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Actomyosin Dynamics Determine the Extension and Retraction of Filopodia on Neuronal Dendrites

Olena O. Marchenko, Sulagna Das, Ji Yu, Igor L. Novak, Vladimir I. Rodionov, Nadia Efimova, Tatiana Svitkina, Charles W. Wolgemuth, View ORCID ProfileLeslie M. Loew
doi: https://doi.org/10.1101/057919
Olena O. Marchenko
1R. D. Berlin Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, CT
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Sulagna Das
2Department of Anatomy and Structural Biology, Albert Einstein College of Medicine, New York, NY
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Ji Yu
1R. D. Berlin Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, CT
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Igor L. Novak
1R. D. Berlin Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, CT
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Vladimir I. Rodionov
1R. D. Berlin Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, CT
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Nadia Efimova
3Department of Biology, University of Pennsylvania, Philadelphia, PA
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Tatiana Svitkina
3Department of Biology, University of Pennsylvania, Philadelphia, PA
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Charles W. Wolgemuth
4Departments of Physics and Molecular and Cellular Biology University of Arizona Tucson, AZ
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Leslie M. Loew
1R. D. Berlin Center for Cell Analysis and Modeling, University of Connecticut Health Center, Farmington, CT
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  • ORCID record for Leslie M. Loew
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Abstract

Impact Statement In this study, using a combination of computational and experimental approaches we show that a complex dynamic behavior of dendritic filopodia that is essential for synaptogenesis is explained by an interplay among forces generated by actin retrograde flow, myosin contractility, and substrate adhesion.

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 the 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 have 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.

Footnotes

  • Authors Information: Olena O. Marchenko R.D.Berlin Center for Cell Analysis and Modeling Uconn Health Center 400 Farmington Ave, Farmington, CT 06030 Phone: 860-697-6724 Email: omarchenko{at}uchc.edu

  • Sulagna Das Department of Anatomy and Structural Biology, Albert Einstein College of Medicine 1300 Morris Park Ave, Bronx, NY 10461, New York, NY Phone: 718-430-8598 Email: sulagna.das{at}einstein.yu.edu

  • Ji Yu R.D.Berlin Center for Cell Analysis and Modeling Uconn Health Center 400 Farmington Ave, Farmington, CT 06030 Phone: 860-697-6727 Email: jiyu{at}uchc.edu

  • Igor L. Novak R.D.Berlin Center for Cell Analysis and Modeling Uconn Health Center 400 Farmington Ave, Farmington, CT 06030 Phone: 860-697-6724 Email: novak{at}uchc.edu

  • Vladimir I. Rodionov R.D.Berlin Center for Cell Analysis and Modeling Uconn Health Center 400 Farmington Ave, Farmington, CT 06030 Phone: 860 679-1850 Email: rodionov{at}uchc.edu

  • Nadia Efimova Department of Biology University of Pennsylvania Philadelphia, PA Phone: 215-898-5736 Email: nadezdae{at}sas.upenn.edu

  • Tatiana Svitkina Department of Biology University of Pennsylvania Philadelphia, PA Phone: 215-898-5736 Email: svitkina{at}sas.upenn.edu

  • Charles W. Wolgemuth Departments of Physics and Molecular and Cellular Biology University of Arizona Tucson, AZ 85721 Phone: 520-626-1622 Email: wolg{at}email.arizona.edu

  • Leslie M. Loew R.D. Berlin Center for Cell Analysis and Modeling Uconn Health Center Farmington, CT 06030 Phone: 860-697-3568 Email: les{at}volt.uchc.edu

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted June 09, 2016.
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Actomyosin Dynamics Determine the Extension and Retraction of Filopodia on Neuronal Dendrites
Olena O. Marchenko, Sulagna Das, Ji Yu, Igor L. Novak, Vladimir I. Rodionov, Nadia Efimova, Tatiana Svitkina, Charles W. Wolgemuth, Leslie M. Loew
bioRxiv 057919; doi: https://doi.org/10.1101/057919
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Actomyosin Dynamics Determine the Extension and Retraction of Filopodia on Neuronal Dendrites
Olena O. Marchenko, Sulagna Das, Ji Yu, Igor L. Novak, Vladimir I. Rodionov, Nadia Efimova, Tatiana Svitkina, Charles W. Wolgemuth, Leslie M. Loew
bioRxiv 057919; doi: https://doi.org/10.1101/057919

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