Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers

Bolmatov, Dima; Collier, Charles Patrick; Zav’yalov, Dmitry; Egami, Takeshi; Katsaras, John

doi:10.3390/membranes13040442

Title: Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers

Journal Article · 17 April 2023 · Membranes

DOI: https://doi.org/10.3390/membranes13040442 · OSTI ID:1971016

^[1];

^[2]; Zav’yalov, Dmitry ^[3];

^[4];

^[5]

Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull-Wollan Center
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Sciences (CNMS)
Volgograd State Technical University (Russia)
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull-Wollan Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Materials Science and Technology Division
Univ. of Tennessee, Knoxville, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Shull-Wollan Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Neutron Scattering Division

Lipid bilayers are supramolecular structures responsible for a range of processes, such as transmembrane transport of ions and solutes, and sorting and replication of genetic materials, to name just a few. Some of these processes are transient and currently, cannot be visualized in real space and time. Here, we developed an approach using 1D, 2D, and 3D Van Hove correlation functions to image collective headgroup dipole motions in zwitterionic phospholipid bilayers. We show that both 2D and 3D spatiotemporal images of headgroup dipoles are consistent with commonly understood dynamic features of fluids. However, analysis of the 1D Van Hove function reveals lateral transient and re-emergent collective dynamics of the headgroup dipoles—occurring at picosecond time scales—that transmit and dissipate heat at longer times, due to relaxation processes. At the same time, the headgroup dipoles also generate membrane surface undulations due a collective tilting of the headgroup dipoles. A continuous intensity band of headgroup dipole spatiotemporal correlations—at nanometer length and nanosecond time scales—indicates that dipoles undergo stretching and squeezing elastic deformations. Importantly, the above mentioned intrinsic headgroup dipole motions can be externally stimulated at GHz-frequency scale, enhancing their flexoelectric and piezoelectric capabilities (i.e., increased conversion efficiency of mechanical energy into electric energy). In conclusion, we discuss how lipid membranes can provide molecular-level insights about biological learning and memory, and as platforms for the development of the next generation of neuromorphic computers.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Materials Sciences & Engineering Division (MSE); National Science Foundation (NSF); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1971016

Journal Information:: Membranes, Journal Name: Membranes Journal Issue: 4 Vol. 13; ISSN 2077-0375

Publisher:: MDPICopyright Statement

Country of Publication:: United States

Language:: English

References (82)

Accurate Binding of Sodium and Calcium to a POPC Bilayer by Effective Inclusion of Electronic Polarization Melcr, Josef; Martinez-Seara, Hector; Nencini, Ricky The Journal of Physical Chemistry B, Vol. 122, Issue 16 https://doi.org/10.1021/acs.jpcb.7b12510	journal	April 2018
Two cations, two mechanisms: interactions of sodium and calcium with zwitterionic lipid membranes Javanainen, Matti; Melcrová, Adéla; Magarkar, Aniket Chemical Communications, Vol. 53, Issue 39 https://doi.org/10.1039/C7CC02208E	journal	January 2017
Role of polyunsaturated phospholipids in liquid-ordered and liquid-disordered phases Yang, Jing; Jin, Jianyu; Li, Shiben RSC Advances, Vol. 11, Issue 44 https://doi.org/10.1039/D1RA02692E	journal	January 2021
Mechano-capacitive properties of polarized membranes Mosgaard, Lars D.; Zecchi, Karis A.; Heimburg, Thomas Soft Matter, Vol. 11, Issue 40 https://doi.org/10.1039/C5SM01519G	journal	January 2015
Hydration dynamics of a lipid membrane: Hydrogen bond networks and lipid-lipid associations Srivastava, Abhinav; Debnath, Ananya The Journal of Chemical Physics, Vol. 148, Issue 9 https://doi.org/10.1063/1.5011803	journal	March 2018
Revealing the Mechanism of the Viscous-to-Elastic Crossover in Liquids Bolmatov, Dima; Zhernenkov, Mikhail; Zav’yalov, Dmitry The Journal of Physical Chemistry Letters, Vol. 6, Issue 15 https://doi.org/10.1021/acs.jpclett.5b01338	journal	July 2015
Unified phonon-based approach to the thermodynamics of solid, liquid and gas states Bolmatov, Dima; Zav’yalov, Dmitry; Zhernenkov, Mikhail Annals of Physics, Vol. 363 https://doi.org/10.1016/j.aop.2015.09.018	journal	December 2015
The dynamic face of lipid membranes Gupta, Sudipta; Ashkar, Rana Soft Matter, Vol. 17, Issue 29 https://doi.org/10.1039/D1SM00646K	journal	January 2021
Calcium Ion Binding at the Lipid–Water Interface Alters the Ion Permeability of Phospholipid Bilayers Deplazes, Evelyne; Tafalla, Beatriu Domingo; Murphy, Christopher Langmuir, Vol. 37, Issue 48 https://doi.org/10.1021/acs.langmuir.1c02016	journal	November 2021
Determination of Elastic Parameters of Lipid Membranes with Molecular Dynamics: A Review of Approaches and Theoretical Aspects Pinigin, Konstantin V. Membranes, Vol. 12, Issue 11 https://doi.org/10.3390/membranes12111149	journal	November 2022
Observation of dynamic atom-atom correlation in liquid helium in real space Dmowski, W.; Diallo, S. O.; Lokshin, K. Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/ncomms15294	journal	May 2017
Experimental determination of the temperature-dependent Van Hove function in a Zr ₈₀ Pt ₂₀ liquid Ashcraft, R.; Wang, Z.; Abernathy, D. L. The Journal of Chemical Physics, Vol. 152, Issue 7 https://doi.org/10.1063/1.5144256	journal	February 2020
Seeing real-space dynamics of liquid water through inelastic x-ray scattering Iwashita, Takuya; Wu, Bin; Chen, Wei-Ren Science Advances, Vol. 3, Issue 12 https://doi.org/10.1126/sciadv.1603079	journal	December 2017
Understanding Conformational Dynamics of Complex Lipid Mixtures Relevant to Biology Friedman, Ran; Khalid, Syma; Aponte-Santamaría, Camilo The Journal of Membrane Biology, Vol. 251, Issue 5-6 https://doi.org/10.1007/s00232-018-0050-y	journal	October 2018
Dynamic response on a nanometer scale of binary phospholipid-cholesterol vesicles: Low-frequency Raman scattering insight Surovtsev, N. V.; Adichtchev, S. V. Physical Review E, Vol. 104, Issue 5 https://doi.org/10.1103/PhysRevE.104.054406	journal	November 2021
A Brief History of Long-Term Potentiation Nicoll, Roger A. Neuron, Vol. 93, Issue 2 https://doi.org/10.1016/j.neuron.2016.12.015	journal	January 2017
The excitable fluid mosaic Heimburg, Thomas Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1865, Issue 3 https://doi.org/10.1016/j.bbamem.2022.184104	journal	March 2023
Remote control of ion channels and neurons through magnetic-field heating of nanoparticles Huang, Heng; Delikanli, Savas; Zeng, Hao Nature Nanotechnology, Vol. 5, Issue 8 https://doi.org/10.1038/nnano.2010.125	journal	June 2010
Soft learning Ball, Philip Nature Materials, Vol. 22, Issue 1 https://doi.org/10.1038/s41563-022-01457-1	journal	January 2023
Coexistence of lipid phases in multilayer phospholipid films probed by Raman mapping Shamaeva, Daria V.; Okotrub, Konstantin A.; Surovtsev, Nikolay V. The Analyst, Vol. 147, Issue 16 https://doi.org/10.1039/D2AN00490A	journal	January 2022
Lipid Vesicles and Other Polymolecular Aggregates—From Basic Studies of Polar Lipids to Innovative Applications Walde, Peter; Ichikawa, Sosaku Applied Sciences, Vol. 11, Issue 21 https://doi.org/10.3390/app112110345	journal	November 2021
Phonon-mediated lipid raft formation in biological membranes Bolmatov, Dima; Kinnun, Jacob J.; Katsaras, John Chemistry and Physics of Lipids, Vol. 232 https://doi.org/10.1016/j.chemphyslip.2020.104979	journal	October 2020
Molecular Picture of the Transient Nature of Lipid Rafts Bolmatov, Dima; Soloviov, Dmytro; Zhernenkov, Mikhail Langmuir, Vol. 36, Issue 18 https://doi.org/10.1021/acs.langmuir.0c00125	journal	April 2020
Measuring shape fluctuations in biological membranes Monzel, C.; Sengupta, K. Journal of Physics D: Applied Physics, Vol. 49, Issue 24 https://doi.org/10.1088/0022-3727/49/24/243002	journal	May 2016
Perspective on the Martini model Marrink, Siewert J.; Tieleman, D. Peter Chemical Society Reviews, Vol. 42, Issue 16 https://doi.org/10.1039/c3cs60093a	journal	January 2013
Long-term memory and synapse-like dynamics in two-dimensional nanofluidic channels Robin, P.; Emmerich, T.; Ismail, A. Science, Vol. 379, Issue 6628 https://doi.org/10.1126/science.adc9931	journal	January 2023
Disentangling Memristive and Memcapacitive Effects in Droplet Interface Bilayers Using Dynamic Impedance Spectroscopy Sacci, Robert L.; Scott, Haden L.; Liu, Zening Advanced Electronic Materials, Vol. 8, Issue 5 https://doi.org/10.1002/aelm.202200121	journal	April 2022
Optimal estimates of self-diffusion coefficients from molecular dynamics simulations Bullerjahn, Jakob Tómas; von Bülow, Sören; Hummer, Gerhard The Journal of Chemical Physics, Vol. 153, Issue 2 https://doi.org/10.1063/5.0008312	journal	July 2020
Emergent Optical Phononic Modes upon Nanoscale Mesogenic Phase Transitions Bolmatov, Dima; Zhernenkov, Mikhail; Sharpnack, Lewis Nano Letters, Vol. 17, Issue 6 https://doi.org/10.1021/acs.nanolett.7b01324	journal	May 2017
Piezoelectricity of phospholipids: a possible mechanism for mechanoreception and magnetoreception in biology Jákli, A.; Harden, J.; Notz, C. Liquid Crystals, Vol. 35, Issue 4 https://doi.org/10.1080/02678290801905658	journal	April 2008
Wireless magnetothermal deep brain stimulation Chen, R.; Romero, G.; Christiansen, M. G. Science, Vol. 347, Issue 6229 https://doi.org/10.1126/science.1261821	journal	March 2015
Quantification of in-plane flexoelectricity in lipid bilayers Thomas, Nidhin; Agrawal, Ashutosh EPL (Europhysics Letters), Vol. 134, Issue 6 https://doi.org/10.1209/0295-5075/134/68003	journal	June 2021
Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path Bliss, T. V. P.; Lømo, T. The Journal of Physiology, Vol. 232, Issue 2 https://doi.org/10.1113/jphysiol.1973.sp010273	journal	July 1973
Probing lipid membrane bending mechanics using gold nanorod tracking Molaei, Mehdi; Kandy, Sreeja Kutti; Graber, Zachary T. Physical Review Research, Vol. 4, Issue 1 https://doi.org/10.1103/PhysRevResearch.4.L012027	journal	March 2022
Multiple Interacting Collective Modes and Phonon Gap in Phospholipid Membranes D’Angelo, Giovanna; Nibali, Valeria Conti; Wanderlingh, Ulderico The Journal of Physical Chemistry Letters, Vol. 9, Issue 15 https://doi.org/10.1021/acs.jpclett.8b01658	journal	July 2018
Infrared light excites cells by changing their electrical capacitance Shapiro, Mikhail G.; Homma, Kazuaki; Villarreal, Sebastian Nature Communications, Vol. 3, Issue 1 https://doi.org/10.1038/ncomms1742	journal	January 2012
CHARMM-GUI Membrane Builder toward realistic biological membrane simulations Wu, Emilia L.; Cheng, Xi; Jo, Sunhwan Journal of Computational Chemistry, Vol. 35, Issue 27 https://doi.org/10.1002/jcc.23702	journal	August 2014
Is the tilt of the lipid head group correlated with the number of intermolecular interactions at the bilayer interface? Baczynski, Krzysztof; Markiewicz, Michal; Pasenkiewicz‐Gierula, Marta FEBS Letters, Vol. 592, Issue 9 https://doi.org/10.1002/1873-3468.13048	journal	April 2018
Thermally triggered phononic gaps in liquids at THz scale Bolmatov, Dima; Zhernenkov, Mikhail; Zav’yalov, Dmitry Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19469	journal	January 2016
Functional lipid pairs as building blocks of phase-separated membranes Soloviov, Dmytro; Cai, Yong Q.; Bolmatov, Dima Proceedings of the National Academy of Sciences, Vol. 117, Issue 9 https://doi.org/10.1073/pnas.1919264117	journal	February 2020
Symmetry breaking gives rise to energy spectra of three states of matter Bolmatov, Dima; Musaev, Edvard T.; Trachenko, K. Scientific Reports, Vol. 3, Issue 1 https://doi.org/10.1038/srep02794	journal	September 2013
Thermal effects on neurons during stimulation of the brain Kim, TaeKen; Kadji, Herve; Whalen, Andrew J. Journal of Neural Engineering, Vol. 19, Issue 5 https://doi.org/10.1088/1741-2552/ac9339	journal	October 2022
The phonon theory of liquid thermodynamics Bolmatov, D.; Brazhkin, V. V.; Trachenko, K. Scientific Reports, Vol. 2, Issue 1 https://doi.org/10.1038/srep00421	journal	May 2012
Role of lipid rafts in persistent Helicobacter pylori infection: a narrative review Liu, Renjie; Chen, Yuzuo; Yang, Lu Annals of Translational Medicine, Vol. 10, Issue 6 https://doi.org/10.21037/atm-22-1000	journal	March 2022
The mechanoelectrical response of droplet interface bilayer membranes Freeman, E. C.; Najem, J. S.; Sukharev, S. Soft Matter, Vol. 12, Issue 12 https://doi.org/10.1039/C5SM02779A	journal	January 2016
Clarification of the ripple phase of lecithin bilayers using fully hydrated, aligned samples Katsaras, J.; Tristram-Nagle, S.; Liu, Y. Physical Review E, Vol. 61, Issue 5 https://doi.org/10.1103/PhysRevE.61.5668	journal	May 2000
Dynamic Water Hydrogen-Bond Networks at the Interface of a Lipid Membrane Containing Palmitoyl-Oleoyl Phosphatidylglycerol Karathanou, Konstantina; Bondar, Ana-Nicoleta The Journal of Membrane Biology, Vol. 251, Issue 3 https://doi.org/10.1007/s00232-018-0023-1	journal	March 2018
The Phonon Theory of Liquids and Biological Fluids: Developments and Applications Bolmatov, Dima The Journal of Physical Chemistry Letters, Vol. 13, Issue 31 https://doi.org/10.1021/acs.jpclett.2c01779	journal	August 2022
Real-Space Local Dynamics of Molten Inorganic Salts Using Van Hove Correlation Function Shinohara, Yuya; Ivanov, Alexander S.; Maltsev, Dmitry The Journal of Physical Chemistry Letters, Vol. 13, Issue 25 https://doi.org/10.1021/acs.jpclett.2c01230	journal	June 2022
Deciphering Melatonin-Stabilized Phase Separation in Phospholipid Bilayers Bolmatov, Dima; McClintic, William T.; Taylor, Graham Langmuir, Vol. 35, Issue 37 https://doi.org/10.1021/acs.langmuir.9b01534	journal	August 2019
The push-to-open mechanism of the tethered mechanosensitive ion channel NompC Wang, Yang; Guo, Yifeng; Li, Guanluan eLife, Vol. 10 https://doi.org/10.7554/eLife.58388	journal	June 2021
Heterosynaptic plasticity in biomembrane memristors controlled by pH McClintic, William T.; Scott, Haden L.; Moore, Nick MRS Bulletin, Vol. 48, Issue 1 https://doi.org/10.1557/s43577-022-00344-z	journal	August 2022
X-ray diffraction studies of oriented lipid bilayers Katsaras, J. Biochemistry and Cell Biology, Vol. 73, Issue 5-6 https://doi.org/10.1139/o95-025	journal	May 1995
Split-pulse X-ray photon correlation spectroscopy with seeded X-rays from X-ray laser to study atomic-level dynamics Shinohara, Yuya; Osaka, Taito; Inoue, Ichiro Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-20036-z	journal	December 2020
Curvature–undulation coupling as a basis for curvature sensing and generation in bilayer membranes Bradley, Ryan P.; Radhakrishnan, Ravi Proceedings of the National Academy of Sciences, Vol. 113, Issue 35 https://doi.org/10.1073/pnas.1605259113	journal	August 2016
Multiscale lipid membrane dynamics as revealed by neutron spectroscopy Sharma, V. K.; Mamontov, E. Progress in Lipid Research, Vol. 87 https://doi.org/10.1016/j.plipres.2022.101179	journal	July 2022
Neutron diffraction from aligned stacks of lipid bilayers using the WAND instrument Marquardt, Drew; Frontzek, Matthias D.; Zhao, Yu Journal of Applied Crystallography, Vol. 51, Issue 2 https://doi.org/10.1107/S1600576718001243	journal	February 2018
Probing molecular forces in multi-component physiological membranes Ray, Arjun; Gräter, Frauke; Thukral, Lipi Physical Chemistry Chemical Physics, Vol. 20, Issue 4 https://doi.org/10.1039/C7CP05981G	journal	January 2018
A lateral electric field inhibits gel-to-fluid transition in lipid bilayers Thomas, Nidhin; Agrawal, Ashutosh Soft Matter, Vol. 18, Issue 34 https://doi.org/10.1039/D2SM00740A	journal	January 2022
Lipid Bilayer Structure Determined by the Simultaneous Analysis of Neutron and X-Ray Scattering Data Kučerka, Norbert; Nagle, John F.; Sachs, Jonathan N. Biophysical Journal, Vol. 95, Issue 5 https://doi.org/10.1529/biophysj.108.132662	journal	September 2008
Lipid–protein forces predict conformational changes in a mechanosensitive channel Daday, Csaba; de Groot, Bert L. European Biophysics Journal, Vol. 50, Issue 2 https://doi.org/10.1007/s00249-020-01488-z	journal	December 2020
Passive transport of Ca2+ ions through lipid bilayers imaged by widefield second harmonic microscopy Eremchev, Maksim; Roesel, David; Poojari, Chetan S. Biophysical Journal, Vol. 122, Issue 4 https://doi.org/10.1016/j.bpj.2023.01.018	journal	February 2023
Lipid Domain Co-localization Induced by Membrane Undulations Haataja, Mikko P. Biophysical Journal, Vol. 112, Issue 4 https://doi.org/10.1016/j.bpj.2016.12.030	journal	February 2017
Neuromorphic functions with a polyelectrolyte-confined fluidic memristor Xiong, Tianyi; Li, Changwei; He, Xiulan Science, Vol. 379, Issue 6628 https://doi.org/10.1126/science.adc9150	journal	January 2023
Evidence for long-term potentiation in phospholipid membranes Scott, Haden L.; Bolmatov, Dima; Podar, Peter T. Proceedings of the National Academy of Sciences, Vol. 119, Issue 50 https://doi.org/10.1073/pnas.2212195119	journal	December 2022
Low-THz Vibrations of Biological Membranes Luyet, Chloe; Elvati, Paolo; Vinh, Jordan Membranes, Vol. 13, Issue 2 https://doi.org/10.3390/membranes13020139	journal	January 2023
Dynamical nonlinear memory capacitance in biomimetic membranes Najem, Joseph S.; Hasan, Md Sakib; Williams, R. Stanley Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11223-8	journal	July 2019
Feeling the hidden mechanical forces in lipid bilayer is an original sense Anishkin, A.; Loukin, S. H.; Teng, J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 22 https://doi.org/10.1073/pnas.1313364111	journal	May 2014
Ion-Induced Defect Permeation of Lipid Membranes Vorobyov, Igor; Olson, Timothy E.; Kim, Jung H. Biophysical Journal, Vol. 106, Issue 3 https://doi.org/10.1016/j.bpj.2013.12.027	journal	February 2014
Intermolecular Hydrogen-Bond Interactions in DPPE and DMPC Phospholipid Membranes Revealed by Far-Infrared Spectroscopy Conti Nibali, Valeria; Branca, Caterina; Wanderlingh, Ulderico Applied Sciences, Vol. 11, Issue 21 https://doi.org/10.3390/app112110038	journal	October 2021
Stress Propagation through Biological Lipid Bilayers in Silico Aponte-Santamaría, Camilo; Brunken, Jan; Gräter, Frauke Journal of the American Chemical Society, Vol. 139, Issue 39 https://doi.org/10.1021/jacs.7b04724	journal	September 2017
Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations Zhernenkov, Mikhail; Bolmatov, Dima; Soloviov, Dmitry Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11575	journal	May 2016
Crossover from picosecond collective to single particle dynamics defines the mechanism of lateral lipid diffusion Bolmatov, Dima; Cai, Yong Q.; Zav’yalov, Dmitry Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1860, Issue 11 https://doi.org/10.1016/j.bbamem.2018.07.004	journal	November 2018
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
Modulation of Membrane Fluidity to Control Interfacial Water Structure and Dynamics in Saturated and Unsaturated Phospholipid Vesicles Mondal, Dipankar; Malik, Sheeba; Banerjee, Pavel Langmuir, Vol. 36, Issue 41 https://doi.org/10.1021/acs.langmuir.0c02736	journal	October 2020
Mesoscopic Undulations and Thickness Fluctuations in Lipid Bilayers from Molecular Dynamics Simulations Lindahl, Erik; Edholm, Olle Biophysical Journal, Vol. 79, Issue 1 https://doi.org/10.1016/S0006-3495(00)76304-1	journal	July 2000
Correlations in Space and Time and Born Approximation Scattering in Systems of Interacting Particles Van Hove, Léon Physical Review, Vol. 95, Issue 1 https://doi.org/10.1103/PhysRev.95.249	journal	July 1954
Correlated atomic dynamics in liquid seen in real space and time Egami, Takeshi; Shinohara, Yuya The Journal of Chemical Physics, Vol. 153, Issue 18 https://doi.org/10.1063/5.0024013	journal	November 2020
Anomalous Nanoscale Optoacoustic Phonon Mixing in Nematic Mesogens Bolmatov, Dima; Soloviov, Dmytro; Zav’yalov, Dmitry The Journal of Physical Chemistry Letters, Vol. 9, Issue 10 https://doi.org/10.1021/acs.jpclett.8b00926	journal	April 2018
Double membrane formation in heterogeneous vesicles Bolmatov, Dima; Carrillo, Jan-Michael Y.; Sumpter, Bobby G. Soft Matter, Vol. 16, Issue 38 https://doi.org/10.1039/D0SM01167C	journal	January 2020
Nanoscale Structure and Dynamics of Model Membrane Lipid Raft Systems, Studied by Neutron Scattering Methods Ahmadi, Delaram; Thompson, Katherine C.; García Sakai, Victoria Frontiers in Physics, Vol. 10 https://doi.org/10.3389/fphy.2022.864746	journal	April 2022
Chirality of lipids makes fluid lamellar phases piezoelectric Harden, John; Diorio, Nicholas; Petrov, Alexander G. Physical Review E, Vol. 79, Issue 1 https://doi.org/10.1103/PhysRevE.79.011701	journal	January 2009

Similar Records

Evidence for long-term potentiation in phospholipid membranes

Journal Article · 2022 · Proceedings of the National Academy of Sciences of the United States of America · OSTI ID:1905385

Scott, Haden L.; Bolmatov, Dima; Podar, Peter T.; +7 more

Freezing of phosphocholine headgroup in fully hydrated sphingomyelin bilayers and its effect on the dynamics of nonfreezable water at subzero temperatures

Journal Article · 1991 · Journal of Biological Chemistry; (United States) · OSTI ID:5394079

Wu, W G; Chi, L M; Yang, T S; +1 more

Magnetic resonance studies of membrane and model membrane systems. V. Comparisons of aqueous dispersions of pure and mixed phospholipids

Journal Article · 1973 · Ann. N.Y. Acad. Sci.; (United States) · OSTI ID:6478229

Horwitz, A F; Klein, M P; Michaelson, D M; +1 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
zwitterionic lipid bilayers
POPC
DPPC
headgroup dipoles
collective dipole motions
Van Hove correlation functions
heat transfer
surface undulations
piezoelectricity
flexoelectricity

Title: Real Space and Time Imaging of Collective Headgroup Dipole Motions in Zwitterionic Lipid Bilayers

Citation Formats

References (82)

Similar Records

Related Subjects