Actin filaments regulate microtubule growth at the centrosome

The centrosome is the main microtubule‐organizing centre. It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are...

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Veröffentlicht in:The EMBO journal 2019-06, Vol.38 (11), p.n/a
Hauptverfasser: Inoue, Daisuke, Obino, Dorian, Pineau, Judith, Farina, Francesca, Gaillard, Jérémie, Guerin, Christophe, Blanchoin, Laurent, Lennon‐Duménil, Ana‐Maria, Théry, Manuel
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container_issue 11
container_start_page
container_title The EMBO journal
container_volume 38
creator Inoue, Daisuke
Obino, Dorian
Pineau, Judith
Farina, Francesca
Gaillard, Jérémie
Guerin, Christophe
Blanchoin, Laurent
Lennon‐Duménil, Ana‐Maria
Théry, Manuel
description The centrosome is the main microtubule‐organizing centre. It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are correlated with reduced amounts of microtubules. Furthermore, lymphocyte activation resulted in disassembly of centrosomal actin and an increase in microtubule number. To further investigate the direct crosstalk between actin and microtubules at the centrosome, we performed in vitro reconstitution assays based on (i) purified centrosomes and (ii) on the co‐micropatterning of microtubule seeds and actin filaments. These two assays demonstrated that actin filaments constitute a physical barrier blocking elongation of nascent microtubules. Finally, we showed that cell adhesion and cell spreading lead to lower densities of centrosomal actin, thus resulting in higher microtubule growth. We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture. Synopsis Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation. Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules. The amount of centrosomal actin is negatively correlated to the amount of microtubules. In vitro reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules. Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules. Graphical Abstract Increasing density of F‐actin nucleating from the main interphase microtubule‐organizing center creates a physical barrier for nascent microtubules in lymphocytes and in vitro .
doi_str_mv 10.15252/embj.201899630
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We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture. Synopsis Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation. Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules. The amount of centrosomal actin is negatively correlated to the amount of microtubules. In vitro reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules. Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules. 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It also organizes a local network of actin filaments. However, the precise function of the actin network at the centrosome is not well understood. Here, we show that increasing densities of actin filaments at the centrosome of lymphocytes are correlated with reduced amounts of microtubules. Furthermore, lymphocyte activation resulted in disassembly of centrosomal actin and an increase in microtubule number. To further investigate the direct crosstalk between actin and microtubules at the centrosome, we performed in vitro reconstitution assays based on (i) purified centrosomes and (ii) on the co‐micropatterning of microtubule seeds and actin filaments. These two assays demonstrated that actin filaments constitute a physical barrier blocking elongation of nascent microtubules. Finally, we showed that cell adhesion and cell spreading lead to lower densities of centrosomal actin, thus resulting in higher microtubule growth. We therefore propose a novel mechanism, by which the number of centrosomal microtubules is regulated by cell adhesion and actin‐network architecture. Synopsis Centrosomes, the main interphase microtubule‐organizing centers of the cell, also nucleate local actin filament networks, which are now found to form a physical barrier blocking microtubule elongation. Activation of B lymphocytes is associated with reduction of centrosomal actin and increase in the number of microtubules. The amount of centrosomal actin is negatively correlated to the amount of microtubules. In vitro reconstitutions show negative correlation between the amount of centrosomal actin and the number of microtubules. Cell spreading proportionally affects the amount of centrosomal actin and the number of centrosomal microtubules. Graphical Abstract Increasing density of F‐actin nucleating from the main interphase microtubule‐organizing center creates a physical barrier for nascent microtubules in lymphocytes and in vitro .</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>30902847</pmid><doi>10.15252/embj.201899630</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0002-9968-1779</orcidid><orcidid>https://orcid.org/0000-0002-4108-2714</orcidid><orcidid>https://orcid.org/0000-0001-8146-9254</orcidid><orcidid>https://orcid.org/0000-0003-4383-1034</orcidid><orcidid>https://orcid.org/0000-0003-0665-1210</orcidid><orcidid>https://orcid.org/0000-0002-5124-6970</orcidid><oa>free_for_read</oa></addata></record>
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subjects Actin
Actin Cytoskeleton - physiology
Actins - metabolism
Adhesion
Animals
Barriers
Cattle
Cell activation
Cell adhesion
Cell adhesion & migration
Cell spreading
Cells, Cultured
centrosome
Centrosome - metabolism
Centrosomes
Correlation
Crosstalk
Dismantling
Elongation
EMBO05
EMBO19
Filaments
Humans
Jurkat Cells
Life Sciences
Lymphocytes
Lymphocytes B
Mice
Micropatterning
microtubule
Microtubule-Associated Proteins - metabolism
Microtubules
Microtubules - metabolism
Seeds
Spreading
Vegetal Biology
title Actin filaments regulate microtubule growth at the centrosome
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