Curvature-Driven Migration of Colloids on Tense Lipid Bilayers

Nov 29, 2016 - Inspired by proteins that generate membrane curvature, sense the underlying membrane geometry, and migrate driven by curvature gradient...
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Curvature-driven migration of colloids on tense lipid bilayers Ningwei Li, Nima Sharifi-Mood, Fuquan Tu, Daeyeon Lee, Ravi Radhakrishnan, Tobias Baumgart, and Kate J. Stebe Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.6b03406 • Publication Date (Web): 29 Nov 2016 Downloaded from http://pubs.acs.org on December 1, 2016

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Langmuir

Curvature-driven migration of colloids on tense lipid bilayers

N. Li,1† N. Sharifi-Mood,1†, F. Tu,1 D. Lee,1 R. Radhakrishnan,1,2,T. Baumgart,3*‡ K. J. Stebe1*‡

1.Department of Chemical and Biomolecular Engineering, University of Pennsylvania, 220 South 33rd Street, 311A Towne Building, Philadelphia, PA 19104, USA. 2.Department of Bioengineering, University of Pennsylvania, 210 S. 33rd St., 240 Skirkanich Hall, Philadelphia, PA 19104, USA. 3. Department of Chemistry, University of Pennsylvania, 231 S. 34 Street, Philadelphia, PA 19104, USA. * [email protected], [email protected] † These authors contributed equally to this work. ‡ These authors are co-corresponding authors. They contributed equally to this work.

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Abstract Inspired by proteins that generate membrane curvature, sense the underlying membrane geometry, and migrate driven by curvature gradients, we explore the question: Can colloids, adhered to lipid bilayers, also sense and respond to membrane geometry? We report the migration of Janus microparticles adhered to giant unilamellar vesicles elongated to present spatially varying curvatures. In our experiments, colloids migrate only when the membranes are tense, suggesting that they migrate to minimize membrane area. By determining the energy dissipated along a trajectory, the energy field is inferred to depend on the local deviatoric curvature, like curvature driven capillary migration on interfaces between immiscible fluids. In this latter system, energy gradients are larger, so colloids move deterministically, whereas the paths traced by colloids on vesicles have significant fluctuations. By addressing the role of Brownian motion, we show that the observed migration is analogous to curvature driven capillary migration, with membrane tension playing the role of interfacial tension. Since this motion is mediated by membrane shape, it can be turned on and off by dynamically deforming the vesicle. While particle-particle interactions on lipid membranes have been considered in many contributions, we report here an exciting and previously unexplored modality to actively direct the migration of colloids to desired locations on lipid bilayers.

Keywords: Vesicles; membrane trafficking; Janus particle; micropipette aspiration; directed assembly; self assembly; inclusions; Helfrich energy; capillarity; adhesion

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1. Introduction Curvature generating and sensing proteins are exciting to biologists and materials scientists alike. When such proteins associate with a lipid bilayer membrane, they can be moved about simply by changing the membrane shape 1–3. For example, when a tether is pulled from a giant unilamellar vesicle (GUV) whose membrane initially contains sparse concentrations of such peripherally bound proteins, they may concentrate on the tether

4,5

. This remarkable coupling of chemical

potential to geometry is not only a key mechanism in membrane-mediated trafficking of proteins in cells, it is also an inspiring and powerful tool for directing assembly of synthetic particles. Could related interactions occur for materials at the microscale? This would imply that, by simply dictating the geometry of a vesicle, materials like microscale colloids associated with membranes could be spatially relocated.

This could enable material organization on lipid

bilayers, which is a system of broad significance in biology and biophysics

6,7

. However, the

motivating system of curvature generating proteins is in some ways quite specific; while there are several groups of proteins that have been identified to be curvature generators and sensors, most membrane-associated proteins do not respond in this way 1,2. When colloids adhere to membranes, the associated distortion field can, in principle, depend on the underlying membrane geometry. Isolated colloids adhered to vesicles have been reported to accumulate at curved sites; their preferred localization was attributed to minimization of bending energy Similarly, trajectories for interacting particle pairs were reported 8. What role could membrane tension play? We explore this question here. For bilayers with finite bending rigidity κ and membrane tension σ, the natural length scale λ = κ / σ

determines whether

minimization of bending energy or of excess area dictate system behavior 9. For colloids of

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radius a, tension and excess area minimization would determine system response only if λ