Increased adhesion between neutral lipid bilayers: interbilayer bridges formed by tannic acid

Abstract

Tannic acid (TA) is a naturally occurring polyphenolic compound that aggregates membranes and neutral phosolipid vesicles and precipitates many proteins. This study analyzes TA binding to lipid membranes and the ensuing aggregation. The optical density of dispersions of phosphatidylcholine (PC) vesicles increased upon the addition of TA and electron micrographs showed that TA caused the vesicles to aggregate and form stacks of tightly packed disks. Solution calorimetry showed that TA bound to PC bilayers with a molar binding enthalpy of -8.3 kcal/mol and zeta potential measurements revealed that TA imparted a small negative charge to PC vesicles. Monolayer studies showed that TA bound to PC with a dissociation constant of 1.5 microM and reduced the dipole potential by up to 250 mV. Both the increase in optical density and decrease in dipole potential produced by TA could be reversed by the addition of polyvinylpyrrolidone, a compound that chelates TA by providing H-bond acceptor groups. NMR, micropipette aspiration, and x-ray diffraction experiments showed that TA incorporated into liquid crystalline PC membranes, increasing the area per lipid molecule and decreasing the bilayer thickness by 2 to 4%. 2H-NMR quadrupole splitting measurements also showed that TA associated with a PC molecule for times much less than 10(-4) s. In gel phase bilayers, TA caused the hydrocarbon chains from apposing monolayers to fully interdigitate. X-ray diffraction measurements of both gel and liquid crystalline dispersions showed that TA, at a critical concentration of about 1 mM, reduced the fluid spacing between adjacent bilayers by 8-10 A. These data place severe constraints on how TA can pack between adjacent bilayers and cause vesicles to adhere. We conclude that TA promotes vesicle aggregation by reducing the fluid spacing between bilayers by the formation of transient interbilayer bridges by inserting its digallic acid residues into the interfacial regions of adjacent bilayers and spanning the interbilayer space.

Probing the Interaction of Polyphenols with Lipid Bilayers by Solid-State NMR Spectroscopy

“…PGG is a small, very hydrophobic molecule that is able to interact with both the membrane surface and the hydrophobic core. It has been suggested that at low concentrations TA increases outer membrane surface area and decreases membrane thickness but that at higher concentrations the inner membrane cannot expand or the lipid and TA cannot exchange fast enough, so the bilayer breaks into smaller vesicles (39). The isotropic component we noted in both 31 P and 2 H spectra of the PGG incorporated into the lipid bilayer suggests a similar mechanism for PGG.…”

Adsorption of tannic acid on polyelectrolyte monolayers determined in situ by streaming potential measurements

“…Indeed, in the literature the interaction of tannin molecules with biological macromolecules has been widely described. It was shown that tannin can promote aggregation or precipitation of various polymers and proteins [19][20][21][22] but it can also form a useful complex with multilamellar vesicles, phosphatidylcholines and sphingomyelins [23,24]. Tannin was also used as negatively charged structural blocks for the layer-by-layer (LbL) assembly in alternation with http cations in order to obtain pH-responsive capsules and micelles for drug delivery [25][26][27].…”

Plant polyphenols in cell-cell interaction and communication

“…13 Tannins are able to bind on the membrane surface, establish bridges between apposing bilayers and initiate their interaction and adhesion. 14 The process is accompanied by reduction of the membrane dipole potential, lipid interdigitation and the decrease of interbilayer spacing from 15 Å to 5 Å. According to authors 13 this happens because tannins (1) are amphipathic and partition into the bilayers interfacial region, (2) are long enough to span the interbilayer space, (3) contain several gallic acids distributed so that they can partition simultaneously into apposing bilayers, and (4) have sufficient gallic acid residues to interact with all lipid headgroups and cover the bilayer surface.…”