Effects of Sugars on Lipid Bilayers during Dehydration − SAXS/WAXS Measurements and Quantitative Model

Lenné, Thomas; Garvey, Christopher J.; Koster, Karen L.; Bryant, Gary

doi:10.1021/jp808670t

Cited by 40 publications

(66 citation statements)

References 39 publications

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“…These rings are radially averaged to produce intensity versus scattering vector data, as shown in Figure 9. The analysis is similar to that reported previously for interactions between membranes and sugars (Lenné et al, 2009Kent et al, 2010;Garvey et al, 2013). The peaks are fit with a Gaussian function to determine the repeat spacings that are further illustrated in Supplemental Figure S2.…”

Section: Saxs and Waxs Experimentsmentioning

confidence: 73%

Disordered Cold Regulated15 Proteins Protect Chloroplast Membranes during Freezing through Binding and Folding, But Do Not Stabilize Chloroplast Enzymes in Vivo

et al. 2014

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Freezing can severely damage plants, limiting geographical distribution of natural populations and leading to major agronomical losses. Plants native to cold climates acquire increased freezing tolerance during exposure to low nonfreezing temperatures in a process termed cold acclimation. This involves many adaptative responses, including global changes in metabolite content and gene expression, and the accumulation of cold-regulated (COR) proteins, whose functions are largely unknown. Here we report that the chloroplast proteins COR15A and COR15B are necessary for full cold acclimation in Arabidopsis (Arabidopsis thaliana). They protect cell membranes, as indicated by electrolyte leakage and chlorophyll fluorescence measurements. Recombinant COR15 proteins stabilize lactate dehydrogenase during freezing in vitro. However, a transgenic approach shows that they have no influence on the stability of selected plastidic enzymes in vivo, although cold acclimation results in increased enzyme stability. This indicates that enzymes are stabilized by other mechanisms. Recombinant COR15 proteins are disordered in water, but fold into amphipathic a-helices at high osmolyte concentrations in the presence of membranes, a condition mimicking molecular crowding induced by dehydration during freezing. X-ray scattering experiments indicate protein-membrane interactions specifically under such crowding conditions. The COR15-membrane interactions lead to liposome stabilization during freezing. Collectively, our data demonstrate the requirement for COR15 accumulation for full cold acclimation of Arabidopsis. The function of these intrinsically disordered proteins is the stabilization of chloroplast membranes during freezing through a folding and binding mechanism, but not the stabilization of chloroplastic enzymes. This indicates a high functional specificity of these disordered plant proteins.

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Section: Saxs and Waxs Experimentsmentioning

confidence: 73%

Disordered Cold Regulated15 Proteins Protect Chloroplast Membranes during Freezing through Binding and Folding, But Do Not Stabilize Chloroplast Enzymes in Vivo

et al. 2014

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“…An alternative mechanism for the effect has been suggested, ascribing a key role to non-specific volumetric and osmotic effects of the sugars which mediate the compressive stresses induced in membranes brought into close contact by dehydration 3,[20][21] . This explanation is supported by a model which quantitatively predicts the hydration dependence of the fluid-gel transition temperature 22 , as well as (indirect) experimental evidence that sugars tend to be excluded from the regions close to the membranes [23][24][25][26] . Andersen et.…”

Section: Introductionmentioning

confidence: 70%

Direct Comparison of Disaccharide Interaction with Lipid Membranes at Reduced Hydrations

et al. 2015

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Abstract:Understanding sugar-lipid interactions during desiccation and freezing is an important step in the elucidation of cryo-and anhydro-protection mechanisms. We determine sucrose, trehalose and water concentration distributions in intra-bilayer volumes between opposing dioleoylphosphatidylcholine bilayers over a range of reduced hydrations and sugar concentrations. Stacked lipid bilayers at reduced hydration provide a suitable system to mimic environmental dehydration effects, as well as a suitable system for direct probing of sugar locations by neutron membrane diffraction. Sugar distributions show that sucrose and trehalose both behave as typical uncharged solutes, largely excluded from the lipid bilayers regardless of sugar identity, and with no correlation between sugar distribution and the lipid headgroup position as the hydration is changed. These results are discussed in terms of current opinions about cryo-and anhydro-protection mechanisms.2

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“…This theory is supported by direct measurement of the forces between bilayers [21], solid-state nuclear magnetic resonance (NMR) [22], and more recently a range of X-ray and neutron scattering studies [17 -20,23,24]. Moreover, this explanation provides a quantitative prediction of the effects of sugars on the fluid-gel transition temperature as a function of hydration [19].…”

Section: Introductionmentioning

confidence: 84%

Localization of trehalose in partially hydrated DOPC bilayers: insights into cryoprotective mechanisms

Kent

Hunt

Darwish

et al. 2014

J. R. Soc. Interface.

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Trehalose, a natural disaccharide with bioprotective properties, is widely recognized for its ability to preserve biological membranes during freezing and dehydration events. Despite debate over the molecular mechanisms by which this is achieved, and that different mechanisms imply quite different distributions of trehalose molecules with respect to the bilayer, there are no direct experimental data describing the location of trehalose within lipid bilayer membrane systems during dehydration. Here, we use neutron membrane diffraction to conclusively show that the trehalose distribution in a dioleoylphosphatidylcholine (DOPC) system follows a Gaussian profile centred in the water layer between bilayers. The absence of any preference for localizing near the lipid headgroups of the bilayers indicates that the bioprotective effects of trehalose at physiologically relevant concentrations are the result of non-specific mechanisms that do not rely on direct interactions with the lipid headgroups.

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Effects of Sugars on Lipid Bilayers during Dehydration − SAXS/WAXS Measurements and Quantitative Model

Cited by 40 publications

References 39 publications

Disordered Cold Regulated15 Proteins Protect Chloroplast Membranes during Freezing through Binding and Folding, But Do Not Stabilize Chloroplast Enzymes in Vivo

Disordered Cold Regulated15 Proteins Protect Chloroplast Membranes during Freezing through Binding and Folding, But Do Not Stabilize Chloroplast Enzymes in Vivo

Direct Comparison of Disaccharide Interaction with Lipid Membranes at Reduced Hydrations

Localization of trehalose in partially hydrated DOPC bilayers: insights into cryoprotective mechanisms

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