- Letter
- Open Access
Probing lipid membrane bending mechanics using gold nanorod tracking
Phys. Rev. Research 4, L012027 – Published 7 March, 2022
DOI: https://doi.org/10.1103/PhysRevResearch.4.L012027
Abstract
Lipid bilayer membranes undergo rapid bending undulations with wavelengths from tens of nanometers to tens of microns due to thermal fluctuations. Here, we probe such undulations and the membranes' mechanics by measuring the time-varying orientation of single gold nanorods (GNRs) adhered to the membrane, using high-speed dark field microscopy. In a lipid vesicle, such measurements allow the determination of the membrane's viscosity, bending rigidity, and tension as well as the friction coefficient for sliding of the monolayers over one another. The in-plane rotation of the GNR is hindered by undulations in a tension dependent manner, consistent with simulations. The motion of single GNRs adhered to the plasma membrane of living cultured cells similarly reveals the membrane's complex physics and coupling to the cell's actomyosin cortex.
Physics Subject Headings (PhySH)
Article Text
Supplemental Material
References (60)
- Z. T. Graber, Z. Shi, and T. Baumgart, Cations induce shape remodeling of negatively charged phospholipid membranes, Phys. Chem. Chem. Phys. 19, 15285 (2017).
- Z. Shi, Z. T. Graber, T. Baumgart, H. A. Stone, and A. E. Cohen, Cell membranes resist flow, Cell 175, 1769 (2018).
- J.-B. Fournier, D. Lacoste, and E. Raphaël, Fluctuation Spectrum of Fluid Membranes Coupled to an Elastic Meshwork: Jump of the Effective Surface Tension at the Mesh Size, Phys. Rev. Lett. 92, 018102 (2004).
- R. Dimova, Recent developments in the field of bending rigidity measurements on membranes, Adv. Colloid Interface Sci. 208, 225 (2014). Special issue in honour of Wolfgang Helfrich.
- J. I. Kilpatrick, I. Revenko, and B. J. Rodriguez, Nanomechanics of cells and biomaterials studied by atomic force microscopy, Adv. Healthcare Mater. 4, 2456 (2015).
- M. Kocun and A. Janshoff, Pulling tethers from pore-spanning bilayers: Towards simultaneous determination of local bending modulus and lateral tension of membranes, Small 8, 847 (2012).
- H. Engelhardt, H. Gaub, and E. Sackmann, Viscoelastic properties of erythrocyte membranes in high-frequency electric fields, Nature (London) 307, 378 (1984).
- R. Dimova, N. Bezlyepkina, M. D. Jordö, R. L. Knorr, K. A. Riske, M. Staykova, P. M. Vlahovska, T. Yamamoto, P. Yang, and R. Lipowsky, Vesicles in electric fields: Some novel aspects of membrane behavior, Soft Matter 5, 3201 (2009).
- M. Kummrow and W. Helfrich, Deformation of giant lipid vesicles by electric fields, Phys. Rev. A 44, 8356 (1991).
- M. P. Sheetz and J. Dai, Modulation of membrane dynamics and cell motility by membrane tension, Trends Cell Biol. 6, 85 (1996).
- J. Dai and M. P. Sheetz, Mechanical properties of neuronal growth cone membranes studied by tether formation with laser optical tweezers, Biophys. J. 68, 988 (1995).
- B. R. Capraro, Y. Yoon, W. Cho, and T. Baumgart, Curvature sensing by the Epsin N-terminal homology domain measured on cylindrical lipid membrane tethers, J. Am. Chem. Soc. 132, 1200 (2010).
- R. M. Hochmuth, Micropipette aspiration of living cells, J. Biomech. 33, 15 (2000).
- Y. Park, C. A. Best, K. Badizadegan, R. R. Dasari, M. S. Feld, T. Kuriabova, M. L. Henle, A. J. Levine, and G. Popescu, Measurement of red blood cell mechanics during morphological changes, Proc. Natl. Acad. Sci. USA 107, 6731 (2010).
- X. Feng, W.-H. Leong, K. Xia, C.-F. Liu, G.-Q. Liu, T. Rendler, J. Wrachtrup, R.-B. Liu, and Q. Li, Association of nanodiamond rotation dynamics with cell activities by translation-rotation tracking, Nano Lett. 21, 3393 (2021).
- T. T. Hormel, S. Q. Kurihara, M. K. Brennan, M. C. Wozniak, and R. Parthasarathy, Measuring Lipid Membrane Viscosity Using Rotational and Translational Probe Diffusion, Phys. Rev. Lett. 112, 188101 (2014).
- W. Xie, L. Wang, Y. Zhang, L. Su, A. Shen, J. Tan, and J. Hu, Nuclear targeted nanoprobe for single living cell detection by surface-enhanced Raman scattering, Bioconjugate Chem. 20, 768 (2009).
- M. I. Angelova and D. S. Dimitrov, Liposome electroformation, Faraday Discuss. Chem. Soc. 81, 303 (1986).
- A. Tian and T. Baumgart, Sorting of lipids and proteins in membrane curvature gradients, Biophys. J. 96, 2676 (2009).
- See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevResearch.4.L012027 for the additional information about the experimental methods, details of the MC simulation, and details of the theoretical models, and additional figures for the simulation and experimental results, which includes Refs. [21, 22].
- M. Khan and T. G. Mason, Random walks of colloidal probes in viscoelastic materials, Phys. Rev. E 89, 042309 (2014).
- N. Ramakrishnan, K. K. Sreeja, A. Roychoudhury, D. M. Eckmann, P. S. Ayyaswamy, T. Baumgart, T. Pucadyil, S. Patil, V. M. Weaver, and R. Radhakrishnan, Excess area dependent scaling behavior of nano-sized membrane tethers, Phys. Biol. 15, 026002 (2018).
- M. Molaei, E. Atefi, and J. C. Crocker, Nanoscale Rheology and Anisotropic Diffusion Using Single Gold Nanorod Probes, Phys. Rev. Lett. 120, 118002 (2018).
- J. C. Crocker and D. G. Grier, Methods of digital video microscopy for colloidal studies, J. Colloid Interface Sci. 179, 298 (1996).
- K. A. Rose, M. Molaei, M. J. Boyle, D. Lee, J. C. Crocker, and R. J. Composto, Particle tracking of nanoparticles in soft matter, J. Appl. Phys. 127, 191101 (2020).
- A. J. Levine, T. B. Liverpool, and F. C. MacKintosh, Dynamics of Rigid and Flexible Extended Bodies in Viscous Films and Membranes, Phys. Rev. Lett. 93, 038102 (2004).
- P. G. Saffman and M. Delbrück, Brownian motion in biological membranes, Proc. Natl. Acad. Sci. USA 72, 3111 (1975).
- C. A. Stanich, A. R. Honerkamp-Smith, G. G. Putzel, C. S. Warth, A. K. Lamprecht, P. Mandal, E. Mann, T.-A. D. Hua, and S. L. Keller, Coarsening dynamics of domains in lipid membranes, Biophys. J. 105, 444 (2013).
- E. P. Petrov, R. Petrosyan, and P. Schwille, Translational and rotational diffusion of micrometer-sized solid domains in lipid membranes, Soft Matter 8, 7552 (2012).
- A. R. Honerkamp-Smith, F. G. Woodhouse, V. Kantsler, and R. E. Goldstein, Membrane Viscosity Determined from Shear-Driven Flow in Giant Vesicles, Phys. Rev. Lett. 111, 038103 (2013).
- N. Kučerka, M.-P. Nieh, and J. Katsaras, Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature, Biochim. Biophys. Acta (BBA) - Biomembranes 1808, 2761 (2011).
- G. Espinosa, I. López-Montero, F. Monroy, and D. Langevin, Shear rheology of lipid monolayers and insights on membrane fluidity, Proc. Natl. Acad. Sci. USA 108, 6008 (2011).
- K. Bacia, P. Schwille, and T. Kurzchalia, Sterol structure determines the separation of phases and the curvature of the liquid-ordered phase in model membranes, Proc. Natl. Acad. Sci. USA 102, 3272 (2005).
- M. B. Boggara, A. Faraone, and R. Krishnamoorti, Effect of pH and ibuprofen on the phospholipid bilayer bending modulus, J. Phys. Chem. B 114, 8061 (2010).
- M. Nagao, E. G. Kelley, R. Ashkar, R. Bradbury, and P. D. Butler, Probing elastic and viscous properties of phospholipid bilayers using neutron spin echo spectroscopy, J. Phys. Chem. Lett. 8, 4679 (2017).
- Z. Yi, M. Nagao, and D. P. Bossev, Bending elasticity of saturated and monounsaturated phospholipid membranes studied by the neutron spin echo technique, J. Phys.: Condens. Matter 21, 155104 (2009).
- T. Takeda, Y. Kawabata, H. Seto, S. Komura, S. K. Ghosh, M. Nagao, and D. Okuhara, Neutron spin–echo investigations of membrane undulations in complex fluids involving amphiphiles, J. Phys. Chem. Solids 60, 1375 (1999).
- F. Brochard and J. F. Lennon, Frequency spectrum of the flicker phenomenon in erythrocytes, J. Phys. (France) 36, 1035 (1975).
- U. Seifert and S. A. Langer, Viscous modes of fluid bilayer membranes, Europhys. Lett. 23, 71 (1993).
- S. A. Shkulipa, W. K. den Otter, and W. J. Briels, Thermal Undulations of Lipid Bilayers Relax by Intermonolayer Friction at Submicrometer Length Scales, Phys. Rev. Lett. 96, 178302 (2006).
- M. C. Watson, E. G. Brandt, P. M. Welch, and F. L. H. Brown, Determining Biomembrane Bending Rigidities from Simulations of Modest Size, Phys. Rev. Lett. 109, 028102 (2012).
- M. Sadeghi and F. Noé, Large-scale simulation of biomembranes incorporating realistic kinetics into coarse-grained models, Nat. Commun. 11, 2951 (2020).
- R. Rodríguez-García, L. R. Arriaga, M. Mell, L. H. Moleiro, I. López-Montero, and F. Monroy, Bimodal Spectrum for the Curvature Fluctuations of Bilayer Vesicles: Pure Bending plus Hybrid Curvature-Dilation Modes, Phys. Rev. Lett. 102, 128101 (2009).
- R. M. Raphael and R. E. Waugh, Accelerated interleaflet transport of phosphatidylcholine molecules in membranes under deformation, Biophys. J. 71, 1374 (1996).
- T. Pott and P. Méléard, The dynamics of vesicle thermal fluctuations is controlled by intermonolayer friction, Europhys. Lett. 59, 87 (2002).
- W. Rawicz, K. C. Olbrich, T. McIntosh, D. Needham, and E. Evans, Effect of chain length and unsaturation on elasticity of lipid bilayers, Biophys. J. 79, 328 (2000).
- E. Evans and W. Rawicz, Entropy-Driven Tension and Bending Elasticity in Condensed-Fluid Membranes, Phys. Rev. Lett. 64, 2094 (1990).
- M. Mell, L. H. Moleiro, Y. Hertle, P. Fouquet, R. Schweins, I. López-Montero, T. Hellweg, and F. Monroy, Bending stiffness of biological membranes: What can be measured by neutron spin echo? Eur. Phys. J. E 36, 75 (2013).
- M. Mell, L. H. Moleiro, Y. Hertle, I. López-Montero, F. J. Cao, P. Fouquet, T. Hellweg, and F. Monroy, Fluctuation dynamics of bilayer vesicles with intermonolayer sliding: Experiment and theory, Chem. Phys. Lipids 185, 61 (2015).
- J. S. Ho and A. Baumgärtner, Self-Avoiding Tethered Membranes, Phys. Rev. Lett. 63, 1324 (1989).
- W. Helfrich, Elastic properties of lipid bilayers: Theory and possible experiments, Z. Naturforsch. C 28, 693 (1973).
- N. Ramakrishnan, P. B. Sunil Kumar, and J. H. Ipsen, Monte Carlo simulations of fluid vesicles with in-plane orientational ordering, Phys. Rev. E 81, 041922 (2010).
- I. W. Hamley and V. Castelletto, Biological soft materials, Angew. Chem., Int. Ed. 46, 4442 (2007).
- A. Kusumi, C. Nakada, K. Ritchie, K. Murase, K. Suzuki, H. Murakoshi, R. S. Kasai, J. Kondo, and T. Fujiwara, Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules, Annu. Rev. Biophys. Biomol. Struct. 34, 351 (2005).
- N. Morone, T. Fujiwara, K. Murase, R. S. Kasai, H. Ike, S. Yuasa, J. Usukura, and A. Kusumi, Three-dimensional reconstruction of the membrane skeleton at the plasma membrane interface by electron tomography, J. Cell Biol. 174, 851 (2006).
- H. T. McMahon and E. Boucrot, Membrane curvature at a glance, J. Cell Sci. 128, 1065 (2015).
- G. J. Doherty and H. T. McMahon, Mediation, modulation, and consequences of membrane-cytoskeleton interactions, Annu. Rev. Biophys. 37, 65 (2008).
- B. D. Hoffman and J. C. Crocker, Cell mechanics: Dissecting the physical responses of cells to force, Annu. Rev. Biomed. Eng. 11, 259 (2009).
- J. Steinkühler, E. Sezgin, I. Urbančič, C. Eggeling, and R. Dimova, Mechanical properties of plasma membrane vesicles correlate with lipid order, viscosity and cell density, Commun. Biol. 2, 1 (2019).
- R. W. Tourdot, N. Ramakrishnan, T. Baumgart, and R. Radhakrishnan, Application of a free-energy-landscape approach to study tension-dependent bilayer tubulation mediated by curvature-inducing proteins, Phys. Rev. E 92, 042715 (2015).