Interdigitation-Induced Order and Disorder in Asymmetric Membranes

Frewein, Moritz P. K.; Piller, Paulina; Semeraro, Enrico F.; Batchu, Krishna C.; Heberle, Frederick A.; Scott, Haden L.; Gerelli, Yuri; Porcar, Lionel; Pabst, Georg

doi:10.1007/s00232-022-00234-0

Interdigitation-Induced Order and Disorder in Asymmetric Membranes

Journal Article · Tue Apr 26 00:00:00 EDT 2022 · Journal of Membrane Biology

DOI:https://doi.org/10.1007/s00232-022-00234-0· OSTI ID:2471416

Frewein, Moritz P. K. ^[1]; Piller, Paulina ^[2]; Semeraro, Enrico F. ^[2]; Batchu, Krishna C. ^[3]; Heberle, Frederick A. ^[4]; Scott, Haden L. ^[5]; Gerelli, Yuri ^[6]; Porcar, Lionel ^[3]; ^[2]

University of Graz (Austria); Institut Laue-Langevin, Grenoble (France); BioTechMed Graz (Austria); Field of Excellence BioHealth, Graz (Austria)
University of Graz (Austria); BioTechMed Graz (Austria); Field of Excellence BioHealth, Graz (Austria)
Institut Laue-Langevin, Grenoble (France)
University of Tennessee, Knoxville, TN (United States)
University of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Università Politecnica delle Marche, Ancona (Italy)

We studied the transleaflet coupling of compositionally asymmetric liposomes in the fluid phase. The vesicles were produced by cyclodextrin-mediated lipid exchange and contained dipalmitoyl phosphatidylcholine (DPPC) in the inner leaflet and different mixed-chain phosphatidylcholines (PCs) as well as milk sphingomyelin (MSM) in the outer leaflet. In order to jointly analyze the obtained small-angle neutron and X-ray scattering data, we adapted existing models of trans-bilayer structures to measure the overlap of the hydrocarbon chain termini by exploiting the contrast of the terminal methyl ends in X-ray scattering. In all studied systems, the bilayer-asymmetry has large effects on the lipid packing density. Fully saturated mixed-chain PCs interdigitate into the DPPC-containing leaflet and evoke disorder in one or both leaflets. The long saturated acyl chains of MSM penetrate even deeper into the opposing leaflet, which in turn has an ordering effect on the whole bilayer. These results are qualitatively understood in terms of a balance of entropic repulsion of fluctuating hydrocarbon chain termini and van der Waals forces, which is modulated by the interdigitation depth. Monounsaturated PCs in the outer leaflet also induce disorder in DPPC despite vestigial or even absent interdigitation. Instead, the transleaflet coupling appears to emerge here from a matching of the inner leaflet lipids to the larger lateral lipid area of the outer leaflet lipids.

View Accepted Manuscript (DOE)

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

Sponsoring Organization:: Austrian Science Fund (FWF); ILL graduate school; USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 2471416

Journal Information:: Journal of Membrane Biology, Journal Name: Journal of Membrane Biology Journal Issue: 4-5 Vol. 255; ISSN 0022-2631

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (26)

The asymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microscopy Verkleij, A. J.; Zwaal, R. F. A.; Roelofsen, B. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 323, Issue 2 https://doi.org/10.1016/0005-2736(73)90143-0	journal	October 1973
Interdigitation does not affect translational diffusion of lipids in liquid crystalline bilayers Schram, V.; Thompson, T. E. Biophysical Journal, Vol. 69, Issue 6 https://doi.org/10.1016/S0006-3495(95)80122-0	journal	December 1995
Interdigitation of long-chain sphingomyelin induces coupling of membrane leaflets in a cholesterol dependent manner Róg, Tomasz; Orłowski, Adam; Llorente, Alicia Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 2 https://doi.org/10.1016/j.bbamem.2015.12.003	journal	February 2016
Acyl Chain Length and Saturation Modulate Interleaflet Coupling in Asymmetric Bilayers: Effects on Dynamics and Structural Order Chiantia, Salvatore; London, Erwin Biophysical Journal, Vol. 103, Issue 11 https://doi.org/10.1016/j.bpj.2012.10.033	journal	December 2012
Intrinsic Curvature-Mediated Transbilayer Coupling in Asymmetric Lipid Vesicles Eicher, Barbara; Marquardt, Drew; Heberle, Frederick A. Biophysical Journal, Vol. 114, Issue 1 https://doi.org/10.1016/j.bpj.2017.11.009	journal	January 2018
Spontaneous Curvature, Differential Stress, and Bending Modulus of Asymmetric Lipid Membranes Hossein, Amirali; Deserno, Markus Biophysical Journal, Vol. 118, Issue 3 https://doi.org/10.1016/j.bpj.2019.11.3398	journal	February 2020
From zero to six double bonds: phospholipid unsaturation and organelle function Antonny, Bruno; Vanni, Stefano; Shindou, Hideo Trends in Cell Biology, Vol. 25, Issue 7 https://doi.org/10.1016/j.tcb.2015.03.004	journal	July 2015
Revisiting Volumes of Lipid Components in Bilayers Nagle, John F.; Venable, Richard M.; Maroclo-Kemmerling, Ezekiel The Journal of Physical Chemistry B, Vol. 123, Issue 12 https://doi.org/10.1021/acs.jpcb.8b12010	journal	March 2019
Subnanometer Structure of an Asymmetric Model Membrane: Interleaflet Coupling Influences Domain Properties Heberle, Frederick A.; Marquardt, Drew; Doktorova, Milka Langmuir, Vol. 32, Issue 20 https://doi.org/10.1021/acs.langmuir.5b04562	journal	May 2016
Peptide-Induced Lipid Flip-Flop in Asymmetric Liposomes Measured by Small Angle Neutron Scattering Nguyen, Michael H. L.; DiPasquale, Mitchell; Rickeard, Brett W. Langmuir, Vol. 35, Issue 36 https://doi.org/10.1021/acs.langmuir.9b01625	journal	August 2019
Curvature Effect on the Structure of Phospholipid Bilayers Kučerka, Norbert; Pencer, Jeremy; Sachs, Jonathan N. Langmuir, Vol. 23, Issue 3 https://doi.org/10.1021/la062455t	journal	January 2007
Asymmetrical Lipid Bilayer Structure for Biological Membranes Bretscher, Mark S. Nature New Biology, Vol. 236, Issue 61 https://doi.org/10.1038/newbio236011a0	journal	March 1972
Plasma membranes are asymmetric in lipid unsaturation, packing and protein shape Lorent, J. H.; Levental, K. R.; Ganesan, L. Nature Chemical Biology, Vol. 16, Issue 6 https://doi.org/10.1038/s41589-020-0529-6	journal	May 2020
SciPy 1.0: fundamental algorithms for scientific computing in Python Virtanen, Pauli; Gommers, Ralf; Oliphant, Travis E. Nature Methods https://doi.org/10.1038/s41592-019-0686-2	journal	February 2020
Preparation of asymmetric phospholipid vesicles for use as cell membrane models Doktorova, Milka; Heberle, Frederick A.; Eicher, Barbara Nature Protocols, Vol. 13, Issue 9 https://doi.org/10.1038/s41596-018-0033-6	journal	September 2018
Increasing complexity in small-angle X-ray and neutron scattering experiments: from biological membrane mimics to live cells Semeraro, Enrico F.; Marx, Lisa; Frewein, Moritz P. K. Soft Matter, Vol. 17, Issue 2 https://doi.org/10.1039/C9SM02352F	journal	January 2021
Antimicrobial peptide activity in asymmetric bacterial membrane mimics Marx, Lisa; Frewein, Moritz P. K.; Semeraro, Enrico F. Faraday Discussions, Vol. 232 https://doi.org/10.1039/D1FD00039J	journal	January 2021
Dynamic Transbilayer Lipid Asymmetry van Meer, G. Cold Spring Harbor Perspectives in Biology, Vol. 3, Issue 5 https://doi.org/10.1101/cshperspect.a004671	journal	March 2011
Long and Short Lipid Molecules Experience the Same Interleaflet Drag in Lipid Bilayers Horner, Andreas; Akimov, Sergey A.; Pohl, Peter Physical Review Letters, Vol. 110, Issue 26 https://doi.org/10.1103/PhysRevLett.110.268101	journal	June 2013
X-ray scattering from unilamellar lipid vesicles Brzustowicz, Michael R.; Brunger, Axel T. Journal of Applied Crystallography, Vol. 38, Issue 1 https://doi.org/10.1107/S0021889804029206	journal	January 2005
Method of separated form factors for polydisperse vesicles Pencer, Jeremy; Krueger, Susan; Adams, Carl P. Journal of Applied Crystallography, Vol. 39, Issue 3 https://doi.org/10.1107/S0021889806005255	journal	May 2006
The rise of BioSAXS at the ESRF: BM29 beamline for SAXS on proteins in solution Pernot, Petra; Brennich, Martha; Tully, Mark Acta Crystallographica Section A Foundations and Advances, Vol. 74, Issue a1 https://doi.org/10.1107/S0108767318099920	journal	July 2018
Joint small-angle X-ray and neutron scattering data analysis of asymmetric lipid vesicles Eicher, Barbara; Heberle, Frederick A.; Marquardt, Drew Journal of Applied Crystallography, Vol. 50, Issue 2 https://doi.org/10.1107/S1600576717000656	journal	February 2017
The Fluid Mosaic Model of the Structure of Cell Membranes Singer, S. J.; Nicolson, G. L. Science, Vol. 175, Issue 4023 https://doi.org/10.1126/science.175.4023.720	journal	February 1972
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
Structure and Interdigitation of Chain-Asymmetric Phosphatidylcholines and Milk Sphingomyelin in the Fluid Phase Frewein, Moritz P. K.; Doktorova, Milka; Heberle, Frederick A. Symmetry, Vol. 13, Issue 8 https://doi.org/10.3390/sym13081441	journal	August 2021

Similar Records

Structure and Interdigitation of Chain-Asymmetric Phosphatidylcholines and Milk Sphingomyelin in the Fluid Phase

Journal Article · Wed Aug 04 20:00:00 EDT 2021 · Symmetry · OSTI ID:2471481

Binary mixtures of asymmetric phosphatidylcholines with one acyl chain twice as long as the other

Journal Article · Tue Aug 25 00:00:00 EDT 1987 · Biochemistry; (United States) · OSTI ID:5876785

Joint small-angle X-ray and neutron scattering data analysis of asymmetric lipid vesicles

Journal Article · Mon Feb 27 19:00:00 EST 2017 · Journal of Applied Crystallography (Online) · OSTI ID:1351774

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Asymmetric membranes
Biochemistry & Molecular Biology
Cell Biology
Cyclodextrin
Physiology
Small-angle X-ray scattering
Small-angle neutron scattering
Transleaflet coupling

Interdigitation-Induced Order and Disorder in Asymmetric Membranes

Citation Formats

References (26)

Similar Records

Related Subjects