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Design principles of Cdr2 node patterns in fission yeast cells

Pattern forming networks have diverse roles in cell biology. Rod-shaped fission yeast cells use pattern formation to control the localization of mitotic signaling proteins and the cytokinetic ring. During interphase, the kinase Cdr2 forms membrane-bound multiprotein complexes termed nodes, which are...

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Autores principales: Opalko, Hannah, Geng, Shuhan, Hall, Aaron R., Vavylonis, Dimitrios, Moseley, James B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10153186/
https://www.ncbi.nlm.nih.gov/pubmed/37131752
http://dx.doi.org/10.1101/2023.04.19.537536
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author Opalko, Hannah
Geng, Shuhan
Hall, Aaron R.
Vavylonis, Dimitrios
Moseley, James B.
author_facet Opalko, Hannah
Geng, Shuhan
Hall, Aaron R.
Vavylonis, Dimitrios
Moseley, James B.
author_sort Opalko, Hannah
collection PubMed
description Pattern forming networks have diverse roles in cell biology. Rod-shaped fission yeast cells use pattern formation to control the localization of mitotic signaling proteins and the cytokinetic ring. During interphase, the kinase Cdr2 forms membrane-bound multiprotein complexes termed nodes, which are positioned in the cell middle due in part to the node inhibitor Pom1 enriched at cell tips. Node positioning is important for timely cell cycle progression and positioning of the cytokinetic ring. Here, we combined experimental and modeling approaches to investigate pattern formation by the Pom1-Cdr2 system. We found that Cdr2 nodes accumulate near the nucleus, and Cdr2 undergoes nucleocytoplasmic shuttling when cortical anchoring is reduced. We generated particle-based simulations based on tip inhibition, nuclear positioning, and cortical anchoring. We tested model predictions by investigating Pom1-Cdr2 localization patterns after perturbing each positioning mechanism, including in both anucleate and multinucleated cells. Experiments show that tip inhibition and cortical anchoring alone are sufficient for the assembly and positioning of nodes in the absence of the nucleus, but that the nucleus and Pom1 facilitate the formation of unexpected node patterns in multinucleated cells. These findings have implications for spatial control of cytokinesis by nodes and for spatial patterning in other biological systems.
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spelling pubmed-101531862023-05-03 Design principles of Cdr2 node patterns in fission yeast cells Opalko, Hannah Geng, Shuhan Hall, Aaron R. Vavylonis, Dimitrios Moseley, James B. bioRxiv Article Pattern forming networks have diverse roles in cell biology. Rod-shaped fission yeast cells use pattern formation to control the localization of mitotic signaling proteins and the cytokinetic ring. During interphase, the kinase Cdr2 forms membrane-bound multiprotein complexes termed nodes, which are positioned in the cell middle due in part to the node inhibitor Pom1 enriched at cell tips. Node positioning is important for timely cell cycle progression and positioning of the cytokinetic ring. Here, we combined experimental and modeling approaches to investigate pattern formation by the Pom1-Cdr2 system. We found that Cdr2 nodes accumulate near the nucleus, and Cdr2 undergoes nucleocytoplasmic shuttling when cortical anchoring is reduced. We generated particle-based simulations based on tip inhibition, nuclear positioning, and cortical anchoring. We tested model predictions by investigating Pom1-Cdr2 localization patterns after perturbing each positioning mechanism, including in both anucleate and multinucleated cells. Experiments show that tip inhibition and cortical anchoring alone are sufficient for the assembly and positioning of nodes in the absence of the nucleus, but that the nucleus and Pom1 facilitate the formation of unexpected node patterns in multinucleated cells. These findings have implications for spatial control of cytokinesis by nodes and for spatial patterning in other biological systems. Cold Spring Harbor Laboratory 2023-07-21 /pmc/articles/PMC10153186/ /pubmed/37131752 http://dx.doi.org/10.1101/2023.04.19.537536 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Opalko, Hannah
Geng, Shuhan
Hall, Aaron R.
Vavylonis, Dimitrios
Moseley, James B.
Design principles of Cdr2 node patterns in fission yeast cells
title Design principles of Cdr2 node patterns in fission yeast cells
title_full Design principles of Cdr2 node patterns in fission yeast cells
title_fullStr Design principles of Cdr2 node patterns in fission yeast cells
title_full_unstemmed Design principles of Cdr2 node patterns in fission yeast cells
title_short Design principles of Cdr2 node patterns in fission yeast cells
title_sort design principles of cdr2 node patterns in fission yeast cells
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10153186/
https://www.ncbi.nlm.nih.gov/pubmed/37131752
http://dx.doi.org/10.1101/2023.04.19.537536
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