Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces

Mahajan, Kalpesh D.; Cui, Yixiao; Dorcéna, C. Jenny; Bouxsien, Nathan F.; Bachand, George D.; Chalmers, Jeffrey J.; Winter, Jessica O.

doi:10.1002/biot.201700402

Title: Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces

Abstract

The microtubule (MT)‐kinesin system has been extensively studied because of its role in cellular processes, as well as its potential use for controllably transporting objects at the nanoscale. Thus, there is substantial interest in methods to evaluate MT properties, including bending radius and the binding energy of kinesin motor proteins to MT tracks. Current methods to identify these properties include optical tweezers, microfluidic devices, and magnetic fields. Here, the use of magnetic quantum dots (i.e., MagDots) is evaluated as a method to study MT‐kinesin interactions via applied magnetic forces. Magnetic fields are generated using a magnetic needle whose field gradient is quantified by finite element modeling (FEM). Magnetic force is applied to MagDot‐labeled MTs and demonstrated sufficient to steer and detach MTs from kinesin‐coated surfaces. Taking advantage of the dual‐functionality of MagDots, the magnetic force experienced by a single MagDot and the number of MagDots on MTs are determined. The total force exerted on MTs by MagDots is estimated to be ≈0.94–2.47 pN. This approach could potentially be used to interrogate MT properties and MT‐kinesin interactions, enhancing our biological understanding of this system and enabling further development of MT shuttles for nanotransport.

Authors:

Mahajan, Kalpesh D. ^[1]; Cui, Yixiao ^[2]; Dorcéna, C. Jenny ^[1]; Bouxsien, Nathan F. ^[3];

^[3];

^[1];

^[4]

William G. Lowrie Department of Chemical and Biomolecular Engineering, The Ohio State University Columbus OH USA
Department of Biomedical Engineering, The Ohio State University Columbus OH USA
Center for Integrated Nanotechnologies, Sandia National Laboratories Albuquerque NM USA
William G. Lowrie Department of Chemical and Biomolecular Engineering, The Ohio State University Columbus OH USA, Department of Biomedical Engineering, The Ohio State University Columbus OH USA

Publication Date:: Mon Oct 09 00:00:00 EDT 2017

Sponsoring Org.:: USDOE

OSTI Identifier:: 1398723

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Biotechnology Journal

Additional Journal Information:: Journal Name: Biotechnology Journal Journal Volume: 13 Journal Issue: 1; Journal ID: ISSN 1860-6768

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: Germany

Language:: English

Citation Formats


                    Mahajan, Kalpesh D., Cui, Yixiao, Dorcéna, C. Jenny, Bouxsien, Nathan F., Bachand, George D., Chalmers, Jeffrey J., and Winter, Jessica O. Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces.  Germany: N. p., 2017. 
Web.  doi:10.1002/biot.201700402.

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                    Mahajan, Kalpesh D., Cui, Yixiao, Dorcéna, C. Jenny, Bouxsien, Nathan F., Bachand, George D., Chalmers, Jeffrey J., & Winter, Jessica O. Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces.  Germany.  https://doi.org/10.1002/biot.201700402

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                    Mahajan, Kalpesh D., Cui, Yixiao, Dorcéna, C. Jenny, Bouxsien, Nathan F., Bachand, George D., Chalmers, Jeffrey J., and Winter, Jessica O. Mon .  
"Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces".  Germany.  https://doi.org/10.1002/biot.201700402.

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@article{osti_1398723,

  title        = {Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces},

  author       = {Mahajan, Kalpesh D. and Cui, Yixiao and Dorcéna, C. Jenny and Bouxsien, Nathan F. and Bachand, George D. and Chalmers, Jeffrey J. and Winter, Jessica O.},

  abstractNote = {The microtubule (MT)‐kinesin system has been extensively studied because of its role in cellular processes, as well as its potential use for controllably transporting objects at the nanoscale. Thus, there is substantial interest in methods to evaluate MT properties, including bending radius and the binding energy of kinesin motor proteins to MT tracks. Current methods to identify these properties include optical tweezers, microfluidic devices, and magnetic fields. Here, the use of magnetic quantum dots (i.e., MagDots) is evaluated as a method to study MT‐kinesin interactions via applied magnetic forces. Magnetic fields are generated using a magnetic needle whose field gradient is quantified by finite element modeling (FEM). Magnetic force is applied to MagDot‐labeled MTs and demonstrated sufficient to steer and detach MTs from kinesin‐coated surfaces. Taking advantage of the dual‐functionality of MagDots, the magnetic force experienced by a single MagDot and the number of MagDots on MTs are determined. The total force exerted on MTs by MagDots is estimated to be ≈0.94–2.47 pN. This approach could potentially be used to interrogate MT properties and MT‐kinesin interactions, enhancing our biological understanding of this system and enabling further development of MT shuttles for nanotransport.},

  doi          = {10.1002/biot.201700402},

  journal      = {Biotechnology Journal},

  number       = 1,

  volume       = 13,

  place        = {Germany},

  year         = {Mon Oct 09 00:00:00 EDT 2017},

  month        = {Mon Oct 09 00:00:00 EDT 2017}

}

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Title: Magnetic Quantum Dots Steer and Detach Microtubules From Kinesin‐Coated Surfaces

Abstract

Citation Formats

Linear Arrangement of Motor Protein on a Mechanically Deposited Fluoropolymer Thin Film journal, July 1995

Equilibrium and Transition between Single- and Double-Headed Binding of Kinesin as Revealed by Single-Molecule Mechanics journal, February 2003

Effect of Path Persistence Length of Molecular Shuttles on Two-stage Analyte Capture in Biosensors journal, December 2012

Kinesin Motor Mechanics: Binding, Stepping, Tracking, Gating, and Limping journal, May 2007

Simultaneous Magnetic Manipulation and Fluorescent Tracking of Multiple Individual Hybrid Nanostructures journal, June 2010

Ratchet patterns sort molecular shuttles journal, August 2002

Millimeter Scale Alignment of Magnetic Nanoparticle Functionalized Microtubules in Magnetic Fields journal, November 2005

Controlling kinesin motor proteins in nanoengineered systems through a metal-binding on/off switch journal, October 2008

Light-Controlled Molecular Shuttles Made from Motor Proteins Carrying Cargo on Engineered Surfaces journal, May 2001

Efficient Designs for Powering Microscale Devices with Nanoscale Biomolecular Motors journal, February 2006

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

Effects of potential environmental interferents on kinesin-powered molecular shuttles journal, January 2012

Directing Transport of CoFe2O4-Functionalized Microtubules with Magnetic Fields journal, January 2007

Probing the kinesin reaction cycle with a 2D optical force clamp journal, February 2003

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

Microtubule-based nanomaterials: Exploiting nature's dynamic biopolymers: Microtubule-Based Nanomaterials journal, April 2015

Biomolecular motors at the intersection of nanotechnology and polymer science journal, January 2010

Molecular shuttles powered by motor proteins: loading and unloading stations for nanocargo integrated into one device journal, January 2010

Steering microtubule shuttle transport with dynamically controlled magnetic fields journal, January 2016

Powering Nanodevices with Biomolecular Motors journal, May 2004

A metal switch for controlling the activity of molecular motor proteins journal, December 2011

Reversible Switching of Microtubule Motility Using Thermoresponsive Polymer Surfaces journal, September 2006

Kinetics of force generation by single kinesin molecules activated by laser photolysis of caged ATP journal, April 1997

Cytoskeletal motor-driven active self-assembly in in vitro systems journal, January 2016

Complete ON/OFF Photoswitching of the Motility of a Nanobiomolecular Machine journal, April 2014

Reversible control of kinesin activity and microtubule gliding speeds by switching the doping states of a conducting polymer support journal, January 2007

Molecular Sorting by Electrical Steering of Microtubules in Kinesin-Coated Channels journal, May 2006

Assembly and Transport of Nanocrystal CdSe Quantum Dot Nanocomposites Using Microtubules and Kinesin Motor Proteins journal, May 2004

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

Microtubule Alignment and Manipulation Using AC Electrokinetics journal, September 2008

Scalable, Semicontinuous Production of Micelles Encapsulating Nanoparticles via Electrospray journal, March 2014

Advanced Optical Imaging Reveals the Dependence of Particle Geometry on Interactions Between CdSe Quantum Dots and Immune Cells journal, December 2010

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

Patterns of molecular motors that guide and sort filaments journal, January 2012

Linear Arrangement of Motor Protein on a Mechanically Deposited Fluoropolymer Thin Film
journal, July 1995

Equilibrium and Transition between Single- and Double-Headed Binding of Kinesin as Revealed by Single-Molecule Mechanics
journal, February 2003

Effect of Path Persistence Length of Molecular Shuttles on Two-stage Analyte Capture in Biosensors
journal, December 2012

Kinesin Motor Mechanics: Binding, Stepping, Tracking, Gating, and Limping
journal, May 2007

Simultaneous Magnetic Manipulation and Fluorescent Tracking of Multiple Individual Hybrid Nanostructures
journal, June 2010

Ratchet patterns sort molecular shuttles
journal, August 2002

Millimeter Scale Alignment of Magnetic Nanoparticle Functionalized Microtubules in Magnetic Fields
journal, November 2005

Controlling kinesin motor proteins in nanoengineered systems through a metal-binding on/off switch
journal, October 2008

Light-Controlled Molecular Shuttles Made from Motor Proteins Carrying Cargo on Engineered Surfaces
journal, May 2001

Efficient Designs for Powering Microscale Devices with Nanoscale Biomolecular Motors
journal, February 2006

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

Effects of potential environmental interferents on kinesin-powered molecular shuttles
journal, January 2012

Directing Transport of CoFe2O4-Functionalized Microtubules with Magnetic Fields
journal, January 2007

Probing the kinesin reaction cycle with a 2D optical force clamp
journal, February 2003

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

Microtubule-based nanomaterials: Exploiting nature's dynamic biopolymers: Microtubule-Based Nanomaterials
journal, April 2015

Biomolecular motors at the intersection of nanotechnology and polymer science
journal, January 2010

Molecular shuttles powered by motor proteins: loading and unloading stations for nanocargo integrated into one device
journal, January 2010

Steering microtubule shuttle transport with dynamically controlled magnetic fields
journal, January 2016

Powering Nanodevices with Biomolecular Motors
journal, May 2004

A metal switch for controlling the activity of molecular motor proteins
journal, December 2011

Reversible Switching of Microtubule Motility Using Thermoresponsive Polymer Surfaces
journal, September 2006

Kinetics of force generation by single kinesin molecules activated by laser photolysis of caged ATP
journal, April 1997

Cytoskeletal motor-driven active self-assembly in in vitro systems
journal, January 2016

Complete ON/OFF Photoswitching of the Motility of a Nanobiomolecular Machine
journal, April 2014

Reversible control of kinesin activity and microtubule gliding speeds by switching the doping states of a conducting polymer support
journal, January 2007

Molecular Sorting by Electrical Steering of Microtubules in Kinesin-Coated Channels
journal, May 2006

Assembly and Transport of Nanocrystal CdSe Quantum Dot Nanocomposites Using Microtubules and Kinesin Motor Proteins
journal, May 2004

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

Microtubule Alignment and Manipulation Using AC Electrokinetics
journal, September 2008

Scalable, Semicontinuous Production of Micelles Encapsulating Nanoparticles via Electrospray
journal, March 2014

Advanced Optical Imaging Reveals the Dependence of Particle Geometry on Interactions Between CdSe Quantum Dots and Immune Cells
journal, December 2010

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

Patterns of molecular motors that guide and sort filaments
journal, January 2012