Drebrin-mediated microtubule–actomyosin coupling steers cerebellar granule neuron nucleokinesis and migration pathway selection

Trivedi, Niraj; Stabley, Daniel R.; Cain, Blake; Howell, Danielle; Laumonnerie, Christophe; Ramahi, Joseph S.; Temirov, Jamshid; Kerekes, Ryan A.; Gordon-Weeks, Phillip R.; Solecki, David J.

doi:10.1038/ncomms14484

Drebrin-mediated microtubule–actomyosin coupling steers cerebellar granule neuron nucleokinesis and migration pathway selection

Journal Article · Thu Feb 23 00:00:00 EST 2017 · Nature Communications

DOI:https://doi.org/10.1038/ncomms14484· OSTI ID:1346667

Trivedi, Niraj ^[1]; Stabley, Daniel R. ^[1]; Cain, Blake ^[1]; Howell, Danielle ^[1]; Laumonnerie, Christophe ^[1]; Ramahi, Joseph S. ^[1]; Temirov, Jamshid ^[2]; Kerekes, Ryan A. ^[3]; Gordon-Weeks, Phillip R. ^[4]; Solecki, David J. ^[1]

St. Jude Children's Research Hospital, Memphis, TN (United States). Department of Developmental Neurobiology
St. Jude Children's Research Hospital, Memphis, TN (United States). Cell & Tissue Imaging Center
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Imaging, Signals and Machine Learning Group
King's College London (United Kingdom). Medical Research Council MRC Centre for Developmental Neurobiology

Neuronal migration from a germinal zone to a final laminar position is essential for the morphogenesis of neuronal circuits. While it is hypothesized that microtubule–actomyosin crosstalk is required for a neuron’s ‘two-stroke’ nucleokinesis cycle, the molecular mechanisms controlling such crosstalk are not defined. By using the drebrin microtubule–actin crosslinking protein as an entry point into the cerebellar granule neuron system in combination with super-resolution microscopy, we investigate how these cytoskeletal systems interface during migration. Lattice light-sheet and structured illumination microscopy reveal a proximal leading process nanoscale architecture wherein f-actin and drebrin intervene between microtubules and the plasma membrane. Functional perturbations of drebrin demonstrate that proximal leading process microtubule–actomyosin coupling steers the direction of centrosome and somal migration, as well as the switch from tangential to radial migration. Finally, the Siah2 E3 ubiquitin ligase antagonizes drebrin function, suggesting a model for control of the microtubule–actomyosin interfaces during neuronal differentiation.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: ORNL work for others; USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1346667

Journal Information:: Nature Communications, Journal Name: Nature Communications Vol. 8; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Nesprins and opposing microtubule motors generate a point force that drives directional nuclear motion in migrating neurons Wu, You Kure; Umeshima, Hiroki; Kurisu, Junko Development, Vol. 145, Issue 5 https://doi.org/10.1242/dev.158782	journal	March 2018
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PlexinD1 signaling controls morphological changes and migration termination in newborn neurons Sawada, Masato; Ohno, Nobuhiko; Kawaguchi, Mitsuyasu The EMBO Journal, Vol. 37, Issue 4 https://doi.org/10.15252/embj.201797404	journal	January 2018
Seven in Absentia E3 Ubiquitin Ligases: Central Regulators of Neural Cell Fate and Neuronal Polarity Ong, Taren; Solecki, David J. Frontiers in Cellular Neuroscience, Vol. 11 https://doi.org/10.3389/fncel.2017.00322	journal	October 2017
Inter-dependent apical microtubule and actin dynamics orchestrate centrosome retention and neuronal delamination Kasioulis, Ioannis; Das, Raman M.; Storey, Kate G. eLife, Vol. 6 https://doi.org/10.7554/elife.26215	journal	October 2017

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