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Effects of Mechanical Properties of Lipid Bilayers on the Entry of Cell-Penetrating Peptides into Single Vesicles

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† § ∥ Integrated Bioscience Section, Graduate School of Science and Technology, §Nanomaterials Research Division, Research Institute of Electronics, and Department of Physics, Graduate School of Science, Shizuoka University, Shizuoka 422-8529, Japan
Theoretical Problem Center of Physico-Chemical Pharmacology, Russian Academy of Sciences, Kosugina, 4, 117977, Moscow, Russia
*Tel/Fax: 81-54-238-4741. E-mail: [email protected]
Cite this: Langmuir 2017, 33, 9, 2433–2443
Publication Date (Web):February 6, 2017
https://doi.org/10.1021/acs.langmuir.6b03111
Copyright © 2017 American Chemical Society

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    Abstract

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    The translocation of cell-penetrating peptides (CPPs) through plasma membranes of living cells is an important physiological phenomenon in biomembranes. To reveal the mechanism underlying the translocation of a CPP, transportan 10 (TP10), through lipid bilayers, we examined the effects of the mechanical properties of lipid bilayers on the entry of carboxyfluorescein (CF)-labeled TP10 (CF-TP10) into a giant unilamellar vesicle (GUV) using the single GUV method. First, we examined the effect of lateral tension in membranes on the entry of CF-TP10 into single GUVs comprising a mixture of dioleoylphosphatidylglycerol (DOPG) and dioleoylphosphatidylcholine (DOPC) (2/8). CF-TP10 entered the GUV lumen before the membrane permeation of Alexa Fluor 647 hydrazide (AF647) from the GUV and thus before pore formation in the membrane. The fraction of entry of CF-TP10 before pore formation and the rate of membrane rupture increased with tension. The CF-TP10-induced fractional change in the membrane area increased continuously with time until membrane rupture, but it increased more slowly than did the CF-TP10 concentration in the GUV membrane. A high mole fraction of cholesterol inhibited the entry of CF-TP10 into single GUVs by suppressing the translocation of CF-TP10 from the external to the internal monolayer, although higher concentrations of CF-TP10 induced the formation of pores through which CF-TP10 rapidly translocated. Suppression of the translocation of CF-TP10 by cholesterol can be reasonably explained by the large line tension of a prepore. We discussed the role of mechanical properties in membranes on the entry of CF-TP10 into single GUVs and proposed a hypothesis of the mechanism that CF-TP10 translocates across a bilayer through transient hydrophilic prepores in the membrane.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.6b03111.

    • Relationship between the rim intensity and the CF-TP10 concentration in a GUV membrane, a schematic diagram for the elementary processes for the entry of CF-TP10, time course of the CF-TP10 concentration in DOPG/DOPC/chol-GUV, and a scheme of a prepore in a lipid bilayer (PDF)

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