Modulation of lipid phase behavior by kosmotropic and chaotropic solutes

Koynova, Rumiana; Brankov, J.G.; Tenchov, Boris

doi:10.1007/s002490050038

Cited by 130 publications

(109 citation statements)

References 41 publications

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“…The important parameter for sugar effects on T m is the unfavorable interaction of fluid membranes and sucrose at moderate and high concentration. This interpretation is in line with the exclusion theory (34,54), and we conclude that although this approach neglects the binding mode, exclusion theories may provide reasonable results on phase behavior because the binding mode has little effect on ΔΓ 3 . This limited effect of the binding mode on phase behavior is in strong contrast to the structural changes that couple to the binding.…”

Section: Discussionsupporting

confidence: 87%

“…At higher sugar concentration, the binding mode appears to saturate and to be exceeded by the exclusion mode, which drives Γ 3 to negative values. This is in accord with the general kosmotropic nature of small sugars, which tend to exclude them from aqueous interfaces (49) and thereby affecting lipid phase behavior (25,27,29,34,37,50). It is important to note that the two suggested modes overlap and that the (thermodynamic) function Γ 3 will quantify the sum of these contributions (and possibly other, as of yet unidentified effects).…”

Section: Discussionsupporting

confidence: 60%

“…The former is likely to reflect hydrogen bonding and to saturate at intermediate sugar concentrations. The latter is driven by the kosmotropic or "water-structuremaking" effect (55), which causes a general depletion of sugars from aqueous interfaces (34,54). The kosmotropic contribution dominates except at low sugar concentrations, where the attractive contribution is stronger.…”

Section: Discussionmentioning

confidence: 99%

“…21-23 and references therein), which consistently reported membrane-sugar attraction and an associated buildup of sugar at the membrane interface. Conversely, the exclusion hypothesis is supported by a multitude of studies on the phase behavior of fully hydrated phospholipids showing that the addition of sugars and other kosmotropic solutes consistently stabilize the phase with the smallest surface area (34,35). For example, the gel phase is stabilized over the fluid phase (25, 27), hexagonal phases are favored over lamellar phases (34,36), and the lateral expansion associated with interdigitation is strongly disfavored (37).…”

mentioning

confidence: 99%

“…Conversely, the exclusion hypothesis is supported by a multitude of studies on the phase behavior of fully hydrated phospholipids showing that the addition of sugars and other kosmotropic solutes consistently stabilize the phase with the smallest surface area (34,35). For example, the gel phase is stabilized over the fluid phase (25,27), hexagonal phases are favored over lamellar phases (34,36), and the lateral expansion associated with interdigitation is strongly disfavored (37). This ubiquitous correlation is explained by a preferential expulsion or exclusion that increases the interfacial free energy and thus promotes the stability of lipid phases with low water accessible areas.…”

mentioning

confidence: 99%

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Reconciliation of opposing views on membrane–sugar interactions

Andersen

Wang

Arleth

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

140

177

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It is well established that small sugars exert different types of stabilization of biomembranes both in vivo and in vitro. However, the essential question of whether sugars are bound to or expelled from membrane surfaces, i.e., the sign and size of the free energy of the interaction, remains unresolved, and this prevents a molecular understanding of the stabilizing mechanism. We have used smallangle neutron scattering and thermodynamic measurements to show that sugars may be either bound or expelled depending on the concentration of sugar. At low concentration, small sugars bind quite strongly to a lipid bilayer, and the accumulation of sugar at the interface makes the membrane thinner and laterally expanded. Above ∼0.2 M the sugars gradually become expelled from the membrane surface, and this repulsive mode of interaction counteracts membrane thinning. The dual nature of sugar-membrane interactions offers a reconciliation of conflicting views in earlier reports on sugar-induced modulations of membrane properties.membrane interface | membrane structure | preferential binding | preferential exclusion | interaction free energy S mall sugars such as the disaccharides sucrose and trehalose are among the so-called osmolytes (1) or compensatory solutes (2), which are accumulated in response to environmental stress in virtually all taxa. Their function is to act as inert regulators of the osmotic pressure, but they also optimize the physical properties of the cytosol (3) and stabilize biomolecular conformations against cold, drought, and heat (4-7). The same small carbohydrates have also proven useful in vitro as protectants or excipients for biopreservation (8). Many reports have shown that membranous structures are particularly stabilized by small sugars (4, 6, 9), but the definition of stabilization covers a wide range of biological and physical parameters. Thus, studies on intact cells have documented improved survival following exposure to heat, cold, drought, or chemical stressors (6,10,11). Other works have analyzed stabilization on the basis of phenomenological properties of model membranes, for example, the leakage or intermixing of probes in liposomes (12, 13). Finally, stability has been discussed with respect to rigorous physical parameters such as the structure or mechanical properties of lipid bilayers (14, 15). The current work addresses membrane dimensions and the thermodynamics of interaction with the purpose of elucidating fundamental aspects of membrane-sugar interrelationships. The different observations of sugar stabilization have sparked a large number of studies on sugars and model membranes (usually phospholipid bilayers) over the past 30 y. Investigations of fully hydrated membranes show an interesting tendency to fall into two groups with mutually conflicting conclusions. Thus, many investigations have suggested direct (favorable) interaction of sugars and the phospholipid interface (16-23), and it is obvious that such interactions could be the origin of sugar effects, for example, through int...

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Section: Discussionsupporting

confidence: 87%

Section: Discussionsupporting

confidence: 60%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Reconciliation of opposing views on membrane–sugar interactions

Andersen

Wang

Arleth

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

140

177

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Lipids: Phase Transitions

Koynova

Tenchov

2008

Wiley Encyclopedia of Chemical Biology

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Lipids constitute a diverse group of biomolecules of varied biologic roles. Their major function is to serve as building blocks of the biologic membranes. According to the fluid‐mosaic model, the biomembranes are liquid‐crystalline lipid bilayers with embedded proteins. This model includes two references to the lipid phase state— liquid crystalline and bilayer —both of which are of critical importance for the proper membrane functioning. The majority of lipids are amphiphilic compounds, which, similarly to other surfactants, also can form a large variety of other, non‐liquid‐crystalline and nonbilayer phases by transforming into each other via different kinds of phase transitions. In particular, the impressive variety of lipids in the biomembranes includes a large fraction of species that in isolation prefer to adopt curved, hexagonal, or cubic phases rather than the lamellar phase. The physiologic importance of the lipid diversity and mesomorphic behavior stems from the possibility of finely tuning and optimizing the properties of the biomembranes by regulating their lipid composition.

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Organic and Inorganic Osmolytes at Lipid Membrane Interfaces

Westh

Peters

2008

Structure and Dynamics of Membranous Interfaces

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Modulation of lipid phase behavior by kosmotropic and chaotropic solutes

Cited by 130 publications

References 41 publications

Reconciliation of opposing views on membrane–sugar interactions

Reconciliation of opposing views on membrane–sugar interactions

Lipids: Phase Transitions

Organic and Inorganic Osmolytes at Lipid Membrane Interfaces

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