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Electrostatic Control of Spontaneous Vesicle Aggregation 5076 Langmuir 1997, 13, 5076-5081 Electrostatic Control of Spontaneous Vesicle Aggregation Scott A. Walker† and Joseph A. Zasadzinski* Department of Chemical Engineering, University of California, Santa Barbara, Santa Barbara, California 93106-5080 Received January 29, 1997. In Final Form: July 11, 1997X Aqueous mixtures of cationic cetyltrimethylammonium p-toluenesulfonate (CTAT) and anionic sodium dodecylbenzenesulfonate (SDBS) spontaneously form equilibrium “catanionic” vesicles whose charge depends on the relative amounts of each surfactant. Aggregation of these vesicles was induced by incorporating a small concentration of biotin-lipid in the bilayer, followed by addition of streptavidin as a cross-linking receptor. Freeze-fracture transmission electron microscopy shows that almost no aggregation occurred in solutions with no added electrolyte, in which the Debye length was much larger than the dimensions of the streptavidin biotin linkage, about 2.5 nm. Much higher levels of aggregation (multivesicle aggregates) were observed for solutions with 0.1 M NaCl, in which the Debye length was smaller than the linkage dimensions. At an electrolyte concentration of 0.025 M, in which the Debye length is comparable to the linkage dimensions, significant aggregation, which depended on vesicle concentration, occurred. The short-range nature of the specific recognition interaction makes controlling aggregation via electrostatics possible. These results also suggest that electrostatic interactions are at least somewhat responsible for the stability of the spontaneous vesicles against aggregation. As these catanionic vesicles do not flatten upon aggregation, they can maintain an applied osmotic stress across their bilayer much like phospholipid vesicles. Introduction plications, it would be useful to be able to control the vesicle 1 aggregation to make clusters of a given size. One way to Biotin binds with a very high affinity ( 30 kBT/bond ) in an aqueous solution to one of four streptavidin∼ binding do this is to slow the aggregation kinetics; it might be sites; the pairs of binding sites lie on opposite faces of possible to grow aggregates irreversibly at a slower rate streptavidin, allowing for the cross-linking of biotin- but still get compact, highly stable aggregates. labeled surfaces.2,3 What renders this system so versatile One way to slow the aggregation rate is to use charged is that biotin can be conjugated to the headgroup of a vesicles. Charged bilayers provide an added barrier to phospholipid while (1) the biotin maintains its ability to vesicle “contact”. The specific recognition reaction is bind to streptavidin and (2) the phospholipid maintains retarded by electrostatic “double-layer” repulsions that its ability to be incorporated into bilayers.4,5 Hence, reduce the number of collisions between vesicles.8,9 The vesicles labeled with biotin lipids can be subsequently double-layer repulsion creates an energy barrier to aggregated by adding streptavidin.6 Uncharged, biotin aggregation, somewhat analogous to the existence of an labeled phosphatidylcholine vesicles aggregate quickly and activation energy barrier for chemical reactions. Classical at specific contact points upon addition of streptavidin to theory shows that the rate of colloidal aggregation is form multimicron, multivesicle clusters that sediment governed by the maximum of the total interaction energy under gravity. This aggregation is complete within between the aggregating colloids, that is, the height of minutes and irreversible due to the strong binding between the energy barrier along the line of approach.8 When biotin and streptavidin. The vesicles are undamaged by electrolyte is added to a system of charged catanionic this aggregation process and retain their contents.6 vesicles, the maximum of the interaction potential can be However, mainly due to steric effects, lipid-conjugated decreased10 and hence the rate of specific aggregation can biotin (15-16 kT/bond) has a lower binding energy with be increased; aggregation increases with decreasing streptavidin7 than does free biotin and vesicle aggregation electrostatic repulsion. The range of the electrostatic 6 can be reversed. Added soluble-free biotin competes for interaction is also decreased with increasing electrolyte the binding sites on the streptavidin and causes the concentration as given by the Debye length (see eqn 2).9,10 vesicles to redisperse. While rapid, complete aggregation, The short-range nature of the specific recognition interac- or total redispersion is easily achieved, for certain ap- tion11 means that biotin-streptavidin binding can only occur when the two come into close contact. * To whom correspondence should be sent. E-mail: gorilla@ engineering.ucsb.edu. Telephone: 805-893-4769. Fax: 805-893- In this study, we have used equilibrium, charged vesicles 47831. formed from mixtures of anionic and cationic single-tailed † Current address: Imation Corporation, Advanced Technology surfactants. Equilibrium unilamellar vesicles (ULVs) Center, 3M Center Building 201-3S-01, St. Paul, Minnesota 55144- form spontaneously in dilute aqueous mixtures of these 1000. mixed surfactants12-14 and other mixed surfactants in- X Abstract published in Advance ACS Abstracts, September 1, 1997. (1) Green, N. M. Meth. Enzymol. 1990, 184, 51. (8) Hunter, R. J. Foundations of Colloid Science; Cambridge Press: (2) Green, N. M. Adv. Protein Chem. 1975, 29, 85. Oxford, U.K., 1986; Vol. 1. (3) Blankenburg, R.; Meller, P.; Ringsdorf, H.; Salesse, C. Biochem- (9) Israelachvili, J. N. Intermolecular and Surface Forces; Academic istry 1989, 28, 8214. Press: London, 1992. (4) Bayer, E. A.; Rivnay, B.; Skutelsky, E. Biochim. Biophys. Acta (10) Chiruvolu, S.; Israelachvili, J. N.; Naranjo, E.; Xu, Z.; Zasadz- 1979, 550, 464. inski, J. A.; Kaler, E. W.; Herrington, K. L. Langmuir 1995, 11, 4256. (5) Plant, A. L.; Brizgys, M. V.; Locasio-Brown, L.; Durst, R. A. Anal. (11) Leckband, D. E.; Schmitt, F.-J.; Israelachvili, J. N.; Knoll, W. Biochem. 1989, 176, 420. Biochemistry 1994, 33, 4611. (6) Chiruvolu, S.; Walker, S.; Israelachvili, J. N.; Schmitt, F.-J.; (12) Kaler, E. W.; Herrington, K. L.; Zasadzinski, J. A. Structure and Leckband, D.; Zasadzinski, J. A. Science 1994, 264, 1753. Dynamics of Strongly Interacting Colloids and Supermolecular Ag- (7) Powers, D. D.; Willard, B. L.; Carbonell, R. G.; Kilpatrick, P. K. gregates in Solution; Chen, S. H., Huang, J. S., Tartaglia, P., Eds.; Biotechnol. Prog. 1992, 8, 436. Kluwer Academic Publishers: Dordrecht, The Netherlands, 1992. S0743-7463(97)00094-2 CCC: $14.00 © 1997 American Chemical Society Control of Spontaneous Vesicle Aggregation Langmuir, Vol. 13, No. 19, 1997 5077 cluding double-tailed gangliosides,15 single-chain amino energy, E, per unit area, A, for bilayers with monolayers acid surfactants,16 and surfactant-alcohol cosurfactant of differing spontaneous curvatures:20,24 mixtures.17,18 Equilibrium vesicles are formed from mixtures of cetyltrimethylammonium p-toluenesulfonate E 1 ) K[(c + c )2 + (c - c )2] (1) (CTAT), a single-tailed, cationic surfactant, and sodium A 2 o i dodecylbenzenesulfonate (SDBS), a single-tailed, anionic surfactant, hence, the shortened term “catanionic” vesicle. where K is the bilayer bending modulus, c the vesicle The vesicles form by adding dry surfactants to water or curvature (the reciprocal of the vesicle radius, c ) 1/R), mixing micellar solutions of the two surfactants.12-14 c the outer monolayer spontaneous curvature, and c the CTAT-rich vesicles (overall positive charge) have a o i inner monolayer spontaneous curvature. For single- diameter, D, ranging from 10 to 250 nm with a mean size component bilayers, c necessarily equals c and the of D 70 nm.14 SDBS-rich vesicles (overall negative i o minimum energy occurs when c ) 0; the spontaneous charge)≈ are somewhat smaller, with fewer larger (>200 curvatures of the opposing monolayers are in competition, nm) vesicles, and have a mean size of D 60 nm.14 and the net result is a “flat” or zero spontaneous curvature Single-equilibrium phases of spontaneous≈ vesicles have bilayer. Nonideal mixing of surfactants in two or more only been observed in mixtures of surfactants or surfac- component bilayers can lead to monolayers with equal tant-cosurfactant mixtures. Pure CTAT forms rod mi- and opposite spontaneous curvatures, i.e., c )-c)c,in celles, while pure SDBS forms spherical micelles in dilute i o which a vesicle of radius 1/c is the minimum-energy aqueous solution. On mixing, however, the critical structure.20,24 aggregation concentration (cac) of CTAT/SDBS (cac However, nonideal mixing cannot account for the 0.000 17 wt %) measured by changes in surface tension≈ observed stability against aggregation of CTAT/SDBS or with concentration12 is about 100 times lower than the other spontaneous vesicles, except in the limit of a very critical micelle concentration (cmc) of CTAT (cmc 0.01 large bending modulus, K. Interactions between the wt %) and 1000 times lower than that of SDBS (cmc≈ 0.1 bilayers must play an important role in the transition wt %). Because of the surprising drop in the cac in≈ the from unilamellar vesicles to multilamellar phases. Sur- mixed system, it is believed14,16 that the oppositely charged face force apparatus (SFA) measurements of adsorbed surfactants form a neutral dimer complex that resembles bilayers of CTAT and SDBS10 show that electrostatic a zwitterionic double-tailed surfactant that is able to form double-layer forces dominate all other interactions
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