Shear stress induced lipid order and permeability changes of giant unilamellar vesicles
The permeability of a lipid bilayer is a function of its phase state and depends non-linearly on thermodynamic variables such as temperature, pressure or pH. We investigated how shear forces influence the phase state of giant unilamellar vesicles and their membrane permeability. We determined the pe...
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Published in | Biochimica et biophysica acta. General subjects Vol. 1866; no. 10; p. 130199 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
Published |
Elsevier B.V
01.10.2022
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Subjects | |
Online Access | Get full text |
ISSN | 0304-4165 1872-8006 1872-8006 |
DOI | 10.1016/j.bbagen.2022.130199 |
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Abstract | The permeability of a lipid bilayer is a function of its phase state and depends non-linearly on thermodynamic variables such as temperature, pressure or pH. We investigated how shear forces influence the phase state of giant unilamellar vesicles and their membrane permeability.
We determined the permeability of giant unilamellar vesicles composed of different phospholipid species under shear flow in a tube at various temperatures around and far off the melting point by analyzing the release of fluorescently labelled dextran. Furthermore, we quantified phase state changes of these vesicles under shear forces using spectral decomposition of the membrane embedded fluorescent dye Laurdan.
We observed that the membrane permeability follows a step function with increasing permeability at the transition from the gel to the fluid phase and vice versa. Second, there was an all-or-nothing permeabilization near the main phase transition temperature and a gradual dye release far off the melting transition. Third, the Laurdan phase state analysis suggests that shear forces induce a reversible melting temperature shift in giant unilamellar vesicle membranes.
The observed effects can be explained best in a scenario in which shear forces directly induce membrane pores that possess relatively long pore lifetimes in proximity to the phase transition.
Our study elucidates the release mechanism of thermo-responsive drug carriers as we found that liposome permeabilization is not continuous but quantized. Furthermore, the shear force induced melting temperature shift must be taken into consideration when thermo-responsive liposomes are designed.
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•Membrane permeability increase by transition from gel to fluid phase and vice versa.•All-or-nothing GUV permeabilization under shear flow near the phase transition.•Gradual GUV permeabilization under shear flow far off the phase transition.•Phase state dependent membrane permeability increase induced by shear forces.•Lipid membrane melting temperature shift induced by shear forces. |
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AbstractList | The permeability of a lipid bilayer is a function of its phase state and depends non-linearly on thermodynamic variables such as temperature, pressure or pH. We investigated how shear forces influence the phase state of giant unilamellar vesicles and their membrane permeability. We determined the permeability of giant unilamellar vesicles composed of different phospholipid species under shear flow in a tube at various temperatures around and far off the melting point by analyzing the release of fluorescently labelled dextran. Furthermore, we quantified phase state changes of these vesicles under shear forces using spectral decomposition of the membrane embedded fluorescent dye Laurdan. We observed that the membrane permeability follows a step function with increasing permeability at the transition from the gel to the fluid phase and vice versa. Second, there was an all-or-nothing permeabilization near the main phase transition temperature and a gradual dye release far off the melting transition. Third, the Laurdan phase state analysis suggests that shear forces induce a reversible melting temperature shift in giant unilamellar vesicle membranes. The observed effects can be explained best in a scenario in which shear forces directly induce membrane pores that possess relatively long pore lifetimes in proximity to the phase transition. Our study elucidates the release mechanism of thermo-responsive drug carriers as we found that liposome permeabilization is not continuous but quantized. Furthermore, the shear force induced melting temperature shift must be taken into consideration when thermo-responsive liposomes are designed. The permeability of a lipid bilayer is a function of its phase state and depends non-linearly on thermodynamic variables such as temperature, pressure or pH. We investigated how shear forces influence the phase state of giant unilamellar vesicles and their membrane permeability.BACKGROUNDThe permeability of a lipid bilayer is a function of its phase state and depends non-linearly on thermodynamic variables such as temperature, pressure or pH. We investigated how shear forces influence the phase state of giant unilamellar vesicles and their membrane permeability.We determined the permeability of giant unilamellar vesicles composed of different phospholipid species under shear flow in a tube at various temperatures around and far off the melting point by analyzing the release of fluorescently labelled dextran. Furthermore, we quantified phase state changes of these vesicles under shear forces using spectral decomposition of the membrane embedded fluorescent dye Laurdan.METHODSWe determined the permeability of giant unilamellar vesicles composed of different phospholipid species under shear flow in a tube at various temperatures around and far off the melting point by analyzing the release of fluorescently labelled dextran. Furthermore, we quantified phase state changes of these vesicles under shear forces using spectral decomposition of the membrane embedded fluorescent dye Laurdan.We observed that the membrane permeability follows a step function with increasing permeability at the transition from the gel to the fluid phase and vice versa. Second, there was an all-or-nothing permeabilization near the main phase transition temperature and a gradual dye release far off the melting transition. Third, the Laurdan phase state analysis suggests that shear forces induce a reversible melting temperature shift in giant unilamellar vesicle membranes.RESULTSWe observed that the membrane permeability follows a step function with increasing permeability at the transition from the gel to the fluid phase and vice versa. Second, there was an all-or-nothing permeabilization near the main phase transition temperature and a gradual dye release far off the melting transition. Third, the Laurdan phase state analysis suggests that shear forces induce a reversible melting temperature shift in giant unilamellar vesicle membranes.The observed effects can be explained best in a scenario in which shear forces directly induce membrane pores that possess relatively long pore lifetimes in proximity to the phase transition.MAJOR CONCLUSIONSThe observed effects can be explained best in a scenario in which shear forces directly induce membrane pores that possess relatively long pore lifetimes in proximity to the phase transition.Our study elucidates the release mechanism of thermo-responsive drug carriers as we found that liposome permeabilization is not continuous but quantized. Furthermore, the shear force induced melting temperature shift must be taken into consideration when thermo-responsive liposomes are designed.GENERAL SIGNIFICANCEOur study elucidates the release mechanism of thermo-responsive drug carriers as we found that liposome permeabilization is not continuous but quantized. Furthermore, the shear force induced melting temperature shift must be taken into consideration when thermo-responsive liposomes are designed. The permeability of a lipid bilayer is a function of its phase state and depends non-linearly on thermodynamic variables such as temperature, pressure or pH. We investigated how shear forces influence the phase state of giant unilamellar vesicles and their membrane permeability. We determined the permeability of giant unilamellar vesicles composed of different phospholipid species under shear flow in a tube at various temperatures around and far off the melting point by analyzing the release of fluorescently labelled dextran. Furthermore, we quantified phase state changes of these vesicles under shear forces using spectral decomposition of the membrane embedded fluorescent dye Laurdan. We observed that the membrane permeability follows a step function with increasing permeability at the transition from the gel to the fluid phase and vice versa. Second, there was an all-or-nothing permeabilization near the main phase transition temperature and a gradual dye release far off the melting transition. Third, the Laurdan phase state analysis suggests that shear forces induce a reversible melting temperature shift in giant unilamellar vesicle membranes. The observed effects can be explained best in a scenario in which shear forces directly induce membrane pores that possess relatively long pore lifetimes in proximity to the phase transition. Our study elucidates the release mechanism of thermo-responsive drug carriers as we found that liposome permeabilization is not continuous but quantized. Furthermore, the shear force induced melting temperature shift must be taken into consideration when thermo-responsive liposomes are designed. [Display omitted] •Membrane permeability increase by transition from gel to fluid phase and vice versa.•All-or-nothing GUV permeabilization under shear flow near the phase transition.•Gradual GUV permeabilization under shear flow far off the phase transition.•Phase state dependent membrane permeability increase induced by shear forces.•Lipid membrane melting temperature shift induced by shear forces. |
ArticleNumber | 130199 |
Author | Kamenac, Andrej Färber, Nicolas Reitler, Jonas Westerhausen, Christoph |
Author_xml | – sequence: 1 givenname: Nicolas surname: Färber fullname: Färber, Nicolas organization: Experimental Physics I, Institute of Physics, University of Augsburg, Universitätsstr. 1, 86159 Augsburg, Germany – sequence: 2 givenname: Jonas surname: Reitler fullname: Reitler, Jonas organization: Physiology, Institute of Theoretical Medicine, University of Augsburg, Universitätsstraße 2, 86159 Augsburg, Germany – sequence: 3 givenname: Andrej surname: Kamenac fullname: Kamenac, Andrej organization: Experimental Physics I, Institute of Physics, University of Augsburg, Universitätsstr. 1, 86159 Augsburg, Germany – sequence: 4 givenname: Christoph surname: Westerhausen fullname: Westerhausen, Christoph email: christoph.westerhausen@gmail.com organization: Experimental Physics I, Institute of Physics, University of Augsburg, Universitätsstr. 1, 86159 Augsburg, Germany |
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Keywords | Laurdan Order disorder phase transitions Lipid membrane state Generalized polarization Shear flow Membrane permeability |
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SubjectTerms | dextran drugs fluorescent dyes gels Generalized polarization Laurdan lipid bilayers Lipid membrane state Membrane permeability Order disorder phase transitions phase transition phospholipids Shear flow shear stress species temperature thermodynamics |
Title | Shear stress induced lipid order and permeability changes of giant unilamellar vesicles |
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