Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes
There is mounting evidence that lipid bilayers display conductive properties. However, when interpreting the electrical response of biological membranes to voltage changes, they are commonly considered as inert insulators. Lipid bilayers under voltage-clamp conditions display current traces with dis...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2021-01-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2020.592520/full |
| _version_ | 1818596484605542400 |
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| author | Karis Amata Zecchi Thomas Heimburg |
| author_facet | Karis Amata Zecchi Thomas Heimburg |
| author_sort | Karis Amata Zecchi |
| collection | DOAJ |
| description | There is mounting evidence that lipid bilayers display conductive properties. However, when interpreting the electrical response of biological membranes to voltage changes, they are commonly considered as inert insulators. Lipid bilayers under voltage-clamp conditions display current traces with discrete conduction-steps, which are indistinguishable from those attributed to the presence of protein channels. In current-voltage (I-V) plots they may also display outward rectification, i.e., voltage-gating. Surprisingly, this has even been observed in chemically symmetric lipid bilayers. Here, we investigate this phenomenon using a theoretical framework that models the electrostrictive effect of voltage on lipid membranes in the presence of a spontaneous polarization, which can be recognized by a voltage offset in electrical measurements. It can arise from an asymmetry of the membrane, for example from a non-zero spontaneous curvature of the membrane. This curvature can be caused by voltage via the flexoelectric effect, or by hydrostatic pressure differences across the membrane. Here, we describe I-V relations for lipid membranes formed at the tip of patch pipettes situated close to an aqueous surface. We measured at different depths relative to air/water surface, resulting in different pressure gradients across the membrane. Both linear and non-linear I-V profiles were observed. Non-linear conduction consistently takes the form of outward rectified currents. We explain the conductance properties by two mechanisms: One leak current with constant conductance without pores, and a second process that is due to voltage-gated pore opening correlating with the appearance of channel-like conduction steps. In some instances, these non-linear I-V relations display a voltage regime in which dI/dV is negative. This has also been previously observed in the presence of sodium channels. Experiments at different depths reveal channel formation that depends on pressure gradients. Therefore, we find that the channels in the lipid membrane are both voltage-gated and mechanosensitive. We also report measurements on black lipid membranes that also display rectification. In contrast to the patch experiments they are always symmetric and do not display a voltage offset. |
| first_indexed | 2024-12-16T11:32:39Z |
| format | Article |
| id | doaj.art-36c45889b5284a11950d0b494f35ebdd |
| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-12-16T11:32:39Z |
| publishDate | 2021-01-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-36c45889b5284a11950d0b494f35ebdd2022-12-21T22:33:13ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2021-01-01810.3389/fcell.2020.592520592520Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid MembranesKaris Amata ZecchiThomas HeimburgThere is mounting evidence that lipid bilayers display conductive properties. However, when interpreting the electrical response of biological membranes to voltage changes, they are commonly considered as inert insulators. Lipid bilayers under voltage-clamp conditions display current traces with discrete conduction-steps, which are indistinguishable from those attributed to the presence of protein channels. In current-voltage (I-V) plots they may also display outward rectification, i.e., voltage-gating. Surprisingly, this has even been observed in chemically symmetric lipid bilayers. Here, we investigate this phenomenon using a theoretical framework that models the electrostrictive effect of voltage on lipid membranes in the presence of a spontaneous polarization, which can be recognized by a voltage offset in electrical measurements. It can arise from an asymmetry of the membrane, for example from a non-zero spontaneous curvature of the membrane. This curvature can be caused by voltage via the flexoelectric effect, or by hydrostatic pressure differences across the membrane. Here, we describe I-V relations for lipid membranes formed at the tip of patch pipettes situated close to an aqueous surface. We measured at different depths relative to air/water surface, resulting in different pressure gradients across the membrane. Both linear and non-linear I-V profiles were observed. Non-linear conduction consistently takes the form of outward rectified currents. We explain the conductance properties by two mechanisms: One leak current with constant conductance without pores, and a second process that is due to voltage-gated pore opening correlating with the appearance of channel-like conduction steps. In some instances, these non-linear I-V relations display a voltage regime in which dI/dV is negative. This has also been previously observed in the presence of sodium channels. Experiments at different depths reveal channel formation that depends on pressure gradients. Therefore, we find that the channels in the lipid membrane are both voltage-gated and mechanosensitive. We also report measurements on black lipid membranes that also display rectification. In contrast to the patch experiments they are always symmetric and do not display a voltage offset.https://www.frontiersin.org/articles/10.3389/fcell.2020.592520/fullpermeabilityion channelsrectificationlipid membraneflexoelectricitythermodynamics |
| spellingShingle | Karis Amata Zecchi Thomas Heimburg Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes Frontiers in Cell and Developmental Biology permeability ion channels rectification lipid membrane flexoelectricity thermodynamics |
| title | Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes |
| title_full | Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes |
| title_fullStr | Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes |
| title_full_unstemmed | Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes |
| title_short | Non-linear Conductance, Rectification, and Mechanosensitive Channel Formation of Lipid Membranes |
| title_sort | non linear conductance rectification and mechanosensitive channel formation of lipid membranes |
| topic | permeability ion channels rectification lipid membrane flexoelectricity thermodynamics |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2020.592520/full |
| work_keys_str_mv | AT karisamatazecchi nonlinearconductancerectificationandmechanosensitivechannelformationoflipidmembranes AT thomasheimburg nonlinearconductancerectificationandmechanosensitivechannelformationoflipidmembranes |