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Adhesion, Intake, and Release of Nanoparticles by Lipid Bilayers ⇑ Sean Burgess A, Zhengjia Wang A,B, Aleksey Vishnyakov A,C, Alexander V

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Adhesion, Intake, and Release of Nanoparticles by Lipid Bilayers ⇑ Sean Burgess A, Zhengjia Wang A,B, Aleksey Vishnyakov A,C, Alexander V Journal of Colloid and Interface Science 561 (2020) 58–70 Contents lists available at ScienceDirect Journal of Colloid and Interface Science journal homepage: www.elsevier.com/locate/jcis Adhesion, intake, and release of nanoparticles by lipid bilayers ⇑ Sean Burgess a, Zhengjia Wang a,b, Aleksey Vishnyakov a,c, Alexander V. Neimark a, a Department of Chemical and Biochemical Engineering, Rutgers, The State University of New Jersey, 98 Brett Road, Piscataway, NJ 08854, USA b Harbin Institute of Technology, 92 Xidazhi St, Nangang Qu, Haerbin Shi, Heilongjiang Sheng 150001, China c Skolkovo Institute of Science and Technology, Nobel St. 1, 121205 Moscow, Russia graphical abstract article info abstract Article history: Understanding the interactions between nanoparticles (NP) and lipid bilayers (LB), which constitute the Received 17 October 2019 foundations of cell membranes, is important for emerging biomedical technologies, as well as for assess- Revised 17 November 2019 ing health threats related to nanoparticle commercialization. Applying dissipative particle dynamic sim- Accepted 27 November 2019 ulations, we explore adhesion, intake, and release of hydrophobic nanoparticles by DMPC bilayers. To Available online 28 November 2019 replicate experimental conditions, we develop a novel simulation setup for modeling membranes at isotension conditions. NP-LB interactions are quantified by the free energy landscape calculated by the Keywords: ghost tweezers method. NPs are studied z of diameter 2 nm (comparable with the LB hydrophobic core), Lipid membranes 4 nm (comparable with the LB thickness) and 8 nm (exceeding the LB thickness). NPs are pre-covered by Nanoparticles Nanoparticle translocation an adsorbed lipid monolayer. It is shown that NP translocation across LB includes (1) NP intake into the Adhesion hydrophobic core via merging of the monolayer adsorbed on NP with the outer leaflet of bilayer (2) NP release via formation and rupture of a lipid junction connecting NP and LB. Both stages are associated with free energy barriers. The barrier for the intake stage increases with the NP size and becomes pro- hibitively high for 8 nm NP. The barriers for the release stage are significantly higher which implies that the release stage controls the translocation rate and dynamics. The release energy barrier of 4 nm NP is found smaller than those for 2 and 8 nm NPs which implies the existence of the optimal NP size for unforced trans-membrane transport. Based on the calculated free energy landscape, the dynamics of unforced transport of NP across LB is evaluated using the Fokker-Planck equation, which mimics NP ⇑ Corresponding author. E-mail address: [email protected] (A.V. Neimark). https://doi.org/10.1016/j.jcis.2019.11.106 0021-9797/Ó 2019 Elsevier Inc. All rights reserved. S. Burgess et al. / Journal of Colloid and Interface Science 561 (2020) 58–70 59 diffusion along the free energy landscape with multiple attempts to reach the barrier. We found that the number of attempts required for successful translocation scales exponentially with the energy barrier. Ó 2019 Elsevier Inc. All rights reserved. 1. Introduction [30] employed thermodynamic integration to explore the free energy landscapes of NPs functionalized with hydrophilic/ Understanding of physico-chemical mechanisms of nanoparti- hydrophobic ligands upon penetration into LBs. The authors pulled cle (NP) adhesion to, encapsulation by, and translocation through the NP with a spring towards the membrane of fixed area and mea- lipid bilayers (LB) is of utmost importance for development of sured the applied force as a function of the NP distance to the cen- biomedical nanotechnologies for imaging and drug delivery [1], ter line of LB [21,30–32]. Van Lehn et al. [33] reported theoretical design of novel bio-inspired materials and devices [2,3], as well studies of embedding hydrophobic NPs functionalized with differ- as for assessing health threats related to the expansion of nanopar- ent sidechains into LBs. The free energies showed a strong depen- ticle commercialization. NP-LB interactions are affected by a vari- dence on NP size and ligand type and density. Remarkably, the free ety of physico-chemical factors such as particle size, shape, energy dependence on NP size exhibited minima at NP diameter hydrophobicity, charge density, and physisorption of lipids and between 2 and 4 nm. Free energy landscapes have also been calcu- proteins [4–6]. Silica NPs penetration into cells has been found to lated with the single-chain mean field theory [21,31,32]. be largely dependent upon particle size [7,8]. These and many It should be mentioned that in most of the simulation studies the other experimental observations related to interfacial interactions membrane sample had a constant surface area, (e.g. [15,30])whilein of NPs with lipid membranes are still poorly understood, and their practical situations (e.g. during NP transport across a cell mem- effects are hardly predictable by using classical approaches of brane), the membrane tension (and, correspondingly, the chemical interfacial and colloidal science. Consequently, a more robust sim- potential of the lipid molecules, which is directly related to the ulation technique must be applied to gain a greater understanding membrane tension) remains constant, because a cell or liposome is of these interactions. large compared to a NP. In order to maintain the membrane tension, In this work, we explore adhesion, intake, and release of the semi-isotropic pressure coupling for the simulation box resizing hydrophobic NPs by 1,2-dimyristoyl-sn-glycero-3-phosphocholine was employed in several studies, e.g. [19,29].Inourrecentwork[34] (DMPC) membranes using dissipative particle dynamics (DPD) on studies of the stability of NP loaded lipid membranes, the simulations [9,10]. DPD is a coarse-grained simulation technique required control of the membrane tension and membrane stabiliza- popularly employed for modeling soft matter, including lipid tion was achieved with a special simulation set-up that is employed membranes, due to its versatility and computational efficiency. and modified in this work for efficient modeling of NP adhesion and The feasibility of DPD modeling in simulating NP adhesion to and translocation. In this work, we study the equilibrium adhesion states engulfing by LBs has been demonstrated in many publications and the dynamics of intake and release of hydrophobic NPs by a [11–14]. In particular, DPD has been employed to mimic transloca- DMPC membrane using original simulation methods implemented tion of NPs of different shapes, sizes and ligand functionalization into the DPD computational framework. Calculations are performed [15–17]. While the aforementioned studies provided valuable for NPs of diameter 2 nm (comparable with the width of the LB qualitative insights into the process of NP translocation, to make hydrophobic core), 4 nm (comparable with the LB thickness), and NP-LB simulation results applicable to real experimental systems, 8 nm. To replicate the experimental conditions, we develop a novel the translocation dynamics must be analyzed by evaluating the simulation setup that maintains the LB at a constant tension and energy barriers of the interfacial transitions. For very small (up allows for the lipids to be freely exchanged between the membrane to 2 nm in diameter) hydrophobic NPs, the energy barriers for and solution; this is equivalent to the condition of the lipid chemical intake are small and their transport can be followed in a straight- potential constancy [34]. At this condition, a hydrophobic NP in solu- forward manner in coarse-grained simulations due to short obser- tion is coated by an equilibrium lipid monolayer (LM). We examine vation times required [18–20]. Such NPs tend to penetrate into the previously unexplored mechanisms of NP translocation relevant pro- hydrophobic core of the LB and accumulate there, as observed in cesses: merging of the lipid monolayer adhered to the hydrophobic simulations and experiments alike [21–25]. However, in most NP with the outer leaflet of LB during NP intake and formation and cases, unforced transport of NPs through LBs is too slow to be rupture of a lipid junction connecting the NP and LB during NP directly followed even in coarse-grained simulations. The mecha- release. Both these mechanisms are associated with the energy bar- nisms and dynamics of NP transport can be elucidated from the riers with depends on the NP size. To monitor, visualize and quantify free energy landscapes - the dependence of the free energy of these mechanisms, we employ the ghost tweezers (GT) method [35], NP-LB interactions on the particle position with respect to the which mimics the experiments with optical and magnetic tweezers. LB. The potential of mean force and different versions of umbrella The GT method allows us to calculate the free energy landscapes and sampling methods are commonly used to study the free energy of energy barriers associated with intake and release of NPs. Addition- NP-LB interactions [19,26–29]. In particular, Jusufi et al. [29] calcu- ally, the dynamics of unforced transport of NP across LB is evaluated lated the free energy of absorption of fullerenes by a lipid bilayer using the Fokker-Planck (FP) method [36], which mimics NP diffu- using umbrella sampling with weighted histogram analysis with sion along the calculated free energy landscapes. fullerene coordinate as the integration variable. The distance between NP and LB was controlled by an external field and the 2. Modeling methods interfacial tension of the bilayer was kept constant with anisotro- pic NPT conditions. The largest fullerene was 2.4 nm in size, twice Dissipative particle dynamics implementation, lipid and as small as the membrane thickness. All fullerenes entered the LB water models. Dissipative particle dynamics [9,10] is a coarse- without any noticeable potential barrier, and the free energy land- grained simulation method, which uses Newton’s equations of scape along the translocation trajectory was continuous. Li et al. motion governed by interparticle interaction forces, 60 S.
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