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Microtubule number and length determine cellular shape and function in Plasmodium

Microtubules are cytoskeletal filaments essential for many cellular processes, including establishment and maintenance of polarity, intracellular transport, division and migration. In most metazoan cells, the number and length of microtubules are highly variable, while they can be precisely defined...

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Autores principales: Spreng, Benjamin, Fleckenstein, Hannah, Kübler, Patrick, Di Biagio, Claudia, Benz, Madlen, Patra, Pintu, Schwarz, Ulrich S, Cyrklaff, Marek, Frischknecht, Friedrich
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6669926/
https://www.ncbi.nlm.nih.gov/pubmed/31368598
http://dx.doi.org/10.15252/embj.2018100984
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author Spreng, Benjamin
Fleckenstein, Hannah
Kübler, Patrick
Di Biagio, Claudia
Benz, Madlen
Patra, Pintu
Schwarz, Ulrich S
Cyrklaff, Marek
Frischknecht, Friedrich
author_facet Spreng, Benjamin
Fleckenstein, Hannah
Kübler, Patrick
Di Biagio, Claudia
Benz, Madlen
Patra, Pintu
Schwarz, Ulrich S
Cyrklaff, Marek
Frischknecht, Friedrich
author_sort Spreng, Benjamin
collection PubMed
description Microtubules are cytoskeletal filaments essential for many cellular processes, including establishment and maintenance of polarity, intracellular transport, division and migration. In most metazoan cells, the number and length of microtubules are highly variable, while they can be precisely defined in some protozoan organisms. However, in either case the significance of these two key parameters for cells is not known. Here, we quantitatively studied the impact of modulating microtubule number and length in Plasmodium, the protozoan parasite causing malaria. Using a gene deletion and replacement strategy targeting one out of two α‐tubulin genes, we show that chromosome segregation proceeds in the oocysts even in the absence of microtubules. However, fewer and shorter microtubules severely impaired the formation, motility and infectivity of Plasmodium sporozoites, the forms transmitted by the mosquito, which usually contain 16 microtubules. We found that α‐tubulin expression levels directly determined the number of microtubules, suggesting a high nucleation barrier as supported by a mathematical model. Infectious sporozoites were only formed in parasite lines featuring at least 10 microtubules, while parasites with 9 or fewer microtubules failed to transmit.
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spelling pubmed-66699262019-08-06 Microtubule number and length determine cellular shape and function in Plasmodium Spreng, Benjamin Fleckenstein, Hannah Kübler, Patrick Di Biagio, Claudia Benz, Madlen Patra, Pintu Schwarz, Ulrich S Cyrklaff, Marek Frischknecht, Friedrich EMBO J Articles Microtubules are cytoskeletal filaments essential for many cellular processes, including establishment and maintenance of polarity, intracellular transport, division and migration. In most metazoan cells, the number and length of microtubules are highly variable, while they can be precisely defined in some protozoan organisms. However, in either case the significance of these two key parameters for cells is not known. Here, we quantitatively studied the impact of modulating microtubule number and length in Plasmodium, the protozoan parasite causing malaria. Using a gene deletion and replacement strategy targeting one out of two α‐tubulin genes, we show that chromosome segregation proceeds in the oocysts even in the absence of microtubules. However, fewer and shorter microtubules severely impaired the formation, motility and infectivity of Plasmodium sporozoites, the forms transmitted by the mosquito, which usually contain 16 microtubules. We found that α‐tubulin expression levels directly determined the number of microtubules, suggesting a high nucleation barrier as supported by a mathematical model. Infectious sporozoites were only formed in parasite lines featuring at least 10 microtubules, while parasites with 9 or fewer microtubules failed to transmit. John Wiley and Sons Inc. 2019-05-24 2019-08-01 /pmc/articles/PMC6669926/ /pubmed/31368598 http://dx.doi.org/10.15252/embj.2018100984 Text en © 2019 The Authors. Published under the terms of the CC BY 4.0 license This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Spreng, Benjamin
Fleckenstein, Hannah
Kübler, Patrick
Di Biagio, Claudia
Benz, Madlen
Patra, Pintu
Schwarz, Ulrich S
Cyrklaff, Marek
Frischknecht, Friedrich
Microtubule number and length determine cellular shape and function in Plasmodium
title Microtubule number and length determine cellular shape and function in Plasmodium
title_full Microtubule number and length determine cellular shape and function in Plasmodium
title_fullStr Microtubule number and length determine cellular shape and function in Plasmodium
title_full_unstemmed Microtubule number and length determine cellular shape and function in Plasmodium
title_short Microtubule number and length determine cellular shape and function in Plasmodium
title_sort microtubule number and length determine cellular shape and function in plasmodium
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6669926/
https://www.ncbi.nlm.nih.gov/pubmed/31368598
http://dx.doi.org/10.15252/embj.2018100984
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