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)Department of Microbiology, Immunology and Molecular Genetics, University of California, Los Angeles (UCLA)Abstract Eukaryotic flagella (synonymous with cilia) rely on a microtubule-based axoneme, together with accessory filaments to carryout motility and signaling functions. While axoneme structures are well characterized, 3D ultrastructure of accessory filaments and their axoneme interface are mostly unknown, presenting a critical gap in understanding structural foundations of eukaryotic flagella. In the flagellum of the protozoan parasite Trypanosoma brucei (T. brucei), the axoneme is accompanied by a paraflagellar rod (PFR) that supports non-planar motility and signaling necessary for disease transmission and pathogenesis. Here, we employed cryogenic electron tomography (cryoET) with sub-tomographic averaging, to obtain structures of the PFR, PFR-axoneme connectors (PACs), and the axonemal central pair complex (CPC). The structures resolve how the 8 nm repeat of the axonemal tubulin dimer interfaces with the 54 nm repeat of the PFR, which consist of proximal, intermediate, and distal zones. In the distal zone, stacked “density scissors” connect with one another to form a “scissors stack network (SSN)” plane oriented 45° to the axoneme axis; and ~370 parallel SSN planes are connected by helix-rich wires into a paracrystalline array with ~90% empty space. Connections from these wires to the intermediate zone, then to overlapping layers of the proximal zone and to the PACs, and ultimately to the CPC, point to a contiguous pathway for signal transmission. Together, our findings provide insights into flagellum-driven, non-planar helical motility of T. brucei and have broad implications ranging from cell motility and tensegrity in biology, to engineering principles in bionics.https://doi.org/10.1038/s41421-021-00281-2 |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Jiayan Zhang Hui Wang Simon Imhof Xueting Zhou Shiqing Liao Ivo Atanasov Wong H. Hui Kent L. Hill Z. Hong Zhou |
spellingShingle |
Jiayan Zhang Hui Wang Simon Imhof Xueting Zhou Shiqing Liao Ivo Atanasov Wong H. Hui Kent L. Hill Z. Hong Zhou Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells Cell Discovery |
author_facet |
Jiayan Zhang Hui Wang Simon Imhof Xueting Zhou Shiqing Liao Ivo Atanasov Wong H. Hui Kent L. Hill Z. Hong Zhou |
author_sort |
Jiayan Zhang |
title |
Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells |
title_short |
Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells |
title_full |
Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells |
title_fullStr |
Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells |
title_full_unstemmed |
Structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells |
title_sort |
structure of the trypanosome paraflagellar rod and insights into non-planar motility of eukaryotic cells |
publisher |
Nature Publishing Group |
series |
Cell Discovery |
issn |
2056-5968 |
publishDate |
2021-07-01 |
description |
Abstract Eukaryotic flagella (synonymous with cilia) rely on a microtubule-based axoneme, together with accessory filaments to carryout motility and signaling functions. While axoneme structures are well characterized, 3D ultrastructure of accessory filaments and their axoneme interface are mostly unknown, presenting a critical gap in understanding structural foundations of eukaryotic flagella. In the flagellum of the protozoan parasite Trypanosoma brucei (T. brucei), the axoneme is accompanied by a paraflagellar rod (PFR) that supports non-planar motility and signaling necessary for disease transmission and pathogenesis. Here, we employed cryogenic electron tomography (cryoET) with sub-tomographic averaging, to obtain structures of the PFR, PFR-axoneme connectors (PACs), and the axonemal central pair complex (CPC). The structures resolve how the 8 nm repeat of the axonemal tubulin dimer interfaces with the 54 nm repeat of the PFR, which consist of proximal, intermediate, and distal zones. In the distal zone, stacked “density scissors” connect with one another to form a “scissors stack network (SSN)” plane oriented 45° to the axoneme axis; and ~370 parallel SSN planes are connected by helix-rich wires into a paracrystalline array with ~90% empty space. Connections from these wires to the intermediate zone, then to overlapping layers of the proximal zone and to the PACs, and ultimately to the CPC, point to a contiguous pathway for signal transmission. Together, our findings provide insights into flagellum-driven, non-planar helical motility of T. brucei and have broad implications ranging from cell motility and tensegrity in biology, to engineering principles in bionics. |
url |
https://doi.org/10.1038/s41421-021-00281-2 |
work_keys_str_mv |
AT jiayanzhang structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT huiwang structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT simonimhof structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT xuetingzhou structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT shiqingliao structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT ivoatanasov structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT wonghhui structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT kentlhill structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells AT zhongzhou structureofthetrypanosomeparaflagellarrodandinsightsintononplanarmotilityofeukaryoticcells |
_version_ |
1721295765859467264 |