Beyond the standard model of solubilization: Non-ionic surfactants induce collapse of lipid vesicles into rippled bilamellar nanodiscs

Bjørnestad, Victoria Ariel; Soto-Bustamante, Fernando; Tria, Giancarlo; Laurati, Marco; Lund, Reidar

doi:10.1016/j.jcis.2023.03.037

Cited by 8 publications

(8 citation statements)

References 89 publications

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“…The formation of the ripples is also extremely slow, having time scales equivalent to that of the mixtures at 10 °C to reach the multilamellar end-state, suggesting that the formation follows a similar mechanism, although the end-structure of the bilayer itself is different. The findings in this other study support the theory that a collapse of the vesicles also occur at 10 °C, forming flat and multilamellar structures 48 but not ripples. Solubilization of DPPC vesicles at 20 °C requires very high amounts of TX-100, as will be shown later in the presentation of the kinetic data where the solubilization process can be observed at a mass ratio of 1:16.…”

Section: Resultssupporting

confidence: 85%

“…This pattern of peaks is very characteristic for TX-100 mixed at these temperatures, and the structures have proven to be much too complex to be described by any simple analytical SAXS model. We previously found 48 that the peak pattern overlaps well with what has been characterized for the metastable ripple phase of DPPC. 49 We have further investigated this structure using cryo-TEM in a separate study 48 where we found the structures to be collapsed and rippled bilayers, yielding nanostructures that resemble ridged potato chips.…”

Section: Resultssupporting

confidence: 76%

“…We previously found 48 that the peak pattern overlaps well with what has been characterized for the metastable ripple phase of DPPC. 49 We have further investigated this structure using cryo-TEM in a separate study 48 where we found the structures to be collapsed and rippled bilayers, yielding nanostructures that resemble ridged potato chips. The formation of the ripples is also extremely slow, having time scales equivalent to that of the mixtures at 10 °C to reach the multilamellar end-state, suggesting that the formation follows a similar mechanism, although the end-structure of the bilayer itself is different.…”

Section: Resultssupporting

confidence: 76%

“…The kinetics of the formation of the rippled nano-flakes seen at 20 °C with TX-100:DPPC mixtures is likely governed by a similar process as at 10 °C, and this has been discussed further in a separate paper. 48 There we concluded that the pathway was an implosion of the vesicle followed by ripples induced by the few inserted TX-100 molecules, which stabilizes the structure from solubilization. At high enough detergent concentration, however, solubilization will take place also at the low temperatures.…”

Section: Resultsmentioning

confidence: 89%

“…In a separate study on these unique structures, we found by cryo-TEM that the structures at 10 °C are in fact stacks of flat bilayers, potentially formed from collapsing vesicles. 48 Regardless, TX-100 must cause bilayers to adhere to one another in a stronger manner forming the multilamellar structures. A collapse of the vesicle structure could then be expected since TX-100 is expected to flip into the inner leaflet of the vesicle within milliseconds to seconds, 10 and so any attractive force caused by TX-100 would be present also on the inside of the vesicle.…”

Section: Resultsmentioning

confidence: 99%

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Pathways of Membrane Solubilization: A Structural Study of Model Lipid Vesicles Exposed to Classical Detergents

Bjørnestad

Lund

2023

Langmuir

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Understanding the pathways of solubilization of lipid membranes is of high importance for their use in biotechnology and industrial applications. Although lipid vesicle solubilization by classical detergents has been widely investigated, there are few systematic structural and kinetic studies where different detergents are compared under varying conditions. This study used small-angle X-ray scattering to determine the structures of lipid/detergent aggregates at different ratios and temperatures and studied the solubilization in time using the stopped-flow technique. Membranes composed of either of two zwitterionic lipids, DMPC or DPPC, and their interactions with three different detergents, sodium dodecyl sulfate (SDS), n-dodecyl-beta-maltoside (DDM), and Triton X-100 (TX-100), were tested. The detergent TX-100 can cause the formation of collapsed vesicles with a rippled bilayer structure that is highly resistant to TX-100 insertion at low temperatures, while at higher temperatures, it partitions and leads to the restructuring of vesicles. DDM also causes this restructuring into multilamellar structures at subsolubilizing concentrations. In contrast, partitioning of SDS does not alter the vesicle structure below the saturation limit. Solubilization is more efficient in the gel phase for TX-100 but only if the cohesive energy of the bilayer does not prevent sufficient partitioning of the detergent. DDM and SDS show less temperature dependence compared to TX-100. Kinetic measurements reveal that solubilization of DPPC largely occurs through a slow extraction of lipids, whereas DMPC solubilization is dominated by fast and burst-like solubilization of the vesicles. The final structures obtained seem to preferentially be discoidal micelles where the detergent can distribute in excess along the rim of the disc, although we do observe the formation of worm-and rodlike micelles in the case of solubilization of DDM. Our results are in line with the suggested theory that bilayer rigidity is the main factor influencing which aggregate is formed.

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Section: Resultssupporting

confidence: 85%