Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions
Abstract
1. Introduction
2. Free Energy of Phase Separation
3. Phase Separation in Charged Membranes
4. Phase Separation Induced by Chemical Reactions within a Bilayer
5. Effect of Membrane Tension on Phase Separation
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Alberts, B.; Johnson, A.; Walter, P.; Lewis, J.; Raff, M. Molecular Biology of the Cell; Garland Science: New York, NY, USA, 2008. [Google Scholar]
- Simons, K.; Ikonen, E. Functional rafts in cell membranes. Nature 1997, 387, 569–572. [Google Scholar] [CrossRef] [PubMed]
- Hancock, J.F. Lipid rafts: Contentious only from simplistic standpoints. Nat. Rev. Mol. Cell Biol. 2006, 7, 456–462. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Simons, K.; Sampaion, J.L. Membrane Organization and Lipid Rafts. Cold Spring Harb. Perspect. Biol. 2011, 3, a004697. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Brown, D.A.; London, E. Structure and function of sphingolipid- and cholesterol-rich membrane rafts. J. Biol. Chem. 2000, 275, 17221–17224. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Varshney, P.; Yadav, V.; Saini, N. Lipid rafts in immune signalling: Current progress and future perspective. Immunology 2016, 149, 13–24. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Yang, S.-T.; Kiessling, V.; Yamm, L.K. Line tension at lipid phase boundaries as driving force for HIV fusion peptide-mediated fusion. Nat. Commun. 2016, 7, 11401. [Google Scholar] [CrossRef]
- Shen, Y.; Zhao, Z.; Zhang, L.; Shi, L.; Shahriar, S.; Chan, R.B.; Paolo, G.D.; Min, W. Metabolic activity induces membrane phase separation in endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 2017, 114, 13394–13399. [Google Scholar] [CrossRef][Green Version]
- King, C.; Sengupta, P.; Seo, A.Y.; Lippincott-Schwartz, J. ER membranes exhibit phase behavior at sites of organelle contact. Proc. Natl. Acad. Sci. USA 2020, 117, 7225–7235. [Google Scholar] [CrossRef][Green Version]
- Walde, P.; Cosentino, K.; Engel, H.; Stano, P. Giant Vesicles: Preparations and Applications. ChemBioChem 2010, 11, 848–865. [Google Scholar] [CrossRef]
- Hamada, T.; Yoshikawa, K. Cell-Sized Liposomes and Droplets: Real-World Modeling of Living Cells. Materials 2012, 5, 2292–2305. [Google Scholar] [CrossRef]
- Dimova, R. Giant Vesicles and Their Use in Assays for Assessing Membrane Phase State, Curvature, Mechanics, and Electrical Properties. Annu. Rev. Phys. 2019, 48, 93–119. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Wang, X.; Du, H.; Wang, Z.; Mu, W.; Han, X. Versatile Phospholipid Assemblies for Functional Synthetic Cells and Artificial Tissues. Adv. Mat. 2021, 33, 2002635. [Google Scholar] [CrossRef] [PubMed]
- Miele, Y.; Holló, G.; Lagzi, I.; Rossi, F. Shape Deformation, Budding and Division of Giant Vesicles and Artificial Cells: A Review. Life 2022, 12, 841. [Google Scholar] [CrossRef]
- Suzuki, Y.; Nagai, K.H.; Zinchenko, A.; Hamada, T. Photoinduced Fusion of Lipid Bilayer Membranes. Langmuir 2017, 33, 2671–2676. [Google Scholar] [CrossRef] [PubMed]
- Dietrich, C.; Bagatolli, L.A.; Volovyk, Z.N.; Thompson, N.L.; Levi, M.; Jacobson, K.; Gratton, E. Lipid Rafts Reconstituted in Model Membranes. Biophys. J. 2001, 80, 1417–1428. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Korlach, J.; Schwille, P.; Webb, W.W.; Feigenson, G.W. Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. USA 1999, 96, 8461–8466. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Baumgart, T.; Hess, S.T.; Webb, W.W. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 2003, 425, 821–824. [Google Scholar] [CrossRef]
- Baumgart, T.; Hammond, A.T.; Sengupta, P.; Webb, W.W. Large-scale fluid/fluid phase separation of proteins and lipids in giant plasma membrane vesicles. Proc. Natl. Acad. Sci. USA 2007, 104, 3165–3170. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Hamada, T.; Morita, M.; Miyakawa, M.; Sugimoto, R.; Hatanaka, A.; Vestergaard, M.C.; Takagi, M. Size-dependent partitioning of nano/microparticles mediated by membrane lateral heterogeneity. J. Am. Chem. Soc. 2012, 134, 13990–13996. [Google Scholar] [CrossRef] [PubMed]
- Jones, R.A.L. Soft Condensed Matter; Oxford University Press: Oxford, UK, 2002. [Google Scholar]
- Veatch, S.L.; Keller, S.L. Separation of Liquid Phases in Giant Vesicles of Ternary Mixtures of Phospholipids and Cholesterol. Biophys. J. 2003, 85, 3074–3083. [Google Scholar] [CrossRef][Green Version]
- Veatch, S.L.; Keller, S.L. Organization in Lipid Membranes Containing Cholesterol. Phys. Rev. Lett. 2002, 89, 268101. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Veatch, S.L.; Keller, S.L. Miscibility Phase Diagrams of Giant Vesicles Containing Sphingomyelin. Phys. Rev. Lett. 2005, 94, 148101. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Johnson, S.A.; Stinson, B.M.; Go, M.S.; Carmona, L.M.; Reminick, J.I.; Fang, X.; Baumgart, T. Temperature-dependent phase behavior and protein partitioning in giant plasma membrane vesicles. Biochim. Biophys. Acta 2010, 1798, 1427–1435. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Hamada, T.; Miura, Y.; Ishii, K.; Araki, S.; Yoshikawa, K.; Vestergaard, M.; Takagi, M. Dynamic Processes in Endocytic Transformation of a Raft-Exhibiting Giant Liposome. J. Phys. Chem. B 2007, 111, 10853–10857. [Google Scholar] [CrossRef] [PubMed]
- Flory, P.J. Thermodynamics of High Polymer Solutions. J. Chem. Phys. 1942, 10, 51. [Google Scholar] [CrossRef]
- Huggins, M.L. Some Properties of Solutions of Long-chain Compounds. J. Phys. Chem. 1942, 46, 151–158. [Google Scholar] [CrossRef]
- Wagner, J.; Loew, S.; May, S. Influence of monolayer-monolayer coupling on the phase behavior of a fluid lipid bilayer. Biophys. J. 2007, 93, 4268–4277. [Google Scholar] [CrossRef][Green Version]
- Shimokawa, N.; Hishida, M.; Seto, H.; Yoshikawa, K. Phase separation of a mixture of charged and neutral lipids on a giant vesicle induced by small cations. Chem. Phys. Lett. 2010, 496, 59–63. [Google Scholar] [CrossRef][Green Version]
- Komura, S.; Andelman, D. Physical aspects of heterogeneities in multi-component lipid membranes. Adv. Colloid Interface Sci. 2014, 208, 34–46. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Komura, S.; Shirotori, H.; Olmsted, P.D.; Andelman, D. Lateral phase separation in mixtures of lipids and cholesterol. EPL 2004, 67, 321–327. [Google Scholar] [CrossRef][Green Version]
- Komura, S.; Shirotori, H.; Olmsted, P.D. Phase behaviour of three-component lipid mixtures. J. Phys. Condens. Matter 2005, 17, S2951–S2956. [Google Scholar] [CrossRef][Green Version]
- Shimokawa, N.; Komura, S.; Andelman, D. The phase behavior of mixed lipid membranes in the presence of the rippled phase. Eur. Phys. J. E 2008, 26, 197–204. [Google Scholar] [CrossRef]
- Shimokawa, N.; Himeno, H.; Hamada, T.; Takagi, M.; Komura, S.; Andelman, D. Phase Diagrams and Ordering in Charged Membranes: Binary Mixtures of Charged and Neutral Lipids. J. Phys. Chem. B 2016, 120, 6358–6367. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Vist, M.R.; Davis, J.H. Phase equilibria of cholesterol/dipalmitoylphosphatidylcholine mixtures: Deuterium nuclear magnetic resonance and differential scanning calorimetry. Biochemistry 1990, 29, 451–464. [Google Scholar] [CrossRef]
- Putzel, G.G.; Schick, M. Phase Behavior of a Model Bilayer Membrane with Coupled Leaves. Biophys. J. 2008, 94, 869–877. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Rozovsky, S.; Kaizuka, Y.; Groves, J.T. Formation and Spatio-Temporal Evolution of Periodic Structures in Lipid Bilayers. J. Am. Chem. Soc. 2005, 127, 36–37. [Google Scholar] [CrossRef] [PubMed]
- Yanagisawa, M.; Shimokawa, N.; Ichikawa, M.; Yoshikawa, K. Micro-segregation induced by bulky-head lipids: Formation of characteristic patterns in a giant vesicle. Soft Matter 2012, 8, 488–495. [Google Scholar] [CrossRef]
- Shimobayashi, S.F.; Ichikawa, M.; Taniguchi, T. Direct observations of transition dynamics from macro- to micro-phase separation in asymmetric lipid bilayers induced by externally added glycolipids. EPL 2016, 113, 56005. [Google Scholar] [CrossRef]
- Shimokawa, N.; Mukai, R.; Nagata, M.; Takagi, M. Formation of modulated phases and domain rigidification in fatty acid-containing lipid membranes. Phys. Chem. Chem. Phys. 2017, 19, 13252–13263. [Google Scholar] [CrossRef]
- Leibler, S.; Andelman, D. Ordered and curved meso-structures in membranes and amphiphilic films. J. Phys. Fr. 1987, 48, 2013–2018. [Google Scholar] [CrossRef][Green Version]
- Komura, S.; Shimokawa, N.; Andelman, D. Tension-induced morphological transition in mixed lipid bilayers. Langmuir 2006, 22, 6771–6774. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Hirose, Y.; Komura, S.; Andelman, D. Coupled Modulated Bilayers: A Phenomenological Model. Chem. Phys. Chem. 2009, 10, 2839–2846. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Brewster, R.; Safran, A. Line Active Hybrid Lipids Determine Domain Size in Phase Separation of Saturated and Unsaturated Lipids. Biophys. J. 2010, 98, L21–L23. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Scheve, C.S.; Gonzales, P.A.; Momin, N.; Stachowiak, J.C. Steric Pressure between Membrane-Bound Proteins Opposes Lipid Phase Separation. J. Am. Chem. Soc. 2013, 135, 1185–1188. [Google Scholar] [CrossRef]
- Vequi-Suplicy, C.C.; Riske, K.A.; Knorr, R.L.; Dimova, R. Vesicles with charged domains. Biochim. Biophys. Acta 2010, 1798, 1338–1347. [Google Scholar] [CrossRef]
- Blosser, M.C.; Starr, J.B.; Turtle, C.W.; Ashcraft, J.; Keller, S.L. Minimal effect of lipid charge on membrane miscibility phase behavior in three ternary systems. Biophys. J. 2013, 104, 2629–2638. [Google Scholar] [CrossRef][Green Version]
- Himeno, H.; Shimokawa, N.; Komura, S.; Andelman, D.; Hamada, T.; Takagi, M. Charge-induced phase separation in lipid membranes. Soft Matter 2014, 10, 7959–7967. [Google Scholar] [CrossRef][Green Version]
- May, S.; Harries, D.; Ben-Shaul, A. Macroion-Induced Compositional Instability of Binary Fluid Membranes. Phys. Rev. Lett. 2002, 89, 268102. [Google Scholar] [CrossRef][Green Version]
- Harries, D.; May, S.; Ben-Shaul, A. Adsorption of charged macromolecules on mixed fluid membranes. Colloids Surf. A 2002, 208, 41–50. [Google Scholar] [CrossRef]
- Mbamala, E.C.; Ben-Shaul, A.; May, S. Domain Formation Induced by the Adsorption of Charged Proteins on Mixed Lipid Membranes. Biophys. J. 2005, 88, 1702–1714. [Google Scholar] [CrossRef][Green Version]
- Baciu, C.L.; May, S. Stability of charged, mixed lipid bilayers: Effect of electrostatic coupling between the monolayers. J. Phys. Condens. Matter 2004, 16, S2455. [Google Scholar] [CrossRef]
- Wagner, A.J.; May, S. Electrostatic interactions across a charged lipid bilayer. Eur. Biophys. J. 2007, 36, 293–303. [Google Scholar] [CrossRef][Green Version]
- Shimokawa, N.; Komura, S.; Andelman, D. Charged bilayer membranes in asymmetric ionic solutions: Phase diagrams and critical behavior. Phys. Rev. E 2011, 84, 031919. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Verwey, E.J.W.; Overbeek, J.T.G. Theory of the Stability of Lyophobic Colloids; Elsevier: Amsterdam, The Netherlands, 1948. [Google Scholar]
- Evans, D.F.; Wennerström, H. The Colloidal Domain; John Wiley: New York, NY, USA, 1999. [Google Scholar]
- Israelachvili, J. Intermolecular and Surface Forces; University of California-Santa Barbara: Santa Barbara, CA, USA, 2011. [Google Scholar]
- Kubsch, B.; Robinson, T.; Lipowsky, R.; Dimova, R. Solution Asymmetry and Salt Expand Fluid-Fluid Coexistence Regions of Charged Membranes. Biophys. J. 2016, 110, 2581–2584. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Guo, J.; Ito, H.; Higuchi, Y.; Bohinc, K.; Shimokawa, N.; Takagi, M. Three-Phase Coexistence in Binary Charged Lipid Membranes in a Hypotonic Solution. Langmuir 2021, 37, 9683–9693. [Google Scholar] [CrossRef]
- Lingwood, D.; Simons, K. Lipid rafts as a membrane-organizing principle. Science 2010, 327, 46–50. [Google Scholar] [CrossRef][Green Version]
- Hamada, T.; Sugimoto, R.; Nagasaki, T.; Takagi, M. Photochemical control of membrane raft organization. Soft Matter 2011, 7, 220–224. [Google Scholar] [CrossRef]
- Hamada, T.; Sato, Y.T.; Nagasaki, T.; Yoshikawa, K. Reversible photoswitching in a cell-sized vesicle. Langmuir 2005, 21, 7626–7628. [Google Scholar] [CrossRef][Green Version]
- Ishii, K.; Hamada, T.; Hatakeyama, M.; Sugimoto, R.; Nagasaki, T.; Takagi, M. Reversible Control of Exo- and Endo-Budding Transitions in a Photosensitive Lipid Membrane. ChemBioChem 2009, 10, 251–256. [Google Scholar] [CrossRef]
- Hamada, T.; Sugimoto, R.; Vestergaard, M.; Nagasaki, T.; Takagi, M. Membrane disc and sphere: Controllable mesoscopic structures for the capture and release of a targeted object. J. Am. Chem. Soc. 2010, 132, 10528–10532. [Google Scholar] [CrossRef]
- Yasuhara, K.; Sasaki, Y.; Kikuchi, J. A photo-responsive cholesterol capable of inducing a morphological transformation of the liquid-ordered microdomain in lipid bilayers. Colloid Polym. Sci. 2008, 286, 1675–1680. [Google Scholar] [CrossRef]
- Urban, P.; Pritzl, S.D.; Konrad, D.B.; Frank, J.A.; Pernpeintner, C.; Roeske, C.R.; Trauner, D.; Lohmuller, T. Light-Controlled Lipid Interaction and Membrane Organization in Photolipid Bilayer Vesicles. Langmuir 2018, 34, 13368–13374. [Google Scholar] [CrossRef] [PubMed]
- Frank, J.A.; Franquelim, H.G.; Schwille, P.; Trauner, D. Optical Control of Lipid Rafts with Photoswitchable Ceramides. J. Am. Chem. Soc. 2016, 138, 12981–12986. [Google Scholar] [CrossRef] [PubMed]
- Tsubone, T.M.; Baptista, M.S.; Itri, R. Understanding membrane remodelling initiated by photosensitized lipid oxidation. Biophys. Chem. 2019, 254, 106263. [Google Scholar] [CrossRef]
- Yoda, T.; Vestergaard, M.C.; Akazawa-Ogawa, Y.; Yoshida, Y.; Hamada, T.; Takagi, M. Dynamic response of a cholesterol-containing model membrane to oxidative stress. Chem. Lett. 2010, 39, 1273–1274. [Google Scholar] [CrossRef][Green Version]
- Meijering, J.L. Segregation in regular ternary solutions PART I. Philips Res. Rep. 1950, 5, 333–356. [Google Scholar]
- Knobler, C.M.; Scott, R.L. Phase Transitions and Critical Phenomena; Domb, C., Lebowitz, J.L., Eds.; Academic Press: New York, NY, USA, 1984; Volume 9, p. 164. [Google Scholar]
- Hammond, A.T.; Heberle, F.A.; Baumgart, T.; Holowka, D.; Baird, B.; Feigenson, G.W. Crosslinking a lipid raft component triggers liquid ordered-liquid disordered phase separation in model plasma membranes. Proc. Natl. Acad. Sci. USA 2005, 102, 6320–6325. [Google Scholar] [CrossRef][Green Version]
- Roffay, C.; Molinard, G.; Kim, K.; Urbanska, M.; Andrade, V.; Barbarasa, V.; Nowak, P.; Mercier, V.; García-Calvo, J.; Matile, S.; et al. Passive coupling of membrane tension and cell volume during active response of cells to osmosis. Proc. Natl. Acad. Sci. USA 2021, 118, e2103228118. [Google Scholar] [CrossRef]
- Colom, A.; Derivery, E.; Soleimanpour, S.; Tomba, C.; Molin, M.D.; Sakai, N.; González-Gaitán, M.; Matile, S.; Roux, A. A fluorescent membrane tension probe. Nat. Chem. 2018, 10, 1118–1125. [Google Scholar] [CrossRef]
- Sachs, F. Stretch-Activated Ion Channels: What Are They? Physiology 2010, 25, 50–56. [Google Scholar] [CrossRef]
- Sukharev, S.I.; Blount, P.; Martinac, B.; Blattner, F.R.; Kung, C. A large-conductance mechanosensitive channel in E. coli encoded by mscL alone. Nature 1994, 368, 265–268. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, K.; Ando, J. Vascular endothelial cell membranes differentiate between stretch and shear stress through transitions in their lipid phases. Am. J. Physiol. Heart Circ. Physiol. 2015, 309, H1178–H1185. [Google Scholar] [CrossRef] [PubMed]
- Hamada, T.; Kishimoto, Y.; Nagasaki, T.; Takagi, M. Lateral phase separation in tense membranes. Soft Matter 2011, 7, 9061–9068. [Google Scholar] [CrossRef]
- Rathe, V.; Kuckla, D.; Monzel, C. Phase separation in biological membranes: An overview with focus on experimental effects of illumination and osmotic pressure changes. Adv. Biomembr. Lipid Self-Assem. 2021, 34, 31–66. [Google Scholar]
- Li, L.; Cheng, J.-X. Coexisting Stripe and Patch Shaped Domains in Giant Unilamellar Vesicles. Biochemistry 2006, 45, 11819–11826. [Google Scholar] [CrossRef][Green Version]
- Ayuyan, A.G.; Cohen, F.S. Raft Composition at Physiological Temperature and pH in the Absence of Detergents. Biophys. J. 2008, 94, 2654–2666. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Oglȩcka, K.; Rangamani, P.; Liedberg, B.; Kraut, R.S.; Parikh, A.N. Oscillatory phase separation in giant lipid vesicles induced by transmembrane osmotic differentials. eLife 2014, 3, e03695. [Google Scholar] [CrossRef]
- Knop, J.M.; Mukherjee, S.; Jaworek, M.W.; Kriegler, S.; Manisegaran, M.; Fetahaj, Z.; Ostermeier, L.; Oliva, R.; Gault, S.; Cockell, C.S.; et al. Life in Multi-Extreme Environments: Brines, Osmotic and Hydrostatic Pressure—A Physicochemical View. Chem. Rev. 2023, 123, 73–104. [Google Scholar] [CrossRef]
- Helfrich, W.Z. Steric Interaction of Fluid Membranes in Multilayer Systems. Naturforsch 1978, 33, 305–315. [Google Scholar] [CrossRef]
- Gordon, V.D.; Deserno, M.; Andrew, C.M.J.; Egelhaaf, S.U.; Poon, W.C.K. Adhesion promotes phase separation in mixed-lipid membranes. EPL 2008, 84, 48003. [Google Scholar] [CrossRef][Green Version]
- Wongsirojkul, N.; Shimokawa, N.; Opaprakasit, P.; Takagi, M.; Hamada, T. Osmotic-Tension-Induced Membrane Lateral Organization. Langmuir 2020, 36, 2937–2945. [Google Scholar] [CrossRef] [PubMed]
- Wongsirojkul, N.; Masuta, A.; Shimokawa, N.; Takagi, M. Control of Line Tension at Phase-Separated Lipid Domain Boundaries: Monounsaturated Fatty Acids with Different Chain Lengths and Osmotic Pressure. Membranes 2022, 12, 781. [Google Scholar] [CrossRef] [PubMed]
- Robinson, T.; Dittrich, P.S. Observations of Membrane Domain Reorganization in Mechanically Compressed Artificial Cells. ChemBioChem 2019, 20, 2666–2673. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Sturzenegger, F.; Robinson, T.; Hessa, D.; Dittrich, P.S. Membranes under shear stress: Visualization of non-equilibrium domain patterns and domain fusion in a microfluidic device. Soft Matter 2016, 12, 5072–5076. [Google Scholar] [CrossRef] [PubMed]
- Hamada, T.; Mizuno, S.; Kitahata, H. Domain dynamics of phase-separated lipid membranes under shear flow. Soft Matter 2022, 18, 9069–9075. [Google Scholar] [CrossRef] [PubMed]
- Veatch, S.L.; Rogers, N.; Decker, A.; Shelby, S.A. The plasma membrane as an adaptable fluid mosaic. Biochim. Biophys. Acta (BBA)-Biomembr. 2023, 1865, 184114. [Google Scholar] [CrossRef]
- Goh, M.W.S.; Tero, R. Non-raft submicron domain formation in cholesterol-containing lipid bilayers induced by polyunsaturated phosphatidylethanolamine. Colloids Surf. B Biointerfaces 2022, 210, 112235. [Google Scholar] [CrossRef]
- Hirschi, S.; Ward, T.R.; Meier, W.P.; Müller, D.J.; Fotiadis, D. Synthetic Biology: Bottom-Up Assembly of Molecular Systems. Chem. Rev. 2022, 122, 16294–16328. [Google Scholar] [CrossRef]
- Schwille, P.; Spatz, J.; Landfester, K.; Bodenschatz, E.; Herminghaus, S.; Sourjik, V.; Erb, T.J.; Bastiaens, P.; Lipowsky, R.; Hyman, A.; et al. MaxSynBio: Avenues Towards Creating Cells from the Bottom Up. Angew. Chem. 2018, 57, 13382–13392. [Google Scholar] [CrossRef]
- Stano, P. Minimal cells: Relevance and interplay of physical and biochemical factors. Biotech. J. 2011, 6, 850–859. [Google Scholar] [CrossRef]
- Imai, M.; Sakuma, Y.; Kurisu, M.; Walde, P. From vesicles toward protocells and minimal cells. Soft Matter 2022, 18, 4823–4849. [Google Scholar] [CrossRef]
- Lipowsky, R. Remodeling of Membrane Shape and Topology by Curvature Elasticity and Membrane Tension. Adv. Biol. 2022, 6, 102613. [Google Scholar] [CrossRef]
- Hamada, T.; Fujimoto, R.; Shimobayashi, S.F.; Ichikawa, M.; Takagi, M. Molecular behavior of DNA in a cell-sized compartment coated by lipids. Phys. Rev. E 2015, 91, 062717. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Sato, Y.; Hiratsuka, Y.; Kawamata, I.; Murata, S.; Nomura, S.-I.M. Micrometer-sized molecular robot changes its shape in response to signal molecules. Sci. Robot. 2017, 2, eaal3735. [Google Scholar] [CrossRef] [PubMed]
- Takiue, T. Heterogeneity and deformation behavior of lipid vesicles. Curr. Opin. Colloid Interface Sci. 2022, 62, 101646. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Shimokawa, N.; Hamada, T. Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions. Life 2023, 13, 1105. https://doi.org/10.3390/life13051105
Shimokawa N, Hamada T. Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions. Life. 2023; 13(5):1105. https://doi.org/10.3390/life13051105
Chicago/Turabian StyleShimokawa, Naofumi, and Tsutomu Hamada. 2023. "Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions" Life 13, no. 5: 1105. https://doi.org/10.3390/life13051105
APA StyleShimokawa, N., & Hamada, T. (2023). Physical Concept to Explain the Regulation of Lipid Membrane Phase Separation under Isothermal Conditions. Life, 13(5), 1105. https://doi.org/10.3390/life13051105