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

Title: Electrostatic shape control of a charged molecular membrane from ribbon to scroll

Abstract

Bilayers of amphiphiles can organize into spherical vesicles, nanotubes, planar, undulating, and helical nanoribbons, and scroll-like cochleates. These bilayer-related architectures interconvert under suitable conditions. Here, a charged, chiral amphiphile (palmitoyl-lysine, C16-K1) is used to elucidate the pathway for planar nanoribbon to cochleate transition induced by salt (NaCl) concentration. In situ small- and wide-angle X-ray scattering (SAXS/WAXS), atomic force and cryogenic transmission electron microscopies (AFM and cryo-TEM) tracked these transformations over angstrom to micrometer length scales. AFM reveals that the large length (L) to width (W) ratio nanoribbons (L/W > 10) convert to sheets (L/W → 1) before rolling into cochleates. Furthermore, a theoretical model based on electrostatic and surface energies shows that the nanoribbons convert to sheets via a first-order transition, at a critical Debye length, with 2 shallow minima of the order of thermal energy at L/W >> 1 and at L/W = 1. SAXS shows that interbilayer spacing (D) in the cochleates scales linearly with the Debye length, and ranges from 13 to 35 nm for NaCl concentrations from 100 to 5 mM. Theoretical arguments that include electrostatic and elastic energies explain the membrane rolling and the bilayer separation–Debye length relationship. These models suggest that the salt-induced ribbonmore » to cochleate transition should be common to all charged bilayers possessing an intrinsic curvature, which in the present case originates from molecular chirality. Our studies show how electrostatic interactions can be tuned to attain and control cochleate structures, which have potential for encapsulating, and releasing macromolecules in a size-selective manner.« less

Authors:
; ; ; ; ; ORCiD logo; ORCiD logo
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States). Advanced Photon Source (APS)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1570475
Alternate Identifier(s):
OSTI ID: 1576003
Grant/Contract Number:  
FG02-08ER46539; AC02-06CH11357
Resource Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Volume: 116 Journal Issue: 44; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; bilayer assembly; electrostatics; nanoribbon; cochleate

Citation Formats

Gao, Changrui, Kewalramani, Sumit, Valencia, Dulce Maria, Li, Honghao, McCourt, Joseph M., Olvera de la Cruz, Monica, and Bedzyk, Michael J. Electrostatic shape control of a charged molecular membrane from ribbon to scroll. United States: N. p., 2019. Web. doi:10.1073/pnas.1913632116.
Gao, Changrui, Kewalramani, Sumit, Valencia, Dulce Maria, Li, Honghao, McCourt, Joseph M., Olvera de la Cruz, Monica, & Bedzyk, Michael J. Electrostatic shape control of a charged molecular membrane from ribbon to scroll. United States. doi:10.1073/pnas.1913632116.
Gao, Changrui, Kewalramani, Sumit, Valencia, Dulce Maria, Li, Honghao, McCourt, Joseph M., Olvera de la Cruz, Monica, and Bedzyk, Michael J. Mon . "Electrostatic shape control of a charged molecular membrane from ribbon to scroll". United States. doi:10.1073/pnas.1913632116.
@article{osti_1570475,
title = {Electrostatic shape control of a charged molecular membrane from ribbon to scroll},
author = {Gao, Changrui and Kewalramani, Sumit and Valencia, Dulce Maria and Li, Honghao and McCourt, Joseph M. and Olvera de la Cruz, Monica and Bedzyk, Michael J.},
abstractNote = {Bilayers of amphiphiles can organize into spherical vesicles, nanotubes, planar, undulating, and helical nanoribbons, and scroll-like cochleates. These bilayer-related architectures interconvert under suitable conditions. Here, a charged, chiral amphiphile (palmitoyl-lysine, C16-K1) is used to elucidate the pathway for planar nanoribbon to cochleate transition induced by salt (NaCl) concentration. In situ small- and wide-angle X-ray scattering (SAXS/WAXS), atomic force and cryogenic transmission electron microscopies (AFM and cryo-TEM) tracked these transformations over angstrom to micrometer length scales. AFM reveals that the large length (L) to width (W) ratio nanoribbons (L/W > 10) convert to sheets (L/W → 1) before rolling into cochleates. Furthermore, a theoretical model based on electrostatic and surface energies shows that the nanoribbons convert to sheets via a first-order transition, at a critical Debye length, with 2 shallow minima of the order of thermal energy at L/W >> 1 and at L/W = 1. SAXS shows that interbilayer spacing (D) in the cochleates scales linearly with the Debye length, and ranges from 13 to 35 nm for NaCl concentrations from 100 to 5 mM. Theoretical arguments that include electrostatic and elastic energies explain the membrane rolling and the bilayer separation–Debye length relationship. These models suggest that the salt-induced ribbon to cochleate transition should be common to all charged bilayers possessing an intrinsic curvature, which in the present case originates from molecular chirality. Our studies show how electrostatic interactions can be tuned to attain and control cochleate structures, which have potential for encapsulating, and releasing macromolecules in a size-selective manner.},
doi = {10.1073/pnas.1913632116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 44,
volume = 116,
place = {United States},
year = {2019},
month = {10}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1073/pnas.1913632116

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Supramolecular control of self-assembling terthiophene–peptide conjugates through the amino acid side chain
journal, January 2012

  • Lehrman, Jessica A.; Cui, Honggang; Tsai, Wei-Wen
  • Chemical Communications, Vol. 48, Issue 78
  • DOI: 10.1039/c2cc34375d

Recent advances with liposomes as pharmaceutical carriers
journal, February 2005

  • Torchilin, Vladimir P.
  • Nature Reviews Drug Discovery, Vol. 4, Issue 2
  • DOI: 10.1038/nrd1632

Phase behavior of charged lipid bilayer membranes with added electrolyte
journal, July 2003

  • Komura, Shigeyuki; Shirotori, Hisashi; Kato, Tadashi
  • The Journal of Chemical Physics, Vol. 119, Issue 2
  • DOI: 10.1063/1.1579675

The swelling of montmorillonite
journal, January 1954


Self-assembling peptide scaffolds for regenerative medicine
journal, January 2012

  • Matson, John B.; Stupp, Samuel I.
  • Chem. Commun., Vol. 48, Issue 1
  • DOI: 10.1039/C1CC15551B

Understanding cochleate formation: insights into structural development
journal, January 2016

  • Nagarsekar, Kalpa; Ashtikar, Mukul; Steiniger, Frank
  • Soft Matter, Vol. 12, Issue 16
  • DOI: 10.1039/C5SM01469G

Self-assembling hydrogel scaffolds for photocatalytic hydrogen production
journal, October 2014

  • Weingarten, Adam S.; Kazantsev, Roman V.; Palmer, Liam C.
  • Nature Chemistry, Vol. 6, Issue 11
  • DOI: 10.1038/nchem.2075

Self-assembly of peptide amphiphiles: From molecules to nanostructures to biomaterials
journal, January 2010

  • Cui, Honggang; Webber, Matthew J.; Stupp, Samuel I.
  • Biopolymers, Vol. 94, Issue 1, p. 1-18
  • DOI: 10.1002/bip.21328

UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations
journal, December 1992

  • Rappe, A. K.; Casewit, C. J.; Colwell, K. S.
  • Journal of the American Chemical Society, Vol. 114, Issue 25, p. 10024-10035
  • DOI: 10.1021/ja00051a040

Semiconductor Nanohelices Templated by Supramolecular Ribbons
journal, May 2002


Self-assembly of amphiphilic peptides
journal, January 2011


Experimental evidence of the electrostatic contribution to membrane bending rigidity
journal, July 2004


Atomic force microscopy measurements of bacterial adhesion and biofilm formation onto clay-sized particles
journal, November 2015

  • Huang, Qiaoyun; Wu, Huayong; Cai, Peng
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep16857

Structure of lipid bilayers
journal, November 2000

  • Nagle, John F.; Tristram-Nagle, Stephanie
  • Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes, Vol. 1469, Issue 3
  • DOI: 10.1016/S0304-4157(00)00016-2

Advanced drug delivery devices via self-assembly of amphiphilic block copolymers
journal, December 2012

  • Rösler, Annette; Vandermeulen, Guido W. M.; Klok, Harm-Anton
  • Advanced Drug Delivery Reviews, Vol. 64
  • DOI: 10.1016/j.addr.2012.09.026

Amino Acid Sequence in Constitutionally Isomeric Tetrapeptide Amphiphiles Dictates Architecture of One-Dimensional Nanostructures
journal, August 2014

  • Cui, Honggang; Cheetham, Andrew G.; Pashuck, E. Thomas
  • Journal of the American Chemical Society, Vol. 136, Issue 35
  • DOI: 10.1021/ja507051w

Novel Electrochemical Biosensing Platform Using Self-Assembled Peptide Nanotubes
journal, January 2005

  • Yemini, Miri; Reches, Meital; Rishpon, Judith
  • Nano Letters, Vol. 5, Issue 1
  • DOI: 10.1021/nl0484189

Electrostatics-Driven Hierarchical Buckling of Charged Flexible Ribbons
journal, April 2016


Membrane curvature elasticity in weakly charged lamellar phases
journal, April 1992


Adjustable twisting periodic pitch of amyloid fibrils
journal, January 2011

  • Adamcik, Jozef; Mezzenga, Raffaele
  • Soft Matter, Vol. 7, Issue 11
  • DOI: 10.1039/c1sm05382e

Surface tension of electrolytes: Hydrophilic and hydrophobic ions near an interface
journal, June 2008

  • Onuki, Akira
  • The Journal of Chemical Physics, Vol. 128, Issue 22
  • DOI: 10.1063/1.2936992

Electron Microscopy and Theoretical Modeling of Cochleates
journal, October 2014

  • Nagarsekar, Kalpa; Ashtikar, Mukul; Thamm, Jana
  • Langmuir, Vol. 30, Issue 44
  • DOI: 10.1021/la502775b

Supramolecular Packing Controls H 2 Photocatalysis in Chromophore Amphiphile Hydrogels
journal, November 2015

  • Weingarten, Adam S.; Kazantsev, Roman V.; Palmer, Liam C.
  • Journal of the American Chemical Society, Vol. 137, Issue 48
  • DOI: 10.1021/jacs.5b10027

Intrinsic bending force in anisotropic membranes made of chiral molecules
journal, September 1988


An insight into cochleates, a potential drug delivery system
journal, January 2015

  • Pawar, Atmaram; Bothiraja, C.; Shaikh, Karimunnisa
  • RSC Advances, Vol. 5, Issue 99
  • DOI: 10.1039/C5RA08550K

Self-Assembled Proteins and Peptides for Regenerative Medicine
journal, March 2013

  • Hosseinkhani, Hossein; Hong, Po-Da; Yu, Dah-Shyong
  • Chemical Reviews, Vol. 113, Issue 7
  • DOI: 10.1021/cr300131h

Theory of chiral lipid tubules
journal, December 1993


Theory of Self-Assembled Tubules and Helical Ribbons
journal, August 2001

  • Selinger, Jonathan V.; Spector, Mark S.; Schnur, Joel M.
  • The Journal of Physical Chemistry B, Vol. 105, Issue 30
  • DOI: 10.1021/jp010452d

Crystal-Phase Transitions and Photocatalysis in Supramolecular Scaffolds
journal, April 2017

  • Kazantsev, Roman V.; Dannenhoffer, Adam J.; Weingarten, Adam S.
  • Journal of the American Chemical Society, Vol. 139, Issue 17
  • DOI: 10.1021/jacs.6b13156

Fibrillar superstructure from extended nanotapes formed by a collagen-stimulating peptide
journal, January 2010

  • Castelletto, Valeria; Hamley, Ian W.; Perez, Javier
  • Chemical Communications, Vol. 46, Issue 48
  • DOI: 10.1039/c0cc03793a

Nanostructured materials for applications in drug delivery and tissue engineering
journal, January 2007

  • Goldberg, Michael; Langer, Robert; Jia, Xinqiao
  • Journal of Biomaterials Science, Polymer Edition, Vol. 18, Issue 3
  • DOI: 10.1163/156856207779996931

Supported Lipid Bilayer Membranes for Water Purification by Reverse Osmosis
journal, May 2010

  • Kaufman, Yair; Berman, Amir; Freger, Viatcheslav
  • Langmuir, Vol. 26, Issue 10
  • DOI: 10.1021/la904411b

Pharmaceutical applications for catanionic mixtures
journal, October 2007

  • Bramer, Tobias; Dew, Noel; Edsman, Katarina
  • Journal of Pharmacy and Pharmacology, Vol. 59, Issue 10
  • DOI: 10.1211/jpp.59.10.0001

Electrostatic Control of Polymorphism in Charged Amphiphile Assemblies
journal, February 2017

  • Gao, Changrui; Li, Honghao; Li, Yue
  • The Journal of Physical Chemistry B, Vol. 121, Issue 7
  • DOI: 10.1021/acs.jpcb.6b11602

Short- and Long-Range Attractive Forces That Influence the Structure of Montmorillonite Osmotic Hydrates
journal, November 2016


Cochleate lipid cylinders: formation by fusion of unilamellar lipid vesicles
journal, July 1975

  • Papahadjopoulos, D.; Vail, W. J.; Jacobson, K.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 394, Issue 3
  • DOI: 10.1016/0005-2736(75)90299-0

Self-Assembly of Giant Peptide Nanobelts
journal, March 2009

  • Cui, Honggang; Muraoka, Takahiro; Cheetham, Andrew G.
  • Nano Letters, Vol. 9, Issue 3
  • DOI: 10.1021/nl802813f