Abstract
Biological membranes are both barriers and communication interfaces of cells. Transport across membranes is therefore essential for life. It encompasses both endocytotic and exocytotic processes important for cell function, but also the invasion of cells by parasites and viruses, and targeted drug delivery. Whereas interactions on the molecular scale are important for particles with sizes comparable with the thickness of the membrane, the mechanical properties of the entire membrane determine its interaction with larger particles. We focus here on large particles and parasites and discuss wrapping of single particles by homogeneous and complex membranes. Both solid particles with various shapes as well as soft particles are considered. Membrane-mediated interactions of many particles lead to aggregation and tubulation. Finally, active biological mechanisms are shown to support the invasion of parasites, such as the malaria parasite, and to drive phagocytosis.
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References
Abbena E, Salamon S, Gray A (2006) Modern differential geometry of curves and surfaces with Mathematica. Chapman and Hall/CRC, Boca Raton
Agudo-Canalejo J, Lipowsky R (2015) Critical particle sizes for the engulfment of nanoparticles by membranes and vesicles with bilayer asymmetry. ACS Nano 9(4):3704–3720
Atilgan E, Sun SX (2007) Shape transitions in lipid membranes and protein mediated vesicle fusion and fission. J Chem Phys 126(9):095102
Auth T, Gompper G (2009) Budding and vesiculation induced by conical membrane inclusions. Phys Rev E 80(3):031901
Auth T, Gov NS (2009) Diffusion in a fluid membrane with a flexible cortical cytoskeleton. Biophys J 96(3):818–830
Auth T, Safran SA, Gov NS (2007) Fluctuations of coupled fluid and solid membranes with application to red blood cells. Phys Rev E 76(5):051910
Bahrami AH, Lipowsky R, Weikl TR (2012) Tubulation and aggregation of spherical nanoparticles adsorbed on vesicles. Phys Rev Lett 109(18):188102
Bahrami AH et al (2014) Wrapping of nanoparticles by membranes. Adv Colloid Interf Sci 208:214–224
Bao G, Bao XR (2005) Shedding light on the dynamics of endocytosis and viral budding. Proc Natl Acad Sci USA 102(29):9997–9998
Barnoud J, Rossi G, Monticelli L (2014) Lipid membranes as solvents for carbon nanoparticles. Phys Rev Lett 112(6):068102
Barua S et al (2013) Particle shape enhances specificity of antibody-displaying nanoparticles. Proc Natl Acad Sci USA 110(9):3270–3275
Baumgart T, Hess ST, Webb WW (2003) Imaging coexisting fluid domains in biomembrane models coupling curvature and line tension. Nature 425(6960):821–824
Beningo KA, Wang Y-l (2002) Fc-receptor-mediated phagocytosis is regulated by mechanical properties of the target. J Cell Sci 115(4):849–856
Brakke KA (1992) The surface evolver. Exp Math 1(2):141–165
Brewster R, Pincus PA, Safran SA (2009) Hybrid lipids as a biological surface-active component. Biophys J 97(4):1087–1094
Canton I, Battaglia G (2012) Endocytosis at the nanoscale. Chem Soc Rev 41(7):2718–2739
Champion JA, Mitragotri S (2006) Role of target geometry in phagocytosis. Proc Natl Acad Sci USA 103(13):4930–4934
Champion JA, Katare YK, Mitragotri S (2007) Making polymeric micro-and nanoparticles of complex shapes. Proc Natl Acad Sci USA 104(29):11901–11904
Chaudhuri A, Battaglia G, Golestanian R (2011) The effect of interactions on the cellular uptake of nanoparticles. Phys Biol 8(4):046002
Chithrani BD, Chan WCW (2007) Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett 7(6):1542–1550
Chithrani BD, Ghazani AA, Chan WCW (2006) Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett 6(4):662–668
Cho EC, Zhang Q, Xia Y (2011) The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat Nanotech 6(6):385–391
Churchman AH et al (2013) Serum albumin enhances the membrane activity of ZnO nanoparticles. Chem Commun 49(39):4172–4174
Copolovici DM et al (2014) Cell-penetrating peptides: design, synthesis, and applications. ACS Nano 8(3):1972–1994
Cowman AF, Crabb BS (2006) Invasion of red blood cells by malaria parasites. Cell 124(4):755–766
Crick AJ et al (2014) Quantitation of malaria parasite-erythrocyte cell-cell interactions using optical tweezers. Biophys J 107(4):846–853
Dan N et al (1994) Membrane-induced interactions between inclusions. J Phys II (France) 4(10):1713–1725
Dasgupta S, Auth T, Gompper G (2013) Wrapping of ellipsoidal nano-particles by fluid membranes. Soft Matter 9(22):5473–5482
Dasgupta S, Auth T, Gompper G (2014) Shape and orientation matter for the cellular uptake of nonspherical particles. Nano Lett 14(2):687–693
Dasgupta S et al (2014) Membrane-wrapping contributions to malaria parasite invasion of the human erythrocyte. Biophys J 107(1):43–54
Dasgupta S, Auth T, Gompper G (2015) Wrapping of ellipsoidal nano-particles by fluid membranes. Soft Matter 11:7441–7444
Dasgupta S, Auth T, Gompper G (2017) Nano-and microparticles at fluid and biological interfaces. J Phys Condens Matter 29:373003
Decuzzi P, Ferrari M (2006) The adhesive strength of non-spherical particles mediated by specific interactions. Biomaterials 27(30):5307–5314
Decuzzi P, Ferrari M (2007) The role of specific and non-specific interactions in receptor-mediated endocytosis of nanoparticles. Biomaterials 28(18):2915–2922
Decuzzi P, Ferrari M (2008) The receptor-mediated endocytosis of nonspherical particles. Biophys J 94(10):3790–3797
Decuzzi P et al (2009) Intravascular delivery of particulate systems: does geometry really matter? Pharm Res 26(1):235–243
Deserno M (2004) Elastic deformation of a fluid membrane upon colloid binding. Phys Rev E 69(3):031903
Deserno M (2004) When do fluid membranes engulf sticky colloids? J Phys Condens Matter 16(22):S2061
Deserno M, Bickel T (2003) Wrapping of a spherical colloid by a fluid membrane. Europhys Lett 62(5):767
Deserno M, Gelbart WM (2002) Adhesion and wrapping in colloid-vesicle complexes. J Phys Chem B 106(21):5543–5552
Ding H-m, Tian W-de, Ma Y-q (2012) Designing nanoparticle translocation through membranes by computer simulations. ACS Nano 6(2):1230–1238
Ehrig J, Petrov EP, Schwille P (2011) Near-critical fluctuations and cytoskeleton-assisted phase separation lead to subdiffusion in cell membranes. Biophys J 100(1):80–89
Ewers H et al (2010) GM1 structure determines SV40-induced membrane invagination and infection. Nat Cell Biol 12(1):11–18
Fish et al MB (2015) Emergence and utility of nonspherical particles in biomedicine. Ind Eng Chem Res 54(16):4043–4059
Florez L et al (2012) How shape influences uptake: interactions of anisotropic polymer nanoparticles and human mesenchymal stem cells. Small 8(14):2222–2230
Fošnarič M et al (2009) Monte carlo simulations of complex formation between a mixed fluid vesicle and a charged colloid. J Chem Phys 131(10):105103
Gao Y, Yu Y (2013) How half-coated janus particles enter cells. J Am Chem Soc 135(51):19091–19094
Gao H, Shi W, Freund LB (2005) Mechanics of receptor-mediated endocytosis. Proc Natl Acad Sci USA 102(27):9469–9474
Ge P et al (2010) Cryo-em model of the bullet-shaped vesicular stomatitis virus. Science 327(5966):689–693
Gompper G, Kroll DM (2004) Triangulated surface models of fluctuating membranes. In: Nelson DR, Piran T, Weinberg S (eds) Statistical mechanics of membranes and surfaces. World Scientific, Singapore
Gózdz WT (2007) Deformations of lipid vesicles induced by attached spherical particles. Langmuir 23(10):5665–5669
Hamada T et al (2012) Size-dependent partitioning of nano/microparticles mediated by membrane lateral heterogeneity. J Am Chem Soc 134(34):13990–13996
Hansen JC et al (1997) Influence of network topology on the elasticity of the red blood cell membrane skeleton. Biophys J 72(5):2369
Hashemi SM, Sens P, Mohammad-Rafiee F (2014) Regulation of the membrane wrapping transition of a cylindrical target by cytoskeleton adhesion. J R Soc Interface 11(100):20140769
Helfrich W (1973) Elastic properties of lipid bilayers: theory and possible experiments. Z Naturforsch C 28(11–12):693–703
Herant M, Heinrich V, Dembo M (2006) Mechanics of neutrophil phagocytosis: experiments and quantitative models. J Cell Sci 119(9):1903–1913
Herant M et al (2011) Protrusive push versus enveloping embrace: computational model of phagocytosis predicts key regulatory role of cytoskeletal membrane anchors. PLoS Comput Biol 7(1):e1001068
Hoffmann I et al (2014) Softening of phospholipid membranes by the adhesion of silica nanoparticles–as seen by neutron spin-echo (NSE). Nanoscale 6(12):6945–6952
Huang C et al (2013) Role of nanoparticle geometry in endocytosis: laying down to stand up. Nano Lett 13(9):4546–4550
Hurley et al JH (2010) Membrane budding. Cell 143(6):875–887
Ivask A et al (2014) Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, crustaceans and mammalian cells in vitro. PLOS One 9(7):e102108
Jaskiewicz K et al (2012) Incorporation of nanoparticles into polymersomes: size and concentration effects. ACS Nano 6(8):7254–7262
Jaskiewicz K et al (2012) Probing bioinspired transport of nanoparticles into polymersomes. Angew Chem 124(19):4691–4695
Killian JA (1998) Hydrophobic mismatch between proteins and lipids in membranes. Biochim Biophys Acta Rev Biomembr 1376(3):401–416
Koltover I, Raedler JO, Safinya CR (1999) Membrane mediated attraction and ordered aggregation of colloidal particles bound to giant phospholipid vesicles. Phys Rev Lett 82(9):1991
Le Bihan O et al (2009) Cryo-electron tomography of nanoparticle transmigration into liposome. J Struct Biol 168(3):419–425
Lesniak A et al (2012) Effects of the presence or absence of a protein corona on silica nanoparticle uptake and impact on cells. ACS Nano 6(7):5845–5857
Li S, Malmstadt N (2013) Deformation and poration of lipid bilayer membranes by cationic nanoparticles. Soft Matter 9(20):4969–4976
Lin J et al (2010) Penetration of lipid membranes by gold nanoparticles: insights into cellular uptake, cytotoxicity, and their relationship. ACS Nano 4(9):5421–5429
Lipowsky R (1992) Budding of membranes induced by intramembrane domains. J Phys II (France) 2(10):1825–1840
Masters TA et al (2013) Plasma membrane tension orchestrates membrane trafficking, cytoskeletal remodeling, and biochemical signaling during phagocytosis. Proc Natl Acad Sci USA 110(29):11875–11880
Michel R et al (2014) Internalization of silica nanoparticles into fluid liposomes: formation of interesting hybrid colloids. Angew Chem Int Ed 53(46):12441–12445
Mihut AM et al (2013) Tunable adsorption of soft colloids on model biomembranes. ACS Nano 7(12):10752–10763
Möller J et al (2012) The race to the pole: how high-aspect ratio shape and heterogeneous environments limit phagocytosis of filamentous escherichia coli bacteria by macrophages. Nano Lett 12(6):2901–2905
Monopoli MP et al (2012) Biomolecular coronas provide the biological identity of nanosized materials. Nat Nanotechnol 7(12):779–786
Monticelli L et al (2009) Effects of carbon nanoparticles on lipid membranes: a molecular simulation perspective. Soft Matter 5(22):4433–4445
Nicolson GL (2014) The fluid—mosaic model of membrane structure: still relevant to understanding the structure, function and dynamics of biological membranes after more than 40 years. Biochim Biophys Acta Rev Biomembr 1838(6):1451–1466
Noda T et al (2006) Assembly and budding of ebolavirus. PLoS Pathog 2(9):e99–e99
Nowak SA, Chou T (2008) Membrane lipid segregation in endocytosis. Phys Rev E 78(2):021908
Nowak SA, Chou T (2009) Mechanisms of receptor/coreceptor-mediated entry of enveloped viruses. Biophys J 96(7):2624–2636
Osaki F et al (2004) A quantum dot conjugated sugar ball and its cellular uptake. on the size effects of endocytosis in the subviral region. J Am Chem Soc 126(21):6520–6521
Park J-G, Forster JD, Dufresne ER (2010) High-yield synthesis of monodisperse dumbbell-shaped polymer nanoparticles. J Am Chem Soc 132(17):5960–5961
Pletikapić G et al (2012) Atomic force microscopy characterization of silver nanoparticles interactions with marine diatom cells and extracellular polymeric substance. J Mol Recognit 25(5):309–317
Pogodin S, Baulin VA (2010) Can a carbon nanotube pierce through a phospholipid bilayer? ACS Nano 4(9):5293–5300
Raatz M, Lipowsky R, Weikl TR (2014) Cooperative wrapping of nanoparticles by membrane tubes. Soft Matter 10(20):3570–3577
Reynwar BJ, Deserno M (2011) Membrane-mediated interactions between circular particles in the strongly curved regime. Soft Matter 7(18):8567–8575
Reynwar BJ et al (2007) Aggregation and vesiculation of membrane proteins by curvature-mediated interactions. Nature 447(7143):461–464
Richards DM, Endres RG (2014) The mechanism of phagocytosis: two stages of engulfment. Biophys J 107(7):1542–1553
Roiter Y et al (2008) Interaction of nanoparticles with lipid membrane. Nano Lett 8(3):941–944
Rossi G, Monticelli L (2014) Modeling the effect of nano-sized polymer particles on the properties of lipid membranes. J Phys Condens Matter 26(50):503101
Sackmann E (1995) Biological membranes architecture and function. In: Lipowsky R, Sackmann E (eds) Structure and dynamics of membranes. Elsevier, Amsterdam
Šarić A, Cacciuto A (2011) Soft elastic surfaces as a platform for particle self-assembly. Soft Matter 7(18):8324–8329
Šarić A, Cacciuto A (2012) Fluid membranes can drive linear aggregation of adsorbed spherical nanoparticles. Phys Rev Lett 108(11):118101
Šarić A, Cacciuto A (2012) Mechanism of membrane tube formation induced by adhesive nanocomponents. Phys Rev Lett 109(18):188101
Šarić A, Cacciuto A (2013) Self-assembly of nanoparticles adsorbed on fluid and elastic membranes. Soft Matter 9(29):6677–6695
Schäfer LV et al (2011) Lipid packing drives the segregation of transmembrane helices into disordered lipid domains in model membranes. Proc Natl Acad Sci USA 108(4):1343–1348
Smith KA, Jasnow D, Balazs AC (2007) Designing synthetic vesicles that engulf nanoscopic particles. J Chem Phys 127(8):084703
Sondi I, Salopek-Sondi B (2004) Silver nanoparticles as antimicrobial agent: a case study on e. coli as a model for gram-negative bacteria. J Colloid Int Sci 275(1):177–182
Taturet S et al (2013) Effect of functionalized gold nanoparticles on floating lipid bilayers. Langmuir 29(22):6606–6614
Tian F, Zhang X, Dong W (2014) How hydrophobic nanoparticles aggregate in the interior of membranes: a computer simulation. Phys Rev E 90(5):052701
Tollis S et al (2010) The zipper mechanism in phagocytosis: energetic requirements and variability in phagocytic cup shape. BMC Syst Biol 4(1):149
Tzlil S et al (2004) A statistical-thermodynamic model of viral budding. Biophys J 86(4):2037–2048
Upadhyaya A, Sheetz MP (2004) Tension in tubulovesicular networks of golgi and endoplasmic reticulum membranes. Biophys J 86(5):2923–2928
Vácha R, Martinez-Veracoechea FJ, Frenkel D (2011) Receptor-mediated endocytosis of nanoparticles of various shapes. Nano Lett 11(12):5391–5395
Van Lehn RC, Alexander-Katz A (2014) Fusion of ligand-coated nanoparticles with lipid bilayers: effect of ligand flexibility. J Phys Chem A 118(31):5848–5856
Van Lehn RC, Alexander-Katz A (2014) Membrane-embedded nanoparticles induce lipid rearrangements similar to those exhibited by biological membrane proteins. J Phys Chem B 118(44):12586–12598
Van Lehn RC et al (2014) Lipid tail protrusions mediate the insertion of nanoparticles into model cell membranes. Nat Commun 5:Article No 4482
van Zon JS et al (2009) A mechanical bottleneck explains the variation in cup growth during fcγr phagocytosis. Mol Syst Biol 5(1):298
Vandoolaeghe P et al (2008) Adsorption of cubic liquid crystalline nanoparticles on model membranes. Soft Matter 4(11):2267–2277
Vasir JK, Labhasetwar V (2008) Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. Biomaterials 29(31):4244–4252
Verma A et al (2008) Surface-structure-regulated cell-membrane penetration by monolayer-protected nanoparticles. Nat Mater 7(7):588–595
Wang T et al (2012) Cellular uptake of nanoparticles by membrane penetration: a study combining confocal microscopy with FTIR spectroelectrochemistry. ACS Nano 6(2):1251–1259
Welsch S et al (2010) Electron tomography reveals the steps in filovirus budding. PLoS Pathog 6(4):e1000875
Werner M, Sommer J-U, Baulin VA (2012) Homo-polymers with balanced hydrophobicity translocate through lipid bilayers and enhance local solvent permeability. Soft Matter 8(46):11714–11722
Wu H-J et al (2012) Membrane-protein binding measured with solution-phase plasmonic nanocube sensors. Nat Methods 9:1189–1191
Yang K, Ma Y-Q (2010) Computer simulation of the translocation of nanoparticles with different shapes across a lipid bilayer. Nat Nanotechnol 5(8):579–583
Yi X, Gao H (2015) Cell membrane wrapping of a spherical thin elastic shell. Soft Matter 11(6):1107–1115
Yi X, Shi X, Gao H (2011) A universal law for cell uptake of one-dimensional nanomaterials. Nano Lett 107(9):098101
Yi X, Shi X, Gao H (2014) Cellular uptake of elastic nanoparticles. Phys Rev Lett 14(2):1049–1055
Yuan H et al (2010) Variable nanoparticle-cell adhesion strength regulates cellular uptake. Phys Rev Lett 105(13):138101
Yue T, Zhang X (2013) Molecular modeling of the pathways of vesicle–membrane interaction. Soft Matter 9(2):559–569
Zemel A, Ben-Shaul A, May S (2005) Perturbation of a lipid membrane by amphipathic peptides and its role in pore formation. Eur Biophys J 34(3):230–242
Zhang S et al (2009) Size-dependent endocytosis of nanoparticles. Adv Mater 21(4):419–424
Zhang Y et al (2012) Permission to enter cell by shape: nanodisk vs nanosphere. ACS Appl Mater Interfaces 4(8):4099–4105
Acknowledgements
Our research on the interaction of particles with biological membranes has been supported by the EU FP7 NMP collaborative project PreNanoTox (309666).
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Auth, T., Dasgupta, S., Gompper, G. (2018). Interaction of Particles and Pathogens with Biological Membranes. In: Bassereau, P., Sens, P. (eds) Physics of Biological Membranes. Springer, Cham. https://doi.org/10.1007/978-3-030-00630-3_17
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