Electric field-driven water dipoles: nanoscale architecture of electroporation.
Electroporation is the formation of permeabilizing structures in the cell membrane under the influence of an externally imposed electric field. The resulting increased permeability of the membrane enables a wide range of biological applications, including the delivery of normally excluded substances...
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2013-01-01
|
| Series: | PLoS ONE |
| Online Access: | http://europepmc.org/articles/PMC3623848?pdf=render |
| _version_ | 1818326949804638208 |
|---|---|
| author | Mayya Tokman Jane HyoJin Lee Zachary A Levine Ming-Chak Ho Michael E Colvin P Thomas Vernier |
| author_facet | Mayya Tokman Jane HyoJin Lee Zachary A Levine Ming-Chak Ho Michael E Colvin P Thomas Vernier |
| author_sort | Mayya Tokman |
| collection | DOAJ |
| description | Electroporation is the formation of permeabilizing structures in the cell membrane under the influence of an externally imposed electric field. The resulting increased permeability of the membrane enables a wide range of biological applications, including the delivery of normally excluded substances into cells. While electroporation is used extensively in biology, biotechnology, and medicine, its molecular mechanism is not well understood. This lack of knowledge limits the ability to control and fine-tune the process. In this article we propose a novel molecular mechanism for the electroporation of a lipid bilayer based on energetics analysis. Using molecular dynamics simulations we demonstrate that pore formation is driven by the reorganization of the interfacial water molecules. Our energetics analysis and comparisons of simulations with and without the lipid bilayer show that the process of poration is driven by field-induced reorganization of water dipoles at the water-lipid or water-vacuum interfaces into more energetically favorable configurations, with their molecular dipoles oriented in the external field. Although the contributing role of water in electroporation has been noted previously, here we propose that interfacial water molecules are the main players in the process, its initiators and drivers. The role of the lipid layer, to a first-order approximation, is then reduced to a relatively passive barrier. This new view of electroporation simplifies the study of the problem, and opens up new opportunities in both theoretical modeling of the process and experimental research to better control or to use it in new, innovative ways. |
| first_indexed | 2024-12-13T12:08:30Z |
| format | Article |
| id | doaj.art-d8f81dbb207443db897fa26dd59803e2 |
| institution | Directory Open Access Journal |
| issn | 1932-6203 |
| language | English |
| last_indexed | 2024-12-13T12:08:30Z |
| publishDate | 2013-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS ONE |
| spelling | doaj.art-d8f81dbb207443db897fa26dd59803e22022-12-21T23:46:54ZengPublic Library of Science (PLoS)PLoS ONE1932-62032013-01-0184e6111110.1371/journal.pone.0061111Electric field-driven water dipoles: nanoscale architecture of electroporation.Mayya TokmanJane HyoJin LeeZachary A LevineMing-Chak HoMichael E ColvinP Thomas VernierElectroporation is the formation of permeabilizing structures in the cell membrane under the influence of an externally imposed electric field. The resulting increased permeability of the membrane enables a wide range of biological applications, including the delivery of normally excluded substances into cells. While electroporation is used extensively in biology, biotechnology, and medicine, its molecular mechanism is not well understood. This lack of knowledge limits the ability to control and fine-tune the process. In this article we propose a novel molecular mechanism for the electroporation of a lipid bilayer based on energetics analysis. Using molecular dynamics simulations we demonstrate that pore formation is driven by the reorganization of the interfacial water molecules. Our energetics analysis and comparisons of simulations with and without the lipid bilayer show that the process of poration is driven by field-induced reorganization of water dipoles at the water-lipid or water-vacuum interfaces into more energetically favorable configurations, with their molecular dipoles oriented in the external field. Although the contributing role of water in electroporation has been noted previously, here we propose that interfacial water molecules are the main players in the process, its initiators and drivers. The role of the lipid layer, to a first-order approximation, is then reduced to a relatively passive barrier. This new view of electroporation simplifies the study of the problem, and opens up new opportunities in both theoretical modeling of the process and experimental research to better control or to use it in new, innovative ways.http://europepmc.org/articles/PMC3623848?pdf=render |
| spellingShingle | Mayya Tokman Jane HyoJin Lee Zachary A Levine Ming-Chak Ho Michael E Colvin P Thomas Vernier Electric field-driven water dipoles: nanoscale architecture of electroporation. PLoS ONE |
| title | Electric field-driven water dipoles: nanoscale architecture of electroporation. |
| title_full | Electric field-driven water dipoles: nanoscale architecture of electroporation. |
| title_fullStr | Electric field-driven water dipoles: nanoscale architecture of electroporation. |
| title_full_unstemmed | Electric field-driven water dipoles: nanoscale architecture of electroporation. |
| title_short | Electric field-driven water dipoles: nanoscale architecture of electroporation. |
| title_sort | electric field driven water dipoles nanoscale architecture of electroporation |
| url | http://europepmc.org/articles/PMC3623848?pdf=render |
| work_keys_str_mv | AT mayyatokman electricfielddrivenwaterdipolesnanoscalearchitectureofelectroporation AT janehyojinlee electricfielddrivenwaterdipolesnanoscalearchitectureofelectroporation AT zacharyalevine electricfielddrivenwaterdipolesnanoscalearchitectureofelectroporation AT mingchakho electricfielddrivenwaterdipolesnanoscalearchitectureofelectroporation AT michaelecolvin electricfielddrivenwaterdipolesnanoscalearchitectureofelectroporation AT pthomasvernier electricfielddrivenwaterdipolesnanoscalearchitectureofelectroporation |