Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy

Jiang, Xi; Spencer, Ryan K.; Sun, Jing; Ophus, Colin; Zuckermann, Ronald N.; Downing, Kenneth H.; Balsara, Nitash P.

doi:10.1021/acs.jpcb.8b11752

Title: Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy

Abstract

Vesicle formation in a series of amphiphilic sequence-defined polypeptoid block co-polymers comprising a phosphonated hydrophilic block and an amorphous hydrophobic block, poly-N-(2-ethyl)hexylglycine-block-poly-N-phosphonomethylglycine (pNeh-b-pNpm), is studied. The hydrophobic/hydrophilic block ratio was varied keeping the total chain length of the co-polymers constant. A new approach for characterizing the vesicle membrane morphology based on low-dose cryogenic electron microscopy (cryo-EM) is described. The individual low-dose micrographs cannot be interpreted directly due to low signal-to-noise ratio. Sorting and averaging techniques, developed in the context of protein structure determination, were thus applied to vesicle micrographs. Molecular dynamic simulations of the vesicles were used to establish the relationship between membrane morphology and averaged cryo-EM images. This approach enables resolution of the local thickness of the hydrophobic membrane core at the 1 nm length scale. The thickness of the hydrophobic core of the pNeh-b-pNpm membranes increases linearly with the length of the hydrophobic block.

Authors:

; Spencer, Ryan K.;

^[1]; Ophus, Colin;

;

^[2]

Key Laboratory of Biobased Polymer Materials, Shandong Provincial Education Department, School of Polymer Science and Engineering, Qingdao University of Science and Technology, Qingdao 266042, China
Department of Chemical and Biomolecular Engineering, University of California, Berkeley, California 94720, United States

Publication Date:: Thu Jan 10 00:00:00 EST 2019

Research Org.:: University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1492105

Alternate Identifier(s):: OSTI ID: 1508807; OSTI ID: 1594906

Grant/Contract Number:: AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Journal of Physical Chemistry. B

Additional Journal Information:: Journal Name: Journal of Physical Chemistry. B Journal Volume: 123 Journal Issue: 5; Journal ID: ISSN 1520-6106

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

Subject:: 36 MATERIALS SCIENCE

Citation Formats


                    Jiang, Xi, Spencer, Ryan K., Sun, Jing, Ophus, Colin, Zuckermann, Ronald N., Downing, Kenneth H., and Balsara, Nitash P. Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy.  United States: N. p., 2019. 
Web.  doi:10.1021/acs.jpcb.8b11752.

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                    Jiang, Xi, Spencer, Ryan K., Sun, Jing, Ophus, Colin, Zuckermann, Ronald N., Downing, Kenneth H., & Balsara, Nitash P. Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy.  United States.  https://doi.org/10.1021/acs.jpcb.8b11752

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                    Jiang, Xi, Spencer, Ryan K., Sun, Jing, Ophus, Colin, Zuckermann, Ronald N., Downing, Kenneth H., and Balsara, Nitash P. Thu .  
"Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy".  United States.  https://doi.org/10.1021/acs.jpcb.8b11752.

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@article{osti_1492105,

  title        = {Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy},

  author       = {Jiang, Xi and Spencer, Ryan K. and Sun, Jing and Ophus, Colin and Zuckermann, Ronald N. and Downing, Kenneth H. and Balsara, Nitash P.},

  abstractNote = {Vesicle formation in a series of amphiphilic sequence-defined polypeptoid block co-polymers comprising a phosphonated hydrophilic block and an amorphous hydrophobic block, poly-N-(2-ethyl)hexylglycine-block-poly-N-phosphonomethylglycine (pNeh-b-pNpm), is studied. The hydrophobic/hydrophilic block ratio was varied keeping the total chain length of the co-polymers constant. A new approach for characterizing the vesicle membrane morphology based on low-dose cryogenic electron microscopy (cryo-EM) is described. The individual low-dose micrographs cannot be interpreted directly due to low signal-to-noise ratio. Sorting and averaging techniques, developed in the context of protein structure determination, were thus applied to vesicle micrographs. Molecular dynamic simulations of the vesicles were used to establish the relationship between membrane morphology and averaged cryo-EM images. This approach enables resolution of the local thickness of the hydrophobic membrane core at the 1 nm length scale. The thickness of the hydrophobic core of the pNeh-b-pNpm membranes increases linearly with the length of the hydrophobic block.},

  doi          = {10.1021/acs.jpcb.8b11752},

  journal      = {Journal of Physical Chemistry. B},

  number       = 5,

  volume       = 123,

  place        = {United States},

  year         = {Thu Jan 10 00:00:00 EST 2019},

  month        = {Thu Jan 10 00:00:00 EST 2019}

}

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Figures / Tables:

Table 1: Characteristics of the Diblock Polypeptoids pNeh_m-b-pNpm_n

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Title: Resolving the Morphology of Peptoid Vesicles at the 1 nm Length Scale Using Cryogenic Electron Microscopy

Abstract

Citation Formats

Figures / Tables:

Optical changes in unilamellar vesicles experiencing osmotic stress journal, November 1996

Polymersome Shape Transformation at the Nanoscale journal, September 2013

Morphology and Proton Transport in Humidified Phosphonated Peptoid Block Copolymers journal, April 2016

Using cryo-EM to measure the dipole potential of a lipid membrane journal, November 2006

Scaling Laws for the Swelling of Neutral and Charged Polymer Brushes in Good Solvents. Volume 35, Number 2, 2002, pp 499−507. journal, February 2004

Development and use of an atomistic CHARMM-based forcefield for peptoid simulation journal, November 2013

Bilayers and Interdigitation in Block Copolymer Vesicles journal, June 2005

Self-assembly of crystalline nanotubes from monodisperse amphiphilic diblock copolypeptoid tiles journal, March 2016

Effect of Block Length, Polydispersity, and Salt Concentration on PEO−PDEAMA Block Copolymer Structures in Dilute Solution journal, May 2006

Bilayer thickness and lipid interface area in unilamellar extruded 1,2-diacylphosphatidylcholine liposomes: a small-angle neutron scattering study journal, May 2001

Scalable molecular dynamics with NAMD journal, January 2005

Crystallization in Sequence-Defined Peptoid Diblock Copolymers Induced by Microphase Separation journal, January 2014

Universal Relationship between Molecular Structure and Crystal Structure in Peptoid Polymers and Prevalence of the cis Backbone Conformation journal, January 2018

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

Effect of Polydispersity on the Self-Assembly Structure of Diblock Copolymers under Various Confined States: A Monte Carlo Study journal, July 2008

Vesicle Formation and Microphase Behavior of Amphiphilic ABC Triblock Copolymers in Selective Solvents: A Monte Carlo Study journal, August 2010

Emerging applications of polymersomes in delivery: From molecular dynamics to shrinkage of tumors journal, August 2007

Polymer Vesicles journal, August 2002

Polymersomes for drug delivery: Design, formation and characterization journal, July 2012

Effect of Bilayer Thickness on Membrane Bending Rigidity journal, February 2004

Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions journal, May 2018

Direct Observation of Shear-Induced Structures in Wormlike Micellar Solutions by Freeze-Fracture Electron Microscopy journal, March 1998

Sphere, Cylinder, and Vesicle Nanoaggregates in Poly(styrene- b -isoprene) Diblock Copolymer Solutions. Volume 39, Number 3, February 7, 2006, pp 1199−1208. journal, August 2006

Determination of bilayer thickness and lipid surface area in unilamellar dimyristoylphosphatidylcholine vesicles from small-angle neutron scattering curves: a comparison of evaluation methods journal, September 2003

MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy journal, February 2017

Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol journal, March 2004

Electron microscopy of the stacked disk aggregate of tobacco mosaic virus protein journal, August 1974

Cryogenic Transmission Electron Microscopy Imaging of Vesicles Formed by a Polystyrene−Polyisoprene Diblock Copolymer journal, August 2005

Effects of Polydispersity on Phase Behavior of Diblock Copolymers journal, September 2006

Nanostructure of Complexes Between Cationic Lipids and an Oppositely Charged Polyelectrolyte journal, January 2012

From Vesicle Size Distributions to Bilayer Elasticity via Cryo-Transmission and Freeze-Fracture Electron Microscopy journal, June 2003

Gctf: Real-time CTF determination and correction journal, January 2016

Self-Assembly of β-Cyclodextrin in Water. Part 1: Cryo-TEM and Dynamic and Static Light Scattering journal, February 2006

Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data journal, September 2008

Small-angle neutron scattering study of the lipid bilayer thickness in unilamellar dioleoylphosphatidylcholine vesicles prepared by the cholate dilution method: n-decane effect journal, April 2003

Free-floating ultrathin two-dimensional crystals from sequence-specific peptoid polymers journal, April 2010

Direct Observation of a Defect-Mediated Viscoelastic Transition in a Hydrogel of Lipid Membranes and Polymer Lipids journal, June 1997

Polymersomes from Amphiphilic Glycopolymers Containing Polymeric Liquid Crystal Grafts journal, September 2015

Preirradiation and minimum beam microscopy of periodic biological specimens journal, August 1978

Cryogenic Transmission Electron Microscopy (Cryo-TEM) of Micelles and Vesicles Formed in Water by Poly(ethylene oxide)-Based Block Copolymers journal, April 2002

ABCA Tetrablock Copolymer Vesicles journal, November 2004

A Bayesian View on Cryo-EM Structure Determination journal, January 2012

Advanced Computing in Electron Microscopy book, January 2010

Effect of Polydispersity on the Formation of Vesicles from Amphiphilic Diblock Copolymers journal, July 2005

RELION: Implementation of a Bayesian approach to cryo-EM structure determination journal, December 2012

Cryo transmission electron microscopy of liposomes and related structures journal, November 2000

Selecting analytical tools for characterization of polymersomes in aqueous solution journal, January 2015

Bilayer Membrane Permeability of Ionic Liquid-Filled Block Copolymer Vesicles in Aqueous Solution journal, July 2012

Stacking in lipid vesicle-tubulin mixtures is an artifact of negative staining journal, September 1980

Invited Review Article: Methods for imaging weak-phase objects in electron microscopy journal, November 2013

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

Negative staining and cryo-negative staining of macromolecules and viruses for TEM journal, February 2011

Cross-linking of Phospholipid Membranes is a Conserved Property of Calcium-sensitive Synaptotagmins journal, June 2008

Cryo-electron tomography of nanoparticle transmigration into liposome journal, December 2009

Theory of Polydisperse Inhomogeneous Polymers journal, July 2003

Simulation of transmission electron microscope images of biological specimens: SIMULATION OF TEM IMAGES OF BIOLOGICAL SPECIMENS journal, June 2011

Cross-linked Polymersome Membranes: Vesicles with Broadly Adjustable Properties journal, March 2002

Electron cryotomography of vitrified cells with a Volta phase plate journal, May 2015

Polymersomes hydrophilic brush scaling relations journal, January 2009

Laterally Nanostructured Vesicles, Polygonal Bilayer Sheets, and Segmented Wormlike Micelles journal, June 2006

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

Liposomal drug delivery systems: From concept to clinical applications journal, January 2013

Small Angle Scattering and Zeta Potential of Liposomes Loaded with Octa(carboranyl)porphyrazine journal, August 2007

A new method to measure bilayer thickness: Cryo-electron microscopy of frozen hydrated liposomes and image simulation journal, April 1994

VMD: Visual molecular dynamics journal, February 1996

Cryo-electron microscopy of artificial biological membranes journal, November 1985

Vesicle Membrane Thickness in Aqueous Dispersions of Block Copolymer Blends journal, October 2008

Heterogeneous MAC Initiator and Pore Structures in a Lipid Bilayer by Phase-Plate Cryo-electron Tomography journal, April 2016

Optical changes in unilamellar vesicles experiencing osmotic stress
journal, November 1996

Polymersome Shape Transformation at the Nanoscale
journal, September 2013

Morphology and Proton Transport in Humidified Phosphonated Peptoid Block Copolymers
journal, April 2016

Using cryo-EM to measure the dipole potential of a lipid membrane
journal, November 2006

Scaling Laws for the Swelling of Neutral and Charged Polymer Brushes in Good Solvents. Volume 35, Number 2, 2002, pp 499−507.
journal, February 2004

Development and use of an atomistic CHARMM-based forcefield for peptoid simulation
journal, November 2013

Bilayers and Interdigitation in Block Copolymer Vesicles
journal, June 2005

Self-assembly of crystalline nanotubes from monodisperse amphiphilic diblock copolypeptoid tiles
journal, March 2016

Effect of Block Length, Polydispersity, and Salt Concentration on PEO−PDEAMA Block Copolymer Structures in Dilute Solution
journal, May 2006

Bilayer thickness and lipid interface area in unilamellar extruded 1,2-diacylphosphatidylcholine liposomes: a small-angle neutron scattering study
journal, May 2001

Scalable molecular dynamics with NAMD
journal, January 2005

Crystallization in Sequence-Defined Peptoid Diblock Copolymers Induced by Microphase Separation
journal, January 2014

Universal Relationship between Molecular Structure and Crystal Structure in Peptoid Polymers and Prevalence of the cis Backbone Conformation
journal, January 2018

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

Effect of Polydispersity on the Self-Assembly Structure of Diblock Copolymers under Various Confined States: A Monte Carlo Study
journal, July 2008

Vesicle Formation and Microphase Behavior of Amphiphilic ABC Triblock Copolymers in Selective Solvents: A Monte Carlo Study
journal, August 2010

Emerging applications of polymersomes in delivery: From molecular dynamics to shrinkage of tumors
journal, August 2007

Polymer Vesicles
journal, August 2002

Polymersomes for drug delivery: Design, formation and characterization
journal, July 2012

Effect of Bilayer Thickness on Membrane Bending Rigidity
journal, February 2004

Conformations of peptoids in nanosheets result from the interplay of backbone energetics and intermolecular interactions
journal, May 2018

Direct Observation of Shear-Induced Structures in Wormlike Micellar Solutions by Freeze-Fracture Electron Microscopy
journal, March 1998

Sphere, Cylinder, and Vesicle Nanoaggregates in Poly(styrene- b -isoprene) Diblock Copolymer Solutions. Volume 39, Number 3, February 7, 2006, pp 1199−1208.
journal, August 2006

Determination of bilayer thickness and lipid surface area in unilamellar dimyristoylphosphatidylcholine vesicles from small-angle neutron scattering curves: a comparison of evaluation methods
journal, September 2003

MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy
journal, February 2017

Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol
journal, March 2004

Electron microscopy of the stacked disk aggregate of tobacco mosaic virus protein
journal, August 1974

Cryogenic Transmission Electron Microscopy Imaging of Vesicles Formed by a Polystyrene−Polyisoprene Diblock Copolymer
journal, August 2005

Effects of Polydispersity on Phase Behavior of Diblock Copolymers
journal, September 2006

Nanostructure of Complexes Between Cationic Lipids and an Oppositely Charged Polyelectrolyte
journal, January 2012

From Vesicle Size Distributions to Bilayer Elasticity via Cryo-Transmission and Freeze-Fracture Electron Microscopy
journal, June 2003

Gctf: Real-time CTF determination and correction
journal, January 2016

Self-Assembly of β-Cyclodextrin in Water. Part 1: Cryo-TEM and Dynamic and Static Light Scattering
journal, February 2006

Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data
journal, September 2008

Small-angle neutron scattering study of the lipid bilayer thickness in unilamellar dioleoylphosphatidylcholine vesicles prepared by the cholate dilution method: n-decane effect
journal, April 2003

Free-floating ultrathin two-dimensional crystals from sequence-specific peptoid polymers
journal, April 2010

Direct Observation of a Defect-Mediated Viscoelastic Transition in a Hydrogel of Lipid Membranes and Polymer Lipids
journal, June 1997

Polymersomes from Amphiphilic Glycopolymers Containing Polymeric Liquid Crystal Grafts
journal, September 2015

Preirradiation and minimum beam microscopy of periodic biological specimens
journal, August 1978

Cryogenic Transmission Electron Microscopy (Cryo-TEM) of Micelles and Vesicles Formed in Water by Poly(ethylene oxide)-Based Block Copolymers
journal, April 2002

ABCA Tetrablock Copolymer Vesicles
journal, November 2004

A Bayesian View on Cryo-EM Structure Determination
journal, January 2012

Advanced Computing in Electron Microscopy
book, January 2010

Effect of Polydispersity on the Formation of Vesicles from Amphiphilic Diblock Copolymers
journal, July 2005

RELION: Implementation of a Bayesian approach to cryo-EM structure determination
journal, December 2012

Cryo transmission electron microscopy of liposomes and related structures
journal, November 2000

Selecting analytical tools for characterization of polymersomes in aqueous solution
journal, January 2015

Bilayer Membrane Permeability of Ionic Liquid-Filled Block Copolymer Vesicles in Aqueous Solution
journal, July 2012

Stacking in lipid vesicle-tubulin mixtures is an artifact of negative staining
journal, September 1980

Invited Review Article: Methods for imaging weak-phase objects in electron microscopy
journal, November 2013

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

Negative staining and cryo-negative staining of macromolecules and viruses for TEM
journal, February 2011

Cross-linking of Phospholipid Membranes is a Conserved Property of Calcium-sensitive Synaptotagmins
journal, June 2008

Cryo-electron tomography of nanoparticle transmigration into liposome
journal, December 2009

Theory of Polydisperse Inhomogeneous Polymers
journal, July 2003

Simulation of transmission electron microscope images of biological specimens: SIMULATION OF TEM IMAGES OF BIOLOGICAL SPECIMENS
journal, June 2011

Cross-linked Polymersome Membranes: Vesicles with Broadly Adjustable Properties
journal, March 2002

Electron cryotomography of vitrified cells with a Volta phase plate
journal, May 2015

Polymersomes hydrophilic brush scaling relations
journal, January 2009

Laterally Nanostructured Vesicles, Polygonal Bilayer Sheets, and Segmented Wormlike Micelles
journal, June 2006

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

Liposomal drug delivery systems: From concept to clinical applications
journal, January 2013

Small Angle Scattering and Zeta Potential of Liposomes Loaded with Octa(carboranyl)porphyrazine
journal, August 2007

A new method to measure bilayer thickness: Cryo-electron microscopy of frozen hydrated liposomes and image simulation
journal, April 1994

VMD: Visual molecular dynamics
journal, February 1996

Cryo-electron microscopy of artificial biological membranes
journal, November 1985

Vesicle Membrane Thickness in Aqueous Dispersions of Block Copolymer Blends
journal, October 2008

Heterogeneous MAC Initiator and Pore Structures in a Lipid Bilayer by Phase-Plate Cryo-electron Tomography
journal, April 2016