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Anillin directly crosslinks microtubules with actin filaments

Ilina Bareja,Ondřej Kučera,Irene Istúriz Petitjean,Beatriz Eugenia Orozco Monroy,Ján Sabó,M. Braun,Z. Lansky,G. Koenderink,M. Dogterom

Published 2025 in EMBO Journal

ABSTRACT

Complex morphogenetic processes such as cell division require a tight coordination of the activities of microtubules and actin filaments. There is evidence that anillin, conventionally known as an actin-binding and -bundling protein, regulates microtubule/actin crosstalk during cell division. However, it is unknown whether anillin binds directly to microtubules and whether it is sufficient to establish crosslinking between microtubules and actin filaments. Here we address both questions by developing an in vitro system for observing anillin-mediated interactions with actin filaments and dynamic microtubules via total internal-reflection fluorescence microscopy. We find that anillin can interact directly with microtubules and promote microtubule bundling. We confirm that anillin binds and bundles actin filaments, and find that it has a strong preference for actin bundles over individual filaments. Moreover, we show that anillin can directly crosslink microtubules and actin filaments, cause sliding of actin filaments on the microtubule lattice, and transport actin filaments by the growing microtubule tip. Our findings indicate that anillin can potentially serve as a direct regulator of microtubule/actin crosstalk, e.g., during cell division. Anillin is an actin-binding and -bundling protein that may also affect microtubules. Here, in vitro work shows that anillin directly crosslinks microtubules with actin filaments, enabling it to slide F-actin along the microtubule lattice. Anillin can directly bind to and bundle microtubules (with a preference for GTP/GMPCPP/taxol lattices). Anillin binds diffusively to microtubules and oligomerises in the presence of dynamic microtubules. Anillin also binds simultaneously to actin filaments and can crosslink microtubules and actin filaments. The diffusive capability of anillin along microtubules enables the transport of actin filaments along microtubules, including at the growing microtubule plus-end. Anillin has a strong preference for cytoskeletal overlaps over individual filaments. Anillin can directly bind to and bundle microtubules (with a preference for GTP/GMPCPP/taxol lattices). Anillin binds diffusively to microtubules and oligomerises in the presence of dynamic microtubules. Anillin also binds simultaneously to actin filaments and can crosslink microtubules and actin filaments. The diffusive capability of anillin along microtubules enables the transport of actin filaments along microtubules, including at the growing microtubule plus-end. Anillin has a strong preference for cytoskeletal overlaps over individual filaments. Anillin binds and bundles not just actin filaments, but also microtubules, enabling it to slide the filaments along each other.

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