Journal
BIOPHYSICAL JOURNAL
Volume 109, Issue 2, Pages 330-339Publisher
CELL PRESS
DOI: 10.1016/j.bpj.2015.06.011
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Funding
- National Institutes of Health (NIH)
- Cluster of Excellence RESOLV - Deutsche Forschungsgemeinschaft [EXC 1069]
- National Science Foundation (NSF) through the Materials Research Science and Engineering Centers [DMR 1121053]
- UCSB-Cooperative International Science and Engineering Internship (CISEI) through the NSF Research Experiences for Undergraduates [NSF DMR 0843934]
- Eindhoven University of Technology
- NSF
- Division Of Materials Research
- Direct For Mathematical & Physical Scien [0843934] Funding Source: National Science Foundation
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Dimethyl sulfoxide (DMSO) has been broadly used in biology as a cosolvent, a cryoprotectant, and an enhancer of membrane permeability, leading to the general assumption that DMSO-induced structural changes in cell membranes and their hydration water play important functional roles. Although the effects of DMSO on the membrane structure and the headgroup dehydration have been extensively studied, the mechanism by which DMSO invokes its effect on lipid membranes and the direct role of water in this process are unresolved. By directly probing the translational water diffusivity near unconfined lipid vesicle surfaces, the lipid headgroup mobility, and the repeat distances in multilamellar vesicles, we found that DMSO exclusively weakens the surface water network near the lipid membrane at a bulk DMSO mole fraction (X-DMSO) of <0.1, regardless of the lipid composition and the lipid phase. Specifically, DMSO was found to effectively destabilize the hydration water structure at the lipid membrane surface at X-DMSO <0.1, lower the energetic barrier to dehydrate this surface water, whose displacement otherwise requires a higher activation energy, consequently yielding compressed interbilayer distances in multilamellar vesicles at equilibrium with unaltered bilayer thicknesses. At X-DMSO >0.1, DMSO enters the lipid interface and restricts the lipid headgroup motion. We postulate that DMSO acts as an efficient cryoprotectant even at low concentrations by exclusively disrupting the water network near the lipid membrane surface, weakening the cohesion between water and adhesion of water to the lipid headgroups, and so mitigating the stress induced by the volume change of water during freeze-thaw.
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