Chiral twist drives raft formation and organization in membranes composed of rod-like particles

Abstract

Lipid rafts are hypothesized to facilitate protein interaction, tension regulation, and trafficking in biological membranes, but the mechanisms responsible for their formation and maintenance are not clear. Insights into many other condensed matter phenomena have come from colloidal systems, whose micron-scale particles mimic basic properties of atoms and molecules but permit dynamic visualization with single-particle resolution. Recently, experiments showed that bidisperse mixtures of filamentous viruses can self-assemble into colloidal monolayers with thermodynamically stable rafts exhibiting chiral structure and repulsive interactions. We quantitatively explain these observations by modeling the membrane particles as chiral liquid crystals. Chiral twist promotes the formation of finite-sized rafts and mediates a repulsion that distributes them evenly throughout the membrane. Although this system is composed of filamentous viruses whose aggregation is entropically driven by dextran depletants instead of phospholipids and cholesterol with prominent electrostatic interactions, colloidal and biological membranes share many of the same physical symmetries. Chiral twist can contribute to the behavior of both systems and may account for certain stereospecific effects observed in molecular membranes. membrane rafts | liquid crystals | chirality | self-assembly | colloids F ilamentous viruses have proved to be a fruitful colloidal system (1-19). They serve as monodisperse, rigid, and chiral rods that are ∼1 µm in length and interact effectively through hard-core repulsion (2, 7). When suspended in an aqueous solution at increasing concentrations, they transition from a disordered isotropic phase to a cholesteric (chiral nematic) phase characterized by alignment along a director field that twists with a preferred handedness and wavelength (1, 6). The addition of a nonadsorbing polymer such as dextran induces lateral virusvirus attraction via the depletion interaction (10,12,20,21). The viruses self-assemble into monolayers that exhibit fluid-like dynamics internally (10) and sediment to the bottom of glass containers, which are coated with a polyacrylamide brush to suppress depletion-induced virus-wall attractions (22). The rich physics and phenomenology of membranes formed from singlevirus species have been thoroughly studied (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)19). However, two-species membranes demonstrate a novel set of behaviors that are not adequately understood (18). We review these behaviors now before describing a theory that can explain them.fd-Y21M and M13KO7, which we shorten to fd and M13 for convenience, are two species of filamentous virus that have slightly different lengths and form cholesteric phases of opposite handednesses (Table 1 and Fig. 1A). Membranes composed of both fd and M13 viruses are circular with interior particles aligned largely perpendicularly to the membrane plane and edge particles tilted azimuthally, as in single-species membranes (13). At low dextran concentrations, the two spec...

Conformational switching of chiral colloidal rafts regulates raft–raft attractions and repulsions

“…To gain insight into the structural origin of switchable raft interactions, we have employed theoretical modeling. Previously developed continuum models for binary membranes (28,29,37) explained the assembly and repulsive interactions of chiral rafts in a membrane of opposite chirality. However, since the stability and direction of twist of rafts in these models is assumed a priori to be driven by chirality, they cannot explain the metastability of counter-twisted rafts observed here.…”

Assessing anesthetic activity through modulation of the membrane dipole potential

“…For example, PC possesses a chiral center at the position of the C2 carbon of the glycerol backbone and the plasma membrane comprises L-optical isomers of PC ( 105 ). With the growing recognition that enantioselective interactions between membrane constituents can determine the physical properties of membranes ( 106 ), including the formation and organization of membrane rafts ( 107 ), it is an intriguing hypothesis that enantiomeric anesthetics, interacting at the membrane interface at the site of the membrane dipole potential, may elicit varying degrees of activity without requiring direct protein interactions. Support for this view can be found in recent work by Bandari et al ( 24 ), who present intriguing evidence to suggest that the membrane dipole potential is sensitive to the stereospecificity of cholesterol, which can significantly alter the dipolar field at the membrane interface that can, in turn, modulate membrane protein activity.…”

The Chain of Chirality Transfer as Determinant of Brain Functional Laterality. Breaking the Chirality Silence: Search for New Generation of Biomarkers; Relevance to Neurodegenerative Diseases, Cognitive Psychology, and Nutrition Science

“…The new finding reveals the fundamental significance of the symmetry transfer (1) and symmetry-associated phase transitions (2) in resolving the origin of biological homochirality [44,70,72]. Among them are the chiral recognition/selection during the self-assembly of proteinmimic macro-anions [73], chiral recognition in the transmitter-receptor interactions [74], the chirality-induced conformation of the cell membrane lipid rafts XIII [75,76], and the phase-transfer chiral catalysis XIV [77]. The chiral catalysis is productively utilized for symmetry-asymmetry III The enzymes determine the crystallization of chiral amino acids [25] and the "handedness" (chirality) of the proteins during catalytic synthesis.…”