Liposomes have been a useful tool to analyze membrane behavior. Various studies have attempted to induce biological activities, for example, buddings, divisions, and endocytosis, on liposomes, focusing on lipid rafts that move along electric fields.
Materials and Methods:
Liposomes consisting of soybean lecithin, phosphatidylcholine, and cholesterol were prepared, with inner and outer liquid conductivities of 0.595 and 1.564 S/m, respectively.
Results:
We tried to induce buddings by pulsed electric fields (PEFs) on liposomes. Results demonstrated that 1.248 kV/cm, 400 μs PEF promoted postpulse liposome buddings, which were preceded by a membrane relaxation. Although a transient thick area (a lipid raft-like area) on the membrane just after PEF application preceded buddings, it was not the sufficient factor for buddings.
Conclusion:
We established a brief model as follows: 1.248 kV/cm, 400 μs PEF induced the lipid membrane relaxation without electroporation to trigger buddings. The current results could be a new frontier in bioelectrics.
Get full access to this article
View all access options for this article.
References
1.
PerrierDL, RemsL, BoukanyPE. Lipid vesicles in pulsed electric fields: Fundamental principles of the membrane response and its biomedical applications. Adv Colloid Interface Sci, 2017; 249:248–271.
2.
DimovaR, RiskeKA, ArandaS, et al.Giant vesicles in electric fields. Soft Matter, 2007; 3:817–827.
3.
KnorrRL, StaykovaM, GraciàRS, et al.Wrinkling and electroporation of giant vesicles in the gel phase. Soft Matter, 2010; 6:1990–1996.
4.
RiskeKA, KnorrRL, DimovaR. Bursting of charged multicomponent vesicles subjected to electric pulses. Soft Matter, 2009; 5:1983–1986.
5.
PortetT, DimovaR. A new method for measuring edge tensions and stability of lipid bilayers: Effect of membrane composition. Biophys J, 2010; 99:3264–3273.
6.
CaramazzaL, NardoniM, De AngelisA, et al.Proof-of-concept of electrical activation of liposome nanocarriers: From dry to wet experiments. Front Bioeng Biotechnol, 2020; 8:819.
7.
ReigadaR.Electroporation of heterogeneous lipid membranes. Biochim Biophys Acta, 2014; 1838:814–821.
HoekstraD, MaierO, Van der WoudenJM, et al.Membrane dynamics and cell polarity: The role of sphingolipids. J Lipid Res, 2003; 44:869–877.
10.
HamadaT, MiuraY, IshiiKI, et al.Dynamic processes in endocytic transformation of a raft-exhibiting giant liposome. J Phys Chem B, 2007; 111:10853–10857.
11.
HuttnerWB, ZimmerbergJ. Implications of lipid microdomains for membrane curvature, budding and fission: Commentary. Curr Opin Cell Biol, 2001; 13:478–484.
12.
LinBJ, TsaoSH, ChenA, et al.Lipid rafts sense and direct electric field-induced migration. Proc Natl Acad Sci U S A, 2017; 114:8568–8573.
13.
DanielS, DiazAJ, MartinezKM, et al.Separation of membrane-bound compounds by solid-supported bilayer electrophoresis. J Am Chem Soc, 2007; 129:8072–8073.
14.
LozanoMM, HovisJS, MossFR, et al.Dynamic reorganization and correlation among lipid raft components. J Am Chem Soc, 2016; 138:9996–10001.
15.
GrovesJT, BoxerSG, McConnellHM. Electric field-induced reorganization of two-component supported bilayer membranes. Proc Natl Acad Sci U S A, 1997; 94:13390–13395.
16.
PortetT, CampsI, FebrerF, et al.Visualization of membrane loss during the shrinkage of giant vesicles under electropulsation. Biophys J, 2009; 96:4109–4121.
17.
PortetT, FavardC, TeissiéJ, et al.Insights into the mechanisms of electromediated gene delivery and application to the loading of giant vesicles with negatively charged macromolecules. Soft Matter, 2011; 7:3872–3881.
18.
NishimuraK, HosoiT, SunamiT, et al.Population analysis of structural properties of giant liposomes by flow cytometry. Langmuir, 2009; 25:10439–10443.
19.
OhnishiN, FujiwaraY, KamezakiT, et al.Variations of intracellular Ca 2+ mobilization initiated by nanosecond and microsecond electrical pulses in HeLa cells. IEEE Trans Biomed Eng, 2019; 66:2259–2268.
20.
DimovaR.Giant vesicles and their use in assays for assessing membrane phase state, curvature, mechanics, and electrical properties. Annu Rev Biophys, 2019; 48:93–119.
21.
MarkvoortAJ, Van SantenRA, HilbersPAJ. Vesicle shapes from molecular dynamics simulations. J Phys Chem B, 2006; 110:22780–22785.
22.
DöbereinerHG, KäsJ, NopplD, et al.Budding and fission of vesicles. Biophys J, 1993; 65:1396–1403.
23.
AllainJM, Ben AmarM. Budding and fission of a multiphase vesicle. Eur Phys J E, 2006; 20:409–420.
24.
ZongW, LiQ, ZhangX, et al.Deformation of giant unilamellar vesicles under osmotic stress. Colloids Surfaces B Biointerfaces, 2018; 172:459–463.
25.
KarimiAH, MirdamadiHR, Ziaei-RadS. Mathematical modeling of dynamic behavior of fluid bilayer membranes under the effect of density asymmetry. J Theor Biol, 2018; 454:330–344.
26.
MarkvoortAJ, SmeijersAF, PieterseK, et al.Lipid-based mechanisms for vesicle fission. J Phys Chem B, 2007; 111:5719–5725.
27.
MarkvoortAJ, SpijkerP, SmeijersAF, et al.Vesicle deformation by draining: Geometrical and topological shape changes. J Phys Chem B, 2009; 113:8731–8737.
28.
KahyaN, BrownDA, SchwilleP. Raft partitioning and dynamic behavior of human placental alkaline phosphatase in giant unilamellar vesicles. Biochemistry, 2005; 44:7479–7489.
29.
RissanenS, GrzybekM, OrłowskiA, et al.Phase partitioning of GM1 and its bodipy-labeled analog determine their different binding to Cholera Toxin. Front Physiol, 2017; 8:1–7.
30.
KabbaniAM, KellyCV. Nanoscale membrane budding induced by CTxB and detected via polarized localization microscopy. Biophys J, 2017; 113:1795–1806.
31.
LipowskyR.Remodeling of membrane compartments: Some consequences of membrane fluidity. Biol Chem, 2014; 395:253–274.
32.
KotnikT, PuciharG. Induced transmembrane voltage—Theory, modeling, and experiments. In: Pakhomov AG, Miklavcic D, Markov MS, eds. Advanced Electroporation Techniques in Biology and Medicine. CRC Press: Boca Raton, 2010, pp. 51–70.
33.
SakumaY, ImaiM. Model system of self-reproducing vesicles. Phys Rev Lett, 2011; 107:1–5.
34.
MauroyC, Rico-LattesI, TeissiéJ, et al.Electric destabilization of supramolecular lipid vesicles subjected to fast electric pulses. Langmuir, 2015; 31:12215–12222.
35.
DenziA, Della ValleE, EspositoG, et al.Technological and theoretical aspects for testing electroporation on liposomes. Biomed Res Int, 2017; 2017. DOI: 10.1155/2017/5092704
36.
KaralMAS, AhamedMK, RahmanM, et al.Effects of electrically-induced constant tension on giant unilamellar vesicles using irreversible electroporation. Eur Biophys J, 2019; 48:731–741.
37.
KonyakhinaTM, WuJ, MastroianniJD, et al.Phase diagram of a 4-component lipid mixture: DSPC/DOPC/POPC/chol. Biochim Biophys Acta, 2013; 1828:2204–2214.
38.
PathakP, LondonE. The effect of membrane lipid composition on the formation of lipid ultrananodomains. Biophys J, 2015; 109:1630–1638.
39.
PerrierDL, RemsL, KreutzerMT, et al.The role of gel-phase domains in electroporation of vesicles. Sci Rep, 2018; 8:1–10.
40.
PerrierDL, VahidA, KathaviV, et al.Response of an actin network in vesicles under electric pulses. Sci Rep, 2019; 9:8151.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
