411
Views
7
CrossRef citations to date
0
Altmetric
Review Article

Recent advancements to measure membrane mechanical and transport properties

ORCID Icon
Pages 1-21 | Received 11 Jun 2020, Accepted 06 Nov 2020, Published online: 16 Dec 2020

References

  • Akashi, K.I., et al., 1996. Preparation of giant liposomes in physiological conditions and their characterization under an optical microscope. Biophysical journal, 71 (6), 3242–3250.
  • Alcaraz, J., et al., 2018. Bidirectional mechanobiology between cells and their local extracellular matrix probed by atomic force microscopy. Seminars in cell & developmental biology, 73, 71–81.
  • Alqabandi, M., et al., 2019. The ESCRT-III isoforms CHMP2A and CHMP2B display different effects on membranes upon polymerization. Biorxiv, 756403.
  • Andersen, H.D., et al., 2011. Reconciliation of opposing views on membrane-sugar interactions. Proceedings of the National Academy of Sciences of the United States of America, 108 (5), 1874–1878.
  • Angelova, M.I. and Dimitrov, D.S., 1986. Liposome electroformation. Faraday discussions of the chemical society, 81, 303–311.
  • Arriaga, L.R., et al., 2009. Stiffening effect of cholesterol on disordered lipid phases: a combined neutron spin echo + dynamic light scattering analysis of the bending elasticity of large unilamellar vesicles. Biophysical journal, 96 (9), 3629–3637.
  • Bangham, A.D., Standish, M.M., and Watkins, J.C., 1965. Diffusion of univalent ions across the lamellae of swollen phospholipids. Journal of molecular biology, 13 (1), 238–252.
  • Baron, S., et al., 2000. Electroporation of antibodies, DNA, and other macromolecules into cells: a highly efficient method. Journal of immunological methods, 242 (1-2), 115–126.
  • Basoli, F., et al., 2018. Biomechanical characterization at the cell scale: present and prospects. Frontiers in physiology, 9, 1449.
  • Baumgart, T., et al., 2011. Thermodynamics and mechanics of membrane curvature generation and sensing by proteins and lipids. Annual review of physical chemistry, 62, 483–506.
  • Beblik, G., Servuss, R.M., and Helfrich, W., 1985. Bilayer bending rigidity of some synthetic lecithins. Journal de physique, 46 (10), 1773–1778.
  • Beekman, P., et al., 2019. Immuno-capture of extracellular vesicles for individual multi-modal characterization using AFM, SEM and Raman spectroscopy. Lab on a chip, 19 (15), 2526–2536.
  • Bergström, M., 1996. Thermodynamics of vesicle formation from a mixture of anionic and cationic surfactants. Langmuir : the ACS journal of surfaces and colloids , 12 (10), 2454–2463.
  • Bhatia, T., et al., 2018. Membrane nanotubes increase the robustness of giant vesicles. ACS nano, 12 (5), 4478–4485.
  • Bhatia, T., Cornelius, F., and Ipsen, J.H., 2017. Capturing suboptical dynamic structures in lipid bilayer patches formed from free-standing giant unilamellar vesicles. Nature protocols, 12 (8), 1563–1575.
  • Binnig, G., Quate, C.F., and Gerber, C., 1986. Atomic force microscope. Physical review letters, 56 (9), 930–933.
  • Bivas, I., et al., 1987. An application of the optical microscopy to the determination of the curvature elastic modulus of biological and model membranes. Journal de physique, 48 (5), 855–867.
  • Bloom, M., Evans, E., and Mouritsen, O.G., 1991. Physical properties of the fluid lipid-bilayer component of cell membranes: a perspective. Quarterly reviews of biophysics, 24 (3), 293–397.
  • Bo, L. and Waugh, R.E., 1989. Determination of bilayer membrane bending stiffness by tether formation from giant, thin-walled vesicles. Biophysical journal, 55 (3), 509–517.
  • Bouvrais, H., 2012. Bending rigidities of lipid bilayers: their determination and main inputs in biophysical studies. In: A. Iglič, ed. Advances in planar lipid bilayers and liposomes. Vol. 15. San Diego, CA: Academic Press, 1–75.
  • Bouvrais, H., et al., 2012. Intrinsic reaction-cycle time scale of Na+,K+-ATPase manifests itself in the lipid-protein interactions of nonequilibrium membranes. Proceedings of the National Academy of Sciences of the United States of America, 109 (45), 18442–18446.
  • Bouvrais, H., Duelund, L., and Ipsen, J.H., 2014. Buffers affect the bending rigidity of model lipid membranes. Langmuir : the ACS journal of surfaces and colloids, 30 (1), 13–16.
  • Bouvrais, H., et al., 2010. Mechanics of POPC bilayers in presence of alkali salts. Biophysical journal, 98 (3), 272a.
  • Bouvrais, H., et al., 2013. Analysis of the shape fluctuations of reconstituted membranes using guvs made from lipid extracts of invertebrates. Biology open, 2 (4), 373–378.
  • Bouvrais, H., et al., 2009. Effects of sodium halide solutions of high concentrations on bending elasticity of POPC GUVs. Biophysical journal, 96 (3), 161a.
  • Bouvrais, H., et al., 2008. Softening of POPC membranes by magainin. Biophysical chemistry, 137 (1), 7–12.
  • Brochard, F. and Lennon, J., 1975. Frequency spectrum of the flicker phenomenon in erythrocytes. Journal de physique, 36 (11), 1035–1047.
  • Bucher, P., et al., 1998. Giant vesicles as biochemical compartments: the use of microinjection techniques. Langmuir : the ACS journal of surfaces and colloids , 14 (10), 2712–2721.
  • Bummer, P.M. and Zografi, G., 1988. The association of D-glucose with unilamellar phospholipid vesicles. Biophysical chemistry, 30 (2), 173–183.
  • Calò, A., et al., 2014. Force measurements on natural membrane nanovesicles reveal a composition-independent, high Young’s modulus. Nanoscale, 6 (4), 2275–2285.
  • Cass, A. and Finkelstein, A., 1967. Water permeability of thin lipid membranes. Journal of general physiology, 50 (6), 1765–1784.
  • Chen, J., et al., 2011. Electrodeformation for single cell mechanical characterization. Journal of micromechanics and microengineering, 21 (5), 054012.
  • Chen, Q., Schönherr, H., and Vancso, G.J., 2009. Mechanical properties of block copolymer vesicle membranes by atomic force microscopy. Soft matter, 5 (24), 4944–4950.
  • Cheng, X. and Pinsky, P.M., 2015. The balance of fluid and osmotic pressures across active biological membranes with application to the corneal endothelium. Plos one, 10 (12), e0145422.
  • Colom, A., et al., 2018. A fluorescent membrane tension probe. Nature chemistry, 10 (11), 1118–1125.
  • Cuvelier, D., et al., 2005. Coalescence of membrane tethers: experiments, theory, and applications. Biophysical journal, 88 (4), 2714–2726.
  • Dai, J. and Sheetz, M.P., 1999. Membrane tether formation from blebbing cells. Biophysical journal, 77 (6), 3363–3370.
  • Dai, Z., et al., 2019. Chain-Length- and Saturation-Tuned Mechanics of Fluid Nanovesicles Direct Tumor Delivery. ACS nano, 13 (7), 7676–7689.
  • Dasgupta, R. and Dimova, R., 2014. Inward and outward membrane tubes pulled from giant vesicles. Journal of physics D: applied physics, 47 (28), 282001.
  • Dasgupta, R., et al., 2018. The glycolipid gm1 reshapes asymmetric biomembranes and giant vesicles by curvature generation. Proceedings of the National Academy of Sciences of the United States of America, 115 (22), 5756–5761.
  • De Pablo, P., et al., 1998. Jumping mode scanning force microscopy. Applied physics letters, 73 (22), 3300–3302.
  • Delabre, U., et al., 2015. Deformation of phospholipid vesicles in an optical stretcher. Soft matter, 11 (30), 6075–6088.
  • Delorme, N. and Fery, A., 2006. Direct method to study membrane rigidity of small vesicles based on atomic force microscope force spectroscopy. Physical review E, 74 (3), 030901.
  • Delorme, N., et al., 2006. Surface immobilization and mechanical properties of catanionic hollow faceted polyhedrons. The journal of physical chemistry. B, 110 (4), 1752–1758.
  • Deng, X., et al., 2018. Application of atomic force microscopy in cancer research. Journal of nanobiotechnology, 16 (1), 102.
  • Derényi, I., Jülicher, F., and Prost, J., 2002. Formation and interaction of membrane tubes. Physical review letters, 88 (23), 238101.
  • Dhand, C., et al., 2014. Role of size of drug delivery carriers for pulmonary and intravenous administration with emphasis on cancer therapeutics and lung-targeted drug delivery. RSC advances, 4 (62), 32673–32689.
  • Dieluweit, S., et al., 2010. Mechanical properties of bare and protein-coated giant unilamellar phospholipid vesicles. a comparative study of micropipet aspiration and atomic force microscopy. Langmuir : the ACS journal of surfaces and colloids, 26 (13), 11041–11049.
  • Dimova, R., Pouligny, B., and Dietrich, C., 2000. Pretransitional effects in dimyristoylphosphatidylcholine vesicle membranes: optical dynamometry study. Biophysical journal, 79 (1), 340–356.
  • Dimova, R., et al., 2002. Hyperviscous diblock copolymer vesicles. The European physical journal E, 7 (3), 241–250.
  • Dimova, R., 2014. Recent developments in the field of bending rigidity measurements on membranes. Advances in colloid and interface science, 208, 225–234.
  • Dimova, R., 2019. Giant vesicles and their use in assays for assessing membrane phase state, curvature, mechanics, and electrical properties. Annual review of biophysics, 48, 93–119.
  • Dimova, R., et al., 2006. A practical guide to giant vesicles. probing the membrane nanoregime via optical microscopy. Journal of physics. Condensed matter : an institute of physics journal, 18 (28), S1151–S1176.
  • Dimova, R., et al., 2009. Vesicles in electric fields: some novel aspects of membrane behavior. Soft matter, 5 (17), 3201–3212.
  • Dimova, R. and Riske, K. A., 2019. Using electric fields to assess membrane material properties in giant unilamellar vesicles. In: R. Dimova and C. Marques, eds. The giant vesicle book. Boca Raton, FL: CRC Press, Chapter 15, 18.
  • Dimova, R., et al., 2007. Giant vesicles in electric fields. Soft matter, 3 (7), 817–827.
  • Dimova, R., Riske, K. A., and Damijan, M., 2016. Electrodeformation, electroporation, and electrofusion of giant unilamellar vesicles. In: D. Miklavčič, ed. Handbook of electroporation. Cham, Switzerland: Springer, 235–252.
  • Discher, D.E. and Eisenberg, A., 2002. Polymer vesicles. Science (New York, N.Y.), 297 (5583), 967–973.
  • Döbereiner, H.G., 2000. Properties of giant vesicles. Current opinion in colloid & interface science, 5 (3-4), 256–263. Properties of giant vesicles.
  • Döbereiner, H.G., et al., 2003. Advanced flicker spectroscopy of fluid membranes. Physical review letters, 91 (4), 048301.
  • Doktorova, M., Harries, D., and Khelashvili, G., 2017. Determination of bending rigidity and tilt modulus of lipid membranes from real-space fluctuation analysis of molecular dynamics simulations. Physical chemistry chemical physics : PCCP, 19 (25), 16806–16818.
  • Drabik, D., et al., 2016. The modified fluorescence based vesicle fluctuation spectroscopy technique for determination of lipid bilayer bending properties. Biochimica et biophysica acta, 1858 (2), 244–252.
  • Duan, Y., et al., 2018. Investigation on the nanomechanics of liposome adsorption on titanium alloys: temperature and loading effects. Polymers, 10 (4), 383.
  • Duwe, H., Kaes, J., and Sackmann, E., 1990. Bending elastic moduli of lipid bilayers: modulation by solutes. Journal de physique, 51 (10), 945–961.
  • Ebeling, D., et al., 2006. Imaging of biomaterials in liquids: a comparison between conventional and Q-controlled amplitude modulation (‘tapping mode’) atomic force microscopy. Nanotechnology, 17 (7), S221–S226.
  • El Kirat, K., et al., 2005. Sample preparation procedures for biological atomic force microscopy. Journal of microscopy, 218 (Pt 3), 199–207.
  • Elsayed, M.M., et al., 2007. Lipid vesicles for skin delivery of drugs: reviewing three decades of research. International journal of pharmaceutics, 332 (1-2), 1–16.
  • Elson, E., et al., 2016. Organizational cell biology: an overview. In: R.A. Bradshaw and P.D. Stahl, eds. Encyclopedia of cell biology. Vol. 2. Waltham: Academic Press, 1–4.
  • Engelhardt, H., Duwe, H., and Sackmann, E., 1985. Bilayer bending elasticity measured by Fourier analysis of thermally excited surface undulations of flaccid vesicles. Journal de physique lettres, 46 (8), 395–400.
  • Evans, E. and Metcalfe, M., 1984. Free energy potential for aggregation of giant, neutral lipid bilayer vesicles by van der waals attraction. Biophysical journal, 46 (3), 423–426.
  • Evans, E. and Rawicz, W., 1990. Entropy-driven tension and bending elasticity in condensed-fluid membranes. Physical review letters, 64 (17), 2094–2097.
  • Evans, E. and Rawicz, W., 1997. Elasticity of “fuzzy” biomembranes. Physical review letters, 79 (12), 2379–2382.
  • Evans, E., 1973. New membrane concept applied to the analysis of fluid shear-and micropipette-deformed red blood cells. Biophysical journal, 13 (9), 941–954.
  • Evans, E., et al., 2003. Dynamic tension spectroscopy and strength of biomembranes. Biophysical journal, 85 (4), 2342–2350.
  • Evans, E. and Ludwig, F., 2000. Dynamic strengths of molecular anchoring and material cohesion in fluid biomembranes. Journal of physics: condensed matter, 12 (8A), A315–A320.
  • Evans, E. and Needham, D., 1987. Physical properties of surfactant bilayer membranes: thermal transitions, elasticity, rigidity, cohesion and colloidal interactions. The journal of physical chemistry, 91 (16), 4219–4228.
  • Evans, E.A., 1983. Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophysical journal, 43 (1), 27–30.
  • Evans, E. A. and Skalak, R., 1980. Mechanics and thermodynamics of biomembranes. Boca Raton, FL: CRC Press.
  • Faizi, H.A., et al., 2019. Bending rigidity of charged lipid bilayer membranes. Soft matter, 15 (29), 6006–6013.
  • Faucon, J., et al., 1989. Bending elasticity and thermal fluctuations of lipid membranes. theoretical and experimental requirements. Journal de physique, 50 (17), 2389–2414.
  • Fernandez-Puente, L., et al., 1994. Temperature and chain length effects on bending elasticity of phosphatidylcholine bilayers. Europhysics letters (EPL), 28 (3), 181–186.
  • Foroozandeh, P. and Aziz, A.A., 2018. Insight into cellular uptake and intracellular trafficking of nanoparticles. Nanoscale research letters, 13 (1), 339.
  • Fournier, J.B., Ajdari, A., and Peliti, L., 2001. Effective-area elasticity and tension of micromanipulated membranes. Physical review letters, 86 (21), 4970–4973.
  • Fricke, K., et al., 1986. Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness. European biophysics journal : EBJ, 14 (2), 67–81.
  • Fricke, N. and Dimova, R., 2016. GM1 softens POPC membranes and induces the formation of micron-sized domains. Biophysical journal, 111 (9), 1935–1945.
  • Gadegaard, N., 2006. Atomic force microscopy in biology: technology and techniques. Biotechnic & histochemistry : official publication of the Biological Stain Commission, 81 (2-3), 87–97.
  • Gajos, K., et al., 2017. Immobilization and detection of platelet-derived extracellular vesicles on functionalized silicon substrate: cytometric and spectrometric approach. Analytical and bioanalytical chemistry, 409 (4), 1109–1119.
  • Genova, J., Vitkova, V., and Bivas, I., 2013. Registration and analysis of the shape fluctuations of nearly spherical lipid vesicles. Physical review. E, statistical, nonlinear, and soft matter physics, 88 (2), 022707.
  • Genova, J., Zheliaskova, A., and Mitov, M.D., 2008. Influence of carbohydrates on the elasticity of SOPC membrane. Comptes Rendus de L’académie Bulgare Des Sciences, 61 (7), 879–884.
  • Girard, P., Prost, J., and Bassereau, P., 2005. Passive or active fluctuations in membranes containing proteins. Physical review letters, 94 (8), 088102.
  • Goodhead, L.K. and MacMillan, F.M., 2017. Measuring osmosis and hemolysis of red blood cells. Advances in physiology education, 41 (2), 298–305.
  • Goujon, A., et al., 2019. Mechanosensitive fluorescent probes to image membrane tension in mitochondria, endoplasmic reticulum, and lysosomes. Journal of the American Chemical Society, 141 (8), 3380–3384.
  • Gracià, R.S., et al., 2010. Effect of cholesterol on the rigidity of saturated and unsaturated membranes: fluctuation and electrodeformation analysis of giant vesicles. Soft matter, 6 (7), 1472–1482.
  • Guck, J., et al., 2001. The optical stretcher: a novel laser tool to micromanipulate cells. Biophysical journal, 81 (2), 767–784.
  • Guck, J., et al., 2005. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophysical journal, 88 (5), 3689–3698.
  • Hannesschläger, C., et al., 2018. Quantification of water flux in vesicular systems. Scientific reports, 8 (1), 1–8.
  • Harmandaris, V.A. and Deserno, M., 2006. A novel method for measuring the bending rigidity of model lipid membranes by simulating tethers. The journal of chemical physics, 125 (20), 204905.
  • Has, C. and Sunthar, P., 2020. A comprehensive review on recent preparation techniques of liposomes. Journal of liposome research, 30 (4), 336–365.
  • Has, C. and Pan, S., 2020. Vesicle formation mechanisms: an overview. Journal of liposome research.
  • Has, C., Phapal, S.M., and Sunthar, P., 2018. Rapid single-step formation of liposomes by flow assisted stationary phase interdiffusion. Chemistry and physics of lipids, 212, 144–151.
  • Heinrich, V. and Waugh, R.E., 1996. A piconewton force transducer and its application to measurement of the bending stiffness of phospholipid membranes. Annals of biomedical engineering, 24 (5), 595–605.
  • Helfrich, W., 1974a. Deformation of lipid bilayer spheres by electric fields. Zeitschrift Fur naturforschung. Section C, biosciences, 29 (3), 182–183.
  • Helfrich, W., 1974b. The size of bilayer vesicles generated by sonication. Physics letters A, 50 (2), 115–116.
  • Helfrich, W., 1986. Size distributions of vesicles: the role of the effective rigidity of membranes. Journal de physique, 47 (2), 321–329.
  • Helfrich, W., 1973. Elastic properties of lipid bilayers: theory and possible experiments. Zeitschrift Fur naturforschung. Teil C: biochemie, biophysik, biologie, virologie, 28 (11), 693–703.
  • Helfrich, W. and Servuss, R.M., 1984. Undulations, steric interaction and cohesion of fluid membranes. Il Nuovo Cimento D, 3 (1), 137–151.
  • Henriksen, J., et al., 2006. Universal behavior of membranes with sterols. Biophysical journal, 90 (5), 1639–1649.
  • Henriksen, J., Rowat, A.C., and Ipsen, J.H., 2004. Vesicle fluctuation analysis of the effects of sterols on membrane bending rigidity. European biophysics journal : EBJ, 33 (8), 732–741.
  • Henriksen, J.R., et al., 2010. Understanding detergent effects on lipid membranes: a model study of lysolipids. Biophysical journal, 98 (10), 2199–2205.
  • Henriksen, J.R. and Ipsen, J.H., 2004. Measurement of membrane elasticity by micro-pipette aspiration. The European physical journal. E, soft matter, 14 (2), 149–167.
  • Hertz, H., 1882. Ueber die beruhrung fester elastischer korper. Journal fur die reine und angewandte mathematik, 92, 156–171.
  • Hochmuth, R., et al., 1982. Extensional flow of erythrocyte membrane from cell body to elastic tether. II. experiment. Biophysical journal, 39 (1), 83–89.
  • Hochmuth, R.M., 2000. Micropipette aspiration of living cells. Journal of biomechanics, 33 (1), 15–22.
  • Huang, W.C., et al., 2016. Engineering chimeric receptors to investigate the size- and rigidity-dependent interaction of PEGylated nanoparticles with cells. ACS nano, 10 (1), 648–662.
  • Hui, Y., et al., 2018. Understanding the effects of nanocapsular mechanical property on passive and active tumor targeting. ACS nano, 12 (3), 2846–2857.
  • Ito, H. and Kaneko, M., 2020. On-chip cell manipulation and applications to deformability measurements. ROBOMECH journal, 7 (1), 3.
  • James, H.P. and Jadhav, S., 2020. Mechanical and transport properties of chitosan-zwitterionic phospholipid vesicles. Colloids and surfaces. B, biointerfaces, 188, 110782.
  • Jin, A.J., et al., 2006. Measuring the elasticity of clathrin-coated vesicles via atomic force microscopy. Biophysical journal, 90 (9), 3333–3344.
  • Jubery, T.Z., Srivastava, S.K., and Dutta, P., 2014. Dielectrophoretic separation of bioparticles in microdevices: a review. Electrophoresis, 35 (5), 691–713.
  • Kakorin, S., Liese, T., and Neumann, E., 2003. Membrane curvature and high-field electroporation of lipid bilayer vesicles. The journal of physical chemistry B, 107 (37), 10243–10251.
  • Kaler, E.W., et al., 1989. Spontaneous vesicle formation in aqueous mixtures of single-tailed surfactants. Science (New York, N.Y.), 245 (4924), 1371–1374.
  • Karamdad, K., et al., 2015. Preparation and mechanical characterisation of giant unilamellar vesicles by a microfluidic method. Lab on a chip, 15 (2), 557–562.
  • Klasczyk, B., et al., 2010. Interactions of alkali metal chlorides with phosphatidylcholine vesicles. Langmuir : the ACS journal of surfaces and colloids, 26 (24), 18951–18958.
  • Knorr, R.L., et al., 2010. Wrinkling and electroporation of giant vesicles in the gel phase. Soft matter, 6 (9), 1990–1996.
  • Koslov, M. and Markin, V., 1984. A theory of osmotic lysis of lipid vesicles. Journal of theoretical biology, 109 (1), 17–39.
  • Kotnik, T., et al., 2019. Membrane electroporation and electropermeabilization: mechanisms and models. Annual review of biophysics, 48, 63–91.
  • Krieg, M., et al., 2019. Atomic force microscopy-based mechanobiology. Nature reviews physics, 1 (1), 41–57.
  • Kummrow, M. and Helfrich, W., 1991. Deformation of giant lipid vesicles by electric fields. Physical review. A, atomic, molecular, and optical physics, 44 (12), 8356–8360.
  • Kwok, R. and Evans, E., 1981. Thermoelasticity of large lecithin bilayer vesicles. Biophysical journal, 35 (3), 637–652.
  • Lasic, D. D., 1993. Liposomes: from physics to applications. 1st ed. Amsterdam, The Netherlands: Elsevier.
  • Lee, L.M. and Liu, A.P., 2014. The application of micropipette aspiration in molecular mechanics of single cells. Journal of nanotechnology in engineering and medicine, 5 (4), 040902.
  • Lherbette, M., et al., 2019. The AP2 adaptor enhances clathrin coat stiffness. The FEBS journal, 286 (20), 4074–4085.
  • Li, S., et al., 2011a. Bending and puncturing the influenza lipid envelope. Biophysical journal, 100 (3), 637–645.
  • Li, Y., Lipowsky, R., and Dimova, R., 2011b. Membrane nanotubes induced by aqueous phase separation and stabilized by spontaneous curvature. Proceedings of the National Academy of Sciences of the United States of America, 108 (12), 4731–4736.
  • Liang, X., Mao, G., and Ng, K.Y.S., 2004. Mechanical properties and stability measurement of cholesterol-containing liposome on mica by atomic force microscopy. Journal of colloid and interface science, 278 (1), 53–62.
  • Lieber, A.D., et al., 2013. Membrane tension in rapidly moving cells is determined by cytoskeletal forces. Current biology : CB, 23 (15), 1409–1417.
  • Lipowsky, R., 2013. Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Faraday discussions of the chemical society , 161, 305–331.
  • Lipowsky, R. and Sackmann, E., 1995. Structure and dynamics of membranes: I. From cells to vesicles/II. Generic and specific interactions. Amsterdam, The Netherlands: Elsevier.
  • Liu, Y., et al., 2019. Robotic micropipette aspiration for multiple cells. Micromachines, 10 (5), 348.
  • Loftus, A.F., et al., 2013. Robust measurement of membrane bending moduli using light sheet fluorescence imaging of vesicle fluctuations. Langmuir : the ACS journal of surfaces and colloids, 29 (47), 14588–14594.
  • Lu, L., et al., 2016. Membrane mechanical properties of synthetic asymmetric phospholipid vesicles. Soft matter, 12 (36), 7521–7528.
  • Ly, H.V. and Longo, M.L., 2004. The influence of short-chain alcohols on interfacial tension, mechanical properties, area/molecule, and permeability of fluid lipid bilayers. Biophysical journal, 87 (2), 1013–1033.
  • MacQueen, L.A., Buschmann, M.D., and Wertheimer, M.R., 2010. Mechanical properties of mammalian cells in suspension measured by electro-deformation. Journal of micromechanics and microengineering, 20 (6), 065007.
  • Mahendra, A., James, H.P., and Jadhav, S., 2019. Peg-grafted phospholipids in vesicles: effect of peg chain length and concentration on mechanical properties. Chemistry and physics of lipids, 218, 47–56.
  • Manneville, J.B., et al., 1999. Activity of transmembrane proteins induces magnification of shape fluctuations of lipid membranes. Physical review letters, 82 (21), 4356–4359.
  • McCalden, T.A., 1990. Particulate systems for drug delivery to the lung. Advanced drug delivery reviews, 5 (3), 253–263.
  • Méléard, P., et al., 1992. Pulsed-light microscopy applied to the measurement of the bending elasticity of giant liposomes. Europhysics letters (EPL), 19 (4), 267–271.
  • Méléard, P., et al., 1998. Mechanical properties of model membranes studied from shape transformations of giant vesicles. Biochimie, 80 (5-6), 401–413.
  • Meleard, P., et al., 1997. Bending elasticities of model membranes: influences of temperature and sterol content. Biophysical journal, 72 (6), 2616–2629.
  • Méléard, P. and Pott, T., 2013. Overview of a quest for bending elasticity measurement. In: A. Iglič and J. Genova, eds. Advances in planar lipid bilayers and liposomes. Vol. 17. Oxford, UK: Academic Press, 55–75.
  • Méléard, P., et al., 2011. Advantages of statistical analysis of giant vesicle flickering for bending elasticity measurements. The European physical journal. E, soft matter, 34 (10), 116.
  • Melero, A., et al., 2018. Lysophospholipids facilitate COPII vesicle formation. Current biology : CB, 28 (12), 1950–1958.
  • Mertins, O. and Dimova, R., 2013. Insights on the interactions of chitosan with phospholipid vesicles. Part II: membrane stiffening and pore formation. Langmuir : the ACS journal of surfaces and colloids, 29 (47), 14552–14559.
  • Milner, S.T. and Safran, S., 1987. Dynamical fluctuations of droplet microemulsions and vesicles. Physical review. A, general physics, 36 (9), 4371–4379.
  • Mitkova, D., et al., 2012. Experimental study of the bending elasticity of charged lipid bilayers in aqueous solutions with pH5. Journal of physics: conference series, 398, 012028.
  • Mitkova, D., et al., 2013. Charged lipid bilayers in aqueous surroundings with low ph. In: A. Iglič and C. Kulkarni, eds. Advances in planar lipid bilayers and liposomes. Vol. 18. Oxford, UK: Academic Press, 1–20.
  • Möller, C., et al., 1999. Tapping-mode atomic force microscopy produces faithful high-resolution images of protein surfaces. Biophysical journal, 77 (2), 1150–1158.
  • Monzel, C. and Sengupta, K., 2016. Measuring shape fluctuations in biological membranes. Journal of physics D: applied physics, 49 (24), 243002.
  • Moreno-Herrero, F., et al., 2004. Atomic force microscopy contact, tapping, and jumping modes for imaging biological samples in liquids. Physical review. E, statistical, nonlinear, and soft matter physics, 69 (3 Pt 1), 031915.
  • Mutz, M. and Helfrich, W., 1990. Bending rigidities of some biological model membranes as obtained from the Fourier analysis of contour sections. Journal de physique, 51 (10), 991–1001.
  • Naghdi, P. M., 1973. The theory of shells and plates. In: C. Truesdell, eds. Linear theories of elasticity and thermoelasticity. Berlin, Germany: Springer, 425–640.
  • Nagle, J.F., 2013. Introductory lecture: basic quantities in model biomembranes. Faraday discussions of the chemical society, 161, 11–29.
  • Nagle, J.F., et al., 2015. What are the true values of the bending modulus of simple lipid bilayers? Chemistry and physics of lipids, 185, 3–10.
  • Needham, D. and Hochmuth, R., 1989. Electro-mechanical permeabilization of lipid vesicles. role of membrane tension and compressibility. Biophysical journal, 55 (5), 1001–1009.
  • Neuman, K.C. and Nagy, A., 2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nature methods, 5 (6), 491–505.
  • Niggemann, G., Kummrow, M., and Helfrich, W., 1995. The bending rigidity of phosphatidylcholine bilayers: dependences on experimental method, sample cell sealing and temperature. Journal de physique II, 5 (3), 413–425.
  • Olbrich, K., et al., 2000. Water permeability and mechanical strength of polyunsaturated lipid bilayers. Biophysical journal, 79 (1), 321–327.
  • Pakkanen, K.I., et al., 2011. Mechanics and dynamics of triglyceride-phospholipid model membranes: implications for cellular properties and function. Biochimica et biophysica acta, 1808 (8), 1947–1956.
  • Pan, J., et al., 2008. Cholesterol perturbs lipid bilayers nonuniversally. Physical review letters, 100 (19), 198103.
  • Pan, J., Tristram-Nagle, S., and Nagle, J.F., 2009. Effect of cholesterol on structural and mechanical properties of membranes depends on lipid chain saturation. Physical review. E, statistical, nonlinear, and soft matter physics, 80 (2 Pt 1), 021931.
  • Parisse, P., et al., 2017. Atomic force microscopy analysis of extracellular vesicles. European biophysics journal, 46 (8), 813–820.
  • Paula, S., et al., 1996. Permeation of protons, potassium ions, and small polar molecules through phospholipid bilayers as a function of membrane thickness. Biophysical journal, 70 (1), 339–348.
  • Pécréaux, J., et al., 2004. Refined contour analysis of giant unilamellar vesicles. The European physical journal. E, soft matter, 13 (3), 277–290.
  • Penič, S., et al., 2015. Bending elasticity of vesicle membranes studied by monte carlo simulations of vesicle thermal shape fluctuations. Soft matter, 11 (25), 5004–5009.
  • Pernpeintner, C., et al., 2017. Light-controlled membrane mechanics and shape transitions of photoswitchable lipid vesicles. Langmuir : the ACS journal of surfaces and colloids, 33 (16), 4083–4089.
  • Petrache, H.I., et al., 2006. Swelling of phospholipids by monovalent salt. Journal of lipid research, 47 (2), 302–309.
  • Phapal, S.M., Has, C., and Sunthar, P., 2017. Spontaneous formation of single component liposomes from a solution. Chemistry and physics of lipids, 205, 25–33.
  • Picas, L., Rico, F., and Scheuring, S., 2012. Direct measurement of the mechanical properties of lipid phases in supported bilayers. Biophysical journal, 102 (1), L01–L03.
  • Pinto, O.A. and Disalvo, E.A., 2019. A new model for lipid monolayer and bilayers based on thermodynamics of irreversible processes. Plos one, 14 (4), e0212269.
  • Piontek, M.C., Lira, R.B., and Roos, W.H., 2019. Active probing of the mechanical properties of biological and synthetic vesicles. Biochimica et biophysica acta (BBA) – general subjects, 129486.
  • Pontes, B., et al., 2013. Membrane elastic properties and cell function. Plos one, 8 (7), e67708.
  • Portet, T., Gordon, S.E., and Keller, S.L., 2012. Increasing membrane tension decreases miscibility temperatures; an experimental demonstration via micropipette aspiration. Biophysical journal, 103 (8), L35–L37.
  • Qian, L. and Zhao, H., 2018. Nanoindentation of soft biological materials. Micromachines, 9 (12), 654.
  • Ramahaleo, T., et al., 1999. Osmotic water permeability of isolated protoplasts. modifications during development. Plant physiology, 119 (3), 885–896.
  • Rand, R.P. and Burton, A., 1964. Mechanical properties of the red cell membrane: I. membrane stiffness and intracellular pressure. Biophysical journal, 4 (2), 115–135.
  • Rand, R., 1964. Mechanical properties of the red cell membrane: II. Viscoelastic breakdown of the membrane. Biophysical journal, 4 (4), 303–316.
  • Ratanabanangkoon, P., et al., 2003. Mechanics of streptavidin-coated giant lipid bilayer vesicles: a micropipet study. Langmuir : the ACS journal of surfaces and colloids, 19 (4), 1054–1062.
  • Rautu, S.A., et al., 2017. The role of optical projection in the analysis of membrane fluctuations. Soft matter, 13 (19), 3480–3483.
  • Rawicz, W., et al., 2000. Effect of chain length and unsaturation on elasticity of lipid bilayers. Biophysical journal, 79 (1), 328–339.
  • Rawicz, W., et al., 2008. Elasticity, strength, and water permeability of bilayers that contain raft microdomain-forming lipids. Biophysical journal, 94 (12), 4725–4736.
  • Reeves, J.P. and Dowben, R.M., 1969. Formation and properties of thin-walled phospholipid vesicles. Journal of cellular physiology, 73 (1), 49–60.
  • Riske, K.A. and Dimova, R., 2005. Electro-deformation and poration of giant vesicles viewed with high temporal resolution. Biophysical journal, 88 (2), 1143–1155.
  • Rosa-Zeiser, A., et al., 1997. The simultaneous measurement of elastic, electrostatic and adhesive properties by scanning force microscopy: pulsed-force mode operation. Measurement science and technology, 8 (11), 1333–1338.
  • Rossier, O., et al., 2003. Giant vesicles under flows: extrusion and retraction of tubes. Langmuir : the ACS journal of surfaces and colloids, 19 (3), 575–584.
  • Roux, A., 2013. The physics of membrane tubes: soft templates for studying cellular membranes. Soft matter, 9 (29), 6726–6736.
  • Roux, A., et al., 2002. A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proceedings of the National Academy of Sciences of the United States of America, 99 (8), 5394–5399.
  • Roux, A., et al., 2005. Role of curvature and phase transition in lipid sorting and fission of membrane tubules. The EMBO journal, 24 (8), 1537–1545.
  • Rowat, A.C., Hansen, P.L., and Ipsen, J.H., 2004. Experimental evidence of the electrostatic contribution to membrane bending rigidity. Europhysics letters (EPL), 67 (1), 144–149.
  • Sackmann, E., 1994. Membrane bending energy concept of vesicle-and cell-shapes and shape-transitions. FEBS letters, 346 (1), 3–16.
  • Sackmann, E., Duwe, H.P., and Engelhardt, H., 1986. Membrane bending elasticity and its role for shape fluctuations and shape transformations of cells and vesicles. Faraday discussions of the chemical society, 81, 281–290.
  • Salditt, T., et al., 2015. X-ray optics on a chip: guiding x rays in curved channels. Physical review letters, 115 (20), 203902.
  • Santhosh, P.B., et al., 2014. Influence of iron oxide nanoparticles on bending elasticity and bilayer fluidity of phosphotidylcholine liposomal membranes. Colloids and surfaces A: physicochemical and engineering aspects, 460, 248–253.
  • Schaap, I.A., et al., 2012. Effect of envelope proteins on the mechanical properties of influenza virus. The journal of biological chemistry, 287 (49), 41078–41088.
  • Schäfer, E., et al., 2015. Mechanical response of adherent giant liposomes to indentation with a conical afm-tip. Soft matter, 11 (22), 4487–4495.
  • Schneider, M., Jenkins, J., and Webb, W., 1984. Thermal fluctuations of large quasi-spherical bimolecular phospholipid vesicles. Journal de physique, 45 (9), 1457–1472.
  • Sebaihi, N., et al., 2017. Dimensional characterization of extracellular vesicles using atomic force microscopy. Measurement science and technology, 28 (3), 034006.
  • Semrau, S., et al., 2008. Accurate determination of elastic parameters for multicomponent membranes. Physical review letters, 100 (8), 088101.
  • Servuss, R., Harbich, V., and Helfrich, W., 1976. Measurement of the curvature-elastic modulus of egg lecithin bilayers. Biochimica et biophysica acta (BBA) - biomembranes, 436 (4), 900–903.
  • Shchelokovskyy, P., Tristram-Nagle, S., and Dimova, R., 2011. Effect of the HIV-1 fusion peptide on the mechanical properties and leaflet coupling of lipid bilayers. New journal of physics, 13 (2), 25004.
  • Shi, Z., et al., 2018. Cell membranes resist flow. Cell, 175 (7), 1769–1779.
  • Shibly, S.U.A., et al., 2016. Experimental estimation of membrane tension induced by osmotic pressure. Biophysical journal, 111 (10), 2190–2201.
  • Shnyrova, A.V., et al., 2013. Geometric catalysis of membrane fission driven by flexible dynamin rings. Science (New York, N.Y.), 339 (6126), 1433–1436.
  • Shojaei-Baghini, E., Zheng, Y., and Sun, Y., 2013. Automated micropipette aspiration of single cells. Annals of biomedical engineering, 41 (6), 1208–1216.
  • Simon, S. and McIntosh, T., 1986. [38] Depth of water penetration into lipid bilayers. Methods in enzymology. 127, 511–521.
  • Simunovic, M., et al., 2019. Curving cells inside and out: roles of bar domain proteins in membrane shaping and its cellular implications. Annual review of cell and developmental biology, 35, 111–129.
  • Sneddon, I.N., 1965. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. International journal of engineering science, 3 (1), 47–57.
  • Solmaz, M.E., et al., 2012. Optical stretching of giant unilamellar vesicles with an integrated dual-beam optical trap. Biomedical optics express, 3 (10), 2419–2427.
  • Solmaz, M.E., et al., 2013. Optical stretching as a tool to investigate the mechanical properties of lipid bilayers. RSC advances, 3 (37), 16632–16638.
  • Song, J. and Waugh, R.E., 1990. Bilayer membrane bending stiffness by tether formation from mixed PC-PS lipid vesicles. Journal of biomechanical engineering, 112 (3), 235–240.
  • Sorkin, R., et al., 2018. Nanomechanics of extracellular vesicles reveals vesiculation pathways. Small, 14 (39), 1801650.
  • Sorkin, R., et al., 2020. Synaptotagmin-1 and Doc2b exhibit distinct membrane-remodeling mechanisms. Biophysical journal, 118 (3), 643–656.
  • Sorre, B., et al., 2009. Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proceedings of the National Academy of Sciences of the United States of America, 106 (14), 5622–5626.
  • Sorre, B., et al., 2012. Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proceedings of the National Academy of Sciences of the United States of America, 109 (1), 173–178.
  • Sraj, I., et al., 2012. Erythrocyte deformation in high-throughput optical stretchers. Physical review. E, statistical, nonlinear, and soft matter physics, 85 (4 Pt 1), 041923.
  • Steinkühler, J., et al., 2019. Mechanical properties of plasma membrane vesicles correlate with lipid order, viscosity and cell density. Communications biology, 2 (1), 1–8.
  • Storm, G., et al., 1987. Influence of lipid composition on the antitumor activity exerted by doxorubicin-containing liposomes in a rat solid tumor model. Cancer research, 47 (13), 3366–3372.
  • Takechi-Haraya, Y., et al., 2016. Atomic force microscopic analysis of the effect of lipid composition on liposome membrane rigidity. Langmuir : the ACS journal of surfaces and colloids, 32 (24), 6074–6082.
  • Takechi-Haraya, Y., Sakai-Kato, K., and Goda, Y., 2017. Membrane rigidity determined by atomic force microscopy is a parameter of the permeability of liposomal membranes to the hydrophilic compound calcein. AAPS pharmscitech, 18 (5), 1887–1893.
  • Tanford, C., 1978. The hydrophobic effect and the organization of living matter. Science (New York, N.Y.), 200 (4345), 1012–1018.
  • Tanford, C., 1980. The hydrophobic effect: formation of micelles and biological membranes. 2nd ed. New York, NY: John Wiley.
  • Tian, A. and Baumgart, T., 2009. Sorting of lipids and proteins in membrane curvature gradients. Biophysical journal, 96 (7), 2676–2688.
  • Tian, A., et al., 2009. Bending stiffness depends on curvature of ternary lipid mixture tubular membranes. Biophysical journal, 97 (6), 1636–1646.
  • Tominaga, N., Yoshioka, Y., and Ochiya, T., 2015. A novel platform for cancer therapy using extracellular vesicles. Advanced drug delivery reviews, 95, 50–55.
  • Vader, P., et al., 2016. Extracellular vesicles for drug delivery. Advanced drug delivery reviews, 106 (Pt A), 148–156.
  • Van Der Werf, K.O., et al., 1994. Adhesion force imaging in air and liquid by adhesion mode atomic force microscopy. Applied physics letters, 65 (9), 1195–1197.
  • Vitkova, V., et al., 2004a. Surface charge effect on the bending elasticity of lipid bilayers. Comptes Rendus de L’academie Bulgare Des Sciences, 57 (11), 11–25.
  • Vitkova, V., et al., 2006a. Sugars in the aqueous phase change the mechanical properties of lipid mono-and bilayers. Molecular crystals and liquid crystals, 449 (1), 95–106.
  • Vitkova, V., Genova, J., and Bivas, I., 2004b. Permeability and the hidden area of lipid bilayers. European biophysics journal : EBJ, 33 (8), 706–714.
  • Vitkova, V., et al., 2006b. Alamethicin influence on the membrane bending elasticity. European biophysics journal : EBJ, 35 (3), 281–286.
  • Vitkova, V., et al., 2012. Bending rigidity of lipid membranes and the ph of aqueous surroundings. Comptes Rendus de L’académie Bulgare Des Sciences, 65 (3), 329–334.
  • Vitkova, V. and Petrov, A. G., 2013. Lipid bilayers and membranes: material properties. In: A. Iglič and J. Genova, eds. Advances in planar lipid bilayers and liposomes. Vol. 17. Oxford, UK: Academic Press, 89–138.
  • Vorselen, D., et al., 2016. Controlled tip wear on high roughness surfaces yields gradual broadening and rounding of cantilever tips. Scientific reports, 6, 36972.
  • Vorselen, D., et al., 2017. Competition between bending and internal pressure governs the mechanics of fluid nanovesicles. ACS nano, 11 (3), 2628–2636.
  • Vorselen, D., et al., 2018a. Multilamellar nanovesicles show distinct mechanical properties depending on their degree of lamellarity. Nanoscale, 10 (11), 5318–5324.
  • Vorselen, D., et al., 2018b. The fluid membrane determines mechanics of erythrocyte extracellular vesicles and is softened in hereditary spherocytosis. Nature communications, 9 (1), 1–9.
  • Wang, H. and Chu, P. K., 2013. Surface characterization of biomaterials. In: A. Bandyopadhyay and S. Bose, eds. Characterization of biomaterials. Waltham, MA: Elsevier, 105–174.
  • Waugh, R. and Evans, E., 1979. Thermoelasticity of red blood cell membrane. Biophysical journal, 26 (1), 115–131.
  • Woo, J., Sharma, S., and Gimzewski, J., 2016. The role of isolation methods on a nanoscale surface structure and its effect on the size of exosomes. Journal of circulating biomarkers, 5, 11.
  • Yang, Y., et al., 2018. Extracellular vesicles as a platform for membrane-associated therapeutic protein delivery. Journal of extracellular vesicles, 7 (1), 1440131.
  • Yu, M., et al., 2015. Ellipsoidal relaxation of deformed vesicles. Physical review letters, 115 (12), 128303.
  • Zhou, Y. and Raphael, R.M., 2007. Solution pH alters mechanical and electrical properties of phosphatidylcholine membranes: relation between interfacial electrostatics, intramembrane potential, and bending elasticity. Biophysical journal, 92 (7), 2451–2462.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.