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Title: Cytoskeletal motor-driven active self-assembly in in vitro systems

Abstract

Molecular motor-driven self-assembly has been an active area of soft matter research for the past decade. Because molecular motors transform chemical energy into mechanical work, systems which employ molecular motors to drive self-assembly processes are able to overcome kinetic and thermodynamic limits on assembly time, size, complexity, and structure. Here, we review the progress in elucidating and demonstrating the rules and capabilities of motor-driven active self-assembly. Lastly, we focus on the types of structures created and the degree of control realized over these structures, and discuss the next steps necessary to achieve the full potential of this assembly mode which complements robotic manipulation and passive self-assembly.

Authors:
 [1];  [2];  [3];  [1];  [2];  [4]
  1. Columbia Univ., New York, NY (United States). Dept. of Biomedical Engineering
  2. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States). Nanosystems Synthesis/Analysis Dept.
  3. Hokkaido Univ., Sapporo (Japan). Faculty of Science
  4. Hokkaido Univ., Sapporo (Japan). Faculty of Science. Graduate School of Chemical Sciences and Engineering
Publication Date:
Research Org.:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States); Columbia Univ., New York, NY (United States); Hokkaido Univ., Sapporo (Japan)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); US Army Research Office (ARO); Japan Society for the Promotion of Science (Japan)
OSTI Identifier:
1335667
Alternate Identifier(s):
OSTI ID: 1343058
Report Number(s):
SAND-2016-9575J; SAND2016-7201J
Journal ID: ISSN 1744-683X; SMOABF; 649560
Grant/Contract Number:  
AC04-94AL85000; W911NF-13-1-0390; 24104004
Resource Type:
Accepted Manuscript
Journal Name:
Soft Matter
Additional Journal Information:
Journal Volume: 12; Journal Issue: 4; Journal ID: ISSN 1744-683X
Publisher:
Royal Society of Chemistry
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Lam, A. T., VanDelinder, V., Kabir, A. M. R., Hess, H., Bachand, G. D., and Kakugo, A. Cytoskeletal motor-driven active self-assembly in in vitro systems. United States: N. p., 2015. Web. doi:10.1039/c5sm02042e.
Lam, A. T., VanDelinder, V., Kabir, A. M. R., Hess, H., Bachand, G. D., & Kakugo, A. Cytoskeletal motor-driven active self-assembly in in vitro systems. United States. doi:https://doi.org/10.1039/c5sm02042e
Lam, A. T., VanDelinder, V., Kabir, A. M. R., Hess, H., Bachand, G. D., and Kakugo, A. Wed . "Cytoskeletal motor-driven active self-assembly in in vitro systems". United States. doi:https://doi.org/10.1039/c5sm02042e. https://www.osti.gov/servlets/purl/1335667.
@article{osti_1335667,
title = {Cytoskeletal motor-driven active self-assembly in in vitro systems},
author = {Lam, A. T. and VanDelinder, V. and Kabir, A. M. R. and Hess, H. and Bachand, G. D. and Kakugo, A.},
abstractNote = {Molecular motor-driven self-assembly has been an active area of soft matter research for the past decade. Because molecular motors transform chemical energy into mechanical work, systems which employ molecular motors to drive self-assembly processes are able to overcome kinetic and thermodynamic limits on assembly time, size, complexity, and structure. Here, we review the progress in elucidating and demonstrating the rules and capabilities of motor-driven active self-assembly. Lastly, we focus on the types of structures created and the degree of control realized over these structures, and discuss the next steps necessary to achieve the full potential of this assembly mode which complements robotic manipulation and passive self-assembly.},
doi = {10.1039/c5sm02042e},
journal = {Soft Matter},
number = 4,
volume = 12,
place = {United States},
year = {2015},
month = {11}
}

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Cited by: 11 works
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Works referenced in this record:

Growth of ring-shaped microtubule assemblies through stepwise active self-organisation
journal, January 2013

  • Inoue, Daisuke; Kabir, Arif Md. Rashedul; Mayama, Hiroyuki
  • Soft Matter, Vol. 9, Issue 29
  • DOI: 10.1039/c3sm50704a

Molecular wear of microtubules propelled by surface-adhered kinesins
journal, January 2015

  • Dumont, Emmanuel L. P.; Do, Catherine; Hess, Henry
  • Nature Nanotechnology, Vol. 10, Issue 2
  • DOI: 10.1038/nnano.2014.334

Topological defects and density fluctuations in collectively moving systems
journal, March 2013

  • Schaller, V.; Bausch, A. R.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 12
  • DOI: 10.1073/pnas.1215368110

Depletion force induced collective motion of microtubules driven by kinesin
journal, January 2015

  • Inoue, Daisuke; Mahmot, Bulbul; Kabir, Arif Md. Rashedul
  • Nanoscale, Vol. 7, Issue 43
  • DOI: 10.1039/C5NR02213D

Crosslinking proteins modulate the self-organization of driven systems
journal, January 2013

  • Schaller, Volker; Schmoller, Kurt M.; Karaköse, Esra
  • Soft Matter, Vol. 9, Issue 30
  • DOI: 10.1039/c3sm50506e

Why Microtubules Run in Circles: Mechanical Hysteresis of the Tubulin Lattice
journal, April 2015


Microtubule nanospool formation by active self-assembly is not initiated by thermal activation
journal, January 2011

  • Luria, Isaac; Crenshaw, Jasmine; Downs, Matthew
  • Soft Matter, Vol. 7, Issue 7
  • DOI: 10.1039/C0SM00802H

Prolongation of the Active Lifetime of a Biomolecular Motor for in Vitro Motility Assay by Using an Inert Atmosphere
journal, November 2011

  • Kabir, Arif Md. Rashedul; Inoue, Daisuke; Kakugo, Akira
  • Langmuir, Vol. 27, Issue 22
  • DOI: 10.1021/la202467f

A compositional framework for programming stochastically interacting robots
journal, January 2011

  • Napp, Nils; Klavins, Eric
  • The International Journal of Robotics Research, Vol. 30, Issue 6
  • DOI: 10.1177/0278364911403018

Actin-binding proteins sensitively mediate F-actin bundle stiffness
journal, August 2006

  • Claessens, Mireille M. A. E.; Bathe, Mark; Frey, Erwin
  • Nature Materials, Vol. 5, Issue 9
  • DOI: 10.1038/nmat1718

Directed self-assembly of 1D microtubule nano-arrays
journal, January 2014

  • Bachand, M.; Bouxsein, N. F.; Cheng, S.
  • RSC Adv., Vol. 4, Issue 97
  • DOI: 10.1039/C4RA11765D

Ring-Shaped Assembly of Microtubules Shows Preferential Counterclockwise Motion
journal, September 2008

  • Kawamura, Ryuzo; Kakugo, Akira; Shikinaka, Kazuhiro
  • Biomacromolecules, Vol. 9, Issue 9
  • DOI: 10.1021/bm800639w

Dynamic assembly of polymer nanotube networks via kinesin powered microtubule filaments
journal, January 2015

  • Paxton, Walter F.; Bouxsein, Nathan F.; Henderson, Ian M.
  • Nanoscale, Vol. 7, Issue 25
  • DOI: 10.1039/C5NR00826C

Programmable self-assembly in a thousand-robot swarm
journal, August 2014


Utilization of Myosin and Actin Bundles for the Transport of Molecular Cargo
journal, January 2010


Active self-organization of microtubules in an inert chamber system
journal, April 2012

  • Kabir, Arif Md. Rashedul; Inoue, Daisuke; Kakugo, Akira
  • Polymer Journal, Vol. 44, Issue 6
  • DOI: 10.1038/pj.2012.26

Polar patterns of driven filaments
journal, September 2010

  • Schaller, Volker; Weber, Christoph; Semmrich, Christine
  • Nature, Vol. 467, Issue 7311
  • DOI: 10.1038/nature09312

Dispersion in Active Transport by Kinesin-Powered Molecular Shuttles
journal, July 2005


Formation of motile assembly of microtubules driven by kinesins
journal, November 2011


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


Photodamage and the Importance of Photoprotection in Biomolecular-Powered Device Applications
journal, December 2013

  • VanDelinder, Virginia; Bachand, George D.
  • Analytical Chemistry, Vol. 86, Issue 1
  • DOI: 10.1021/ac403187g

Self-assembly driven by molecular motors
journal, January 2006


Effect of length and rigidity of microtubules on the size of ring-shaped assemblies obtained through active self-organization
journal, January 2015

  • Wada, Shoki; Rashedul Kabir, Arif Md.; Ito, Masaki
  • Soft Matter, Vol. 11, Issue 6
  • DOI: 10.1039/C4SM02292K

Switchable Static and Dynamic Self-Assembly of Magnetic Droplets on Superhydrophobic Surfaces
journal, July 2013


Kinesin follows the microtubule's protofilament axis
journal, June 1993


Self-Assembly at All Scales
journal, March 2002

  • Whitesides, George M.; Grzybowski, Bartosz
  • Science, Vol. 295, Issue 5564, p. 2418-2421
  • DOI: 10.1126/science.1070821

Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape
journal, February 1993


Unidirectional Adsorbate Motion on a High-Symmetry Surface: “Walking” Molecules Can Stay the Course
journal, October 2005


Tracking the ends: a dynamic protein network controls the fate of microtubule tips
journal, April 2008

  • Akhmanova, Anna; Steinmetz, Michel O.
  • Nature Reviews Molecular Cell Biology, Vol. 9, Issue 4
  • DOI: 10.1038/nrm2369

Selective Formation of a Linear-Shaped Bundle of Microtubules
journal, January 2010

  • Kawamura, Ryuzo; Kakugo, Akira; Osada, Yoshihito
  • Langmuir, Vol. 26, Issue 1
  • DOI: 10.1021/la902197f

Formation of ring-shaped assembly of microtubules with a narrow size distribution at an air–buffer interface
journal, January 2012

  • Rashedul Kabir, Arif Md.; Wada, Shoki; Inoue, Daisuke
  • Soft Matter, Vol. 8, Issue 42
  • DOI: 10.1039/c2sm26441b

New data on the microtubule surface lattice
journal, January 1991


A Cellular Automaton Approach to the Simulation of Active Self-Assembly of Kinesin-Powered Molecular Shuttles
journal, October 2011

  • Crenshaw, Jasmine D.; Liang, Tao; Hess, Henry
  • Journal of Computational and Theoretical Nanoscience, Vol. 8, Issue 10
  • DOI: 10.1166/jctn.2011.1916

Controlling self-assembly of microtubule spools via kinesin motor density
journal, January 2014

  • Lam, A. T.; Curschellas, C.; Krovvidi, D.
  • Soft Matter, Vol. 10, Issue 43
  • DOI: 10.1039/C4SM01518E

Large-scale vortex lattice emerging from collectively moving microtubules
journal, March 2012

  • Sumino, Yutaka; Nagai, Ken H.; Shitaka, Yuji
  • Nature, Vol. 483, Issue 7390
  • DOI: 10.1038/nature10874

Dynamic self-organization and polymorphism of microtubule assembly through active interactions with kinesin
journal, January 2011

  • Tamura, Yoshiki; Kawamura, Ryuzo; Shikinaka, Kazuhiro
  • Soft Matter, Vol. 7, Issue 12
  • DOI: 10.1039/c1sm05413a

Transport and self-organization across different length scales powered by motor proteins and programmed by DNA
journal, November 2013

  • Wollman, Adam J. M.; Sanchez-Cano, Carlos; Carstairs, Helen M. J.
  • Nature Nanotechnology, Vol. 9, Issue 1
  • DOI: 10.1038/nnano.2013.230

Biomolecular Motor-Powered Self-Assembly of Dissipative Nanocomposite Rings
journal, December 2008

  • Liu, Haiqing; Spoerke, Erik D.; Bachand, Marlene
  • Advanced Materials, Vol. 20, Issue 23
  • DOI: 10.1002/adma.200801291

Nanoscale Transport Enables Active Self-Assembly of Millimeter-Scale Wires
journal, December 2011

  • Idan, Ofer; Lam, Amy; Kamcev, Jovan
  • Nano Letters, Vol. 12, Issue 1
  • DOI: 10.1021/nl203450h

Understanding energy dissipation and thermodynamics in biomotor-driven nanocomposite assemblies
journal, January 2011


Self-organization of microtubules and motors
journal, September 1997

  • Ndlec, F. J.; Surrey, T.; Maggs, A. C.
  • Nature, Vol. 389, Issue 6648
  • DOI: 10.1038/38532

Microtubule bundle formation driven by ATP: the effect of concentrations of kinesin, streptavidin and microtubules
journal, March 2010


Principles and Implementations of Dissipative (Dynamic) Self-Assembly
journal, February 2006

  • Fialkowski, Marcin; Bishop, Kyle J. M.; Klajn, Rafal
  • The Journal of Physical Chemistry B, Vol. 110, Issue 6
  • DOI: 10.1021/jp054153q

Molecular Self-Assembly of “Nanowires” and “Nanospools” Using Active Transport
journal, April 2005

  • Hess, Henry; Clemmens, John; Brunner, Christian
  • Nano Letters, Vol. 5, Issue 4
  • DOI: 10.1021/nl0478427

Cilia-Like Beating of Active Microtubule Bundles
journal, July 2011


Frozen steady states in active systems
journal, November 2011

  • Schaller, V.; Weber, C. A.; Hammerich, B.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 48
  • DOI: 10.1073/pnas.1107540108

Asters, Vortices, and Rotating Spirals in Active Gels of Polar Filaments
journal, February 2004


Toward complex matter: Supramolecular chemistry and self-organization
journal, April 2002


Polarity and Motility of Large Polymer−Actin Complexes
journal, March 2005

  • Kakugo, Akira; Shikinaka, Kazuhiro; Takekawa, Nozomi
  • Biomacromolecules, Vol. 6, Issue 2
  • DOI: 10.1021/bm0494038

Controlling the Bias of Rotational Motion of Ring-Shaped Microtubule Assembly
journal, December 2014

  • Wada, Shoki; Kabir, Arif Md. Rashedul; Kawamura, Ryuzo
  • Biomacromolecules, Vol. 16, Issue 1
  • DOI: 10.1021/bm501573v

Simulating molecular shuttle movements: Towards computer-aided design of nanoscale transport systems
journal, January 2006

  • Nitta, Takahiro; Tanahashi, Akihito; Hirano, Motohisa
  • Lab on a Chip, Vol. 6, Issue 7
  • DOI: 10.1039/b601754a

Formation of ring-shaped microtubule assemblies through active self-organization on dynein
journal, December 2013

  • Ito, Masaki; Kabir, Arif Md. Rashedul; Inoue, Daisuke
  • Polymer Journal, Vol. 46, Issue 4
  • DOI: 10.1038/pj.2013.89

Biomolecular motors
journal, December 2005


Physical Factors Affecting Kinesin-Based Transport of Synthetic Nanoparticle Cargo
journal, May 2005

  • Bachand, Marlene; Trent, Amanda M.; Bunker, Bruce C.
  • Journal of Nanoscience and Nanotechnology, Vol. 5, Issue 5
  • DOI: 10.1166/jnn.2005.112

Biologistics and the Struggle for Efficiency: Concepts and Perspectives
journal, December 2009

  • Helbing, Dirk; Deutsch, Andreas; Diez, Stefan
  • Advances in Complex Systems, Vol. 12, Issue 06
  • DOI: 10.1142/S0219525909002374

A Continuous Network of Lipid Nanotubes Fabricated from the Gliding Motility of Kinesin Powered Microtubule Filaments
journal, February 2013

  • Bouxsein, Nathan F.; Carroll-Portillo, Amanda; Bachand, Marlene
  • Langmuir, Vol. 29, Issue 9
  • DOI: 10.1021/la304238u

Controlled Clockwise–Counterclockwise Motion of the Ring-Shaped Microtubules Assembly
journal, October 2011

  • Kakugo, Akira; Kabir, Arif Md. Rashedul; Hosoda, Natsuki
  • Biomacromolecules, Vol. 12, Issue 10
  • DOI: 10.1021/bm200829t

    Works referencing / citing this record:

    Non-equilibrium assembly of microtubules: from molecules to autonomous chemical robots
    journal, January 2017

    • Hess, H.; Ross, Jennifer L.
    • Chemical Society Reviews, Vol. 46, Issue 18
    • DOI: 10.1039/c7cs00030h

    Molecular Encapsulation Inside Microtubules Based on Tau-Derived Peptides
    journal, September 2018

    • Inaba, Hiroshi; Yamamoto, Takahisa; Kabir, Arif Md. Rashedul
    • Chemistry - A European Journal, Vol. 24, Issue 56
    • DOI: 10.1002/chem.201802617

    DNA-assisted swarm control in a biomolecular motor system
    journal, January 2018

    • Keya, Jakia Jannat; Suzuki, Ryuhei; Kabir, Arif Md. Rashedul
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-017-02778-5

    Mechanical oscillation of dynamic microtubule rings
    journal, January 2016

    • Ito, Masaki; Rashedul Kabir, Arif Md.; Islam, Md. Sirajul
    • RSC Advances, Vol. 6, Issue 73
    • DOI: 10.1039/c6ra16613j

    Construction of artificial cilia from microtubules and kinesins through a well-designed bottom-up approach
    journal, January 2018

    • Sasaki, Ren; Kabir, Arif Md. Rashedul; Inoue, Daisuke
    • Nanoscale, Vol. 10, Issue 14
    • DOI: 10.1039/c7nr05099b

    How non-bonding domains affect the active assembly of microtubule spools
    journal, January 2019

    • Martinez, Haneen; VanDelinder, Virginia; Imam, Zachary I.
    • Nanoscale, Vol. 11, Issue 24
    • DOI: 10.1039/c9nr02059d

    The model of local axon homeostasis - explaining the role and regulation of microtubule bundles in axon maintenance and pathology
    journal, November 2019