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

Olena O. Marchenko, Sulagna Das, Ji Yu, Igor L. Novak, Vladimir I. Rodionov, Nadia Efimova, Tatyana Svitkina, Charles W. Wolgemuth, Leslie M. Loew

Research output: Research - peer-reviewArticle

Abstract

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.

LanguageEnglish (US)
Pages1021-1033
Number of pages13
JournalMolecular Biology of the Cell
Volume28
Issue number8
DOIs
StatePublished - Apr 15 2017

Fingerprint

Actomyosin
Pseudopodia
Dendrites
Actins
Myosins
Neurogenesis
Microtubules
Polymerization
Neurons

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

Cite this

Marchenko, O. O., Das, S., Yu, J., Novak, I. L., Rodionov, V. I., Efimova, N., ... Loew, L. M. (2017). A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites. Molecular Biology of the Cell, 28(8), 1021-1033. DOI: 10.1091/mbc.E16-06-0461

A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites. / Marchenko, Olena O.; Das, Sulagna; Yu, Ji; Novak, Igor L.; Rodionov, Vladimir I.; Efimova, Nadia; Svitkina, Tatyana; Wolgemuth, Charles W.; Loew, Leslie M.

In: Molecular Biology of the Cell, Vol. 28, No. 8, 15.04.2017, p. 1021-1033.

Research output: Research - peer-reviewArticle

Marchenko, OO, Das, S, Yu, J, Novak, IL, Rodionov, VI, Efimova, N, Svitkina, T, Wolgemuth, CW & Loew, LM 2017, 'A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites' Molecular Biology of the Cell, vol 28, no. 8, pp. 1021-1033. DOI: 10.1091/mbc.E16-06-0461
Marchenko OO, Das S, Yu J, Novak IL, Rodionov VI, Efimova N et al. A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites. Molecular Biology of the Cell. 2017 Apr 15;28(8):1021-1033. Available from, DOI: 10.1091/mbc.E16-06-0461
Marchenko, Olena O. ; Das, Sulagna ; Yu, Ji ; Novak, Igor L. ; Rodionov, Vladimir I. ; Efimova, Nadia ; Svitkina, Tatyana ; Wolgemuth, Charles W. ; Loew, Leslie M./ A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites. In: Molecular Biology of the Cell. 2017 ; Vol. 28, No. 8. pp. 1021-1033
@article{42d7965b3e9045fe974a2663d83c76b7,
title = "A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites",
abstract = "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.",
author = "Marchenko, {Olena O.} and Sulagna Das and Ji Yu and Novak, {Igor L.} and Rodionov, {Vladimir I.} and Nadia Efimova and Tatyana Svitkina and Wolgemuth, {Charles W.} and Loew, {Leslie M.}",
year = "2017",
month = "4",
doi = "10.1091/mbc.E16-06-0461",
volume = "28",
pages = "1021--1033",
journal = "Molecular Biology of the Cell",
issn = "1059-1524",
publisher = "American Society for Cell Biology",
number = "8",

}

TY - JOUR

T1 - A minimal actomyosin-based model predicts the dynamics of filopodia on neuronal dendrites

AU - Marchenko,Olena O.

AU - Das,Sulagna

AU - Yu,Ji

AU - Novak,Igor L.

AU - Rodionov,Vladimir I.

AU - Efimova,Nadia

AU - Svitkina,Tatyana

AU - Wolgemuth,Charles W.

AU - Loew,Leslie M.

PY - 2017/4/15

Y1 - 2017/4/15

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85018528019&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85018528019&partnerID=8YFLogxK

U2 - 10.1091/mbc.E16-06-0461

DO - 10.1091/mbc.E16-06-0461

M3 - Article

VL - 28

SP - 1021

EP - 1033

JO - Molecular Biology of the Cell

T2 - Molecular Biology of the Cell

JF - Molecular Biology of the Cell

SN - 1059-1524

IS - 8

ER -