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1 High-speed atomic force microscopy shows that annexin V stabilizes membranes on the second timescale Atsushi Miyagi, Chris Chipot, Martina Rangl & Simon Scheuring Supplementary Movies: Supplementary Movie 1 File: Supplementary_Movie_1_(A5_trimer_rotation_650ms).gif Movie parameters: Image size: 40nm. Full color scale: 4nm. Image acquisition speed: 650ms Supplementary Movie 2 File: Supplementary_Movie_2_(A5_trimer_rotation_100ms).gif Movie parameters: Image size: 66nm. Full color scale: 4nm. Image acquisition speed: 100ms Supplementary Movie 3 File: Supplementary_Movie_3_(A5_trimer_rotation_20ms).gif Movie parameters: Image size: 30nm. Full color scale: 4nm. Image acquisition speed: 20ms Supplementary Movie 4 File: Supplementary_Movie_4_(A5_+UVlaser_750ms).gif Title: Reversible A5-assembly formation and dissociation by UV-laser uncaging of caged-ca 2+ Description: An A5-2D-crystal is dissociated through inflow of EDTA, and subsequently reassembled through pulsed UV-laser uncaging of caged-ca 2+. Since the focal volume of the UVlaser is only about 1pL and the volume of the fluid cell 120mL, uncaged Ca 2+ dilute in the much NATURE NANOTECHNOLOGY 1
2 larger volume and hence the process can be repeated several times. The A5-assembly kinetics upon Ca 2+ release are about 5s. Movie parameters: Image size: 200nm. Full color scale: 4nm. Image acquisition speed: 750ms Supplementary Movie 5 File: Supplementary_Movie_5_(A5_+EDTA_580ms).gif Title: EDTA-induced dissociation of A5-assemblies Description: High-resolution high-speed AFM image sequence the dissociation of A5-assemblies upon EDTA addition (Ca 2+ removal). Movie parameters: Image size: 150nm. Full color scale: 4nm. Image acquisition speed: 580ms Supplementary Movie 6 File: Supplementary_Movie_6_(A5_0mM-2mM_Ca_1000ms).gif Title: A5-assembly formation upon controlled Ca 2+ addition Description: Formation of A5-assembly followed controlled addition of Ca 2+ by means of the constant pressure and constant flow pump system connected to the HS-AFM fluid cell: Initial buffer contained 0mM Ca 2+ and injected buffer contained 2mM Ca 2+. Movie parameters: Image size: 175nm. Full color scale: 4nm. Image acquisition speed: 1000ms Supplementary Movie 7 File: Supplementary_Movie_7_(A5_2mM-0mM_Ca_1000ms).gif Title: A5-assembly dissociation upon controlled Ca 2+ removal Description: Dissociation of A5-assembly followed controlled removal of Ca 2+ by means of the constant pressure and constant flow pump system connected to the HS-AFM fluid cell: Initial buffer contained 2mM Ca 2+ and injected buffer contained 0mM Ca 2+. Movie parameters: Image size: 300nm. Full color scale: 4nm. Image acquisition speed: 1000ms 2 NATURE NANOTECHNOLOGY
3 Supplementary Information On Molecular Dynamics Simulations Table 1. Summary of the molecular-dynamics simulations performed in this work Simulation Number of atoms Simulation time (ns) Equilibrium simulation, calcium environment 162, Equilibrium simulation, sodium environment 162, Unbinding of annexin from bilayer surface 209, Potential of mean force calculation, toy models 11, Equilibrium simulations of the annexin trimer The strong adherence of the protein to the membrane cannot be solely rationalized by the three calcium binding sites. Whereas the concave side of the annexin trimer (A5) features large patches of positively a b b charged amino acids, the convex side, in immediate contact with the surface of the bilayer appears, in stark Supplementary Figure S1. Projection onto the solvent-accessible surface area of the three-dimensional electrostatic potential of the annexin trimer averaged over the entire simulation: (a) Concave and (b) convex side of the trimer. (c) Secondary structure and calcium binding sites seen from the convex side. contrast, negatively charged (figure S1). In the course of the simulation, calcium ions of the buffered aqueous solution rapidly saturate both the convex side of the trimer and the head-group region of the membrane, which is conducive to the formation additional calcium-mediated protein-lipid interactions (figure S2). The idea of strong cohesive forces can be better understood by considering a toy model that consists of two acetate ions chelating concomitantly one Ca 2+ ion, and estimating the free energy required to disrupt the so-called egg-box motif in an aqueous environment. The potential of mean force (PMF) was determined using the adaptive biasing force algorithm 1 and as a transition coordinate the Euclidian distance separating the divalent cation from one of the two acetate ions (figure S3). The standard Supplementary Figure S2. Calcium-mediated proteinlipid inter-actions contributing to the binding of the annexin trimer to the membrane surface. DOPC and DOPS lipid units are shown in green and red, respectively. Residues Glu72, Glu144 and Asp303 are depicted in an all-atom representation, whilst residues involved in calcium-mediated protein-lipid interactions are highlighted in orange. binding free energy, inferred through the integration of the PMF with the relevant symmetry 2, amounts to about 9.2 kcal/mol for the coplanar association. Assuming additivity and given the nine calcium binding sites in the protein trimer, one anticipates an appreciable free-energy cost for unbinding A5 from the membrane surface about 82.8 kcal/mol. NATURE NANOTECHNOLOGY 3
4 G (kcal/mol) r (Å) Supplementary Figure S3. Potential of mean force characterizing the chelation of two acetate ions with a calcium (black line) and a sodium (light line) ion in a coplanar association obeying C 2 v symmetry, consistent with the entropically restrained approach of A5 from the membrane surface. The transition coordinate is the Euclidian distance separating the cation from one of the two acetate ions. This estimate from the toy model overshoots the experiment-based standard binding free energy 3 of 53 kcal/mol of A5 to a lipid bilayer akin to that used here. The rudimentary toy model, however, does not account for the fact that Ca 2+ can be engaged concomitantly in more than one salt bridge with the protein and the surrounding lipids, nor that the negatively charged protein and membrane surfaces undergo strong repulsive forces. As a basis of comparison, a similar PMF was evaluated, replacing the central Ca 2+ ion by a monovalent sodium ion. Not too surprisingly, the standard binding free energy is notably smaller, i.e., about 3.9 kcal/mol for the coplanar association, respectively. Transposed to A5, this ion substitution would result in a decrease of the binding affinity of about 47.7 kcal/mol, thus, rationalizing the experimental observation of A5 escaping from the surface of the lipid bilayer in the presence of sequestrants and detaching spontaneously in equilibrium simulations at low sodium concentration (figure 6 of the main text). To examine whether the absence of Ca 2+ ions in the buffered aqueous solution would lead to the spontaneous unbinding of the annexin trimer from the membrane surface on a timescale commonly amenable to molecular dynamics, all Ca 2+ ions in the original assay were replaced by z (Å) N protein-lipid t (ns) t (ns) Supplementary Figure S4. Time-evolution of the distance separating the center of mass of the annexin trimer from that of the DOPC:DOPS lipid bilayer, in a 125-mM sodium-chloride aqueous solution. The dashed line represents the average over the simulation. Inset: Number of sodium-mediated protein-dopc (dark line) and protein-dops (light line) interactions, and the sum thereof (black line). Na + ions. Over a trajectory exceeding 200 ns, notwithstanding the weaker binding of the protein to the lipid bilayer, A5 remains steadily bound to the surface formed by the head-group region. Compared to the calcium-rich assay, fluctuations in the relative position of the protein with respect to the membrane in the presence of sodium are somewhat more pronounced. The most striking difference between the two simulations is the tendency of the protein to move deeper in the lipid bilayer, which, in reality, reflects the spontaneous modification of the membrane curvature to adapt to the convex side of the annexin trimer (figure S5) a phenomenon witnessed to a lesser extent in the calcium-rich assay. It is noteworthy that in the sodium-rich assay, the proximity of the protein to the surface of the membrane is conducive to the formation of an appreciably large number of sodium-mediated protein-lipid interactions, all three crystallographic 4 NATURE NANOTECHNOLOGY
5 calcium-binding sites being involved in such interactions. In an assay bereft of calcium ions and with a 125-mM sodium-chloride concentration, no spontaneous unbinding of A5 was observed over the timescale of the simulation, even though the protein appeared to have more freedom to move away and to the membrane surface. This result can be understood in terms of saturation of all negatively charged moieties either the DOPS head groups, or the titratable residues of the protein, and the formation of long-lived sodium-mediated protein-lipid interactions. To promote unbinding, the ionic strength of the aqueous solution was reduced perceptibly by limiting the number of Na + ions to that required for ensuring electric neutrality, which roughly Supplementary Figure S5. Spontaneous modification of the curvature of the DOPC:DOPS lipid bilayer, in the sodium-rich assay. DOPC and DOPS lipid units are shown in green and red, respectively. corresponds to a concentration of 65 mm. In the course of the unbiased molecular-dynamics simulation, the distance separating the protein from the surface of the DOPC:DOPS lipid bilayer fluctuates rapidly over a range of about 9 Å. During that period of time, the number of sodium-mediated protein-lipid interactions decreases steadily to the extent that after nearly 300 ns, A5 has essentially escaped from the head-group region (figure 6 of the main text). One might speculate that over a longer timescale, the annexin trimer will eventually peel off from the membrane surface. Faster, complete unbinding can be observed after removal of all counter-ions, electric neutrality being handled by means of a background charge in the implementation of the particle-mesh Ewald algorithm. Within about 20 ns, the annexin trimer has essentially peeled off from the surface of the lipid bilayer, which is not completely surprising, since in the absence of small electrolytes, the convex side of the protein and the head-group region can be viewed as two negatively charged surfaces undergoing strong repulsive forces (figure 6 of the main text). References 1. Comer J, Gumbart JC, Hénin J, Lelièvre T, Pohorille A, Chipot C. The adaptive biasing force method: Everything you always wanted to know but were afraid to ask. J. Phys. Chem. B 2015, 119: Shoup D, Szabo A. Role of diffusion in ligand binding to macromolecules and cell-bound receptors. Biophys. J. 1982, 40: Jeppesen B, Smith C, Gibson D F, Tait J F Entropic and enthalpic contributions to annexin V-membrane binding: a comprehensive quantitative model. J. Biol. Chem. 2008, 283: NATURE NANOTECHNOLOGY 5
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