Abstract
We present a non-invasive method to monitor the membrane tension of intracellular organelles using a magnetic field as an external control parameter. By exploiting the spontaneous endocytosis of anionic colloidal ferromagnetic nanoparticles, we obtain endosomes possessing a superparamagnetic lumen in eukaryotic cells. Initially flaccid, the endosomal membrane undulates because of thermal fluctuations, restricted in zero field by the resting tension and the curvature energy of the membrane. When submitted to a uniform magnetic field, the magnetized endosomes elongate along the field, resulting in the flattening of the entropic membrane undulations. The quantification of the endosome deformation for different magnetic fields allows in situ measurement of the resting tension and the bending stiffness of the membrane enclosing the intracellular organelle.
Similar content being viewed by others
References
Bacri JC, Cabuil V, Cebers A, Menager C, Perzynski R (1996) Flattening of ferro-vesicle undulations under a magnetic field. Europhys Lett 33:235–240
Bananis E, Murray JW, Stockert RJ, Satir P, Wolkoff AW (2000) Microtubule and motor-dependent endocytic vesicle sorting in vitro. J Cell Biol 151:179–186
Bausch AR, Ziemann F, Boulbitch AA, Jacobson K, Sackmann E (1998) Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry. Biophys J 75:2038–2049
Dai J, Sheetz MP, Wan X, Morris CE (1998) Membrane tension in swelling and shrinking molluscan neurons. J Neurosci 18:6681–6692
Evans EA (1983) Bending elastic modulus of red blood cell membrane derived from buckling instability in micropipet aspiration tests. Biophys J 43:27–30
Evans EA, Rawicz W (1990) Entropy-driven tension and bending elasticity in condensed-fluid membranes. Phys Rev Lett 64:2094–2097
Häckl W, Seifert U, Sackman E (1997) Effect of fully and partially solubilized amphiphiles on bilayer bending stiffness and temperature dependence of the effective tension of giant vesicles. J Phys II (Paris) 7:1141–1157
Hanzlik M, Heunemann C, Holtkamp-Rotzler E, Winklhofer M, Petersen N, Fleissner G (2000) Superparamagnetic magnetite in the upper beak tissue of homing pigeons. Biometals 13:325–331
Helfrich W, Servuss RM (1987) Undulations, steric interaction and cohesion of fluid membranes. Nuovo Cimento 3D:137–151
Hochmuth FM, Shao JY, Dai J, Sheetz MP (1996) Deformation and flow of membrane into tethers extracted from neuronal growth cones. Biophys J 70:358–369
Holtkamp-Rotzler E, Fleissner G, Hanzlik M, Petersen N (1997) The morphological structure of a possible magnetite-based magnetoreceptor in birds. Ann Geophys 15:117
Kobayashi T, Beuchat MH, Chevallier J, Makino A, Mayran N, Escola JM, Lebrand C, Cosson P, Kobayashi T, Gruenberg J (2002) Separation and characterization of late endosomal membrane domains. J Biol Chem 277:32157–32164
Kummrow M, Helfrich W (1991) Deformation of giant lipid vesicles by electric field. Phys Rev A 44:8356–8360
Manneville JB, Bassereau P, Lévy D, Prost J (1999) Activity of transmembrane proteins induces magnification of shape fluctuations of lipid membranes. Phys Rev Lett 82:4356–4359
Ménager C, Meyer M, Cabuil V, Cebers A, Bacri JC, Perzynski R (2002) Magnetic phospholipid tubes connected to magnetoliposomes: pearling instability induced by a magnetic field. Eur Phys J E 7:325–337
Milner ST, Safran SA (1987) Dynamical fluctuations of droplet microemulsions and vesicles. Phys Rev A 36:4371–4379
Monck JR, Alvarez de Toledo G, Fernandez JM (1990) Tension in secretory granule membranes causes extensive membrane transfer through the exocytotic fusion pore. Proc Natl Acad Sci USA 87:7804–7808
Morris CE, Homann U (2001) Cell surface area regulation and membrane tension. J Membr Biol 179:79–102
Raucher D, Sheetz MP (1999) Membrane expansion increases endocytosis rate during mitosis. J Cell Biol 144:497–506
Raucher D, Sheetz MP (2000) Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol 148:127–136
Roux A, Cappello G, Cartaud J, Prost J, Goud B, Bassereau P (2002) A minimal system allowing tubulation with molecular motors pulling on giant liposomes. Proc Natl Acad Sci USA 99:5394–5399
Sackmann E (1994) Membrane bending energy concept of vesicle- and cell-shapes and shape-transitions. FEBS Lett 346:3–16
Sciaky N, Presley J, Smith C, Zaal KJ, Cole N, Moreira JE, Terasaki M, Siggia E, Lippincott-Schwartz J (1997) Golgi tubule traffic and the effects of brefeldin A visualized in living cells. J Cell Biol 139:1137–1155
Shcherbakov VP, Winklhofer M (1999) The osmotic magnetometer: a new model for magnetoreceptors in animals. Eur Biophys J 28:380–392
Togo T, Krasieva TB, Steinhardt RA (2000) A decrease in membrane tension precedes successful cell-membrane repair. Mol Biol Cell 11:4339–4346
Valberg PA (1984) Magnetometry of ingested particles in pulmonary macrophages. Science 224:513–516
Wilhelm C, Gazeau F, Bacri JC (2002a) Magnetophoresis and ferromagnetic resonance of magnetically labeled cells. Eur Biophys J 31:118–125
Wilhelm C, Gazeau F, Roger J, Pons JN, Bacri JC (2002b) Interaction of anionic superparamagnetic nanoparticles with cells: kinetic analyses of membrane adsorption and subsequent internalization. Langmuir 18:8148–8155
Zilker A, Ziegler M, Sackmann E (1992) Spectral analysis of erythrocyte flickering in the 0.3–4-μm−1 regime by microinterferometry combined with fast image processing. Phys Rev A 46:7998–8001
Acknowledgements
We thank L. Legrand for the SQUID measurements, S. Neveu for providing us the nanoparticles, B. Dacrossa for her technical assistance in TEM and E. Coudrier for fruitful discussions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wilhelm, C., Cebers, A., Bacri, JC. et al. Deformation of intracellular endosomes under a magnetic field. Eur Biophys J 32, 655–660 (2003). https://doi.org/10.1007/s00249-003-0312-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00249-003-0312-0