skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Mechanisms underlying the active self-assembly of microtubule rings and spools

Journal Article · · Biomacromolecules
 [1];  [1];  [1]
  1. Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)

Here, active self-assembly offers a powerful route for the creation of dynamic multiscale structures that are presently inaccessible with standard microfabrication techniques. One such system uses the translation of microtubule filaments by surface-tethered kinesin to actively assemble nanocomposites with bundle, ring, and spool morphologies. Attempts to observe mechanisms involved in this active assembly system have been hampered by experimental difficulties with performing observation during buffer exchange and photodamage from fluorescent excitation. In the present work, we used a custom microfluidic device to remove these limitations and directly study ring/spool formation, including the earliest events (nucleation) that drive subsequent nanocomposite assembly. Three distinct formation events were observed: pinning, collisions, and induced curvature. Of these three, collisions accounted for the majority of event leading to ring/spool formation, while the rate of pinning was shown to be dependent on the amount of photodamage in the system. We further showed that formation mechanism directly affects the diameter and rotation direction of the resultant rings and spools. Overall, the fundamental understanding described in this work provides a foundation by which the properties of motor-driven, actively assembled nanocomposites may be tailored toward specific applications.

Research Organization:
Sandia National Lab. (SNL-NM), Albuquerque, NM (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES); USDOE National Nuclear Security Administration (NNSA)
Grant/Contract Number:
AC04-94AL85000
OSTI ID:
1249084
Report Number(s):
SAND-2016-2347J; 621994
Journal Information:
Biomacromolecules, Vol. 17, Issue 3; ISSN 1525-7797
Publisher:
American Chemical SocietyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 14 works
Citation information provided by
Web of Science

References (35)

Flexural Rigidity of Individual Microtubules Measured by a Buckling Force with Optical Traps journal March 2006
Silver Nanoparticle and Nanowire Formation by Microtubule Templates journal August 2004
Why Microtubules Run in Circles: Mechanical Hysteresis of the Tubulin Lattice journal April 2015
Measurement of ligand-receptor interactions. journal September 1991
Microtubule nanospool formation by active self-assembly is not initiated by thermal activation journal January 2011
Controlling self-assembly of microtubule spools via kinesin motor density journal January 2014
Analysis of Microtubule Curvature book January 2007
Biomolecular Motor-Powered Self-Assembly of Dissipative Nanocomposite Rings journal December 2008
Understanding energy dissipation and thermodynamics in biomotor-driven nanocomposite assemblies journal January 2011
Ring-Shaped Assembly of Microtubules Shows Preferential Counterclockwise Motion journal September 2008
Dynamic assembly of polymer nanotube networks via kinesin powered microtubule filaments journal January 2015
Molecular Self-Assembly of “Nanowires” and “Nanospools” Using Active Transport journal April 2005
Force and velocity measured for single kinesin molecules journal June 1994
Actomyosin-based Retrograde Flow of Microtubules in the Lamella of Migrating Epithelial Cells Influences Microtubule Dynamic Instability and Turnover and Is Associated with Microtubule Breakage and Treadmilling journal October 1997
Behavior of Kinesin Driven Quantum Dots Trapped in a Microtubule Loop journal October 2015
Microtubule-Templated Cadmium Sulfide Nanotube Assemblies journal March 2014
A Piconewton Forcemeter Assembled from Microtubules and Kinesins journal September 2002
Effects of Confinement on Molecular Motor-Driven Self-Assembly of Ring Structures journal November 2012
Frozen steady states in active systems journal November 2011
Photodamage and the Importance of Photoprotection in Biomolecular-Powered Device Applications journal December 2013
Quantum-dot-assisted characterization of microtubule rotations during cargo transport journal August 2008
Cytoskeletal motor-driven active self-assembly in in vitro systems journal January 2016
Rigidity of microtubules is increased by stabilizing agents journal August 1995
Effect of length and rigidity of microtubules on the size of ring-shaped assemblies obtained through active self-organization journal January 2015
Controlling the Bias of Rotational Motion of Ring-Shaped Microtubule Assembly journal December 2014
Kinesin follows the microtubule's protofilament axis journal June 1993
Single Filament Behavior of Microtubules in the Presence of Added Divalent Counterions journal September 2014
Biomolecular motors in nanoscale materials, devices, and systems: Biomolecular motors in nanoscale materials, devices, and systems
  • Bachand, George D.; Bouxsein, Nathan F.; VanDelinder, Virginia
  • Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology, Vol. 6, Issue 2 https://doi.org/10.1002/wnan.1252
journal December 2013
Model for the orientational ordering of the plant microtubule cortical array journal July 2010
Microtubule-Templated Biomimetic Mineralization of Lepidocrocite journal January 2004
Microtubule-Based Gold Nanowires and Nanowire Arrays journal September 2008
The Solution to the Streptavidin-Biotin Paradox: The Influence of History on the Strength of Single Molecular Bonds journal December 2005
A Continuous Network of Lipid Nanotubes Fabricated from the Gliding Motility of Kinesin Powered Microtubule Filaments journal February 2013
Controlled Clockwise–Counterclockwise Motion of the Ring-Shaped Microtubules Assembly journal October 2011
Flexural rigidity of microtubules measured with the use of optical tweezers journal February 1996

Cited By (6)

From isolated structures to continuous networks: A categorization of cytoskeleton‐based motile engineered biological microstructures journal February 2019
How non-bonding domains affect the active assembly of microtubule spools journal January 2019
Curvature-Sensitive Kinesin Binding Can Explain Microtubule Ring Formation and Reveals Chaotic Dynamics in a Mathematical Model journal September 2018
Instabilities and Spatiotemporal Dynamics of Active Elastic Filaments posted_content August 2019
The model of local axon homeostasis - explaining the role and regulation of microtubule bundles in axon maintenance and pathology journal November 2019
Curvature-sensitive kinesin binding can explain microtubule ring formation and reveals chaotic dynamics in a mathematical model preprint January 2018