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Title: (2 + δ)-dimensional theory of the electromechanics of lipid membranes: Electrostatics

Journal Article · · Physical Review. E
 [1];  [2];  [3]
  1. Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
  2. University of California, Berkeley, CA (United States)
  3. University of California, Berkeley, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

The coupling of electric fields to the mechanics of lipid membranes gives rise to intriguing electromechanical behavior, as, for example, evidenced by the deformation of lipid vesicles in external electric fields. Electromechanical effects are relevant for many biological processes, such as the propagation of action potentials in axons and the activation of mechanically gated ion channels. Currently, a theoretical framework describing the electromechanical behavior of arbitrarily curved and deforming lipid membranes does not exist. Purely mechanical models commonly treat lipid membranes as two-dimensional surfaces, ignoring their finite thickness. While holding analytical and numerical merit, this approach cannot describe the coupling of lipid membranes to electric fields and is thus unsuitable for electromechanical models. In a sequence of articles, we derive an effective surface theory of the electromechanics of lipid membranes, called the (2 + δ)-dimensional theory, which has the advantages of surface descriptions while accounting for finite thickness effects. The present article proposes a generic dimension reduction procedure relying on low-order spectral expansions. This procedure is applied to the electrostatics of lipid membranes to obtain the (2 + δ)-dimensional theory that captures potential differences across and electric fields within lipid membranes. Finally, this model is tested on different geometries relevant for lipid membranes, showing good agreement with the corresponding three-dimensional electrostatics theory.

Research Organization:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Organization:
USDOE; USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division (CSGB)
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
2505101
Journal Information:
Physical Review. E, Journal Name: Physical Review. E Journal Issue: 5 Vol. 109; ISSN 2470-0045
Publisher:
American Physical Society (APS)Copyright Statement
Country of Publication:
United States
Language:
English

References (57)

Transport phenomena in electrolyte solutions: Nonequilibrium thermodynamics and statistical mechanics journal November 2020
Spectral Methods: Evolution to Complex Geometrics and Applications to Fluid Dynamics book January 2007
The construction of a generalized theory of shells from thermopiezoelastic material journal December 1983
Untersuchungen zur Thermodynamik der bioelektrischen Ströme journal June 1906
The mechanism of electrical breakdown in the membranes ofValonia utricularis journal December 1975
Membrane potential of a ranvier node measured after electrical destruction of its membrane journal July 1957
Fluid Films with Curvature Elasticity journal December 1999
Destabilizing Giant Vesicles with Electric Fields: An Overview of Current Applications journal August 2012
Interaction between surface shape and intra-surface viscous flow on lipid membranes journal October 2012
Mechanical changes in squid giant axons associated with production of action potentials journal August 1980
Evidence for a symmetrical uptake of fluorescent dyes through electro‐permeabilized membranes of Avena mesophyll protoplasts journal June 1985
Deformation of spherical vesicles by electric fields journal April 1988
Electro-mechanical permeabilization of lipid vesicles. Role of membrane tension and compressibility journal May 1989
Membrane conductance of an electroporated cell analyzed by submicrosecond imaging of transmembrane potential journal January 1991
Chapter Seven Electroporation of Planar Lipid Bilayers and Membranes book October 2007
Electrophysiological-mechanical coupling in the neuronal membrane and its role in ultrasound neuromodulation and general anaesthesia journal October 2019
Lipid vesicles in pulsed electric fields: Fundamental principles of the membrane response and its biomedical applications journal November 2017
Electrical systems for pulsed electric field applications in the food industry: An engineering perspective journal October 2020
Pulsed electric field: A potential alternative towards a sustainable food processing journal May 2021
An electrokinetic model of drop deformation in an electric field journal November 2002
The Taylor–Melcher leaky dielectric model as a macroscale electrokinetic description journal May 2015
From electrodiffusion theory to the electrohydrodynamics of leaky dielectrics through the weak electrolyte limit journal September 2018
A model for the electric field-driven flow and deformation of a drop or vesicle in strong electrolyte solutions journal June 2022
Imaging Action Potential in Single Mammalian Neurons by Tracking the Accompanying Sub-Nanometer Mechanical Motion journal March 2018
The bending modulus of ionic lamellar phases journal March 1991
The Structure of Ions and Zwitterionic Lipids Regulates the Charge of Dipolar Membranes journal May 2011
Mechanical surface waves accompany action potential propagation journal March 2015
Piezoelectric nanoribbons for monitoring cellular deformations journal July 2012
Vesicle deformation in DC electric pulses journal January 2014
Giant vesicles in electric fields journal January 2007
Vesicles in electric fields: Some novel aspects of membrane behavior journal January 2009
Electric field induced pearling instability in cylindrical vesicles journal January 2013
Stability of charged membranes journal January 1990
Pattern formation of stationary transcellular ionic currents in Fucus journal July 2004
A Poisson–Boltzmann approach for a lipid membrane in an electric field journal September 2010
The intrinsic theory of thin shells and plates. I. General theory journal January 1944
Electromagnetic Theory book March 2000
It sounds like an action potential: unification of electrical, chemical and mechanical aspects of acoustic pulses in lipids journal February 2019
Studies in electrohydrodynamics. I. The circulation produced in a drop by an electric field journal April 1966
The positive and negative heat production associated with a nerve impulse
  • Abbott, B. C.; Hill, Archibald Vivian; Howarth, J. V.
  • Proceedings of the Royal Society of London. Series B - Biological Sciences, Vol. 148, Issue 931, p. 149-187 https://doi.org/10.1098/rspb.1958.0012
journal February 1958
On electromagnetic effects in the theory of shells and plates
  • Green, A. E.; Naghdi, P. M.
  • Philosophical Transactions of the Royal Society of London. Series A, Mathematical and Physical Sciences, Vol. 309, Issue 1510, p. 559-610 https://doi.org/10.1098/rsta.1983.0058
journal November 1983
Deformation of giant lipid vesicles by electric fields journal December 1991
Geometry and dynamics of lipid membranes: The Scriven-Love number journal May 2020
Relaxation dynamics of fluid membranes journal March 2009
Irreversible thermodynamics of curved lipid membranes journal October 2017
Undulation Instability of Lipid Membranes under an Electric Field journal March 2002
Numerical Analysis of Spectral Methods: Theory and Applications book January 1977
Electrostatic and electrokinetic contributions to the elastic moduli of a driven membrane journal January 2009
Electroporation-Based Technologies for Medicine: Principles, Applications, and Challenges journal July 2014
Electrohydrodynamics of Drops and Vesicles journal January 2019
Electrohydrodynamics: A Review of the Role of Interfacial Shear Stresses journal January 1969
Electrohydrodynamics: The Taylor-Melcher Leaky Dielectric Model journal January 1997
On the theoretical foundations of thin solid and liquid shells journal August 2016
Elastic Properties of Lipid Bilayers: Theory and Possible Experiments journal December 1973
Cell electrofusion: past and future perspectives for antibody production and cancer cell vaccines journal July 2014
Electro-Deformation and Poration of Giant Vesicles Viewed with High Temporal Resolution journal February 2005
Mechanical changes in crab nerve fibers during action potentials. journal January 1980