Nonadditivity in interactions between three membrane-wrapped colloidal spheres

Biophysical Journal, vol. 123, pp. 307–316

Abstract

Many cell functions require a concerted effort from multiple membrane proteins, for example, for signaling, cell division, and endocytosis. One contribution to their successful self-organization stems from the membrane deformations that these proteins induce. While the pairwise interaction potential of two membrane-deforming spheres has recently been measured, membrane-deformation-induced interactions have been predicted to be nonadditive, and hence their collective behavior cannot be deduced from this measurement. We here employ a colloidal model system consisting of adhesive spheres and giant unilamellar vesicles to test these predictions by measuring the interaction potential of the simplest case of three membrane-deforming, spherical particles. We quantify their interactions and arrangements and, for the first time, experimentally confirm and quantify the nonadditive nature of membrane-deformation-induced interactions. We furthermore conclude that there exist two favorable configurations on the membrane: (1) a linear and (2) a triangular arrangement of the three spheres. Using Monte Carlo simulations, we corroborate the experimentally observed energy minima and identify a lowering of the membrane deformation as the cause for the observed configurations. The high symmetry of the preferred arrangements for three particles suggests that arrangements of many membrane-deforming objects might follow simple rules.

Authors 5

1. Ali Azadbakht Aachen Soft Matter Physics Huygens-Kamerlingh Onnes Laboratory

   Leiden University

   Affiliation as printed

   Soft Matter Physics, Huygens-Kamerlingh Onnes Laboratory, Leiden University, Leiden, the Netherlands

2. Billie Meadowcroft

   Institute of Science and Technology Austria · University College London

   Affiliation as printed

   Institute of Science and Technology Austria, Klosterneuburg, Austria; Department of Physics and Astronomy, Institute for the Physics of Living Systems, University College London, London, United Kingdom

   Department of Physics and Astronomy, Institute for the Physics of Living Systems, University College London, London, United Kingdom

   Institute of Science and Technology Austria, Klosterneuburg, Austria

3. Juraj Májek

   Institute of Science and Technology Austria

   Affiliation as printed

   Institute of Science and Technology Austria, Klosterneuburg, Austria

4. Anđela Šarić

   Institute of Science and Technology Austria

   Affiliation as printed

   Institute of Science and Technology Austria, Klosterneuburg, Austria

5. Daniela J. Kraft corresponding Aachen Soft Matter Physics Huygens-Kamerlingh Onnes Laboratory

   Leiden University

   Affiliation as printed

   Soft Matter Physics, Huygens-Kamerlingh Onnes Laboratory, Leiden University, Leiden, the Netherlands. Electronic address: kraft@physics.leidenuniv.nl

   Soft Matter Physics, Huygens-Kamerlingh Onnes Laboratory, Leiden University, Leiden, the Netherlands