Multiscale polar theory of microtubule and motor-protein assemblies

Gao, Tong; Blackwell, Robert; Glaser, Matthew A.; Betterton, Meredith D.; Shelley, Michael J.

doi:10.1103/PhysRevLett.114.048101

Title: Multiscale polar theory of microtubule and motor-protein assemblies

Abstract

Microtubules and motor proteins are building blocks of self-organized subcellular biological structures such as the mitotic spindle and the centrosomal microtubule array. These same ingredients can form new “bioactive” liquid-crystalline fluids that are intrinsically out of equilibrium and which display complex flows and defect dynamics. It is not yet well understood how microscopic activity, which involves polarity-dependent interactions between motor proteins and microtubules, yields such larger-scale dynamical structures. In our multiscale theory, Brownian dynamics simulations of polar microtubule ensembles driven by cross-linking motors allow us to study microscopic organization and stresses. Polarity sorting and cross-link relaxation emerge as two polar-specific sources of active destabilizing stress. On larger length scales, our continuum Doi-Onsager theory captures the hydrodynamic flows generated by polarity-dependent active stresses. Finally, the results connect local polar structure to flow structures and defect dynamics.

Authors:

Gao, Tong ^[1]; Blackwell, Robert ^[2]; Glaser, Matthew A. ^[2]; Betterton, Meredith D. ^[2]; Shelley, Michael J. ^[1]

New York Univ. (NYU), New York, NY (United States)
Univ. of Colorado, Boulder, CO (United States)

Publication Date:: Tue Jan 27 00:00:00 EST 2015

Research Org.:: New York Univ. (NYU), NY (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1343759

Alternate Identifier(s):: OSTI ID: 1180164

Grant/Contract Number:: FG02-88ER25053

Resource Type:: Journal Article: Accepted Manuscript

Journal Name:: Physical Review Letters

Additional Journal Information:: Journal Volume: 114; Journal Issue: 4; Journal ID: ISSN 0031-9007

Publisher:: American Physical Society (APS)

Country of Publication:: United States

Language:: English

Subject:: 71 CLASSICAL AND QUANTUM MECHANICS, GENERAL PHYSICS; 36 MATERIALS SCIENCE

Citation Formats


                    Gao, Tong, Blackwell, Robert, Glaser, Matthew A., Betterton, Meredith D., and Shelley, Michael J. Multiscale polar theory of microtubule and motor-protein assemblies.  United States: N. p., 2015. 
        Web.  doi:10.1103/PhysRevLett.114.048101.

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                    Gao, Tong, Blackwell, Robert, Glaser, Matthew A., Betterton, Meredith D., & Shelley, Michael J. Multiscale polar theory of microtubule and motor-protein assemblies.  United States.  https://doi.org/10.1103/PhysRevLett.114.048101

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                    Gao, Tong, Blackwell, Robert, Glaser, Matthew A., Betterton, Meredith D., and Shelley, Michael J. 2015.  
        "Multiscale polar theory of microtubule and motor-protein assemblies".  United States.  https://doi.org/10.1103/PhysRevLett.114.048101.  https://www.osti.gov/servlets/purl/1343759.

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@article{osti_1343759,

  title        = {Multiscale polar theory of microtubule and motor-protein assemblies},

  author       = {Gao, Tong and Blackwell, Robert and Glaser, Matthew A. and Betterton, Meredith D. and Shelley, Michael J.},

  abstractNote = {Microtubules and motor proteins are building blocks of self-organized subcellular biological structures such as the mitotic spindle and the centrosomal microtubule array. These same ingredients can form new “bioactive” liquid-crystalline fluids that are intrinsically out of equilibrium and which display complex flows and defect dynamics. It is not yet well understood how microscopic activity, which involves polarity-dependent interactions between motor proteins and microtubules, yields such larger-scale dynamical structures. In our multiscale theory, Brownian dynamics simulations of polar microtubule ensembles driven by cross-linking motors allow us to study microscopic organization and stresses. Polarity sorting and cross-link relaxation emerge as two polar-specific sources of active destabilizing stress. On larger length scales, our continuum Doi-Onsager theory captures the hydrodynamic flows generated by polarity-dependent active stresses. Finally, the results connect local polar structure to flow structures and defect dynamics.},

  doi          = {10.1103/PhysRevLett.114.048101},

  url          = {https://www.osti.gov/biblio/1343759},
  journal      = {Physical Review Letters},

  issn         = {0031-9007},

  number       = 4,

  volume       = 114,

  place        = {United States},

  year         = {Tue Jan 27 00:00:00 EST 2015},

  month        = {Tue Jan 27 00:00:00 EST 2015}

}

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text, January 2020

Rickman, Jamie; Nédélec, François; Surrey, Thomas
The Francis Crick Institute
https://doi.org/10.25418/crick.11538282.v1

Effects of spatial dimensionality and steric interactions on microtubule-motor self-organization.
text, January 2020

Rickman, Jamie; Nédélec, François; Surrey, Thomas
The Francis Crick Institute
https://doi.org/10.25418/crick.11538282

Tunable dynamics of microtubule based active isotropic gels
text, January 2014

Henkin, Gil; DeCamp, Stephen J.; Chen, Daniel TN
arXiv
https://doi.org/10.48550/arxiv.1409.7663

Orientational order of motile defects in active nematics
text, January 2015

DeCamp, Stephen J.; Redner, Gabriel S.; Baskaran, Aparna
arXiv
https://doi.org/10.48550/arxiv.1501.06228

Instabilities, defects, and defect ordering in an overdamped active nematic
preprint, January 2015

Putzig, Elias; Redner, Gabriel S.; Baskaran, Arvind
arXiv
https://doi.org/10.48550/arxiv.1506.03501

Antipolar ordering of topological defects in active liquid crystals
text, January 2015

Oza, Anand U.; Dunkel, Jörn
arXiv
https://doi.org/10.48550/arxiv.1507.01055

Correlation lengths in hydrodynamic models of active nematics
text, January 2016

Hemingway, E. J.; Mishra, P.; Marchetti, M. C.
arXiv
https://doi.org/10.48550/arxiv.1604.01203

Analytical structure, dynamics, and coarse-graining of a kinetic model of an active fluid
text, January 2017

Gao, Tong; Betterton, Meredith D.; Jhang, An-Sheng
arXiv
https://doi.org/10.48550/arxiv.1703.00969

The interplay between activity and filament flexibility determines the emergent properties of active nematics
preprint, January 2017

Joshi, Abhijeet; Putzig, Elias; Baskaran, Aparna
arXiv
https://doi.org/10.48550/arxiv.1711.05714

Self-organized dynamics and the transition to turbulence of confined active nematics
text, January 2018

Opathalage, Achini; Norton, Michael M.; Juniper, Michael P. N.
arXiv
https://doi.org/10.48550/arxiv.1810.09032

Data-driven quantitative modeling of bacterial active nematics
text, January 2020

Li, He; Shi, Xia-qing; Huang, Mingji
arXiv
https://doi.org/10.48550/arxiv.2011.07894

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Title: Multiscale polar theory of microtubule and motor-protein assemblies

Abstract

Citation Formats

Nonequilibrium structure and dynamics in a microscopic model of thin-film active gels journal, March 2014

Instabilities and topological defects in active nematics journal, January 2014

Defect Annihilation and Proliferation in Active Nematics journal, May 2013

Lennard-Jones sticks: A new model for linear molecules journal, December 2006

Spontaneous motion in hierarchically assembled active matter journal, November 2012

Meso-scale turbulence in living fluids journal, August 2012

The Mechanics and Statistics of Active Matter journal, August 2010

Polar patterns of driven filaments journal, September 2010

Instabilities and nonlinear dynamics of concentrated active suspensions journal, July 2013

Kinetic theory and simulations of active polar liquid crystalline polymers journal, January 2013

Force production by single kinesin motors journal, September 2000

Physical Properties Determining Self-Organization of Motors and Microtubules journal, May 2001

Brownian dynamics of hard spherocylinders journal, August 1994

Brownian motion, hydrodynamics, and the osmotic pressure journal, February 1993

Critical bacterial concentration for the onset of collective swimming journal, July 2009

Actively Contracting Bundles of Polar Filaments journal, August 2000

Single kinesin molecules studied with a molecular force clamp journal, July 1999

Tracing the phase boundaries of hard spherocylinders journal, January 1997

Excitable Patterns in Active Nematics journal, May 2011

A re‐examination of the phase diagram of hard spherocylinders journal, May 1996

Instabilities and Pattern Formation in Active Particle Suspensions: Kinetic Theory and Continuum Simulations journal, April 2008

Living liquid crystals journal, January 2014

Cytoplasmic streaming in plant cells emerges naturally by microfilament self-organization journal, August 2013

Nonlinear dynamics and rheology of active fluids: Simulations in two dimensions journal, April 2011

Polarity Sorting in a Bundle of Actin Filaments by Two-Headed Myosins journal, August 1996

Polar patterns in active fluids journal, January 2012

Self-organization of microtubules and motors journal, September 1997

Swimmers in Thin Films: From Swarming to Hydrodynamic Instabilities journal, December 2010

The stress system in a suspension of force-free particles journal, April 1970

Nonequilibrium steady states in polar active fluids journal, January 2011

Particle-Tracking Microrheology of Living Cells: Principles and Applications journal, June 2009

The Motion of Ellipsoidal Particles Immersed in a Viscous Fluid journal, November 1922

Velocity Correlations in an Active Nematic journal, September 2013

Spontaneous flow transition in active polar gels journal, May 2005

Numerical study of the phase behavior of rodlike colloids with attractive interactions journal, August 1997

Active nematic materials with substrate friction journal, December 2014

Bridging the microscopic and the hydrodynamic in active filament solutions journal, March 2005

Active suspensions and their nonlinear models journal, June 2013

Brownian dynamics simulations of the self- and collective rotational diffusion coefficients of rigid long thin rods journal, June 2005

Statistical hydrodynamics of ordered suspensions of self-propelled particles: waves, giant number fluctuations and instabilities journal, April 2002

Phase behavior of two-dimensional hard rod fluids journal, June 2000

Stability of active suspensions journal, April 2010

Mobility measurement by analysis of fluorescence photobleaching recovery kinetics journal, September 1976

A Quantitative Analysis of Contractility in Active Cytoskeletal Protein Networks journal, April 2008

Eine einfache molekulare Theorie des nematischen kristallinflüssigen Zustandes journal, July 1958

Living Liquid Crystals journal, January 2014

Molecular Biology of the Cell journal, January 1973

Meso-scale turbulence in living fluids text, January 2012

Molecular biology of the cell journal, October 1983

The Mechanics and Statistics of Active Matter text, January 2010

Swimmers in thin films: from swarming to hydrodynamic instabilities text, January 2010

Excitable Patterns in Active Nematics text, January 2010

Nonlinear dynamics and rheology of active fluids: simulations in two dimensions text, January 2010

Spontaneous motion in hierarchically assembled active matter text, January 2013

Velocity Correlations in an Active Nematic text, January 2013

Defect annihilation and proliferation in active nematics text, January 2013

Cytoplasmic Streaming in Plant Cells Emerges Naturally by Microfilament Self-Organization text, January 2013

Non-equilibrium structure and dynamics in a microscopic model of thin film active gels text, January 2013

Bridging the microscopic and the hydrodynamic in active filament solutions text, January 2004

Spontaneous flow transition in active polar gels text, January 2005

Microtubule and microtubule associated protein anomalies in psychiatric disease: MAP Anomalies in Psychiatric Disease journal, May 2016

The instability of a sedimenting suspension of weakly flexible fibres journal, September 2014

Active matter at the interface between materials science and cell biology journal, July 2017

Kinesin-5-independent mitotic spindle assembly requires the antiparallel microtubule crosslinker Ase1 in fission yeast journal, May 2017

Orientational order of motile defects in active nematics journal, August 2015

Selection mechanism at the onset of active turbulence journal, February 2019

Self-straining of actively crosslinked microtubule networks journal, September 2019

Lamellar ordering, droplet formation and phase inversion in exotic active emulsions journal, February 2019

From mechanical resilience to active material properties in biopolymer networks journal, March 2019

An attraction–repulsion transition of force on wedges induced by active particles journal, January 2018

Morphological transitions of axially-driven microfilaments journal, January 2019

Self-assembling outside equilibrium: emergence of structures mediated by dissipation journal, January 2019

Dry active turbulence in a model for microtubule–motor mixtures journal, January 2019

Shape control and compartmentalization in active colloidal cells journal, August 2015

Control of active liquid crystals with a magnetic field journal, May 2016

Filament rigidity and connectivity tune the deformation modes of active biopolymer networks journal, November 2017

Extensile motor activity drives coherent motions in a model of interphase chromatin journal, October 2018

Nonequilibrium structure and dynamics in a microscopic model of thin-film active gels
journal, March 2014

Instabilities and topological defects in active nematics
journal, January 2014

Defect Annihilation and Proliferation in Active Nematics
journal, May 2013

Lennard-Jones sticks: A new model for linear molecules
journal, December 2006

Spontaneous motion in hierarchically assembled active matter
journal, November 2012

Meso-scale turbulence in living fluids
journal, August 2012

The Mechanics and Statistics of Active Matter
journal, August 2010

Polar patterns of driven filaments
journal, September 2010

Instabilities and nonlinear dynamics of concentrated active suspensions
journal, July 2013

Kinetic theory and simulations of active polar liquid crystalline polymers
journal, January 2013

Force production by single kinesin motors
journal, September 2000

Physical Properties Determining Self-Organization of Motors and Microtubules
journal, May 2001

Brownian dynamics of hard spherocylinders
journal, August 1994

Brownian motion, hydrodynamics, and the osmotic pressure
journal, February 1993

Critical bacterial concentration for the onset of collective swimming
journal, July 2009

Actively Contracting Bundles of Polar Filaments
journal, August 2000

Single kinesin molecules studied with a molecular force clamp
journal, July 1999

Tracing the phase boundaries of hard spherocylinders
journal, January 1997

Excitable Patterns in Active Nematics
journal, May 2011

A re‐examination of the phase diagram of hard spherocylinders
journal, May 1996

Instabilities and Pattern Formation in Active Particle Suspensions: Kinetic Theory and Continuum Simulations
journal, April 2008

Living liquid crystals
journal, January 2014

Cytoplasmic streaming in plant cells emerges naturally by microfilament self-organization
journal, August 2013

Nonlinear dynamics and rheology of active fluids: Simulations in two dimensions
journal, April 2011

Polarity Sorting in a Bundle of Actin Filaments by Two-Headed Myosins
journal, August 1996

Polar patterns in active fluids
journal, January 2012

Self-organization of microtubules and motors
journal, September 1997

Swimmers in Thin Films: From Swarming to Hydrodynamic Instabilities
journal, December 2010

The stress system in a suspension of force-free particles
journal, April 1970

Nonequilibrium steady states in polar active fluids
journal, January 2011

Particle-Tracking Microrheology of Living Cells: Principles and Applications
journal, June 2009

The Motion of Ellipsoidal Particles Immersed in a Viscous Fluid
journal, November 1922

Velocity Correlations in an Active Nematic
journal, September 2013

Spontaneous flow transition in active polar gels
journal, May 2005

Numerical study of the phase behavior of rodlike colloids with attractive interactions
journal, August 1997

Active nematic materials with substrate friction
journal, December 2014

Bridging the microscopic and the hydrodynamic in active filament solutions
journal, March 2005

Active suspensions and their nonlinear models
journal, June 2013

Brownian dynamics simulations of the self- and collective rotational diffusion coefficients of rigid long thin rods
journal, June 2005

Statistical hydrodynamics of ordered suspensions of self-propelled particles: waves, giant number fluctuations and instabilities
journal, April 2002

Phase behavior of two-dimensional hard rod fluids
journal, June 2000

Stability of active suspensions
journal, April 2010

Mobility measurement by analysis of fluorescence photobleaching recovery kinetics
journal, September 1976

A Quantitative Analysis of Contractility in Active Cytoskeletal Protein Networks
journal, April 2008

Eine einfache molekulare Theorie des nematischen kristallinflüssigen Zustandes
journal, July 1958

Living Liquid Crystals
journal, January 2014

Molecular Biology of the Cell
journal, January 1973

Meso-scale turbulence in living fluids
text, January 2012

Molecular biology of the cell
journal, October 1983

The Mechanics and Statistics of Active Matter
text, January 2010

Swimmers in thin films: from swarming to hydrodynamic instabilities
text, January 2010

Excitable Patterns in Active Nematics
text, January 2010

Nonlinear dynamics and rheology of active fluids: simulations in two dimensions
text, January 2010

Spontaneous motion in hierarchically assembled active matter
text, January 2013

Velocity Correlations in an Active Nematic
text, January 2013

Defect annihilation and proliferation in active nematics
text, January 2013

Cytoplasmic Streaming in Plant Cells Emerges Naturally by Microfilament Self-Organization
text, January 2013

Non-equilibrium structure and dynamics in a microscopic model of thin film active gels
text, January 2013

Bridging the microscopic and the hydrodynamic in active filament solutions
text, January 2004

Spontaneous flow transition in active polar gels
text, January 2005

Microtubule and microtubule associated protein anomalies in psychiatric disease: MAP Anomalies in Psychiatric Disease
journal, May 2016

The instability of a sedimenting suspension of weakly flexible fibres
journal, September 2014

Active matter at the interface between materials science and cell biology
journal, July 2017

Kinesin-5-independent mitotic spindle assembly requires the antiparallel microtubule crosslinker Ase1 in fission yeast
journal, May 2017

Orientational order of motile defects in active nematics
journal, August 2015

Selection mechanism at the onset of active turbulence
journal, February 2019

Self-straining of actively crosslinked microtubule networks
journal, September 2019

Lamellar ordering, droplet formation and phase inversion in exotic active emulsions
journal, February 2019

From mechanical resilience to active material properties in biopolymer networks
journal, March 2019

An attraction–repulsion transition of force on wedges induced by active particles
journal, January 2018

Morphological transitions of axially-driven microfilaments
journal, January 2019

Self-assembling outside equilibrium: emergence of structures mediated by dissipation
journal, January 2019

Dry active turbulence in a model for microtubule–motor mixtures
journal, January 2019

Shape control and compartmentalization in active colloidal cells
journal, August 2015

Control of active liquid crystals with a magnetic field
journal, May 2016

Filament rigidity and connectivity tune the deformation modes of active biopolymer networks
journal, November 2017

Extensile motor activity drives coherent motions in a model of interphase chromatin
journal, October 2018

Data-driven quantitative modeling of bacterial active nematics
journal, December 2018

Self-organized dynamics and the transition to turbulence of confined active nematics
journal, February 2019

Antipolar ordering of topological defects in active liquid crystals
journal, September 2016