A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites

Dendritic filopodia are actin-filled dynamic subcellular structures that sprout on neuronal dendrites during neurogenesis. The exploratory motion of the filopodia is crucial for synaptogenesis, but the underlying mechanisms are poorly understood. To study filopodial motility, we collected and analyz...

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Bibliographic Details
Published in:Molecular biology of the cell 2017-04, Vol.28 (8), p.1021-1033
Main Authors: Marchenko, Olena O, Das, Sulagna, Yu, Ji, Novak, Igor L, Rodionov, Vladimir I, Efimova, Nadia, Svitkina, Tatyana, Wolgemuth, Charles W, Loew, Leslie M
Format: Article
Language:English
Subjects:
Actin Cytoskeleton - metabolism
Actomyosin - metabolism
Animals
Cell Movement - physiology
Cells, Cultured
Dendrites - metabolism
Dendrites - physiology
Hippocampus - cytology
Hippocampus - metabolism
Hippocampus - physiology
Microtubules - metabolism
Models, Molecular
Neurogenesis
Neurons - cytology
Neurons - metabolism
Neurons - physiology
Pseudopodia - metabolism
Pseudopodia - physiology
Rats
Rats, Sprague-Dawley
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Summary:Dendritic filopodia are actin-filled dynamic subcellular structures that sprout on neuronal dendrites during neurogenesis. The exploratory motion of the filopodia is crucial for synaptogenesis, but the underlying mechanisms are poorly understood. To study filopodial motility, we collected and analyzed image data on filopodia in cultured rat hippocampal neurons. We hypothesized that mechanical feedback among the actin retrograde flow, myosin activity, and substrate adhesion gives rise to various filopodial behaviors. We formulated a minimal one-dimensional partial differential equation model that reproduced the range of observed motility. To validate our model, we systematically manipulated experimental correlates of parameters in the model: substrate adhesion strength, actin polymerization rate, myosin contractility, and the integrity of the putative microtubule-based barrier at the filopodium base. The model predicts the response of the system to each of these experimental perturbations, supporting the hypothesis that our actomyosin-driven mechanism controls dendritic filopodia dynamics.
ISSN:1059-1524
1939-4586
DOI:10.1091/mbc.e16-06-0461