Enzymatically Powered Surface‐Associated Self‐Motile Protocells

Jang, Woo‐Sik; Kim, Hyun Ji; Gao, Chen; Lee, Daeyeon; Hammer, Daniel A.

doi:10.1002/smll.201801715

Title: Enzymatically Powered Surface‐Associated Self‐Motile Protocells

Abstract

Abstract Cell motility is central to processes such as wound healing, immune cell surveillance, and embryonic development. Motility requires the conversion of chemical to mechanical energy. An active area of research is to create motile particles, such as microswimmers, using catalytic and enzymatic reactions. Here, autonomous motion is demonstrated in adhesive polymer‐based protocells by incorporating and harnessing the energy production of an enzymatic reaction. Biotinylated polymer vesicles that encapsulate catalase, an enzyme which converts hydrogen peroxide to water and oxygen, are prepared and these vesicles are adhered weakly to avidin‐coated surfaces. Upon addition of hydrogen peroxide, which diffuses across the membrane, catalase activity generates a differential impulsive force that enables the breakage and reformation of biotin–avidin bonds, leading to diffusive vesicle motion resembling random motility. The random motility requires catalase, increases with the concentration of hydrogen peroxide, and needs biotin–avidin adhesion. Thus, a protocellular mimetic of a motile cell.

Authors:

Jang, Woo‐Sik ^[1]; Kim, Hyun Ji ^[1]; Gao, Chen ^[1]; Lee, Daeyeon ^[1];

^[2]

Department of Chemical and Biomolecular Engineering School of Engineering and Applied Science University of Pennsylvania 220 South 33rd Street, 311A Towne Building Philadelphia PA 19104‐6315 USA
Department of Chemical and Biomolecular Engineering School of Engineering and Applied Science University of Pennsylvania 220 South 33rd Street, 311A Towne Building Philadelphia PA 19104‐6315 USA, Department of Bioengineering School of Engineering and Applied Science University of Pennsylvania 210 South 33rd Street, Suite 240 Skirkanich Hall Philadelphia PA 19104‐6321 USA

Publication Date:: Thu Aug 09 00:00:00 EDT 2018

Sponsoring Org.:: USDOE

OSTI Identifier:: 1463750

Grant/Contract Number:: DE‐SC000232866

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Small

Additional Journal Information:: Journal Name: Small Journal Volume: 14 Journal Issue: 36; Journal ID: ISSN 1613-6810

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: Germany

Language:: English

Citation Formats


                    Jang, Woo‐Sik, Kim, Hyun Ji, Gao, Chen, Lee, Daeyeon, and Hammer, Daniel A. Enzymatically Powered Surface‐Associated Self‐Motile Protocells.  Germany: N. p., 2018. 
Web.  doi:10.1002/smll.201801715.

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                    Jang, Woo‐Sik, Kim, Hyun Ji, Gao, Chen, Lee, Daeyeon, & Hammer, Daniel A. Enzymatically Powered Surface‐Associated Self‐Motile Protocells.  Germany.  https://doi.org/10.1002/smll.201801715

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                    Jang, Woo‐Sik, Kim, Hyun Ji, Gao, Chen, Lee, Daeyeon, and Hammer, Daniel A. Thu .  
"Enzymatically Powered Surface‐Associated Self‐Motile Protocells".  Germany.  https://doi.org/10.1002/smll.201801715.

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@article{osti_1463750,

  title        = {Enzymatically Powered Surface‐Associated Self‐Motile Protocells},

  author       = {Jang, Woo‐Sik and Kim, Hyun Ji and Gao, Chen and Lee, Daeyeon and Hammer, Daniel A.},

  abstractNote = {Abstract Cell motility is central to processes such as wound healing, immune cell surveillance, and embryonic development. Motility requires the conversion of chemical to mechanical energy. An active area of research is to create motile particles, such as microswimmers, using catalytic and enzymatic reactions. Here, autonomous motion is demonstrated in adhesive polymer‐based protocells by incorporating and harnessing the energy production of an enzymatic reaction. Biotinylated polymer vesicles that encapsulate catalase, an enzyme which converts hydrogen peroxide to water and oxygen, are prepared and these vesicles are adhered weakly to avidin‐coated surfaces. Upon addition of hydrogen peroxide, which diffuses across the membrane, catalase activity generates a differential impulsive force that enables the breakage and reformation of biotin–avidin bonds, leading to diffusive vesicle motion resembling random motility. The random motility requires catalase, increases with the concentration of hydrogen peroxide, and needs biotin–avidin adhesion. Thus, a protocellular mimetic of a motile cell.},

  doi          = {10.1002/smll.201801715},

  journal      = {Small},

  number       = 36,

  volume       = 14,

  place        = {Germany},

  year         = {Thu Aug 09 00:00:00 EDT 2018},

  month        = {Thu Aug 09 00:00:00 EDT 2018}

}

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Title: Enzymatically Powered Surface‐Associated Self‐Motile Protocells

Abstract

Citation Formats

Propulsion of a Molecular Machine by Asymmetric Distribution of Reaction Products journal, June 2005

Effect of M1–M2 Polarization on the Motility and Traction Stresses of Primary Human Macrophages journal, April 2016

Chemotactic synthetic vesicles: Design and applications in blood-brain barrier crossing journal, August 2017

Catalytic Nanomotors: Autonomous Movement of Striped Nanorods journal, October 2004

The Effect of Polymer Chain Length and Surface Density on the Adhesiveness of Functionalized Polymersomes journal, June 2004

Protein Expression, Aggregation, and Triggered Release from Polymersomes as Artificial Cell-like Structures journal, May 2012

Motility of Catalytic Nanoparticles through Self-Generated Forces journal, November 2005

Enzymatically triggered rupture of polymersomes journal, January 2016

Catalytically Induced Electrokinetics for Motors and Micropumps journal, November 2006

Substrate Catalysis Enhances Single-Enzyme Diffusion journal, February 2010

Autonomous movement of platinum-loaded stomatocytes journal, February 2012

Impulsive Enzymes: A New Force in Mechanobiology journal, January 2015

Harnessing surface-bound enzymatic reactions to organize microcapsules in solution journal, March 2016

The Role of Cell Contraction and Adhesion in Dictyostelium Motility journal, July 2010

Rapid Fabrication of Bimetallic Spherical Motors journal, August 2010

Stochastic low Reynolds number swimmers journal, April 2009

Enhanced Diffusion of Enzymes that Catalyze Exothermic Reactions journal, September 2015

Self-Propelling Nanomotors in the Presence of Strong Brownian Forces journal, April 2014

Adhesion of Antibody-Functionalized Polymersomes journal, April 2006

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Convective flow reversal in self-powered enzyme micropumps journal, February 2016

Micromotors Powered by Enzyme Catalysis journal, November 2015

Polymersomes: Tough Vesicles Made from Diblock Copolymers journal, May 1999

Self-assembly and properties of diblock copolymers by coarse-grain molecular dynamics journal, August 2004

Actin Flows Mediate a Universal Coupling between Cell Speed and Cell Persistence journal, April 2015

Macrophage motility is driven by frontal-towing with a force magnitude dependent on substrate stiffness journal, January 2015

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Harnessing catalytic pumps for directional delivery of microparticles in microchambers journal, February 2017

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Exothermicity Is Not a Necessary Condition for Enhanced Diffusion of Enzymes journal, June 2017

Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin journal, April 1995

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Molecular Weight Dependence of Polymersome Membrane Structure, Elasticity, and Stability journal, October 2002

Rapid rotation of flagellar bundles in swimming bacteria journal, February 1987

Collective cell durotaxis emerges from long-range intercellular force transmission journal, September 2016

Ligand density elicits a phenotypic switch in human neutrophils journal, January 2014

Identification of Splenic Reservoir Monocytes and Their Deployment to Inflammatory Sites journal, July 2009

Enzyme Molecules as Nanomotors journal, January 2013

Solutal and thermal buoyancy effects in self-powered phosphatase micropumps journal, January 2017

Motile Human Neutrophils Sense Ligand Density Over Their Entire Contact Area journal, July 2015

Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy journal, January 1999

Giant Vesicles: Imitating the Cytological Processes of Cell Membranes journal, December 1998

Bioelectrochemical Propulsion journal, August 2005

Propulsion of a Molecular Machine by Asymmetric Distribution of Reaction Products
journal, June 2005

Effect of M1–M2 Polarization on the Motility and Traction Stresses of Primary Human Macrophages
journal, April 2016

Chemotactic synthetic vesicles: Design and applications in blood-brain barrier crossing
journal, August 2017

Catalytic Nanomotors: Autonomous Movement of Striped Nanorods
journal, October 2004

The Effect of Polymer Chain Length and Surface Density on the Adhesiveness of Functionalized Polymersomes
journal, June 2004

Protein Expression, Aggregation, and Triggered Release from Polymersomes as Artificial Cell-like Structures
journal, May 2012

Motility of Catalytic Nanoparticles through Self-Generated Forces
journal, November 2005

Enzymatically triggered rupture of polymersomes
journal, January 2016

Catalytically Induced Electrokinetics for Motors and Micropumps
journal, November 2006

Substrate Catalysis Enhances Single-Enzyme Diffusion
journal, February 2010

Autonomous movement of platinum-loaded stomatocytes
journal, February 2012

Impulsive Enzymes: A New Force in Mechanobiology
journal, January 2015

Harnessing surface-bound enzymatic reactions to organize microcapsules in solution
journal, March 2016

The Role of Cell Contraction and Adhesion in Dictyostelium Motility
journal, July 2010

Rapid Fabrication of Bimetallic Spherical Motors
journal, August 2010

Stochastic low Reynolds number swimmers
journal, April 2009

Enhanced Diffusion of Enzymes that Catalyze Exothermic Reactions
journal, September 2015

Self-Propelling Nanomotors in the Presence of Strong Brownian Forces
journal, April 2014

Adhesion of Antibody-Functionalized Polymersomes
journal, April 2006

The heat released during catalytic turnover enhances the diffusion of an enzyme
journal, December 2014

The Effect of Stabilizer on the Mechanical Response of Double-Emulsion-Templated Polymersomes
journal, December 2014

Convective flow reversal in self-powered enzyme micropumps
journal, February 2016

Micromotors Powered by Enzyme Catalysis
journal, November 2015

Polymersomes: Tough Vesicles Made from Diblock Copolymers
journal, May 1999

Self-assembly and properties of diblock copolymers by coarse-grain molecular dynamics
journal, August 2004

Actin Flows Mediate a Universal Coupling between Cell Speed and Cell Persistence
journal, April 2015

Macrophage motility is driven by frontal-towing with a force magnitude dependent on substrate stiffness
journal, January 2015

Dendritic Cells Distinguish Individual Chemokine Signals through CCR7 and CXCR4
journal, November 2010

Mechanical Response of a Small Swimmer Driven by Conformational Transitions
journal, January 2008

Harnessing catalytic pumps for directional delivery of microparticles in microchambers
journal, February 2017

Synthesis and Characterization of Model Polyalkane−Poly(ethylene oxide) Block Copolymers
journal, January 1996

Exothermicity Is Not a Necessary Condition for Enhanced Diffusion of Enzymes
journal, June 2017

Hemostatic, inflammatory, and fibroblast responses are blunted in mice lacking gelsolin
journal, April 1995

Chemically Propelled Molecules and Machines
journal, May 2017

Molecular Weight Dependence of Polymersome Membrane Structure, Elasticity, and Stability
journal, October 2002

Rapid rotation of flagellar bundles in swimming bacteria
journal, February 1987

Collective cell durotaxis emerges from long-range intercellular force transmission
journal, September 2016

Ligand density elicits a phenotypic switch in human neutrophils
journal, January 2014

Identification of Splenic Reservoir Monocytes and Their Deployment to Inflammatory Sites
journal, July 2009

Enzyme Molecules as Nanomotors
journal, January 2013

Solutal and thermal buoyancy effects in self-powered phosphatase micropumps
journal, January 2017

Motile Human Neutrophils Sense Ligand Density Over Their Entire Contact Area
journal, July 2015

Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy
journal, January 1999

Giant Vesicles: Imitating the Cytological Processes of Cell Membranes
journal, December 1998

Bioelectrochemical Propulsion
journal, August 2005