Home Life Sciences Reshaping biological membranes in endocytosis: crossing the configurational space of membrane-protein interactions
Article
Licensed
Unlicensed Requires Authentication

Reshaping biological membranes in endocytosis: crossing the configurational space of membrane-protein interactions

  • Mijo Simunovic

    Mijo Simunovic is a PhD student in chemistry at the University of Chicago and in physics at the Curie Institute in Paris. In his research, he combines coarse-grained theoretical techniques in the Voth group with experimental biophysical methods at the Bassereau group to study the physics underlying protein-induced membrane remodeling phenomena. Before joining these two groups, he received his BS and MS in physical chemistry from the University of Zagreb, where he employed theoretical and experimental approaches in investigating problems in synthetic and quantum chemistry.

    and Patricia Bassereau

    Patricia Bassereau is currently Directrice de Recherche, CNRS at the Curie Institute in Paris. After spending 7 years in Montpellier (GDPC) working on the structure of surfactant-based phases, and a year as a visiting scientist at the Almaden IBM Center (San Jose, USA) on the structure of thin polymer films, she moved in 1993 to the Curie Institute. She initially investigated the interactions of soluble proteins with polymer monolayers. In the last 15 years, she has been working in the field of ‘physics for cell biology’. She has developed a multidisciplinary approach to understand the role of lipid membranes in important cellular functions such as intracellular trafficking, endo/exocytosis, transmembrane ion transport (‘active membranes’), or cell adhesion.

    EMAIL logo
Published/Copyright: December 17, 2013

Abstract

Lipid membranes are highly dynamic. Over several decades, physicists and biologists have uncovered a number of ways they can change the shape of membranes or alter their phase behavior. In cells, the intricate action of membrane proteins drives these processes. Considering the highly complex ways proteins interact with biological membranes, molecular mechanisms of membrane remodeling still remain unclear. When studying membrane remodeling phenomena, researchers often observe different results, leading them to disparate conclusions on the physiological course of such processes. Here we discuss how combining research methodologies and various experimental conditions contributes to the understanding of the entire phase space of membrane-protein interactions. Using the example of clathrin-mediated endocytosis we try to distinguish the question ‘how can proteins remodel the membrane?’ from ‘how do proteins remodel the membrane in the cell?’ In particular, we consider how altering physical parameters may affect the way membrane is remodeled. Uncovering the full range of physical conditions under which membrane phenomena take place is key in understanding the way cells take advantage of membrane properties in carrying out their vital tasks.


Corresponding author: Patricia Bassereau, Institut Curie, Centre National de la Recherche Scientifique Unité Mixte de Recherche 168, Université Pierre et Marie Curie, F-75248 Paris, France, e-mail:

About the authors

Mijo Simunovic

Mijo Simunovic is a PhD student in chemistry at the University of Chicago and in physics at the Curie Institute in Paris. In his research, he combines coarse-grained theoretical techniques in the Voth group with experimental biophysical methods at the Bassereau group to study the physics underlying protein-induced membrane remodeling phenomena. Before joining these two groups, he received his BS and MS in physical chemistry from the University of Zagreb, where he employed theoretical and experimental approaches in investigating problems in synthetic and quantum chemistry.

Patricia Bassereau

Patricia Bassereau is currently Directrice de Recherche, CNRS at the Curie Institute in Paris. After spending 7 years in Montpellier (GDPC) working on the structure of surfactant-based phases, and a year as a visiting scientist at the Almaden IBM Center (San Jose, USA) on the structure of thin polymer films, she moved in 1993 to the Curie Institute. She initially investigated the interactions of soluble proteins with polymer monolayers. In the last 15 years, she has been working in the field of ‘physics for cell biology’. She has developed a multidisciplinary approach to understand the role of lipid membranes in important cellular functions such as intracellular trafficking, endo/exocytosis, transmembrane ion transport (‘active membranes’), or cell adhesion.

The P.B. group belongs to the French research consortium ‘CellTiss’ and to the Labex CelTisPhyBio 11-LBX-0038. M.S. is funded by the Chateaubriand fellowship and the France and Chicago Collaborating in the Sciences grant.

References

Alberts, B. (2002). Molecular biology of the cell, 4th edition. (New York, USA: Garland Science).Search in Google Scholar

Ayton, G.S. and Voth, G.A. (2010). Multiscale simulation of protein mediated membrane remodeling. Semin. Cell Dev. Biol. 21, 357–362.10.1016/j.semcdb.2009.11.011Search in Google Scholar PubMed PubMed Central

Bai, J., Hu, Z., Dittman, J.S., Pym, E.C., and Kaplan, J.M. (2010). Endophilin functions as a membrane-bending molecule and is delivered to endocytic zones by exocytosis. Cell 143, 430–441.10.1016/j.cell.2010.09.024Search in Google Scholar PubMed PubMed Central

Baumgart, T., Hess, S.T., and Webb, W.W. (2003). Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425, 821–824.10.1038/nature02013Search in Google Scholar PubMed

Bhatia, V.K., Hatzakis, N.S., and Stamou, D. (2010). A unifying mechanism accounts for sensing of membrane curvature by BAR domains, amphipathic helices and membrane-anchored proteins. Semin. Cell Dev. Biol. 21, 381–390.10.1016/j.semcdb.2009.12.004Search in Google Scholar PubMed

Bhatia, V.K., Madsen, K.L., Bolinger, P.Y., Kunding, A., Hedegard, P., Gether, U., and Stamou, D. (2009). Amphipathic motifs in BAR domains are essential for membrane curvature sensing. EMBO J. 28, 3303–3314.10.1038/emboj.2009.261Search in Google Scholar PubMed PubMed Central

Bickel, T., Jeppesen, C., and Marques, C.M. (2001). Local entropic effects of polymers grafted to soft interfaces. Eur. Phys. J. E. 4, 33–43.10.1007/s101890170140Search in Google Scholar

Blood, P.D. and Voth, G.A. (2006). Direct observation of Bin/amphiphysin/Rvs (BAR). domain-induced membrane curvature by means of molecular dynamics simulations. Proc. Natl. Acad. Sci. USA 103, 15068–15072.10.1073/pnas.0603917103Search in Google Scholar PubMed PubMed Central

Boucrot, E., Pick, A., Camdere, G., Liska, N., Evergren, E., McMahon, H.T., and Kozlov, M.M. (2012). Membrane fission is promoted by insertion of amphipathic helices and is restricted by crescent BAR domains. Cell 149, 124–136.10.1016/j.cell.2012.01.047Search in Google Scholar PubMed PubMed Central

Boulant, S., Kural, C., Zeeh, J.C., Ubelmann, F., and Kirchhausen, T. (2011). Actin dynamics counteract membrane tension during clathrin-mediated endocytosis. Nat. Cell Biol. 13, 1124–1131.10.1038/ncb2307Search in Google Scholar PubMed PubMed Central

Breidenich, M., Netz, R.R., and Lipowsky, R. (2000). The shape of polymer-decorated membranes. Europhys. Lett. 49, 431–437.10.1209/epl/i2000-00167-2Search in Google Scholar

Campelo, F., McMahon, H.T., and Kozlov, M.M. (2008). The hydrophobic insertion mechanism of membrane curvature generation by proteins. Biophys. J. 95, 2325–2339.10.1529/biophysj.108.133173Search in Google Scholar

Cocucci, E., Aguet, F., Boulant, S., and Kirchhausen, T. (2012). The first five seconds in the life of a clathrin-coated pit. Cell 150, 495–507.10.1016/j.cell.2012.05.047Search in Google Scholar

Cullis, P.R. and de Kruijff, B. (1979). Lipid polymorphism and the functional roles of lipids in biological membranes. Biochim. Biophys. Acta 559, 399–420.10.1016/0304-4157(79)90012-1Search in Google Scholar

Dai, J.W. and Sheetz, M.P. (1999). Membrane tether formation from blebbing cells. Biophys. J. 77, 3363–3370.10.1016/S0006-3495(99)77168-7Search in Google Scholar

Dannhauser, P.N. and Ungewickell, E.J. (2012). Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol. 14, 634–639.10.1038/ncb2478Search in Google Scholar

Doyon, J.B., Zeitler, B., Cheng, J., Cheng, A.T., Cherone, J.M., Santiago, Y., Lee, A.H., Vo, T.D., Doyon, Y., Miller, J.C., et al. (2011). Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells. Nat. Cell Biol. 13, 331–337.10.1038/ncb2175Search in Google Scholar

Drin, G. and Antonny, B. (2010). Amphipathic helices and membrane curvature. FEBS Lett 584, 1840–1847.10.1016/j.febslet.2009.10.022Search in Google Scholar

Farsad, K. and De Camilli, P. (2003). Mechanisms of membrane deformation. Curr. Opin. Cell Biol. 15, 372–381.10.1016/S0955-0674(03)00073-5Search in Google Scholar

Fotin, A., Cheng, Y., Sliz, P., Grigorieff, N., Harrison, S.C., Kirchhausen, T., and Walz, T. (2004). Molecular model for a complete clathrin lattice from electron cryomicroscopy. Nature 432, 573–579.10.1038/nature03079Search in Google Scholar PubMed

Frost, A., Perera, R., Roux, A., Spasov, K., Destaing, O., Egelman, E.H., De Camilli, P., and Unger, V.M. (2008). Structural basis of membrane invagination by F-BAR domains. Cell 132, 807–817.10.1016/j.cell.2007.12.041Search in Google Scholar PubMed PubMed Central

Goetz, R., Gompper, G., and Lipowsky, R. (1999). Mobility and elasticity of self-assembled membranes. Phys. Rev. Lett. 82, 221–224.10.1103/PhysRevLett.82.221Search in Google Scholar

Heinrich, M.C., Capraro, B.R., Tian, A., Isas, J.M., Langen, R., and Baumgart, T. (2010). Quantifying membrane curvature generation of amphiphysin N-BAR domains. J. Phys. Chem. Lett. 1, 3401–3406.10.1021/jz101403qSearch in Google Scholar PubMed PubMed Central

Helfrich, W. (1973). Elastic properties of lipid bilayers: theory and possible experiments. Z. Naturforsch. C 28, 693–703.10.1515/znc-1973-11-1209Search in Google Scholar PubMed

Helfrich, W. (1989). Hats and saddles in lipid-membranes. Liquid Crystals 5, 1647–1658.10.1080/02678298908045675Search in Google Scholar

Julicher, F. and Lipowsky, R. (1993). Domain-induced budding of vesicles. Phys. Rev. Lett. 70, 2964–2967.10.1103/PhysRevLett.70.2964Search in Google Scholar PubMed

Kirchhausen, T. (2009). Imaging endocytic clathrin structures in living cells. Trends Cell Biol. 19, 596–605.10.1016/j.tcb.2009.09.002Search in Google Scholar PubMed PubMed Central

Kukulski, W., Schorb, M., Kaksonen, M., and Briggs, J.A. (2012). Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150, 508–520.10.1016/j.cell.2012.05.046Search in Google Scholar PubMed

Kukulski, W., Schorb, M., Welsch, S., Picco, A., Kaksonen, M., and Briggs, J.A. (2011). Correlated fluorescence and 3D electron microscopy with high sensitivity and spatial precision. J. Cell Biol. 192, 111–119.10.1083/jcb.201009037Search in Google Scholar PubMed PubMed Central

Lieber, A.D., Yehudai-Resheff, S., Barnhart, E.L., Theriot, J.A., and Keren, K. (2013). membrane tension in rapidly moving cells is determined by cytoskeletal forces. Curr. Biol., 23, 1409–1417.10.1016/j.cub.2013.05.063Search in Google Scholar PubMed

Lipowsky, R. (1991). The conformation of membranes. Nature 349, 475–481.10.1038/349475a0Search in Google Scholar PubMed

Lipowsky, R. (2013). Spontaneous tubulation of membranes and vesicles reveals membrane tension generated by spontaneous curvature. Farad. Discuss. 161, 305–331.10.1039/C2FD20105DSearch in Google Scholar PubMed

Lipowsky, R. and Dimova, R. (2003). Domains in membranes and vesicles. J. Phys. Condens. Matter. 15, S31–S45.10.1088/0953-8984/15/1/304Search in Google Scholar

Lipowsky, R. and Sackmann, E. (ed). (1995). Structure and Dynamics of Membranes: From Cells to Vesicles. Elsevier: North Holland, Amsterdam.Search in Google Scholar

McMahon, H.T. and Gallop, J.L. (2005). Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438, 590–596.10.1038/nature04396Search in Google Scholar PubMed

Meinecke, M., Boucrot, E., Camdere, G., Hon, W.C., Mittal, R., and McMahon, H.T. (2013). Cooperative Recruitment of Dynamin and BIN/Amphiphysin/Rvs (BAR). Domain-containing Proteins Leads to GTP-dependent Membrane Scission. J. Biol. Chem. 288, 6651–6661.10.1074/jbc.M112.444869Search in Google Scholar PubMed PubMed Central

Mim, C., Cui, H., Gawronski-Salerno, J.A., Frost, A., Lyman, E., Voth, G.A., and Unger, V.M. (2012a). Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149, 137–145.10.1016/j.cell.2012.01.048Search in Google Scholar PubMed PubMed Central

Mim, C., Cui, H.S., Gawronski-Salerno, J.A., Frost, A., Lyman, E., Voth, G.A., and Unger, V.M. (2012b). Structural basis of membrane bending by the N-BAR protein endophilin. Cell 149, 137–145.10.1016/j.cell.2012.01.048Search in Google Scholar

Mim, C. and Unger, V.M. (2012). Membrane curvature and its generation by BAR proteins. Trends Biochem. Sci. 37, 526–533.10.1016/j.tibs.2012.09.001Search in Google Scholar PubMed PubMed Central

Morlot, S., Galli, V., Klein, M., Chiaruttini, N., Manzi, J., Humbert, F., Dinis, L., Lenz, M., Cappello, G., and Roux, A. (2012). Membrane shape at the edge of the dynamin helix sets location and duration of the fission reaction. Cell 151, 619–629.10.1016/j.cell.2012.09.017Search in Google Scholar PubMed PubMed Central

Peter, B.J., Kent, H.M., Mills, I.G., Vallis, Y., Butler, P.J., Evans, P.R., and McMahon, H.T. (2004). BAR domains as sensors of membrane curvature: the amphiphysin BAR structure. Science 303, 495–499.10.1126/science.1092586Search in Google Scholar PubMed

Posor, Y., Eichhorn-Gruenig, M., Puchkov, D., Schoneberg, J., Ullrich, A., Lampe, A., Muller, R., Zarbakhsh, S., Gulluni, F., Hirsch, E., et al. (2013). Spatiotemporal control of endocytosis by phosphatidylinositol-3,4-bisphosphate. Nature 499, 233–237.10.1038/nature12360Search in Google Scholar PubMed

Qualmann, B., Koch, D., and Kessels, M.M. (2011). Let’s go bananas: revisiting the endocytic BAR code. EMBO J. 30, 3501–3515.10.1038/emboj.2011.266Search in Google Scholar

Ramakrishnan, N., Kumar, P.B.S., and Ipsen, J.H. (2013). Membrane-mediated aggregation of curvature-inducing nematogens and membrane tubulation. Biophys. J. 104, 1018–1028.10.1016/j.bpj.2012.12.045Search in Google Scholar

Ramesh, P., Baroji, Y.F., Reihani, S.N., Stamou, D., Oddershede, L.B., and Bendix, P.M. (2013). FBAR syndapin 1 recognizes and stabilizes highly curved tubular membranes in a concentration dependent manner. Sci. Rep. 3, 1565.10.1038/srep01565Search in Google Scholar

Raucher, D. and Sheetz, M.P. (1999). Characteristics of a membrane reservoir buffering membrane tension. Biophys. J. 77, 1992–2002.10.1016/S0006-3495(99)77040-2Search in Google Scholar

Reynwar, B.J., Illya, G., Harmandaris, V.A., Muller, M.M., Kremer, K., and Deserno, M. (2007). Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447, 461–464.10.1038/nature05840Search in Google Scholar PubMed

Saheki, Y. and De Camilli, P. (2012). Synaptic vesicle endocytosis. Cold Spring Harb. Perspect. Biol. 4, a005645.10.1101/cshperspect.a005645Search in Google Scholar PubMed PubMed Central

Saric, A. and Cacciuto, A. (2012). Fluid membranes can drive linear aggregation of adsorbed spherical nanoparticles. Phys. Rev. Lett. 108, 118101.10.1103/PhysRevLett.108.118101Search in Google Scholar PubMed

Seifert, U. (1997). Configurations of fluid membranes and vesicles. Adv. Phys. 46, 13–137.10.1080/00018739700101488Search in Google Scholar

Sens, P., Johannes, L., and Bassereau, P. (2008). Biophysical approaches to protein-induced membrane deformations in trafficking. Curr. Opin. Cell Biol. 20, 476–482.10.1016/j.ceb.2008.04.004Search in Google Scholar PubMed

Simunovic, M., Mim, C., Marlovits, T.C., Resch, G., Unger, V.M., and Voth, G.A. (2013a). Protein-mediated transformation of lipid vesicles into tubular networks. Biophys J. 105, 711–719.10.1016/j.bpj.2013.06.039Search in Google Scholar PubMed PubMed Central

Simunovic, M., Srivastava, A., and Voth, G.A. (2013b). Linear aggregation of proteins on the membrane as a prelude to membrane remodeling. Proc. Natl. Acad. Sci. USA, 110, 20396–20401.10.1073/pnas.1309819110Search in Google Scholar

Singh, P., Mahata, P., Baumgart, T., and Das, S.L. (2012). Curvature sorting of proteins on a cylindrical lipid membrane tether connected to a reservoir. Phys. Rev. E, 85.10.1103/PhysRevE.85.051906Search in Google Scholar

Sorre, B., Callan-Jones, A., Manneville, J.B., Nassoy, P., Joanny, J.F., Prost, J., Goud, B., and Bassereau, P. (2009). Curvature-driven lipid sorting needs proximity to a demixing point and is aided by proteins. Proc. Natl. Acad. Sci. USA 106, 5622–5626.10.1073/pnas.0811243106Search in Google Scholar

Sorre, B., Callan-Jones, A., Manzi, J., Goud, B., Prost, J., Bassereau, P., and Roux, A. (2012). Nature of curvature coupling of amphiphysin with membranes depends on its bound density. Proc. Natl. Acad. Sci. USA 109, 173–178.10.1073/pnas.1103594108Search in Google Scholar

Stachowiak, J.C., Schmid, E.M., Ryan, C.J., Ann, H.S., Sasaki, D.Y., Sherman, M.B., Geissler, P.L., Fletcher, D.A., and Hayden, C.C. (2012). Membrane bending by protein-protein crowding. Nat. Cell Biol. 14, 944–949.10.1038/ncb2561Search in Google Scholar

Taylor, M.J., Perrais, D., and Merrifield, C.J. (2011). A High precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. Plos Biology, 9, e1000604.10.1371/journal.pbio.1000604Search in Google Scholar

van Weering, J.R.T., Sessions, R.B., Traer, C.J., Kloer, D.P., Bhatia, V.K., Stamou, D., Carlsson, S.R., Hurley, J.H., and Cullen, P.J. (2012). Molecular basis for SNX-BAR-mediated assembly of distinct endosomal sorting tubules. EMBO J. 31, 4466–4480.10.1038/emboj.2012.283Search in Google Scholar

Verstreken, P., Kjaerulff, O., Lloyd, T.E., Atkinson, R., Zhou, Y., Meinertzhagen, I.A., and Bellen, H.J. (2002). Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109, 101–112.10.1016/S0092-8674(02)00688-8Search in Google Scholar

Weinberg, J. and Drubin, D.G. (2012). Clathrin-mediated endocytosis in budding yeast. Trends Cell Biol, 22, 1–13.10.1016/j.tcb.2011.09.001Search in Google Scholar PubMed PubMed Central

Yin, Y., Arkhipov, A., and Schulten, K. (2009). Simulations of Membrane Tubulation by Lattices of Amphiphysin N-BAR Domains. Structure 17, 882–892.10.1016/j.str.2009.03.016Search in Google Scholar PubMed PubMed Central

Zhu, C., Das, S.L., and Baumgart, T. (2012). Nonlinear sorting, curvature generation, and crowding of endophilin N-BAR on tubular membranes. Biophys. J. 102, 1837–1845.10.1016/j.bpj.2012.03.039Search in Google Scholar PubMed PubMed Central

Received: 2013-8-20
Accepted: 2013-12-16
Published Online: 2013-12-17
Published in Print: 2014-03-01

©2014 by Walter de Gruyter Berlin Boston

Downloaded on 26.1.2026 from https://www.degruyterbrill.com/document/doi/10.1515/hsz-2013-0242/html?lang=en
Scroll to top button