Abstract
In the plasma membranes of eukaryotic cells, relatively ordered lipid–protein domains can be formed. The characteristics of the interaction of domains can have a significant effect on the processes that require the co-localization of several membrane proteins. The ordered lipid bilayer is thicker than the surrounding disordered membrane. Therefore, it is expected that elastic deformations arise at the boundary of ordered domains, aiming at smoothing the jump in bilayer thickness. The typical length of the deformations equals several nanometers, and, as two domains approach each other, the deformations induced by their boundaries begin to overlap, thereby leading to the effective lateral interaction. In this work, we theoretically considered the influence of amphipathic peptides, adsorbed on the membrane, on the interaction energy of ordered domains. Amphipathic peptides can partially incorporate into the membrane, inducing elastic deformations therein. We used the theory of lipid membrane elasticity to analyze the deformation energy of various configurations of ordered domains and amphipathic peptides. In a membrane without peptides, it is necessary to overcome some energy barrier to bring two parallel boundaries of ordered domains into contact with each other. According to the results of our calculations, the presence of amphipathic peptides in a membrane leads to a severalfold increase in the height of this energy barrier. Thus, amphipathic peptides should significantly hinder the fusion of ordered domains and thereby contribute to the stabilization of the ensemble of nano-domains.
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REFERENCES
Lillemeier B.F., Pfeiffer J.R., Surviladze Z., Wilson B.S., Davis M.M. 2006. Plasma membrane-associated proteins are clustered into islands attached to the cytoskeleton. Proc. Natl. Acad. Sci. USA. 103, 18 992–18 997.
Ayuyan A.G., Cohen F.S. 2008. Raft composition at physiological temperature and pH in the absence of detergents. Biophys. J. 94, 2654–2666.
Yang S.T., Kiessling V., Simmons J.A., White J.M., Tamm L.K. 2015. HIV gp41–mediated membrane fusion occurs at edges of cholesterol-rich lipid domains. Nat. Chem. Biol. 11, 424–431.
Allen J.A., Halverson-Tamboli R.A., Rasenick M.M. 2007. Lipid raft microdomains and neurotransmitter signalling. Nat. Rev. Neurosci. 8, 128–140.
Pike L.J. 2006. Rafts defined: A report on the Keystone Symposium on lipid rafts and cell function. J. Lip. Res. 47, 1597–1598.
Pralle A., Keller P., Florin E.L., Simons K., Hörber J.H. 2000. Sphingolipid–cholesterol rafts diffuse as small entities in the plasma membrane of mammalian cells. J. Cell Biol. 148, 997–1008.
Samsonov A.V., Mihalyov I., Cohen F.S. 2001. Characterization of cholesterol-sphingomyelin domains and their dynamics in bilayer membranes. Biophys. J. 81, 1486–1500.
Petruzielo R.S., Heberle F.A., Drazba P., Katsaras J., Feigenson G.W. 2013. Phase behavior and domain size in sphingomyelin-containing lipid bilayers. Biochim. Biophys. Acta. 1828, 1302–1313.
Veatch S.L., Polozov I.V., Gawrisch K., Keller S.L. 2004. Liquid domains in vesicles investigated by NMR and fluorescence microscopy. Biophys. J. 86, 2910–2922.
Rinia H.A., Snel M.M., van der Eerden J.P., de Kruijff B. 2001. Visualizing detergent resistant domains in model membranes with atomic force microscopy. FEBS Lett. 501, 92–96.
Galimzyanov T.R., Lyushnyak A.S., Aleksandrova V.V., Shilova L.A., Mikhalyov I.I., Molotkovskaya I.M., Akimov S.A., Batishchev O.V. 2017. Line activity of ganglioside GM1 regulates raft size distribution in a cholesterol-dependent manner. Langmuir 33, 3517–3524.
Baumgart T., Hess S.T., Webb W.W. 2003. Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature. 425, 821–824.
Saitov A., Akimov S.A., Galimzyanov T.R., Glasnov T., Pohl P. 2020. Ordered lipid domains assemble via concerted recruitment of constituents from both membrane leaflets. Phys. Rev. Lett. 124, 108102.
Landau L.D., Lifshitz E.M., Pitaevskii L.P. 1981. Theoretical physics. Volume X. Physical kinetics. Butterworth-Heinemann, Oxford.
Frolov V.A.J., Chizmadzhev Y.A., Cohen F.S., Zimmerberg J. 2006. “Entropic traps” in the kinetics of phase separation in multicomponent membranes stabilize nanodomains. Biophys. J. 91, 189–205.
Ayuyan A.G., Forsyth C.B., Zhang L., Keshavarzian A., Cohen F.S. 2009. Protein movement between membrane domains: The epidermal growth factor receptor (EGFR) signaling cascade. Biophys. J. 96, 676a.
Molotkovskaya I.M., Svirshchevskaya E.V., Litvinov I.S., Mikhalev I.I., Dyatlovitskaya E.V., Molotkovsky Yu.G., Bergelson L.D. 1992. Immunosuppressive activity of glycosphingolipids – a study of the interaction of interleukin-2 with gangliosides using cells and model systems. Biol. Membrany (Rus.). 9, 143–151.
Staneva G., Osipenko D.S., Galimzyanov T.R., Pavlov K.V., Akimov S.A. 2016. Metabolic precursor of cholesterol causes formation of chained aggregates of liquid-ordered domains. Langmuir. 32, 1591–1600.
Bao R., Li L., Qiu F., Yang Y. 2011. Atomic force microscopy study of ganglioside GM1 concentration effect on lateral phase separation of sphingomyelin/dioleoyl phosphatidylcholine/cholesterol bilayers. J. Phys. Chem. B 115, 5923–5929.
Dimova R., Dasgupta R., Fricke N., Liu Y., Agudo-Canalejo J., Grafmuller A., Lipowsky R. 2016. Spontaneous tubulation in giant vesicles induced by GM1 or PEG adsorption. Biophys. J. 110, 244a.
Pinigin K.V., Kondrashov O.V., Jiménez-Munguía I., Alexandrova V.V., Batishchev O.V., Galimzyanov T.R., Akimov S.A. 2020. Elastic deformations mediate interaction of the raft boundary with membrane inclusions leading to their effective lateral sorting. Sci. Rep. 10, 4087.
Pinigin K.V., Volovik M.V. Batishchev O.V., Akimov S.A. 2020. Interaction of ordered lipid domain boundaries and amphipathic peptides regulates probability of pore formation in membranes. Biol. Membrany (Rus.). 37, 337–349.
Galimzyanov T.R., Molotkovsky R.J., Kuzmin P.I., Akimov S.A. 2011. Stabilization of the raft bilayer structure due to elastic deformations of the membrane. Biol. Membrany (Rus.). 28, 307–314.
Helfrich W. 1973. Elastic properties of lipid bilayers: Theory and possible experiments. Z. Naturforsch. C. 28, 693–703.
Hamm M., Kozlov M.M. 2000. Elastic energy of tilt and bending of fluid membranes. Eur. Phys. J. E. 3, 323–335.
Terzi M.M., Deserno M. 2017. Novel tilt-curvature coupling in lipid membranes. J. Chem. Phys. 147, 084702.
Terzi M.M., Ergüder M.F., Deserno M. 2019. A consistent quadratic curvature-tilt theory for fluid lipid membranes. J. Chem. Phys. 151, 164108.
Pinigin K.V., Kuzmin P.I., Akimov S.A., Galimzya-nov T.R. 2020. Additional contributions to elastic energy of lipid membranes: Tilt-curvature coupling and curvature gradient. Phys. Rev. E. 102, 042406.
Evans E., Rawicz W. 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys. Rev. Lett. 64, 2094.
Pan J., Tristram-Nagle S., Nagle J.F. 2009. Effect of cholesterol on structural and mechanical properties of membranes depends on lipid chain saturation. Phys. Rev. E. 80, 021931.
Baumgart T., Das S., Webb W.W., Jenkins J.T. 2005. Membrane elasticity in giant vesicles with fluid phase coexistence. Biophys. J. 89, 1067–1080.
Rawicz W., Olbrich K.C., McIntosh T., Needham D., Evans E.A. 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophys. J. 79, 328–339.
Risselada H.J., Marrink S.J. 2008. The molecular face of lipid rafts in model membranes. Proc. Natl. Acad. Sci. USA. 105, 17 367–17 372.
Perlmutter J.D., Sachs J.N. 2011. Interleaflet interaction and asymmetry in phase separated lipid bilayers: Molecular dynamics simulations. J. Am. Chem. Soc. 133, 6563–6577.
Braganza L.F., Worcester D.L. 1986. Structural changes in lipid bilayers and biological membranes caused by hydrostatic pressure. Biochemistry. 25, 7484–7488.
Scarlata S.F. 1991. Compression of lipid membranes as observed at varying membrane positions. Biophys. J. 60, 334–340.
Terzi M.M., Deserno M., Nagle J.F. 2019. Mechanical properties of lipid bilayers: a note on the Poisson ratio. Soft Matter. 15, 9085–9092.
Kondrashov O.V., Galimzyanov T.R., Jiménez-Munguía I., Batishchev O.V., Akimov S.A. 2019. Membrane-mediated interaction of amphipathic peptides can be described by a one-dimensional approach. Phys. Rev. E. 99, 022401.
Galimzyanov T.R., Molotkovsky R.J., Kheyfets B.B., Akimov S.A. 2013. Energy of the interaction between membrane lipid domains calculated from splay and tilt deformations. JETP Lett. 96, 681–686.
Ingólfsson H.I., Melo M.N., van Eerden F.J., Arnarez C., Lopez C.A., Wassenaar T.A., Periole X., de Vries A.H., Tieleman D.P., Marrink S.J. 2014. Lipid organization of the plasma membrane. J. Am. Chem. Soc. 136, 14 554–14 559.
Puff N., Watanabe C., Seigneuret M., Angelova M.I., Staneva G. 2014. Lo/Ld phase coexistence modulation induced by GM1. Biochim. Biophys. Acta. 1838, 2105–2114.
Feigenson G.W. 2009. Phase diagrams and lipid domains in multicomponent lipid bilayer mixtures. Biochim. Biophys. Acta. 1788, 47–52.
Panteleev P.V., Bolosov I.A., Balandin S.V., Ovchinnikova T.V. 2015. Structure and biological functions of β‑hairpin antimicrobial peptides. Acta Naturae. 7, 37–47.
Pérez-Peinado C., Dias S.A., Domingues M.M., Benfield A.H., Freire J.M., Rádis-Baptista G., Gaspar D., Castanho M.A.R.B., Craik D.J., Henriques S.T., Veiga A.S., Andreu D. 2018. Mechanisms of bacterial membrane permeabilization by crotalicidin (Ctn) and its fragment Ctn (15–34), antimicrobial peptides from rattlesnake venom. J. Biol. Chem. 293, 1536–1549.
Staneva G., Chachaty C., Wolf C., Quinn P.J. 2010. Comparison of the liquid-ordered bilayer phases containing cholesterol or 7-dehydrocholesterol in modeling Smith-Lemli-Opitz syndrome. J. Lip. Res. 51, 1810–1822.
Smith D.W., Lemli L., Opitz J.M. 1964. A newly recognized syndrome of multiple congenital anomalies. J. Pediatr. 64, 210–217.
ACKNOWLEDGMENTS
The work was supported in part by the Ministry of Science and Higher Education of the Russian Federation.
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Pinigin, K.V., Galimzyanov, T.R. & Akimov, S.A. Interaction of Ordered Lipid Domains in the Presence of Amphipatic Peptides. Biochem. Moscow Suppl. Ser. A 15, 219–229 (2021). https://doi.org/10.1134/S1990747821030077
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DOI: https://doi.org/10.1134/S1990747821030077