Super-swelling behavior of stacked lipid bilayer systems

Rueben, Jacob; Steer, Dylan; Leal, Cecília

doi:10.1140/epje/s10189-023-00322-6

Super-swelling behavior of stacked lipid bilayer systems

Journal Article · Thu Aug 03 00:00:00 EDT 2023 · European Physical Journal. E, Soft Matter (print)

DOI:https://doi.org/10.1140/epje/s10189-023-00322-6· OSTI ID:2423673

Rueben, Jacob ^[1]; Steer, Dylan ^[1]; ^[1]

Univ. of Illinois at Urbana-Champaign, IL (United States)

Bilayer systems comprising lipid mixtures are the most well-studied model of biological membranes. While the plasma membrane of the cell is a single bilayer, many intra- and extra-cellular biomembranes comprise stacks of bilayers. Most bilayer stacks in nature are periodic, maintaining a precise water layer separation between bilayers. That equilibrium water separation is governed by multiple inter-bilayer forces and is highly responsive. Biomembranes re-configure inter-bilayer spacing in response to temperature, composition, or mass transport cues. In synthetic bilayer systems for applications in cosmetics or topical treatments, control of the hydration level is a critical design handle. Herein we investigate a binary lipid system that leverages key inter-bilayer forces leading to unprecedented levels of aqueous swelling while maintaining a coherent multilamellar form. We found that combining cationic lipids with bicontinuous cubic phase-forming lipids (lipids with positive Gaussian modulus), results in the stabilization of multilamellar phases against repulsive steric forces that typically lead to bilayer delamination at high degrees of swelling. Using ultra-small-angle X-ray scattering alongside confocal laser scanning microscopy, we characterized various super-swelled states of 1,2-dioleoyl-3-trimethylammonium-propane (DOTAP) and glycerol monooleate (GMO) lipids, as well as other analogous systems, at varied concentration and molar ratios. Through these experiments we established swelling profiles of various binary lipid systems that were near-linear with decreasing lipid volume fraction, showing maximum swelling with periodicity well above 200 nanometers.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: USDOE; US Department of the Navy, Office of Naval Research (ONR); National Institutes of Health (NIH)

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 2423673

Journal Information:: European Physical Journal. E, Soft Matter (print), Journal Name: European Physical Journal. E, Soft Matter (print) Journal Issue: 8 Vol. 46; ISSN 1292-8941

Publisher:: EDP SciencesCopyright Statement

Country of Publication:: United States

Language:: English

References (37)

Liquid Crystals as a Potential Ointment Vehicle Wahlgren, Sven; Lindstrom, Anna L.; Fribergx, Stic E. Journal of Pharmaceutical Sciences, Vol. 73, Issue 10 https://doi.org/10.1002/jps.2600731042	journal	October 1984
Architecture of Thylakoid Membrane Networks Nevo, Reinat; Chuartzman, Silvia G.; Tsabari, Onie Lipids in Photosynthesis https://doi.org/10.1007/978-90-481-2863-1_14	book	January 2009
Extreme swelling of a lyotropic lamellar liquid crystal Appell, J.; Bassereau, P.; Marignan, J. Colloid & Polymer Science, Vol. 267, Issue 7 https://doi.org/10.1007/BF01410437	journal	July 1989
Structural relationships between lamellar, cubic and hexagonal phases in monoglyceride-water systems. possibility of cubic structures in biological systems Larsson, K.; Fontell, K.; Krog, N. Chemistry and Physics of Lipids, Vol. 27, Issue 4 https://doi.org/10.1016/0009-3084(80)90026-2	journal	December 1980
Structure and drug release of lamellar liquid crystals containing glycerol Makai, M.; Csányi, E.; Németh, Zs International Journal of Pharmaceutics, Vol. 256, Issue 1-2 https://doi.org/10.1016/S0378-5173(03)00066-8	journal	April 2003
Pulmonary surfactant: functions and molecular composition Goerke, Jon Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1408, Issue 2-3 https://doi.org/10.1016/S0925-4439(98)00060-X	journal	November 1998
Swelling limits for bilayer microstructures: the implosion of lamellar structure versus disordered lamellae Dubois, M.; Zemb, Th Current Opinion in Colloid & Interface Science, Vol. 5, Issue 1-2 https://doi.org/10.1016/S1359-0294(00)00032-7	journal	March 2000
Influence of the emollient structure on the properties of cosmetic emulsion containing lamellar liquid crystals Terescenco, Daria; Picard, Celine; Clemenceau, Florence Colloids and Surfaces A: Physicochemical and Engineering Aspects, Vol. 536 https://doi.org/10.1016/j.colsurfa.2017.08.017	journal	January 2018
Phytantriol based smart nano-carriers for drug delivery applications Akbar, Samina; Anwar, Aneela; Ayish, Abdullah European Journal of Pharmaceutical Sciences, Vol. 101 https://doi.org/10.1016/j.ejps.2017.01.035	journal	April 2017
Stimuli responsive liquid crystals provide ‘on-demand’ drug delivery in vitro and in vivo Fong, Wye-Khay; Hanley, Tracey; Boyd, Ben J. Journal of Controlled Release, Vol. 135, Issue 3 https://doi.org/10.1016/j.jconrel.2009.01.009	journal	May 2009
Structure of Lung-Mimetic Multilamellar Bodies with Lipid Compositions Relevant in Pneumonia Steer, Dylan; Leung, Sherry S. W.; Meiselman, Hannah Langmuir, Vol. 34, Issue 25 https://doi.org/10.1021/acs.langmuir.8b01359	journal	May 2018
Surfactant Systems with Charged Multilamellar Vesicles and Their Rheological Properties Hoffmann, H.; Thunig, C.; Schmiedel, P. Langmuir, Vol. 10, Issue 11 https://doi.org/10.1021/la00023a013	journal	November 1994
Entropic Attraction Condenses Like-Charged Interfaces Composed of Self-Assembled Molecules Steiner, Ariel; Szekely, Pablo; Szekely, Or Langmuir, Vol. 28, Issue 5 https://doi.org/10.1021/la203540p	journal	January 2012
Salt Effects on Lamellar Repeat Distance Depending on Head Groups of Neutrally Charged Lipids Hishida, Mafumi; Yamamura, Yasuhisa; Saito, Kazuya Langmuir, Vol. 30, Issue 35 https://doi.org/10.1021/la502576x	journal	August 2014
Swollen liquid-crystalline lamellar phase based on extended solid-like sheets Gabriel, Jean-Christophe P.; Camerel, Franck; Lemaire, Bruno J. Nature, Vol. 413, Issue 6855 https://doi.org/10.1038/35097046	journal	October 2001
Dynamic regulation of cardiolipin by the lipid pump Atp8b1 determines the severity of lung injury in experimental pneumonia Ray, Nancy B.; Durairaj, Lakshmi; Chen, Bill B. Nature Medicine, Vol. 16, Issue 10 https://doi.org/10.1038/nm.2213	journal	September 2010
U1 snRNP regulates cancer cell migration and invasion in vitro Oh, Jung-Min; Venters, Christopher C.; Di, Chao Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-019-13993-7	journal	January 2020
Revealing the Dynamics of Thylakoid Membranes in Living Cyanobacterial Cells Stingaciu, Laura-Roxana; O’Neill, Hugh; Liberton, Michelle Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep19627	journal	January 2016
The stabilization of primitive bicontinuous cubic phases with tunable swelling over a wide composition range Leung, Sherry S. W.; Leal, Cecilia Soft Matter, Vol. 15, Issue 6 https://doi.org/10.1039/C8SM02059K	journal	January 2019
Engineering bicontinuous cubic structures at the nanoscale—the role of chain splay Kulkarni, Chandrashekhar V.; Tang, Tsing-Young; Seddon, Annela M. Soft Matter, Vol. 6, Issue 14 https://doi.org/10.1039/c0sm00068j	journal	January 2010
Surfactant systems: their use in drug delivery Lawrence, M. Jayne Chemical Society Reviews, Vol. 23, Issue 6 https://doi.org/10.1039/cs9942300417	journal	January 1994
A synchrotron X-ray study of competing undulation and electrostatic interlayer interactions in fluid multimembrane lyotropic phases Roux, D.; Safinya, C. R. Journal de Physique, Vol. 49, Issue 2 https://doi.org/10.1051/jphys:01988004902030700	journal	January 1988
Hydrodynamics of lyotropic smectics : a dynamic light scattering study of dilute lamellar phases Nallet, F.; Roux, D.; Prost, J. Journal de Physique, Vol. 50, Issue 20 https://doi.org/10.1051/jphys:0198900500200314700	journal	January 1989
On the origin of the thermodynamic stability of lyotropic lamellar liquid crystals Ruckenstein, Eli The Journal of Chemical Physics, Vol. 109, Issue 16 https://doi.org/10.1063/1.477335	journal	October 1998
Super-swelled lyotropic single crystals Kim, Hojun; Song, Ziyuan; Leal, Cecilia Proceedings of the National Academy of Sciences, Vol. 114, Issue 41 https://doi.org/10.1073/pnas.1710774114	journal	September 2017
Experimental Study of Swollen Lyotropic Lamellar Phases Marignan, J.; Appell, J.; Bassereau, P. Molecular Crystals and Liquid Crystals Incorporating Nonlinear Optics, Vol. 152, Issue 1 https://doi.org/10.1080/00268948708070950	journal	November 1987
The Structure of the Liquid-Crystalline Phases of Lipid-Water Systems Luzzati, V.; Husson, F. The Journal of Cell Biology, Vol. 12, Issue 2 https://doi.org/10.1083/jcb.12.2.207	journal	February 1962
The hardening transition in swollen lamellar phases Sornette, D. Journal of Physics: Condensed Matter, Vol. 1, Issue 10 https://doi.org/10.1088/0953-8984/1/10/014	journal	March 1989
Quality Control of Photosystem II: Direct Imaging of the Changes in the Thylakoid Structure and Distribution of FtsH Proteases in Spinach Chloroplasts under Light Stress Yoshioka-Nishimura, Miho; Nanba, Daisuke; Takaki, Takashi Plant and Cell Physiology, Vol. 55, Issue 7 https://doi.org/10.1093/pcp/pcu079	journal	June 2014
Complete unbinding and quasi-long-range order in lamellar phases Leibler, Stanislas; Lipowsky, Reinhard Physical Review B, Vol. 35, Issue 13 https://doi.org/10.1103/PhysRevB.35.7004	journal	May 1987
Dynamic light scattering from a highly swollen nonionic lamellar liquid crystal Zhang, C. Y.; Sprunt, S.; Litster, J. D. Physical Review E, Vol. 48, Issue 4 https://doi.org/10.1103/PhysRevE.48.2850	journal	October 1993
Sponge-lamellar instability of fluctuating membranes Pieruschka, P. Physical Review E, Vol. 52, Issue 4 https://doi.org/10.1103/PhysRevE.52.3989	journal	October 1995
Extreme Swelling of a Lyotropic Lamellar Liquid Crystal Larche, F. C.; Appell, J.; Porte, G. Physical Review Letters, Vol. 56, Issue 16 https://doi.org/10.1103/PhysRevLett.56.1700	journal	April 1986
Unbinding Transitions of Interacting Membranes Lipowsky, Reinhard; Leibler, Stanislas Physical Review Letters, Vol. 56, Issue 23 https://doi.org/10.1103/PhysRevLett.56.2541	journal	June 1986
Dispersions of lamellar phases of non‐ionic lipids in cosmetic products Handjani‐Vila, R. M.; Ribier, A.; Rondot, B. International Journal of Cosmetic Science, Vol. 1, Issue 5 https://doi.org/10.1111/j.1467-2494.1979.tb00224.x	journal	October 1979
Non-Linear Effects of Membrane Fluctuations in the Dilute Lamellar Phase Ramaswamy, Sriram; Prost, J.; Lubensky, T. C. Europhysics Letters (EPL), Vol. 27, Issue 4 https://doi.org/10.1209/0295-5075/27/4/006	journal	August 1994
Multiscale compression-induced restructuring of stacked lipid bilayers: From buckling delamination to molecular packing Porras-Gómez, Marilyn; Kim, Hyunchul; Dronadula, Mohan Teja PLOS ONE, Vol. 17, Issue 12 https://doi.org/10.1371/journal.pone.0275079	journal	December 2022

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