Mechanisms of microtubule dynamics and force generation examined with computational modeling and electron cryotomography

Nikita B. Gudimchuk (), Evgeni V. Ulyanov, Eileen O’Toole, Cynthia L. Page, Dmitrii S. Vinogradov, Garry Morgan, Gabriella Li, Jeffrey K. Moore, Ewa Szczesna, Antonina Roll-Mecak, Fazoil I. Ataullakhanov and J. Richard McIntosh
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Nikita B. Gudimchuk: Lomonosov Moscow State University
Evgeni V. Ulyanov: Lomonosov Moscow State University
Eileen O’Toole: University of Colorado
Cynthia L. Page: University of Colorado
Dmitrii S. Vinogradov: Russian Academy of Sciences
Garry Morgan: University of Colorado
Gabriella Li: University of Colorado School of Medicine
Jeffrey K. Moore: University of Colorado School of Medicine
Ewa Szczesna: National Institute of Neurological Disorders and Stroke
Antonina Roll-Mecak: National Institute of Neurological Disorders and Stroke
Fazoil I. Ataullakhanov: Lomonosov Moscow State University
J. Richard McIntosh: University of Colorado

Nature Communications, 2020, vol. 11, issue 1, 1-15

Abstract: Abstract Microtubules are dynamic tubulin polymers responsible for many cellular processes, including the capture and segregation of chromosomes during mitosis. In contrast to textbook models of tubulin self-assembly, we have recently demonstrated that microtubules elongate by addition of bent guanosine triphosphate tubulin to the tips of curving protofilaments. Here we explore this mechanism of microtubule growth using Brownian dynamics modeling and electron cryotomography. The previously described flaring shapes of growing microtubule tips are remarkably consistent under various assembly conditions, including different tubulin concentrations, the presence or absence of a polymerization catalyst or tubulin-binding drugs. Simulations indicate that development of substantial forces during microtubule growth and shortening requires a high activation energy barrier in lateral tubulin-tubulin interactions. Modeling offers a mechanism to explain kinetochore coupling to growing microtubule tips under assisting force, and it predicts a load-dependent acceleration of microtubule assembly, providing a role for the flared morphology of growing microtubule ends.

Date: 2020
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DOI: 10.1038/s41467-020-17553-2

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