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The roles of a flagellar HSP40 ensuring rhythmic beating

HSP40s are regarded as cochaperones, perpetually shuttling client polypeptides to HSP70s for refolding. However, many HSP40s that are central for disparate processes diverge from this paradigm. To elucidate the noncanonical mechanisms, we investigated HSP40 in the radial spoke (RS) complex in flagel...

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Autores principales: Zhu, Xiaoyan, Poghosyan, Emiliya, Rezabkova, Lenka, Mehall, Bridget, Sakakibara, Hitoshi, Hirono, Masafumi, Kamiya, Ritsu, Ishikawa, Takashi, Yang, Pinfen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6589562/
https://www.ncbi.nlm.nih.gov/pubmed/30427757
http://dx.doi.org/10.1091/mbc.E18-01-0047
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author Zhu, Xiaoyan
Poghosyan, Emiliya
Rezabkova, Lenka
Mehall, Bridget
Sakakibara, Hitoshi
Hirono, Masafumi
Kamiya, Ritsu
Ishikawa, Takashi
Yang, Pinfen
author_facet Zhu, Xiaoyan
Poghosyan, Emiliya
Rezabkova, Lenka
Mehall, Bridget
Sakakibara, Hitoshi
Hirono, Masafumi
Kamiya, Ritsu
Ishikawa, Takashi
Yang, Pinfen
author_sort Zhu, Xiaoyan
collection PubMed
description HSP40s are regarded as cochaperones, perpetually shuttling client polypeptides to HSP70s for refolding. However, many HSP40s that are central for disparate processes diverge from this paradigm. To elucidate the noncanonical mechanisms, we investigated HSP40 in the radial spoke (RS) complex in flagella. Disruption of the gene by the MRC1 transposon in Chlamydomonas resulted in jerky flagella. Traditional electron microscopy, cryo-electron tomography, and sub-tomogram analysis revealed RSs of various altered morphologies that, unexpectedly, differed between the two RS species. This indicates that HSP40 locks the RS into a functionally rigid conformation, facilitating its interactions with the adjacent central pair apparatus for transducing locally varied mechanical feedback, which permits rhythmic beating. Missing HSP40, like missing RSs, could be restored in a tip-to-base direction when HSP40 mutants fused with a HSP40 donor cell. However, without concomitant de novo RS assembly, the repair was exceedingly slow, suggesting HSP40/RS-coupled intraflagellar trafficking and assembly. Biochemical analysis and modeling uncovered spoke HSP40’s cochaperone traits. On the basis of our data, we propose that HSP40 accompanies its client RS precursor when traveling to the flagellar tip. Upon arrival, both refold in concert to assemble into the mature configuration. HSP40’s roles in chaperoning and structural maintenance shed new light on its versatility and flagellar biology.
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spelling pubmed-65895622019-06-28 The roles of a flagellar HSP40 ensuring rhythmic beating Zhu, Xiaoyan Poghosyan, Emiliya Rezabkova, Lenka Mehall, Bridget Sakakibara, Hitoshi Hirono, Masafumi Kamiya, Ritsu Ishikawa, Takashi Yang, Pinfen Mol Biol Cell Articles HSP40s are regarded as cochaperones, perpetually shuttling client polypeptides to HSP70s for refolding. However, many HSP40s that are central for disparate processes diverge from this paradigm. To elucidate the noncanonical mechanisms, we investigated HSP40 in the radial spoke (RS) complex in flagella. Disruption of the gene by the MRC1 transposon in Chlamydomonas resulted in jerky flagella. Traditional electron microscopy, cryo-electron tomography, and sub-tomogram analysis revealed RSs of various altered morphologies that, unexpectedly, differed between the two RS species. This indicates that HSP40 locks the RS into a functionally rigid conformation, facilitating its interactions with the adjacent central pair apparatus for transducing locally varied mechanical feedback, which permits rhythmic beating. Missing HSP40, like missing RSs, could be restored in a tip-to-base direction when HSP40 mutants fused with a HSP40 donor cell. However, without concomitant de novo RS assembly, the repair was exceedingly slow, suggesting HSP40/RS-coupled intraflagellar trafficking and assembly. Biochemical analysis and modeling uncovered spoke HSP40’s cochaperone traits. On the basis of our data, we propose that HSP40 accompanies its client RS precursor when traveling to the flagellar tip. Upon arrival, both refold in concert to assemble into the mature configuration. HSP40’s roles in chaperoning and structural maintenance shed new light on its versatility and flagellar biology. The American Society for Cell Biology 2019-01-15 /pmc/articles/PMC6589562/ /pubmed/30427757 http://dx.doi.org/10.1091/mbc.E18-01-0047 Text en © 2019 Zhu, Poghosyan, et al. “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology. http://creativecommons.org/licenses/by-nc-sa/3.0 This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.
spellingShingle Articles
Zhu, Xiaoyan
Poghosyan, Emiliya
Rezabkova, Lenka
Mehall, Bridget
Sakakibara, Hitoshi
Hirono, Masafumi
Kamiya, Ritsu
Ishikawa, Takashi
Yang, Pinfen
The roles of a flagellar HSP40 ensuring rhythmic beating
title The roles of a flagellar HSP40 ensuring rhythmic beating
title_full The roles of a flagellar HSP40 ensuring rhythmic beating
title_fullStr The roles of a flagellar HSP40 ensuring rhythmic beating
title_full_unstemmed The roles of a flagellar HSP40 ensuring rhythmic beating
title_short The roles of a flagellar HSP40 ensuring rhythmic beating
title_sort roles of a flagellar hsp40 ensuring rhythmic beating
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6589562/
https://www.ncbi.nlm.nih.gov/pubmed/30427757
http://dx.doi.org/10.1091/mbc.E18-01-0047
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