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A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells

Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to posit...

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Autores principales: Erb, Marcella L, Kraemer, James A, Coker, Joanna K C, Chaikeeratisak, Vorrapon, Nonejuie, Poochit, Agard, David A, Pogliano, Joe
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4244570/
https://www.ncbi.nlm.nih.gov/pubmed/25429514
http://dx.doi.org/10.7554/eLife.03197
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author Erb, Marcella L
Kraemer, James A
Coker, Joanna K C
Chaikeeratisak, Vorrapon
Nonejuie, Poochit
Agard, David A
Pogliano, Joe
author_facet Erb, Marcella L
Kraemer, James A
Coker, Joanna K C
Chaikeeratisak, Vorrapon
Nonejuie, Poochit
Agard, David A
Pogliano, Joe
author_sort Erb, Marcella L
collection PubMed
description Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to position DNA at mid-cell, without which infectivity is compromised. Here, we show that PhuZ filaments, like microtubules, stochastically switch from growing in a distinctly polar manner to catastrophic depolymerization (dynamic instability) both in vitro and in vivo. One end of each PhuZ filament is stably anchored near the cell pole to form a spindle-like array that orients the growing ends toward the phage nucleoid so as to position it near mid-cell. Our results demonstrate how a bacteriophage can harness the properties of a tubulin-like cytoskeleton for efficient propagation. This represents the first identification of a prokaryotic tubulin with the dynamic instability of microtubules and the ability to form a simplified bipolar spindle. DOI: http://dx.doi.org/10.7554/eLife.03197.001
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spelling pubmed-42445702014-12-18 A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells Erb, Marcella L Kraemer, James A Coker, Joanna K C Chaikeeratisak, Vorrapon Nonejuie, Poochit Agard, David A Pogliano, Joe eLife Cell Biology Dynamic instability, polarity, and spatiotemporal organization are hallmarks of the microtubule cytoskeleton that allow formation of complex structures such as the eukaryotic spindle. No similar structure has been identified in prokaryotes. The bacteriophage-encoded tubulin PhuZ is required to position DNA at mid-cell, without which infectivity is compromised. Here, we show that PhuZ filaments, like microtubules, stochastically switch from growing in a distinctly polar manner to catastrophic depolymerization (dynamic instability) both in vitro and in vivo. One end of each PhuZ filament is stably anchored near the cell pole to form a spindle-like array that orients the growing ends toward the phage nucleoid so as to position it near mid-cell. Our results demonstrate how a bacteriophage can harness the properties of a tubulin-like cytoskeleton for efficient propagation. This represents the first identification of a prokaryotic tubulin with the dynamic instability of microtubules and the ability to form a simplified bipolar spindle. DOI: http://dx.doi.org/10.7554/eLife.03197.001 eLife Sciences Publications, Ltd 2014-11-27 /pmc/articles/PMC4244570/ /pubmed/25429514 http://dx.doi.org/10.7554/eLife.03197 Text en Copyright © 2014, Erb et al http://creativecommons.org/licenses/by/4.0/ This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Erb, Marcella L
Kraemer, James A
Coker, Joanna K C
Chaikeeratisak, Vorrapon
Nonejuie, Poochit
Agard, David A
Pogliano, Joe
A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
title A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
title_full A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
title_fullStr A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
title_full_unstemmed A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
title_short A bacteriophage tubulin harnesses dynamic instability to center DNA in infected cells
title_sort bacteriophage tubulin harnesses dynamic instability to center dna in infected cells
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4244570/
https://www.ncbi.nlm.nih.gov/pubmed/25429514
http://dx.doi.org/10.7554/eLife.03197
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